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A stable sulfur and oxygen isotopic investigation of sulfur cycling in an anoxic marine basin, Framvaren Fjord, Norway
Chemical Geology 195 (2003) 181 – 200 www.elsevier.com/locate/chemgeo
A stable sulfur and oxygen isotopic investigation of sulfur cycling in an anoxic marine basin, Framvaren Fjord, Norway Kevin W. Mandernack a,*, H. Roy Krouse b, Jens M. Skei c a
Department of Chemistry and Geochemistry, Colorado School of Mines, Golden, CO 80401, USA b Department of Physics and Astronomy, University of Calgary, Calgary, AB Canada T2N-1N4 c Norwegian Institute for Water Research, P.O. Box 173 Kjelsas, N-0411 Oslo, Norway Received 28 December 2000; accepted 22 March 2002
Abstract In 1993 we measured the d34S values of total dissolved sulfide (d34SSH2S) and sulfate (d34SSO4) and the d18O of sulfate (d18OSO4) from water samples collected across the oxic – anoxic interface and in the deep permanently anoxic waters of the stratified Framvaren fjord in southern Norway. Near the chemocline, variations in the d34SSO4 and d18OSO4 values were generally less than 1x from ambient seawater values. However, a minimum d34SSO4 value of + 19.7x was detected at 20 m depth, which coincided with the depth that sulfide first appeared and may reflect sulfide oxidation. Small increases in d34SSO4 and d18OSO4 values 3 m below this depth are consistent with a zone of sulfur disproportionation. The d34SSH2S value near the interface at 22 m was 19.8x , which is 41.2x depleted in 34S relative to the sulfate collected at that depth. In close agreement with earlier measurements made at Framvaren in 1982, the d34SSO4 values collected from the deeper anoxic waters showed a marked 34S enrichment with depth, which corresponded with a decrease in the sulfate concentration. These results are interpreted to be the result of active dissimilatory sulfate reduction. A Rayleigh plot for the sulfate data measured in 1993 provides estimates for the sulfur and oxygen isotope enrichment factors (es and eo, respectively) for sulfate reduction of 41.5x and 9.8x , respectively, with the former value matching closely the observed difference in d34S between the dissolved sulfide and sulfate near the interface. Our results from 1993, however, contrast with d34SSO4 and d34SSH2S data in the water column made in 1983 by Anderson et al. [Mar. Chem. 23 (1988) 283). We conclude that the results of 1983 may be anomalous, and as a result this may offer additional interpretations than what was previously provided for the origin of reduced inorganic sulfur in the sediments of Framvaren based on their measured d34S values. We hypothesize that the lower d34Strs values in the sediments relative to d34SSH2S values in the water column could also result from different rates of sulfate reduction, or in shallower sediments just beneath the chemocline, also from disproportionation of SB, S2O 3 , or SO3 . We hypothesize that the observed ratio of 4.4:1 for the measured changes in d34SSO4 versus d18OSO4 within the anoxic waters approximates the 4:1 atom ratio of oxygen to sulfur in the residual sulfate as a result of dissimilatory sulfate reduction and reflects little oxygen isotope exchange between intermediates of sulfur metabolism and water either during bacterial sulfate reduction or from sulfide reoxidation processes. Based on comparisons with other studies, we further propose that this lack of isotopic exchange with water, and the subsequent f 4:1 ratio of d34SSO4 versus d18OSO4, occurs under conditions that promote a unidirectional
* Corresponding author. Tel.: +1-303-384-2224; fax: +1-303-273-3629. E-mail address: [email protected] (K.W. Mandernack). 0009-2541/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0009-2541(02)00394-7
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biochemical reaction for sulfate reduction during which kinetic isotope effects are fully expressed and are consequently reflected in the d34SSO4 and d18OSO4 values. D 2003 Elsevier Science B.V. All rights reserved. Keywords: Sulfide; Sulfate; Biogeochemistry; Stable isotopes; Anoxic; Sulfur cycling
1. Introduction Active sulfur transformations occur near oxic – anoxic interfaces in restricted marine environments such as the Black Sea and anoxic fjords such as Framvaren fjord and Saanich inlet (Jorgensen et al., 1991; Mandernack and Tebo, 1999; Millero, 1991; Sorokin, 1972). Anoxic basins and global oceanic anoxic events are important controls on the temporal variability of d34S values of seawater sulfate (Berner and Raiswell, 1983; Claypool et al., 1980), the global sulfur cycle (Berner, 1987; Kump, 1989), and localization of seafloor hydrothermal sulfide ore deposits of the sedimentary exhalative (SEDEX) class (Goodfellow and Jonasson, 1984; Shanks et al., 1987; Turner, 1992). Below oxic – anoxic interfaces, the decomposition of organic matter is primarily coupled to sulfate reduction, which results in the formation of hydrogen sulfide (HS). The rates of sulfate reduction in marine environments and the subsequent formation of HS are primarily controlled by both the quality and quantity of organic matter available from autochthonous or allochthonous sources (Berner, 1978; Goldhaber and Kaplan, 1975; Jorgensen, 1981; Jorgensen, 1982). Due to large kinetic isotope effects, the sulfide produced from dissimilatory sulfate reduction tends to be very depleted in 34S relative to the reactant sulfate (Goldhaber and Kaplan, 1975; Harrison and Thode, 1958; Kaplan and Rittenberg, 1964; Nakai and Jensen, 1964). Laboratory cultures of sulfate-reducing bacteria fractionate the sulfur isotopes (32S and 34S) of sulfate by 2 – 47xduring dissimilatory reduction (Bolliger et al., 2001; Detmers et al., 2001; Harrison and Thode, 1958; Kaplan and Rittenberg, 1964; Mizutani and Rafter, 1969), whereas field measurements sometimes suggest isotopic enrichment factors for sulfur (es) as large as 60 –70x(Goldhaber and Kaplan, 1975). In addition, fractionation of the oxygen isotopes of sulfate occurs during dissimilatory sulfate reduction, although with smaller and variable values of eo (Ku et al., 1999; Mizutani and Rafter,
1969). Variations in eo can result from kinetic effects due to variable rates of sulfate reduction and from isotopic exchange reactions between water and metabolic intermediates of sulfur reduction and oxidation processes (Aharon and Fu, 2000; Bo¨ttcher et al., 2001; Fritz et al., 1989; Ku et al., 1999; Mizutani and Rafter, 1973). The 34S-depleted HS produced by sulfate reduction below the redox interface can diffuse upward to the oxic or suboxic zone where it can be oxidized by chemoautotrophic bacteria utilizing O2, NO3, and possibly Fe/Mn oxides as electron acceptors (Adams et al., 1971; Aller and Rude, 1988; Brock and Gustafson, 1976; Fossing et al., 1995; Kelly, 1988; Luther et al., 1988; Millero, 1991; Sweerts et al., 1990; Timmer-ten Hoor, 1975, 1981). Diverse populations of sulfur oxidizing bacteria have been identified from near the chemocline of anoxic marine basins (Jannasch et al., 1991; Tuttle and Jannasch, 1973) where microbial oxidation has been measured (Jorgensen et al., 1991; Mandernack and Tebo, 1999; Sorokin, 1972). When sunlight is available, sulfide oxidation can also be mediated by anoxygenic photosynthetic sulfur bacteria (Cohen et al., 1977; Kuenen, 1975; Overmann et al., 1991; Sorensen, 1988). The oxidation of HS in anoxic basins can also proceed rapidly and abiotically with O2 or Fe and Mn oxides as electron acceptors (Luther et al., 1988; Millero, 1991; Sorokin, 1972) or, if light is present, via photooxidation reactions (Luther, 1995; Luther et al., 1988). Sulfide can also be indirectly oxidized from the production of O2 from oxygenic photosynthesis by cyanobacteria (Jorgensen, 1979). In general, sulfur isotope effects associated with the oxidation of sulfide are small in comparison to those from sulfate reduction (Fry et al., 1986). A sulfur isotope enrichment factor (es) of 5xhas been measured for abiotic oxidation of HS (Fry et al., 1988). A reverse isotope effect was measured for the oxidation of sulfide by an anaerobic photosynthetic purple sulfur bacterium where es= + 2x(Fry et
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al., 1984). Neither bacterial nor abiotic oxidation of solid phase metal sulfides produces a significant sulfur isotope effect (McCready and Krouse, 1982; Nakai and Jensen, 1964; Taylor et al., 1984). Consequently, the d34S of the sulfate produced from sulfide oxidation will generally reflect its parent substrates. The d18O value of the sulfate produced during sulfide oxidation will vary considerably due to differences in the relative percent of dissolved oxygen that becomes incorporated into sulfate as a result of chemical versus biological oxidation and differences in ev with respect to O2 (Lloyd, 1968; Taylor et al., 1984; Toran and Harris, 1989; Van Everdingen and Krouse, 1985). In general, it appears that both ev and the percent incorporation of dissolved O2 into sulfate are larger during biological versus abiotic oxidation (Lloyd, 1968; Taylor et al., 1984; Van Everdingen and Krouse, 1985). Analysis of the d34SSH2S, d34SSO4, and d18OSO4 values in aquatic systems can therefore help identify the microbial or abiotic processes involved in sulfur cycling as well as temporal and spatial changes in these processes. Previous reports of d18OSO4 values in modern marine or brackish systems are few (Aharon and Fu, 2000; Bo¨ttcher et al., 1999; Bottrell et al., 2000; Jeffries et al., 1984; Ku et al., 1999; Sheu et al., 1988; Zak et al., 1980). Framvaren fjord is a stratified anoxic marine basin in southern Norway. It has a distinct O2 – H2S interface (chemocline) at approximately 19 m depth, where some of the highest rates of sulfide removal have been reported for any marine system (Mandernack and Tebo, 1999; Millero, 1991; Yao and Millero, 1995). In addition, as a result of a rich assemblage of green and purple sulfur bacteria, as well as phytoplankton, very high rates of CO2 fixation and primary productivity also occur at the interface (Mandernack and Tebo, 1999; Sorensen, 1988). Framvaren represents an ideal environment to study biogeochemical processes associated with sulfur cycling at both the interface and in the deep anoxic water column. In this study, we analyzed d34SSH2S, d34SSO 4, and d18OSO4 values across the oxic – anoxic interface and in the permanently anoxic bottom water of Framvaren fjord. We choose Framvaren for this study because data acquired in 1982 and 1983 (Anderson et al., 1988) allow evaluation of the temporal variations in the stable isotopic values of sulfate and sulfide
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within the deep bottom waters of this fjord. The observed large changes between 1983 and 1993 could suggest ventilation of the deep anoxic waters with oxic waters from outside of the fjord that periodically spill over the sill at the entrance to Framvaren. However, it is difficult to reconcile d34SSO4 data collected in 1983 with d34SSO4 measurements made in 1982 and 1993. The results of our study assist in the interpretation of isotopic evidence preserved in ancient euxinic sulfur deposits within the geological record.
2. Methods Water samples above and near the interface were collected in June 1993 with a submersible pumping system (supplied and operated by B. McKee and J. Todd), whereas deeper samples from 40 m and below were collected with 10-l Go-Flo bottles. Dissolved oxygen concentration, as determined by Winkler titrations, at 18 m depth was 8.3 AM and nondetectable below this, whereas dissolved sulfide was first detected at 20 m (Yao and Millero, 1995). From each water sample collected, 100-ml subsamples were taken with Winkler bottles for stable isotopic analyses of sulfide and sulfate. The bottles were first purged with N2 and then quickly filled without any gas headspace. Prior to sealing the bottle, formaldehyde (2% final concentration) and zinc acetate (50 mg/10 ml) were added as a poison and sulfide trapping agent, respectively. Care was taken to fully sequester the dissolved sulfide as ZnS prior to decanting a small volume of the samples to allow space for freezing immediately on board the ship. The frozen water samples were allowed to thaw and subsequently filtered (0.2 AM Millipore) under an argon atmosphere back in the lab. The filtrate was then reserved for sulfate concentration measurements and a separate portion reserved for extraction of the sulfate for isotopic analyses. The volume of each sample filtered was measured in order to subsequently determine the total sulfide concentrations from the trapped HS (as ZnS) and any Sj and Fe sulfide present in the water column as described elsewhere (Mandernack et al., 2000a). These sulfur compounds were trapped on filters from 20 to 150 m depths and retained for stable isotopic and/or sulfide concentra-
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tion measurements using CrCl2 – HCl methods described previously (Fossing and Jorgensen, 1989; Mandernack et al., 2000a). The CrCl2 – HCl treatment yielded ZnS that was reprecipitated from all sources of reduced sulfur (HS, Sj, FeS2, and ‘‘FeS’’) and subsequently analyzed for d34S and concentrations by iodometric titration (see below). However, based on previous measurements of Millero (1991) and Yao and Millero (1995), HS represents the vast majority of reduced sulfur in our samples (Table 1), and therefore, this fraction will henceforth be referred to as SH2S. It was anticipated that there would be insufficient SH2S at the 20- and 21.5-m depths for isotopic measurements, and therefore, these were reserved only for sulfide concentration measurements. Zinc sulfides collected from the 22-, 23-, and 100-m samples were processed only for stable isotopic analyses, whereas splits were made from the remaining samples for both concentration and d34S measurements. Due to small sample sizes, the zinc sulfide samples prepared from the 22- to 24-m depths were analyzed d34S in March 1994 at the Marine Biological Laboratory in Woods Hole, MA, under the supervision of Dr. Brian Fry. In general, for similar depths there was good agreement in the sulfide concentrations measured with those of Yao and Millero (1995) during the same cruise (Table 1). Sulfate concentrations from the filtrates were determined using ion chromatography with a precision of
F 2%. In order to prepare and concentrate the sulfate from the filtrates for d34S and d18O analyses, 10– 20 ml of each filtrate was acidified at a ratio of 17 Al HCl/10 ml of sample (final pH f 2.5 – 3.0) and then diluted 1:20 with deionized water. Concentrated HCl was added to prevent the possibility of BaCO3 precipitation, which might interfere with the d18O measurements. The diluted filtrate was then passed at 1– 4 ml/min through ion exchange resin (Bio-Rad, AG1 – X8, 100 –200 mesh, chloride form) and eluted with 120 – 130 ml of 0.5 M NaCl using methods similar to those described elsewhere (Mandernack et al., 2000a; Stam et al., 1992; Van Stempvoort, 1989). Sulfate recovery by this method generally exceeded 95%. The sulfate was then precipitated as BaSO4 by addition of 10 ml of 10 wt.% BaCl2, washed five to six times with deionized water, and dried. As a final purification step, all of the BaSO4 powders were baked under an air atmosphere at 500 jC for 2 h. This treatment was previously shown to effectively remove any possible organic material and to not interfere with d18O measurements (Mandernack et al., 2000a). For mass spectrometric analysis, BaSO4 and ZnS precipitates were converted to SO2 by reaction with a 50:50 mixture of SiO2/V2O5 (1:20 ratio of BaSO4:mixture, 1:53 ratio for ZnS) under vacuum (Yanagisawa and Sakai, 1983) and analyzed on-line with a Micro-mass 602 double collecting isotope ratio mass spectrometer. The sulfur isotope data are pre-
Table 1 Sulfur concentrations and stable isotopic values in the water column of Framvaren Fjord, Norway Depth sampled (m)
d34SVCDT SH2S
d34SVCDT SO24
n
d18OVSMOW SO24
n
[SO4]a, mM
[H2S]b, AM
10 15 19 20 21.5 22 23 24 40 100 150
I.S. I.S. I.S. I.S. I.S. 19.8 18.6 19.2 13.4 3.1 4.4
20.1 20.0 20.7 F 0.2 19.7 21.6 F 0.4 21.4 21.9 21.3 F 0.3 22.8 F 0.1 37.8 F 0.05 42.2 F 0.02
1 1 3 1 2 1 1 3 2 3 2
10.4 F 0.4 N.D. 10.4 F 0.3 10.3 F 0.4 11.6 F 0.2 11.1 F 0.5 11.3 10.4 F 0.6 11.0 F 0.4 13.9 F 0.1 15.5 F 0.3
2
13.2 14.0 15.5 14.3 15.7 16.0 16.1 16.6 16.5 12.0 10.0
UD UD UD 4.2, (0.4) 73.6, (97.8) (182) (194) 410.0 1030, (1132) (4528) 4720, (5106)
I.S. = insufficient quantities of chromium reducible sulfur for d34S analyses. N.D. = not determined. UD = undetectable. a For samples depths >24 m; from 1985 data set of Anderson et al. (1988). b Values in parentheses from Yao and Millero (1995).
5 4 3 3 1 4 4 2 2
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sented in terms of the VCDT scale based on reference material IAEA-S1 (formerly NZ-1) having a d34S value of 0.30x, where: d34 Ssample ðx Þ ¼ ½ð34 S=32 Ssample Þ =ð34 S=32 SVCDT Þ 1 103 The d18O values are presented in terms of ocean water sulfate having a value of +9.5xon the VSMOW scale. Intra-laboratory analytical sulfate standards for d34S (+5.4xand +20.4x ) and d18O ( +9.5x and +12.0x) gave reproducibility of F0.15xand F0.4x, respectively, based on multiple analyses.
3. Results Table 1 summarizes all of the concentration and stable isotopic measurements made of reduced sulfur and sulfate in this study. The sulfate concentration measurements made on water samples below the interface (>24 m) are suspect. The addition of zinc acetate and the presence of high concentrations of sulfide (>1 mM) in these samples appeared to interfere with the response of the ion chromatograph, and sulfate con-
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centrations appeared anomalously low. Therefore, for depths of 40 m or more, we have listed in Table 1 the 1985 sulfate data of Anderson et al. (1988), which correspond to the same depths we sampled in our study. In Table 1, we also present in parentheses the sulfide concentrations reported by Yao and Millero (1995), which were measured during our cruise. The variations in the d34SSO4 and d18OSO4 values with depth are small and co-vary from 19 to 24 m near the oxic – anoxic interface (Table 1; Fig. 1). At depths of 20 m and less, the d34SSO4 and d18OSO4 values are close to + 20.0xand + 10.4x, respectively. From 21.5 to 24 m, the d34SSO4 and d18OSO4 values are relatively consistent and increase with increasing depth to + 21.6xand + 11.3x, respectively (Table 1; Fig. 1). The d34SSO4 and d18OSO4 values continue to increase at depths greater than 24 m, along with a decline in sulfate and rise in sulfide concentrations (Table 1; Fig. 1), consistent with the cumulative effects of dissimilatory sulfate reduction occurring throughout the deep anoxic water column. Fig. 2 summarizes all of the d34SSO4, d34SSH2S, and d34STRS values measured in the water column and sediments of Framvaren in this and previous studies (Anderson et al., 1988; Saelen et al., 1993). In gen-
Fig. 1. The d34SVCDT ( ) and d18OVSMOW (o) values of sulfate from samples collected during this study in June 1993 in the water column of Framvaren fjord. Right panel (B) shows more detail across the oxic – anoxic interface where the horizontal dashed line indicates the depth of 20 m at which sulfide was first detected.
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Fig. 2. The d34SVCDT values of sulfate (open symbols) and SH2S (closed symbols) in the water column of Framvaren fjord from samples collected in June 1993 during this study (diamonds) and in 1982 (squares) and 1983 (circles) as reported by Anderson et al., 1988. The d34SVCDT values of total reduced sulfur (TRS) in the sediments of Framvaren reported by Saelen et al. (1993) are also shown ( ). The horizontal dashed line indicates the depth of 20 m at which sulfide was first detected.
eral, there is good agreement between the d34SSO4 values that we measured in 1993 and those in 1982 by Anderson et al. (1988) (Fig. 2). However, for the deep anoxic waters, the d34SSO4 values measured in 1983 by Anderson et al. (1988) are consistently lower by approximately 10xthan what was measured in either 1982 or 1993 (Fig. 2). Framvaren water column sulfide concentrations measured by Yao and Millero (1995) during the same cruise in 1993 agree well with our data (Table 1). The lowest d34SSH2S value that we measured ( 19.8x) occurred just beneath the interface at 22 m and is 41.2xdepleted in 34S relative to sulfate at that depth (Table 1). Below 24 m, the d34SSH2S values gradually increased with depth to values as high as 3.1xand track similar changes in higher d34SSO4 values (Table 1; Fig. 2). As for sulfate, the d34SSH2S values we measured in the deep anoxic waters are more similar to the values measured for sulfide in samples collected in 1982 versus those collected in 1983 as reported by Anderson et al. (1988) (Fig. 2). In Fig. 3, we plot sulfide versus sulfate concentrations using the 1985 sulfate data from Anderson et
al (1988) and the sulfide data of Yao and Millero (1995) for corresponding depths within the deeper anoxic waters ( z 40 m depth). This results in a straight-line fit with an r2 value of 0.98 and a slope equal to 0.65. If there were no loss of sulfide from this system, such a plot would yield a line with a slope equal to 1 where the decline in sulfate is equally balanced by the increase in sulfide. Instead, we can see from Fig. 3 that approximately 35% of the sulfide produced from reduction has been lost from the water column since the onset of anoxia in Framvaren. Loss of sulfide could occur from diffusion upward and subsequent oxidation near the interface. However, this would not result in significant net loss of sulfide from the system over time as it is recycled near the interface. Furthermore, a sulfur repartitioning process such as this would then produce an excess of sulfate relative to sulfide near the redox interface and an apparent depletion of sulfate relative to sulfide in the deeper anoxic waters. Such a process would then produce in Fig. 3 a linear regression with a slope > 1.0 that would bisect the reference line. Because we do not observe this, and the x-intercept of our plot
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anoxic deep waters of Framvaren have experienced stable and steady-state conditions with respect to sulfate during this time. This is also consistent with previous reports that little water renewal occurs in the bottom waters of Framvaren (Dyrssen et al., 1996; Stigebrandt and Molvaer, 1988). In basins like Framvaren, which have restricted mixing, the d34SSO4 value might be expected to increase with depth as it approximates a Rayleigh distillation effect. If there is a finite amount of available reactant (i.e., sulfate), then the fractionation effect is compounded over time as sulfate reduction proceeds and the sulfide formed is separated from the sulfate. This Rayleigh effect can be described by a simple natural log function: Fig. 3. Sulfide concentrations measured in 1993 (from Table 1 of Yao and Millero, 1995) plotted relative to sulfate concentrations measured in 1985 (from Table 3 of Anderson et al., 1988) for corresponding depths in the water column of Framvaren fjord (40, 50, 70, 100, 110, 130, 150, and 170 m). The measured slope of 0.65 deviates from a slope of 1 by 0.35, suggesting that 35% of the sulfide produced from sulfate reduction has been removed from the water column. The x-intercept, where sulfide concentration is zero, of 18.55 reflects the original sulfate concentration (mM) of Framvaren fjord before anoxia was established (see text).
closely approximates the expected value for the initial sulfate concentration in Framvaren (see following discussion), it seems more reasonable that the greatest loss of sulfide occurs from sedimentation, either as iron sulfides or organic sulfur. In addition, some of the reduced sulfur may exist as Sj or other thiols (Dyrssen et al., 1996). An interesting observation from the regression in Fig. 3 is that the sulfate intercept (i.e., corresponding to null levels of sulfide) is 18.55 mM, which is consistent with the initial sulfate concentration estimated for Framvaren (i.e., prior to removal by sulfate reduction). From the maximum salinity of 22.92 measured by Yao and Millero (1995) for the deepest samples collected at 170 m depth in 1993, we can independently estimate the initial sulfate concentration using a sulfate/salinity ratio of 28.28:35 (Anderson et al., 1988). This results in a similar estimate for the initial sulfate concentration of 18.52 mM. This agreement in estimates, and the internal consistency of our calculation using sulfate data from 1985 and sulfide data from 1993 suggests that the permanently
d34 SSO4 ¼ elnð½Xt =½X0 Þ
ð1Þ
where d34SSO4 is the isotopic composition of the reactant at a certain time of the reaction, which in this case is approximated by the d34SSO4 value at a given depth in the deep anoxic waters where sulfate is progressively removed with depth, epsilon (e) is the isotopic enrichment factor [ = 1000(a 1), where a equals the isotopic fractionation], and [X]0 and [X]t are the concentrations of the reactant at t0 and at any time t, respectively. The ratio [X]t/[X]0 equals F, the fraction of the reactant remaining and is also a measure of the extent of the reaction. If sulfate reduction is primarily a unidirectional process, then Eq. (1) should provide a linear relationship when ln F is plotted against d34S of sulfate, with a slope equal to e (Krouse and Tabatabai, 1986; Mariotti et al., 1981). The value for F plotted in Eq. (1) was estimated as the ratio of the sulfate concentration measured for a given depth to the maximum SO42 concentration of 16.6 mM measured at 24 m depth in 1993 (Table 1). Plotting these results for both the d34S and d18O of sulfate in the anoxic waters ( z 24 m) provides linear relationships (Fig. 4). For comparison, we have also plotted in Fig. 4 the individual data from both 1982 and 1983 of Anderson et al. (1988). Because the isotopic data from 1983 are very distinct from those of 1982 or 1993, we plotted them separately and used the sulfate concentrations measured that year as reported by Anderson et al. (1988). Sulfur isotope enrichment factors (e) of 46.1xand 41.5x estimated for the entire anoxic water column from the
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1982 and 1993 are in good agreement. The value of 41.5xmeasured in 1993 also closely approximates the observed difference in d34S between the sulfate and SH2S measured at the shallowest depth of 22 m (Table 1). However, a sulfur isotope enrichment factor of 17.3xis estimated from the sulfate data of 1983 (Fig. 4), which may indicate non-steady-state conditions in 1983. An oxygen isotope enrichment factor of 9.6xis estimated for sulfate undergoing dissimilatory reduction in Framvaren (Fig. 4). This is approximately 25% of the value estimated for the sulfur isotope enrichment factor. Consequently, a slope of 4.36 is obtained
Fig. 5. The d34SVCDT plotted relative to the d18OVSMOW of sulfate measured in this study from anoxic waters (24 – 150 m) of Framvaren fjord.
when the d34SSO4 from the anoxic waters is plotted against the corresponding d18OSO4 value (Fig. 5).
4. Discussion 4.1. Interface
Fig. 4. A Rayleigh plot which expresses the changes in the d34SVCDT and d18OVSMOW of sulfate measured in the water column of Framvaren fjord in June 1993 during this study (open squares and circles, respectively) and in 1982 (d34SVCDT, closed squares) and 1983 (d34SVCDT, closed triangles) as a function of ln F, where F is the fraction of sulfate concentration measured in the anoxic waters relative to the maximum concentration of 16.6 mM measured in 1993 at 24 m depth (see Table 1 and text). Therefore, all d34SSO4 values measured at the chemocline in 1982, 1983, and 1993 were assumed to have an initial and maximum sulfate concentration of 16.6 mM, which closely approximates the maximum sulfate concentration of 17.0 mM measured at 22 m by Anderson et al. (1988). Sulfate concentration and d34SSO4 data for 1982 and 1983 were obtained from Tables 1 and 2, respectively, from Anderson et al. (1988). The sulfate concentration of 13.1 mM measured at 50 m in 1982, however, appears conspicuously low when compared to other sulfate measurements made at that depth (J. Skei, unpublished results). Therefore, a value of 15.9 mM was used for this depth which corresponds to the sulfate concentration measured at 50 m in 1985 (see Table 3, Anderson et al., 1988).
The variations in d34SSO4 and d18OSO4 are small near the redox interface. This is to be expected in a marine-influenced system with high sulfate concentrations and because sulfur isotope enrichment factors associated with abiotic and biotic sulfide oxidation are small, generally varying from + 2 to 5x(Fry et al., 1986, 1984; Schoen and Rye, 1970). However, the minima in d34SSO4 of 19.7xat 20 m, where sulfide was first detected, is consistent with the oxidation of sulfide with a low d34S value of f 20x(Table 1). Rates of sulfide oxidation by either phototrophic or chemoautotrophic sulfide-oxidizing bacteria are very high near the interface in Framvaren fjord (Mandernack and Tebo, 1999; Sorensen, 1988). Low d34SSO4 values were also observed in a sharp transition zone of a stratified lake where brackish water overlays bottom seawater and were attributed to oxidation of biogenic sulfide produced in deeper waters (Jeffries et al., 1984).
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Dissolved oxygen has a d18O value of approximately + 26x(Kroopnick and Craig, 1972) and can be incorporated into sulfate from 0xto 87.5% during abiotic or biotic sulfide oxidation, with the remaining oxygen coming from water (Lloyd, 1968; Taylor et al., 1984; Toran and Harris, 1989; Van Everdingen and Krouse, 1985). During abiotic and biotic sulfide oxidation, the isotopic fractionation of dissolved O2 can be as large as 8.7xand 11.1x , respectively, whereas values of eo with respect to water during abiotic and biological sulfide oxidation generally fall within the range of 0xto + 4.1xat earth surface temperatures (Toran and Harris, 1989; Van Stempvoort and Krouse, 1994). Therefore, as a result of sulfide oxidation, the d18OSO4 value may increase, but is more likely to decrease from its average seawater value of + 9.7x(Lloyd, 1967). Dissolved oxygen was undetectable below 18 m depth, and sulfide did not appear until 20 m; therefore, there was no apparent O2 – H2S interface during the time of sampling (Yao and Millero, 1995). Under these conditions, sulfide oxidation may have been coupled to the reduction of iron and/or manganese oxides or mediated by phototrophic bacteria (Mandernack and Tebo, 1999; Millero, 1991), during which incorporation of molecular oxygen (O2) into sulfate would be unlikely. The d18Ovsmow value of water near the interface (19 – 24 m) and at the deepest depths (100 and 150 m) of Framvaren was measured by the CO2 equilibration method to be 3.6 F 0.1x (n = 3) and 3.0 F 0.1x(n = 2), respectively (Mandernack, unpublished results). Consequently, sulfate produced from sulfide oxidation at the interface of Framvaren would probably not be depleted in 18O by more than f 9.1xto 13.2xrelative to seawater sulfate. It appears that sulfide oxidation did not provide enough ‘‘isotopic leverage’’ to significantly decrease the d18O of sulfate at the interface of Framvaren, in contrast to the brine interface of the Orca Basin in the Gulf of Mexico where a 1.5xdepletion in d18OSO4 was observed (Sheu et al., 1988). Disproportionation of SB to sulfate and HS produces sulfate that is enriched in 34S and 18O by f 18xand 17xrelative to Sj and water, respectively (Bo¨ttcher et al., 2001). This fractionation could explain the increase in d34SSO4 and d18OSO4 values from depths of 21.5 to 23 m. These depths also correspond to the suboxic zone where sulfur disproportionation reactions are generally favored due to the
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presence of sufficient oxidizing agents (e.g., iron and manganese oxides) capable of oxidizing HS to sulfur intermediates (Canfield and Thamdrup, 1994). Therefore, d34SSO4 and d18OSO4 values might reflect different sulfur reactions across the redox interface of anoxic basins, although a more thorough analysis at Framvaren is needed to confirm this. 4.2. Deep anoxic waters At depths z 40 m, it appears that sulfate reduction exerts the primary influence on the sulfur and oxygen isotope composition of sulfate (Table 1; Figs. 1 and 4). What is most striking from the combined data sets of this study and those of Anderson et al. (1988) is the consistency in the d34S values of sulfide and sulfate measured in 1982 and 1993 and the contrasting lower values of each measured in 1983 (Fig. 2). Furthermore, estimates of es of 46.1xand 41.5xfor sulfate reduction using the 1982 and 1993 data sets, respectively, are also in closer agreement than the estimate of 17.3xderived from the data collected in 1983 (Fig. 4). The estimated value of es in 1993 is also in good agreement with the observed DH2S – SO4 value of 41.2xmeasured at 22 m in 1993. This DH2S – SO4 value, because it is shallow, represents the instantaneous isotope effect of sulfate reduction rather than the integrated record at depth. This consistency between the two independent estimates when using the 1993 data, however, suggests that the biogeochemical controls of sulfate reduction throughout the anoxic waters of Framvaren have been relatively consistent over time. Slower rates of sulfate reduction can sometimes lead to higher values of es similar to what we have estimated here for Framvaren (Goldhaber and Kaplan, 1975; Kaplan and Rittenberg, 1964). In particular, when organic substrates become limiting to sulfate reduction, this can slow rates of reduction and result in high values of es (Canfield, 2001). However, slower rates of reduction are not necessarily always associated with larger values of es, as recent evidence has indicated (Bolliger et al., 2001; Canfield, 2001; Detmers et al., 2001). The type of organic substrates utilized for sulfate reduction can also affect es. Substrates such as acetate, which can be completely oxidized to CO2 but which provide lower reducing power for sulfate reduction (i.e., less negative DGj value), generally results in higher values of
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es (Detmers et al., 2001). In contrast, substrates such as lactate, which are incompletely oxidized but provide greater reducing power, generally yielded lower values of es (Detmers et al., 2001). Based on the 1982 and 1993 data, the large value of es estimated for sulfate reduction in Framvaren is consistent with lower rates of sulfate reduction resulting from limiting amounts of organic substrates, or they may be the result of organic substrates such as acetate that have lower reducing power to fuel sulfate reduction. An explanation is still required to explain the anomalous low d34SSO4 and d34SSH2S values and small es estimated for sulfate reduction based on the 1983 data of Anderson et al. (1988). Anderson et al. (1988) originally proposed that the low d34S values of sulfate (from + 14.8x to + 18x) measured from depths of 8 to 50 m in 1983 may have resulted from sulfide oxidation due to a major flushing event whereby oxygenated seawater from outside of the fjord spilled over the sill at the entrance to Framvaren and sulfides with a low d34S value were subsequently oxidized. Such a flushing event would also bring in fresh organic material and other nutrients which might also eventually stimulate faster rates of sulfate reduction in the bottom waters after oxygen was consumed during respiration. The lower es estimated using the data of 1983 is consistent with this (Fig. 4). Flushing events in Framvaren have been reported elsewhere, although evidence indicates that they are generally limited to the shallow and intermediate waters and do not penetrate to depths greater than 100 m (Dyrssen et al., 1996; Stigebrandt and Molvaer, 1988). Therefore, for waters sampled near 150 m, it is still difficult to reconcile the shift in d34S values of sulfate from f + 45xin 1982 to f + 30xin 1983 and back to + 42xby 1993 (Fig. 2; Anderson et al., 1988). It is unlikely that the proposed effects of sulfide oxidation at 10– 50 m depth in 1983 could have also lowered the d34SSO4 values in the bottom waters by 10x. To accomplish this, the amount of 34 S-depleted sulfate produced from sulfide oxidation required to lower the d34SSO4 values in the deep water by this amount can be calculated for X by the isotopic mass balance equation below: ðX Þðd34 Soxid:;SO4 Þ þ ð1 X Þðd34 S1982;SO4 Þ ¼ d34 S1983;SO4
d34Soxid.,SO4, d34S1982,SO4, and d34S1983,SO4 correspond to the isotopic signatures of sulfate produced from oxidation, ‘‘background’’ sulfate in the deep waters in 1982, and sulfate in the deep waters in 1983, respectively. This calculation assumes no isotopic fractionation during sulfide oxidation as previous studies have indicated (Fry et al., 1986, 1984; Ku et al., 1999; Schoen and Rye, 1970). Using d34S values of 20x and 3xfor sulfate formed from oxidation, which correspond to the range of d34SSH2S values measured at the interface and deep waters, respectively, we obtain estimates for X of 23% and 31%, respectively. Therefore, sulfate concentrations in the deep waters of Framvaren would have had to increase from 10 to 12.3 – 13.1 mM between 1982 and 1983 to account for the apparent shift in d34SSO4 values. The data of Anderson et al. (1988) in fact indicate that sulfate concentrations at depths z 130 m in Framvaren varied only between 9.55 and 10.04 mM for 1982 and 1983, and therefore do not indicate significant effects of sulfide oxidation. Because evidence presented earlier suggested that sulfate reduction rates (based on observed values of es) appear to have been relatively consistent throughout the water column (Table 1; Fig. 4), it is also difficult to explain a large shift to lower d34SSO4 values as a result of changes in sulfate reduction rates within the deep waters. If a flushing event did occur at some point between the sampling times of 1982 and 1983, it appears from the d34S measurements that the biogeochemical conditions were completely reestablished by the time the fjord was resampled by us in 1993 (Fig. 2). The low and enigmatic d34S values measured in 1983 have important implications regarding the mechanism of iron sulfide formation and the overall sulfur cycle within the water column and sediments of Framvaren as previously discussed by Saelen et al. (1993). Saelen et al. (1993) interpretation of the mechanisms of iron sulfide formation in the sediments of Framvaren was based on a comparison of the d34S values they measured for total reduced sulfur in the sediments (d34STRS), which is dominated by ‘‘FeS’’ and FeS2, with the d34SSH2S values measured in the water column in 1983 by Anderson et al. (1988). These authors propose different scenarios for iron sulfide formation in shallow ( f 25 m), intermediate ( f 100 m), and deep waters ( f 175 m) to explain
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the overall shift toward higher d34SSH2S values with depth and the lower d34STRS values they measured in the sediments when compared by depth to the d34SSH2S values measured in 1983 in the water column (Fig. 2). For the shallow depths, they reasoned that the d34SSH2S values of 19.6xmeasured in the water column by Anderson et al. (1988) may be atypically high and that the average d34STRS value of f 30xthey measured for the sediments may in fact directly reflect the average d34S value of sulfide produced in the water column at that depth. In order to explain a d34S value of reduced sulfur in the intermediate and deep sediments that is lower or similar, respectively, to the d34SSH2S in the water column, Saelen et al. (1993) suggested that the reduced sulfur in the sediments must be a mixture of sulfides formed in the shallow waters (with lower d34S values) with those formed either at intermediate or deep depths (having higher d34S values). They speculated that this may result from iron monosulfides formed in the shallow waters settling to depths where they can react with free sulfide or Sj from intermediate or deeper depths and form FeS2. Therefore, all of the scenarios presented by Saelen et al. (1993) propose that the sedimentary reduced sulfur at all depths is derived from sulfide produced within the water column and does not include in situ production of reduced sulfur within the sediments. Our 1993 measurements of d34SSH2S do not refute the general interpretations of Saelen et al. (1993); however, they do permit additional scenarios that may explain the overall trends observed for d34S of sulfides in the sediments and water column. Our suggestions are based on the 1982 data of Anderson et al. (1988) and the 1993 data presented here. We briefly discuss these scenarios below. What is most apparent from Fig. 2 is that, for a given depth, the d34STRS values in the sediments appears to be consistently lower than d34SH2S measured from the water column, both at the shallow depths just beneath the oxic – anoxic interface and at the deepest depths. This suggests that sulfate reduction has occurred throughout the entire basin and would also explain the parallel trend of increasing d34SSO4 with depth (Fig. 2). Although the lower d34STRS values in the intermediate and deep sediments may result in part from a mixture of sulfide produced at depth with iron sulfides produced in the water
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column at shallower depths (with lower d34S values) and which have subsequently settled to deeper depths, this does not adequately explain the lower d34STRS values of the shallow sediments relative to reduced sulfur in the water column. Furthermore, sulfides collected from a sediment trap at 175 m depth in the water column had a d34S value that was 2.3xheavier than the d34STRS for sediments at this same depth (Saelen et al., 1993). Although this difference is small, these results are nonetheless consistent with our theory that ‘‘isotopically light’’ sulfide is produced in the sediments. However, the relatively similar d34S values could also result if the sediment trap particles were partly derived from sediment resuspension, but might also suggest that most of the sedimentary sulfides are derived from the water column. We provide an alternative interpretation that the general trend of consistently lighter d34STRS values of the sediments may result from sulfide production within the sediments that has a lighter d34S value than that produced in the water column. This proposed mechanism invokes a different rate of sulfate reduction or different mechanism of sulfide production (i.e., sulfur disproportionation) occurring within the sediments versus the water column. Naes et al. (1988) report that sulfate reduction does occur in the deep sediments of Framvaren. This conclusion was based on a single pore water measurement from the deep sediments that indicated elevated alkalinity and sulfide concentration relative to the deep bottom waters. This observation, along with lower d34STRS values measured for the sediments, suggests that sulfate reduction rates in the sediments may be different than that in the water column. Slower cell-specific rates of reduction often result in larger values of es and consequently lower d34SSH2S (Canfield, 2001; Goldhaber and Kaplan, 1975; Kaplan and Rittenberg, 1964). According to the steady-state model of Rees (1973), faster rates lead to less back reaction at each individual step of sulfate reduction and therefore kinetic isotope effects at some steps are not fully expressed. This will consequently diminish the overall fractionation of sulfur isotopes during sulfate reduction. However, more recent evidence indicates that es is not necessarily related to rates of sulfate reduction, nor to temperature or bacterial phylogeny (Bolliger et al., 2001; Canfield, 2001; Detmers et al., 2001). Nonetheless, different rates of sulfate reduction
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(higher or lower), or different biogeochemical conditions within the sediments of Framvaren relative to the water column, could result in the relatively lower d34STRS values of the sediments (Fig. 2). To preserve a sedimentary d34STRS value distinct from that in the overlying water column, however, requires sufficient iron in the sediments to trap the sulfide produced there. Iron concentrations of f 3.5 – 4.0% have been measured in the top 46 cm of sediments collected at a water depth of 184 m in the F-1 basin of Framvaren (J. Skei, unpublished results). Furthermore, 25– 95% (median value f 75%) of the total iron in surface sediments (0 –4 cm) of Framvaren collected at 45 and 175 – 185 m depths is highly reactive, which includes dithionite-extractable Fe (iron oxides and ‘‘FeS’’) and pyrite (Raiswell and Canfield, 1998). If there is sufficient dithioniteextractable Fe in the sediments, this could then preserve a distinct sedimentary d34 S signature. Because dithionite-extractable Fe was not reported separately from the pyrite (Raiswell and Canfield, 1998), it is not currently possible to assess whether sufficient Fe is available in Framvaren sediments to preserve a sedimentary d34S signature. Degree of pyritization (DOP) and ‘‘potential DOP’’ values of 0.2– 0.8 and 0.7– 1.0, respectively, have been reported for these same sediments of Framvaren (Raiswell and Canfield, 1998). However, these measurements were not made below 4 cm sediment depth. Therefore, the DOP values reported for Framvaren sediments also do not provide sufficient evidence to support or refute our theory that diagenetic pyrite formation records the d34S signal of interstitial sulfate reduction occurring in the deep sediments of Framvaren. We are unaware of any sulfate reduction rate measurements having been made in either the water column or sediments of Framvaren that could also test this hypothesis. Based on observed changes in the concentrations of particulate organic matter (POM) collected from sediment traps, Naes et al. (1988) reported that little remineralization of POM occurs in the water column of Framvaren. This would seemingly contradict our suggestion that substantial rates of sulfate reduction occur in the water column of Framvaren where it should result in the mineralization of POM. Naes et al. (1988) indicate that when they sampled at 2-month intervals, from March 15 through November 29, 1983, there was a significant drop in POM from f 70 mg
m 2 day 1 collected in the 40- and 80-m traps relative to f 50 mg m 2 day 1 collected in the 120- and 160m traps. This evidence suggests mineralization of POM between 80 and 120 m and is consistent with the depth range where large increases in alkalinity have been attributed to the activities of sulfate-reducing bacteria (Yao and Millero, 1995). However, during the final 5-month sampling period from November 29, 1983, to May 3, 1984, Naes et al. (1988) reported a steady increase in the amount of POM collected in sediment traps from 40 to 160 m. When the results of this longer sampling period were averaged with the results from the earlier periods, there was no apparent net annual flux of POM throughout the water column and consequently no apparent mineralization of POM (Naes et al., 1988). However, if activities of sulfatereducing bacteria are in fact highest at depths of 80– 120 m, as the alkalinity data of Yao and Millero (1995) suggests, the combined effects of a prolonged sampling period and the absence of any preservative used in the sediment traps might have permitted sulfate-reducing bacteria to decompose the POM collected in the 40- and 80-m traps. Therefore, we suggest that the final sampling period of Naes et al. (1988) may have been anomalous, and consequently, their sediment trap data may in fact support our suggestion that sulfate reduction occurs to a measurable extent within the water column of Framvaren. This could in turn produce sulfide within the water column that has a unique d34S value distinct from that produced in the sediments. Another possible explanation for the low d34S values of reduced sulfur in the sediments is the disproportionation of Sj or other intermediate sulfur compounds (e.g., S2O3, SO3). The bacterial disproportionation of Sj results in sulfide that is enriched in 32 S by 7.3 –8.6x relative to Sj and sulfate that is enriched in 34 S by 12.6 – 15.3x(Canfield and Thamdrup, 1994). This mechanism requires the formation of Sj or other sulfur intermediate. In general, isotopic fractionation associated with the formation of elemental sulfur during bacterial and abiotic oxidation of HS or FeS is small (Kaplan and Rittenberg, 1964; Nakai and Jensen, 1964; Schoen and Rye, 1970), although enrichments in 32S in the Sj product can sometimes be as large as f 5– 6x(Fry et al., 1988; Kaplan and Rittenberg, 1964). If we assume that any Sj that may be present in the water column is formed
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by oxidation of HS and has a similar d34S value as the total reduced sulfur, the observed difference of 9x between d34STRS in the shallow sediments versus d34SSH2S in the water column is consistent with the formation of 34S-depleted sulfide from sulfur disproportionation within the sediments. The formation of Sj during abiotic oxidation of HS is likely to occur in the shallow waters of Framvaren near the chemocline where there is sufficient oxidizing agents such as NO3, Fe(III), or Mn(IV). It is also possible that disproportionation occurs in the intermediate waters during flushing events that carry in dissolved oxygen (Dyrssen et al., 1996). However, it is still questionable whether an alternative oxidant such as reactive iron oxides in the deep waters could generate Sj, because only iron sulfides were detected below 25 m depth at Framvaren (Cutter and Kluckhohn, 1999; Landing and Westerlund, 1988; Skei, 1988; Skei et al., 1996). Furthermore, as will be discussed later, the d34SSO4 and d34OSO4 values in deep waters of Framvaren do not indicate disproportionation at depths z 40 m. Therefore, the lower d34STRS values of the deepest sediments relative to SH2S in the water column at corresponding depths likely results from a mixture of sulfide derived from shallow ( f 20 m) and deep ( z 150 m) waters, as proposed by Saelen et al. (1993), or as we suggest, by different rates of sulfate reduction occurring within the sediments versus the water column. 4.3. Comparisons with the Black sea Recently, Dyrssen (1999) compared the chemistries of the Black Sea and Framvaren fjord. With respect to sulfur, Dyrssen (1999) interpreted the particularly high sulfide concentrations of 8 mM in the bottom waters of Framvaren, compared with concentrations of f 0.35 mM in the bottom waters of the Black Sea, to result primarily from differences in the surface area to volume ratios of 13.4 and 0.78 km 1 for Framvaren and the Black Sea, respectively. Volume-based rates of sulfate reduction in the water column of the Black Sea are several thousand times lower than rates in the sediments (Albert et al., 1995). This presumably results from relatively less terrestrial input and production of organic matter in the Black Sea water column which becomes more diluted, relative to a smaller basin like Framvaren, with a
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much larger water column. Concentrations of particulate organic carbon and nitrogen are approximately one tenth that in Framvaren (Cutter and Kluckhohn, 1999). In earlier studies, slower rates of sulfate reduction occurring in the water column relative to the sediments of the Black Sea had been suggested to explain the overall higher d34SSH2S values in the sediments and bottom waters relative to that in most of the water column (Sweeney and Kaplan, 1980; Vinogradov et al., 1962). However, as will be discussed below, these earlier studies failed to distinguish the causes for the different d34SSH2S values between the microlaminated Unit I sediments and the muddy turbidites of the Black Sea abyssal plain (Lyons, 1997). As previously mentioned, based on measured changes in alkalinity and sulfide concentrations, the depth range where the majority of sulfate reduction appears to occur in the water column of Framvaren is 60– 100 m beneath the oxic – anoxic interface (Yao and Millero, 1995). Consistent with this, rates of sulfate reduction in the water column of the Black Sea were highest 50 – 70 m beneath the depth at which sulfide first appeared (Albert et al., 1995; Fry et al., 1991; Jorgensen et al., 1991). This depth also corresponded with an enrichment in d34SSH2S that may have been the result of faster rates of sulfate reduction or to sulfide oxidation by O2 or MnO2 (Fry et al., 1991). The mean d34S value of 38.6xfor HS just beneath the chemocline depth of the Black Sea (f100 m) is approximately 2xheavier than HS in the deeper anoxic bottom waters and more closely matches d34S values of particulate reduced sulfur collected from mid-water sediment traps and total reduced sulfur in microlaminated surface (0 –26 cm) sediments of Unit I in the deepest off-shore locations of the basin (Calvert et al., 1996; Fry et al., 1991; Lyons, 1997; Muramoto et al., 1991; Sweeney and Kaplan, 1980). This similarity in d34STRS values in the sediments with sulfide just beneath the chemocline and that collected in sediment traps has led several investigators to conclude that sedimentary pyrite in the deep microlaminated sediments of the Black sea forms within the water column (i.e., syngenetically) just below the chemocline (Calvert et al., 1996; Lyons, 1997; Muramoto et al., 1991). Consequently, once the pyrite forms in the water column, it settles
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f 2100 m to the bottom with relatively little change in its sulfur isotope composition. Analysis of size distributions of sedimentary pyritic framboids also indicates that pyrite in the more recent and uppermost sediments have an origin within the water column (Wilkin et al., 1997). Furthermore, there appears to be little additional pyrite formation in these offshore laminated sediments (i.e., relatively minor diagenetic pyrite) as evidenced by little change in either the DOP or d34STRS values throughout the top 26 cm (Lyons, 1997; Lyons and Berner, 1992). In contrast to the deep offshore laminated sediments of the Black Sea, acid volatile sulfur (AVS) and pyritic sulfur in near-shore sediments collected at a depth of 198 m had higher d34S values of f 25x and f 27.6x , respectively, relative to sulfide in the water column (Lyons, 1997). In addition, the d34S values of pyrite and AVS showed a small but steady increase with sediment depth, evidence for pyrite formation within the sediments as a result of interstitial sulfate reduction (Lyons, 1997). We propose that these shallower sediments of the Black Sea mimic conditions in sediments of Framvaren where interstitial sulfate reduction also occurs. Considering basic differences in surface area to volume ratios between the Black Sea and Framvaren (Dyrssen, 1999), it seems reasonable to predict that the deepest and most offshore sediments of Framvaren could still experience conditions similar to the near-shore sediments of the Black Sea sampled at 198m depth. However, in contrast to the shallow sediments of the Black Sea, at all depths of Framvaren, the d34STRS values are consistently lower in the sediments relative to d34SSH2S in the water column (Fig. 2). Nonetheless, considering recent evidence that suggests sulfate reduction rates cannot always be correlated with d34SSH2S values (Canfield, 2001; Detmers et al., 2001), the lower d34STRS values in Framvaren sediments could still reflect different rates of sulfate reduction occurring in the sediments relative to the water column, as suggested for the shallow Black Sea sediments (Lyons, 1997). 4.4. Biogeochemical controls of d34SSO4 and d18OSO4 values Early field and laboratory studies with enrichment cultures of marine sulfate-reducing bacteria revealed
that the enrichment factor for sulfur in sulfate, es, was approximately four times that of the enrichment factor for oxygen in sulfate, eo (Mizutani and Rafter, 1969; Rafter and Mizutani, 1967). Consequently, when the d34S was plotted relative to the d18O value of the sulfate, this yielded a slope of f 4. However, similar experiments by these authors subsequently revealed that differences in the d18O value of water used in the microbiological media resulted in changes in the measured value of eo, which generally resulted in a slope less than 4 when the d34S was plotted relative to the d18O value (Mizutani and Rafter, 1973). It was suggested by these authors that this effect resulted from isotopic exchange between sulfate and water via sulfite or an unknown metabolic intermediate of the sulfate reduction pathway. Fritz et al. (1989) conducted experiments similar to Mizutani and Rafter (1973) with freshwater lake sediments amended with a pure culture of Desulfovibrio desulfuricans to initiate sulfate reduction. These authors observed that with increased reduction, the d18O values of the residual sulfate trended towards d18O values predicted for equilibrium oxygen isotope exchange between sulfate and water at the respective temperatures the experiments were conducted. They further speculated that there was rapid equilibrium isotope exchange, which is typically very slow for sulfate and water at earth surface temperatures (Lloyd, 1968), which resulted from a SO42 enzyme complex rather than a sulfite intermediate. Based on these earlier studies discussed above, it has been proposed, and a model presented, that the 4:1 ratio of es to eo that sometimes occurs during sulfate reduction may reflect the 1:4 stoichiometric ratio of sulfur to oxygen atoms in the sulfate molecule (Grinenko and Ustinov, 1990). According to this model, the 4:1 ratio of es to eo could result from purely kinetic effects controlled by the bacterial reduction pathway when rates are sufficiently fast to not permit oxygen isotopic exchange between water and an intermediate (e.g., SO32 or a SO42 enzyme complex) of sulfate reduction. Under these conditions, a slope of f 4 will result when d34SSO4 is plotted relative to the d18OSO4 value. However, at slower rates of sulfate reduction, varying degrees of oxygen isotopic exchange can occur between intermediates of sulfate reduction and water, which will subsequently affect the final d18OSO4 value of the residual sulfate and generally
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result in a slope less than 4 when d34SSO4 is plotted relative to the d18OSO4 value. Therefore, the effects of oxygen isotopic exchange with water can complicate interpretations of measured d34SSO4 versus d18OSO4 values derived from anoxic environments. Additional complexities in interpreting d34SSO4 and d18OSO4 values in anoxic environments can result from reoxidation of sulfide or from sulfur disproportionation. Although sulfate produced from bacterial Sj disproportionation is enriched in 18O by f 17xrelative to water, for most marine environments, this will decrease the slope when d34SSO4 is plotted relative to d18OSO4 (Bo¨ttcher et al., 2001). Reoxidation of sulfide in pore waters of anoxic marine carbonate sediments also had a similar effect on this slope (Ku et al., 1999). 4.5. d34S versus d18O values of sulfate in anoxic marine systems Few studies of anoxic marine systems have measured both the d34SSO4 and d18OSO4 values in either interstitial pore waters (Aharon and Fu, 2000; Bo¨ttcher et al., 1999; Bottrell et al., 2000; Ku et al., 1999; Zak et al., 1980) or in the water column (Jeffries et al., 1984). In all of these studies except one (Ku et al., 1999), an increase in both d34SSO4 and d18OSO4 was measured when sulfate concentrations became depleted, and in most cases when d34SSO4 was plotted versus d18OSO 4, a slope of < 3 was measured. Recently, Aharon and Fu (2000) measured d34SSO4 and d18OSO4 collected from pore waters in sediments of oil and gas seeps of the Gulf of Mexico. Relative to non-seep (‘‘reference’’) sediments at the same location, seep sediments had much higher rates of sulfate reduction, as estimated from pore water sulfate profiles. Aharon and Fu (2000) also observed that the fractionation effects for oxygen and sulfur in sulfate were lower when the rates of reduction were highest. For instance, for gas seep, oil seep, and reference sediments, sulfate reduction rates were 2.000, 0.090, and 0.004 Amol SO42 cm 3 day 1, respectively, whereas the corresponding values of es were estimated to be 8.6x, 18.0x, and 27.2x. When d34SSO4 was plotted relative to d18OSO4 from each of these environments, they observed slopes of 3.5, 2.8, and 1.4, respectively (r2>0.9 for each). The authors concluded from these observations that the
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d34S versus d18O ratio of sulfate might be largely controlled by the rates of dissimilatory sulfate reduction, in agreement with Grinenko and Ustinov’s (1990) model. Aharon and Fu (2000) hypothesized that when sulfate reduction rates are highest and fractionation effects small, such as at the gas seeps, kinetic isotope effects, rather than oxygen isotopic exchange with water, are largely responsible for the d34SSO4 and d18OSO4 values. Under these conditions, a plot of d34SSO4 versus d18OSO4 will yield a slope closer to 4. Conversely, Aharon and Fu (2000) speculated that during slow rates of reduction, more oxygen isotope exchange between a sulfate intermediate and water will occur and thus lower this slope. 4.6. d34S versus d18O values of sulfate in the anoxic bottom waters of Framvaren The hypotheses of Aharon and Fu (2000) regarding the kinetic controls of d18OSO4 values during dissimilatory sulfate reduction are insightful; however, they do not completely explain our observations of the deep anoxic waters of Framvaren. Here, we measured a relatively large value of es for sulfate reduction of 41.5xand still observe a slope close to 4 for d34SSO4 versus d18OSO4 (Fig. 5). Based on the results of Aharon and Fu (2000) and other studies (Canfield, 2001; Goldhaber and Kaplan, 1975; Kaplan and Rittenberg, 1964), this large value of es could suggest a slow rate of sulfate reduction. According to Aharon and Fu’s hypothesis, a slow rate would not yield a slope close to 4 as we observe (Fig. 5). However, as previously discussed, the relative availability and type of organic substrates also have important effects on es for sulfate reduction, and es may not always be correlated with sulfate reduction rates (Canfield, 2001; Detmers et al., 2001). As mentioned earlier, we know of no reports of measured rates of sulfate reduction within the sediments or water column of Framvaren fjord. It is possible that the generalizations made by Aharon and Fu (2000) regarding sulfate reduction rates and associated isotope effects may only apply for a given environment where all other parameters (depth, temperature, type of organic matter, water column versus sedimentary environments) are essentially the same. Therefore, we hypothesize that under conditions where dissimilatory sulfate reduction is
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more unidirectional, which would include faster rates, there will be relatively less back reaction at each biochemical step of reduction and consequently less opportunity for oxygen isotopic exchange between reaction intermediates and water. Consequently, during these conditions, a plot of d34SSO4 versus d18OSO4 could have a slope near 4.0. However, unidirectionality of a biochemical reaction is not necessarily restricted to conditions of fast rates. Detmers et al. (2001) suggest that sulfate reduction will be more unidirectional when it is coupled to oxidation of organic substrates that yield a more negative DGj value. These substrates were observed to generally produce a lower value of es for sulfate reduction (Detmers et al., 2001). Low temperatures generally decrease rates of sulfate reduction. However, Canfield (2001) observed smaller values of es for sulfate reduction at lower temperatures. Canfield (2001) proposes that the first step of sulfate reduction, the entry of sulfate into the cell, might become more unidirectional at low temperatures and thus explain this lower value of es. In fact, the relative degree of concurrent forward and back reactions during biochemical reactions represents a major means of regulatory control (Stryer, 1995). The concurrent small changes in the rates of the forward or backward reaction can generate rapid changes in the net forward reaction rate. This is best explained with examples (see below). We simplify our examples by considering only one of the first steps in sulfate reduction, the binding of sulfate to the sulfate reductase enzyme. However, we could have considered any step in the pathway that involves reaction of the oxygen in sulfate
Example A 15 (forward reaction) SO4 X SO4 – enzyme 10 (back reaction) Net reaction: 5
Example B 20 (forward) SO4 X SO4 – enzyme 10 (back) Net reaction: 10
Example C 10 (forward) SO4 X SO4 – enzyme 5 (back) Net reaction: 5
In examples A and B shown, the numbers correspond to arbitrary rates of the forward and reverse reaction. As seen by comparing example A with B, a 33% increase in the gross forward reaction can result in a 100% increase in the net rate of a reaction. Similar changes can also be elicited by lowering the
rate of the back reaction or changing the relative rates of both the forward and back reactions. In example C, the forward and back reactions are each halved with respect to example B, which results in a 50% reduction in the net reaction rate. Although the net rates of sulfate reduction in B and C are clearly different, the relative balance between the forward and back reactions is the same. We hypothesize that these two conditions might result in similar kinetic isotope effects for oxygen and sulfur being preserved in the residual sulfate and may therefore result in a similar slope when d34SSO4 is plotted relative to d18OSO4 during sulfate reduction. Different values of es and eo could still be expressed from shifts in the rate limiting steps of sulfate reduction. Environmental parameters specific to a given site could presumably influence the relative balance of the forward and back reactions of sulfate reduction, the rate limiting steps, and consequently the d18OSO4 and d34SSO4 values. Evidence to support the above hypothesis comes from a recent study by Mandernack et al. (2000b). They observed that the microbial reduction of gaseous N2O to N2 during a soil incubation resulted in a slope of f 0.5 when the d15N value of the residual N2O was plotted relative to the d18O. In this case, the oxygen isotope effect was twice that of the nitrogen and presumably reflects the 1:2 atom ratio of oxygen to nitrogen in the N2O molecule. The reduction of N2O to N2 is a type of anaerobic respiration that is analogous to sulfate reduction, although the reactants and products are gaseous and therefore there is less opportunity for oxygen isotope exchange with water. It appears that N2O reduction is a unidirectional process, perhaps due in part to the chemical stability of the N2 product, which may minimize back reactions from occurring and subsequent oxygen isotopic exchange between the N2O (or N2O – enzyme complex) and water. We hypothesize that a similar phenomena occurs during dissimilatory sulfate reduction when it occurs unidirectionally, including conditions that favor fast rates of sulfate reduction. During these conditions, sulfate reduction will yield a slope near 4.0 when d34SSO4 is plotted relative to d18OSO4, as we observed for the deep anoxic water of Framvaren. If our above hypothesis is correct, it would imply that processes such as Sj disproportionation or reoxidation of sulfide, which would both decrease the slope of d34SSO4 versus d18OSO4 to values < 4
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(Bo¨ttcher et al., 2001; Ku et al., 1999), were not significant within the deep anoxic waters of Framvaren. Therefore, d34SSO4 and d18OSO4 values of sulfate deposits precipitated from euxinic environments and preserved in the geological record might similarly reflect a system where sulfate reduction was a dominant and unidirectional process (m = f 4.0), or where reoxidation of sulfide, sulfur disproportionation, and/ or oxygen isotope exchange reactions with water during (non-unidirectional) sulfate reduction also occurred (m < 4.0).
5. Conclusions Variations in the d34SSO4 and d18OSO4 values are relatively small across the oxic – anoxic interface of Framvaren fjord, although a distinct minimum in d34SSO4 was observed at 20 m depth, consistent with sulfide oxidation, and small enrichments in d34SSO4 and d18OSO4 3 m beneath this depth are consistent with possible sulfur disproportionation. At water depths >24 m, the d34SSO4 and d18OSO4 values steadily increased with depth in response to dissimilatory sulfate reduction. Estimates for es and eo of 41.5xand 9.8x, respectively, for sulfate reduction were obtained from Rayleigh plots. The value for es closely approximates the observed difference between the d34SSO4 and d34SSH2S values near the oxic –anoxic interface. Therefore, a closed system model appears to provide a good approximation of sulfate behavior in the deeper anoxic waters of Framvaren. Consequently, for the deep waters of Framvaren, it is difficult to reconcile our 1993 d34SSO4 data and the 1982 d34SSO4 data of Anderson et al. (1988) with the 1983 d34SSO4 measurements of Anderson et al. (1988). The 1983 d34SSO4 measurements are approximately 10xdepleted relative to both the 1982 and 1993 data. Oxidation of sulfide in the deep bottom waters between 1982 and 1983 does not adequately explain this 10xdepletion. From our measurements made in 1993, a plot of d34SSO4 versus d18OSO4 from water depths >24 m provided a linear relationship with a slope of f 4.4. We hypothesize that this slope results from kinetic isotope effects associated with sulfate reduction, which proceeds unidirectionally in the deeper anoxic waters of Framvaren, and approximates the 4:1 ratio
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of oxygen to sulfur in the residual sulfate. Plots of d34SSO4 versus d18OSO4 from ancient euxinic deposits might provide similar information regarding the biogeochemical controls of sulfur cycling in the geological past. For comparable water depths, the d34STRS of the sediments in Framvaren are consistently lower by f9xthan the d34SSH2S of the water column. As originally proposed by Saelen et al. (1993), the low d34STRS values for the deep sediments could be derived from a mixture of sulfide derived from shallow and deep waters with lower and higher d34SSH2S values, respectively. However, this does not adequately explain the lighter d34STRS values in the shallow sediments relative to d34SSH2S in the water column. Sulfur disproportionation reactions, which can produce sulfide that is very depleted in 34S, in the shallower sediments just beneath the chemocline might provide an alternative explanation, although these reactions are not likely to occur in the deeper sediments of Framvaren. Additionally, we hypothesize that different rates of sulfate reduction, both interstitially in the sediments and within the water column, may explain the consistent depth-dependent offset between sedimentary d34STRS and water column d34SSH2S values. Acknowledgements We thank Drs. Wayne, C. (Pat) Shanks and Vladimir Grinenko for their insightful comments regarding this manuscript; for resources provided by Dr. Mark Morgan, and Maria Mihailescu, Jesusa Overend-Pontoy, and Nenita Lozano for stable isotopic analyses. The authors are also grateful for the helpful comments of Dr. Robert Raiswell, Dr. Timothy Lyons, and an anonymous reviewer. [EO] References Adams, C.A., Warnes, G.M., Nicholas, D.J.D., 1971. A sulphitedependent nitrate reductase from Thiobacillus denitrificans. Biochim. Biophys. Acta 235, 398 – 405. Aharon, P., Fu, B., 2000. Microbial sulfate reduction rates and sulfur and oxygen isotope fractionations at oil and gas seeps in deepwater Gulf of Mexico. Geochim. Cosmochim. Acta 64, 233 – 246. Albert, D.B., Taylor, C., Martens, C.S., 1995. Sulfate reduction rates and low molecular weight fatty acid concentrations in
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A stable sulfur and oxygen isotopic investigation of sulfur cycling in an anoxic marine basin, Framvaren Fjord, Norway Kevin W. Mandernack a,*, H. Roy Krouse b, Jens M. Skei c a
Department of Chemistry and Geochemistry, Colorado School of Mines, Golden, CO 80401, USA b Department of Physics and Astronomy, University of Calgary, Calgary, AB Canada T2N-1N4 c Norwegian Institute for Water Research, P.O. Box 173 Kjelsas, N-0411 Oslo, Norway Received 28 December 2000; accepted 22 March 2002
Abstract In 1993 we measured the d34S values of total dissolved sulfide (d34SSH2S) and sulfate (d34SSO4) and the d18O of sulfate (d18OSO4) from water samples collected across the oxic – anoxic interface and in the deep permanently anoxic waters of the stratified Framvaren fjord in southern Norway. Near the chemocline, variations in the d34SSO4 and d18OSO4 values were generally less than 1x from ambient seawater values. However, a minimum d34SSO4 value of + 19.7x was detected at 20 m depth, which coincided with the depth that sulfide first appeared and may reflect sulfide oxidation. Small increases in d34SSO4 and d18OSO4 values 3 m below this depth are consistent with a zone of sulfur disproportionation. The d34SSH2S value near the interface at 22 m was 19.8x , which is 41.2x depleted in 34S relative to the sulfate collected at that depth. In close agreement with earlier measurements made at Framvaren in 1982, the d34SSO4 values collected from the deeper anoxic waters showed a marked 34S enrichment with depth, which corresponded with a decrease in the sulfate concentration. These results are interpreted to be the result of active dissimilatory sulfate reduction. A Rayleigh plot for the sulfate data measured in 1993 provides estimates for the sulfur and oxygen isotope enrichment factors (es and eo, respectively) for sulfate reduction of 41.5x and 9.8x , respectively, with the former value matching closely the observed difference in d34S between the dissolved sulfide and sulfate near the interface. Our results from 1993, however, contrast with d34SSO4 and d34SSH2S data in the water column made in 1983 by Anderson et al. [Mar. Chem. 23 (1988) 283). We conclude that the results of 1983 may be anomalous, and as a result this may offer additional interpretations than what was previously provided for the origin of reduced inorganic sulfur in the sediments of Framvaren based on their measured d34S values. We hypothesize that the lower d34Strs values in the sediments relative to d34SSH2S values in the water column could also result from different rates of sulfate reduction, or in shallower sediments just beneath the chemocline, also from disproportionation of SB, S2O 3 , or SO3 . We hypothesize that the observed ratio of 4.4:1 for the measured changes in d34SSO4 versus d18OSO4 within the anoxic waters approximates the 4:1 atom ratio of oxygen to sulfur in the residual sulfate as a result of dissimilatory sulfate reduction and reflects little oxygen isotope exchange between intermediates of sulfur metabolism and water either during bacterial sulfate reduction or from sulfide reoxidation processes. Based on comparisons with other studies, we further propose that this lack of isotopic exchange with water, and the subsequent f 4:1 ratio of d34SSO4 versus d18OSO4, occurs under conditions that promote a unidirectional
* Corresponding author. Tel.: +1-303-384-2224; fax: +1-303-273-3629. E-mail address: [email protected] (K.W. Mandernack). 0009-2541/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0009-2541(02)00394-7
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biochemical reaction for sulfate reduction during which kinetic isotope effects are fully expressed and are consequently reflected in the d34SSO4 and d18OSO4 values. D 2003 Elsevier Science B.V. All rights reserved. Keywords: Sulfide; Sulfate; Biogeochemistry; Stable isotopes; Anoxic; Sulfur cycling
1. Introduction Active sulfur transformations occur near oxic – anoxic interfaces in restricted marine environments such as the Black Sea and anoxic fjords such as Framvaren fjord and Saanich inlet (Jorgensen et al., 1991; Mandernack and Tebo, 1999; Millero, 1991; Sorokin, 1972). Anoxic basins and global oceanic anoxic events are important controls on the temporal variability of d34S values of seawater sulfate (Berner and Raiswell, 1983; Claypool et al., 1980), the global sulfur cycle (Berner, 1987; Kump, 1989), and localization of seafloor hydrothermal sulfide ore deposits of the sedimentary exhalative (SEDEX) class (Goodfellow and Jonasson, 1984; Shanks et al., 1987; Turner, 1992). Below oxic – anoxic interfaces, the decomposition of organic matter is primarily coupled to sulfate reduction, which results in the formation of hydrogen sulfide (HS). The rates of sulfate reduction in marine environments and the subsequent formation of HS are primarily controlled by both the quality and quantity of organic matter available from autochthonous or allochthonous sources (Berner, 1978; Goldhaber and Kaplan, 1975; Jorgensen, 1981; Jorgensen, 1982). Due to large kinetic isotope effects, the sulfide produced from dissimilatory sulfate reduction tends to be very depleted in 34S relative to the reactant sulfate (Goldhaber and Kaplan, 1975; Harrison and Thode, 1958; Kaplan and Rittenberg, 1964; Nakai and Jensen, 1964). Laboratory cultures of sulfate-reducing bacteria fractionate the sulfur isotopes (32S and 34S) of sulfate by 2 – 47xduring dissimilatory reduction (Bolliger et al., 2001; Detmers et al., 2001; Harrison and Thode, 1958; Kaplan and Rittenberg, 1964; Mizutani and Rafter, 1969), whereas field measurements sometimes suggest isotopic enrichment factors for sulfur (es) as large as 60 –70x(Goldhaber and Kaplan, 1975). In addition, fractionation of the oxygen isotopes of sulfate occurs during dissimilatory sulfate reduction, although with smaller and variable values of eo (Ku et al., 1999; Mizutani and Rafter,
1969). Variations in eo can result from kinetic effects due to variable rates of sulfate reduction and from isotopic exchange reactions between water and metabolic intermediates of sulfur reduction and oxidation processes (Aharon and Fu, 2000; Bo¨ttcher et al., 2001; Fritz et al., 1989; Ku et al., 1999; Mizutani and Rafter, 1973). The 34S-depleted HS produced by sulfate reduction below the redox interface can diffuse upward to the oxic or suboxic zone where it can be oxidized by chemoautotrophic bacteria utilizing O2, NO3, and possibly Fe/Mn oxides as electron acceptors (Adams et al., 1971; Aller and Rude, 1988; Brock and Gustafson, 1976; Fossing et al., 1995; Kelly, 1988; Luther et al., 1988; Millero, 1991; Sweerts et al., 1990; Timmer-ten Hoor, 1975, 1981). Diverse populations of sulfur oxidizing bacteria have been identified from near the chemocline of anoxic marine basins (Jannasch et al., 1991; Tuttle and Jannasch, 1973) where microbial oxidation has been measured (Jorgensen et al., 1991; Mandernack and Tebo, 1999; Sorokin, 1972). When sunlight is available, sulfide oxidation can also be mediated by anoxygenic photosynthetic sulfur bacteria (Cohen et al., 1977; Kuenen, 1975; Overmann et al., 1991; Sorensen, 1988). The oxidation of HS in anoxic basins can also proceed rapidly and abiotically with O2 or Fe and Mn oxides as electron acceptors (Luther et al., 1988; Millero, 1991; Sorokin, 1972) or, if light is present, via photooxidation reactions (Luther, 1995; Luther et al., 1988). Sulfide can also be indirectly oxidized from the production of O2 from oxygenic photosynthesis by cyanobacteria (Jorgensen, 1979). In general, sulfur isotope effects associated with the oxidation of sulfide are small in comparison to those from sulfate reduction (Fry et al., 1986). A sulfur isotope enrichment factor (es) of 5xhas been measured for abiotic oxidation of HS (Fry et al., 1988). A reverse isotope effect was measured for the oxidation of sulfide by an anaerobic photosynthetic purple sulfur bacterium where es= + 2x(Fry et
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al., 1984). Neither bacterial nor abiotic oxidation of solid phase metal sulfides produces a significant sulfur isotope effect (McCready and Krouse, 1982; Nakai and Jensen, 1964; Taylor et al., 1984). Consequently, the d34S of the sulfate produced from sulfide oxidation will generally reflect its parent substrates. The d18O value of the sulfate produced during sulfide oxidation will vary considerably due to differences in the relative percent of dissolved oxygen that becomes incorporated into sulfate as a result of chemical versus biological oxidation and differences in ev with respect to O2 (Lloyd, 1968; Taylor et al., 1984; Toran and Harris, 1989; Van Everdingen and Krouse, 1985). In general, it appears that both ev and the percent incorporation of dissolved O2 into sulfate are larger during biological versus abiotic oxidation (Lloyd, 1968; Taylor et al., 1984; Van Everdingen and Krouse, 1985). Analysis of the d34SSH2S, d34SSO4, and d18OSO4 values in aquatic systems can therefore help identify the microbial or abiotic processes involved in sulfur cycling as well as temporal and spatial changes in these processes. Previous reports of d18OSO4 values in modern marine or brackish systems are few (Aharon and Fu, 2000; Bo¨ttcher et al., 1999; Bottrell et al., 2000; Jeffries et al., 1984; Ku et al., 1999; Sheu et al., 1988; Zak et al., 1980). Framvaren fjord is a stratified anoxic marine basin in southern Norway. It has a distinct O2 – H2S interface (chemocline) at approximately 19 m depth, where some of the highest rates of sulfide removal have been reported for any marine system (Mandernack and Tebo, 1999; Millero, 1991; Yao and Millero, 1995). In addition, as a result of a rich assemblage of green and purple sulfur bacteria, as well as phytoplankton, very high rates of CO2 fixation and primary productivity also occur at the interface (Mandernack and Tebo, 1999; Sorensen, 1988). Framvaren represents an ideal environment to study biogeochemical processes associated with sulfur cycling at both the interface and in the deep anoxic water column. In this study, we analyzed d34SSH2S, d34SSO 4, and d18OSO4 values across the oxic – anoxic interface and in the permanently anoxic bottom water of Framvaren fjord. We choose Framvaren for this study because data acquired in 1982 and 1983 (Anderson et al., 1988) allow evaluation of the temporal variations in the stable isotopic values of sulfate and sulfide
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within the deep bottom waters of this fjord. The observed large changes between 1983 and 1993 could suggest ventilation of the deep anoxic waters with oxic waters from outside of the fjord that periodically spill over the sill at the entrance to Framvaren. However, it is difficult to reconcile d34SSO4 data collected in 1983 with d34SSO4 measurements made in 1982 and 1993. The results of our study assist in the interpretation of isotopic evidence preserved in ancient euxinic sulfur deposits within the geological record.
2. Methods Water samples above and near the interface were collected in June 1993 with a submersible pumping system (supplied and operated by B. McKee and J. Todd), whereas deeper samples from 40 m and below were collected with 10-l Go-Flo bottles. Dissolved oxygen concentration, as determined by Winkler titrations, at 18 m depth was 8.3 AM and nondetectable below this, whereas dissolved sulfide was first detected at 20 m (Yao and Millero, 1995). From each water sample collected, 100-ml subsamples were taken with Winkler bottles for stable isotopic analyses of sulfide and sulfate. The bottles were first purged with N2 and then quickly filled without any gas headspace. Prior to sealing the bottle, formaldehyde (2% final concentration) and zinc acetate (50 mg/10 ml) were added as a poison and sulfide trapping agent, respectively. Care was taken to fully sequester the dissolved sulfide as ZnS prior to decanting a small volume of the samples to allow space for freezing immediately on board the ship. The frozen water samples were allowed to thaw and subsequently filtered (0.2 AM Millipore) under an argon atmosphere back in the lab. The filtrate was then reserved for sulfate concentration measurements and a separate portion reserved for extraction of the sulfate for isotopic analyses. The volume of each sample filtered was measured in order to subsequently determine the total sulfide concentrations from the trapped HS (as ZnS) and any Sj and Fe sulfide present in the water column as described elsewhere (Mandernack et al., 2000a). These sulfur compounds were trapped on filters from 20 to 150 m depths and retained for stable isotopic and/or sulfide concentra-
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tion measurements using CrCl2 – HCl methods described previously (Fossing and Jorgensen, 1989; Mandernack et al., 2000a). The CrCl2 – HCl treatment yielded ZnS that was reprecipitated from all sources of reduced sulfur (HS, Sj, FeS2, and ‘‘FeS’’) and subsequently analyzed for d34S and concentrations by iodometric titration (see below). However, based on previous measurements of Millero (1991) and Yao and Millero (1995), HS represents the vast majority of reduced sulfur in our samples (Table 1), and therefore, this fraction will henceforth be referred to as SH2S. It was anticipated that there would be insufficient SH2S at the 20- and 21.5-m depths for isotopic measurements, and therefore, these were reserved only for sulfide concentration measurements. Zinc sulfides collected from the 22-, 23-, and 100-m samples were processed only for stable isotopic analyses, whereas splits were made from the remaining samples for both concentration and d34S measurements. Due to small sample sizes, the zinc sulfide samples prepared from the 22- to 24-m depths were analyzed d34S in March 1994 at the Marine Biological Laboratory in Woods Hole, MA, under the supervision of Dr. Brian Fry. In general, for similar depths there was good agreement in the sulfide concentrations measured with those of Yao and Millero (1995) during the same cruise (Table 1). Sulfate concentrations from the filtrates were determined using ion chromatography with a precision of
F 2%. In order to prepare and concentrate the sulfate from the filtrates for d34S and d18O analyses, 10– 20 ml of each filtrate was acidified at a ratio of 17 Al HCl/10 ml of sample (final pH f 2.5 – 3.0) and then diluted 1:20 with deionized water. Concentrated HCl was added to prevent the possibility of BaCO3 precipitation, which might interfere with the d18O measurements. The diluted filtrate was then passed at 1– 4 ml/min through ion exchange resin (Bio-Rad, AG1 – X8, 100 –200 mesh, chloride form) and eluted with 120 – 130 ml of 0.5 M NaCl using methods similar to those described elsewhere (Mandernack et al., 2000a; Stam et al., 1992; Van Stempvoort, 1989). Sulfate recovery by this method generally exceeded 95%. The sulfate was then precipitated as BaSO4 by addition of 10 ml of 10 wt.% BaCl2, washed five to six times with deionized water, and dried. As a final purification step, all of the BaSO4 powders were baked under an air atmosphere at 500 jC for 2 h. This treatment was previously shown to effectively remove any possible organic material and to not interfere with d18O measurements (Mandernack et al., 2000a). For mass spectrometric analysis, BaSO4 and ZnS precipitates were converted to SO2 by reaction with a 50:50 mixture of SiO2/V2O5 (1:20 ratio of BaSO4:mixture, 1:53 ratio for ZnS) under vacuum (Yanagisawa and Sakai, 1983) and analyzed on-line with a Micro-mass 602 double collecting isotope ratio mass spectrometer. The sulfur isotope data are pre-
Table 1 Sulfur concentrations and stable isotopic values in the water column of Framvaren Fjord, Norway Depth sampled (m)
d34SVCDT SH2S
d34SVCDT SO24
n
d18OVSMOW SO24
n
[SO4]a, mM
[H2S]b, AM
10 15 19 20 21.5 22 23 24 40 100 150
I.S. I.S. I.S. I.S. I.S. 19.8 18.6 19.2 13.4 3.1 4.4
20.1 20.0 20.7 F 0.2 19.7 21.6 F 0.4 21.4 21.9 21.3 F 0.3 22.8 F 0.1 37.8 F 0.05 42.2 F 0.02
1 1 3 1 2 1 1 3 2 3 2
10.4 F 0.4 N.D. 10.4 F 0.3 10.3 F 0.4 11.6 F 0.2 11.1 F 0.5 11.3 10.4 F 0.6 11.0 F 0.4 13.9 F 0.1 15.5 F 0.3
2
13.2 14.0 15.5 14.3 15.7 16.0 16.1 16.6 16.5 12.0 10.0
UD UD UD 4.2, (0.4) 73.6, (97.8) (182) (194) 410.0 1030, (1132) (4528) 4720, (5106)
I.S. = insufficient quantities of chromium reducible sulfur for d34S analyses. N.D. = not determined. UD = undetectable. a For samples depths >24 m; from 1985 data set of Anderson et al. (1988). b Values in parentheses from Yao and Millero (1995).
5 4 3 3 1 4 4 2 2
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sented in terms of the VCDT scale based on reference material IAEA-S1 (formerly NZ-1) having a d34S value of 0.30x, where: d34 Ssample ðx Þ ¼ ½ð34 S=32 Ssample Þ =ð34 S=32 SVCDT Þ 1 103 The d18O values are presented in terms of ocean water sulfate having a value of +9.5xon the VSMOW scale. Intra-laboratory analytical sulfate standards for d34S (+5.4xand +20.4x ) and d18O ( +9.5x and +12.0x) gave reproducibility of F0.15xand F0.4x, respectively, based on multiple analyses.
3. Results Table 1 summarizes all of the concentration and stable isotopic measurements made of reduced sulfur and sulfate in this study. The sulfate concentration measurements made on water samples below the interface (>24 m) are suspect. The addition of zinc acetate and the presence of high concentrations of sulfide (>1 mM) in these samples appeared to interfere with the response of the ion chromatograph, and sulfate con-
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centrations appeared anomalously low. Therefore, for depths of 40 m or more, we have listed in Table 1 the 1985 sulfate data of Anderson et al. (1988), which correspond to the same depths we sampled in our study. In Table 1, we also present in parentheses the sulfide concentrations reported by Yao and Millero (1995), which were measured during our cruise. The variations in the d34SSO4 and d18OSO4 values with depth are small and co-vary from 19 to 24 m near the oxic – anoxic interface (Table 1; Fig. 1). At depths of 20 m and less, the d34SSO4 and d18OSO4 values are close to + 20.0xand + 10.4x, respectively. From 21.5 to 24 m, the d34SSO4 and d18OSO4 values are relatively consistent and increase with increasing depth to + 21.6xand + 11.3x, respectively (Table 1; Fig. 1). The d34SSO4 and d18OSO4 values continue to increase at depths greater than 24 m, along with a decline in sulfate and rise in sulfide concentrations (Table 1; Fig. 1), consistent with the cumulative effects of dissimilatory sulfate reduction occurring throughout the deep anoxic water column. Fig. 2 summarizes all of the d34SSO4, d34SSH2S, and d34STRS values measured in the water column and sediments of Framvaren in this and previous studies (Anderson et al., 1988; Saelen et al., 1993). In gen-
Fig. 1. The d34SVCDT ( ) and d18OVSMOW (o) values of sulfate from samples collected during this study in June 1993 in the water column of Framvaren fjord. Right panel (B) shows more detail across the oxic – anoxic interface where the horizontal dashed line indicates the depth of 20 m at which sulfide was first detected.
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Fig. 2. The d34SVCDT values of sulfate (open symbols) and SH2S (closed symbols) in the water column of Framvaren fjord from samples collected in June 1993 during this study (diamonds) and in 1982 (squares) and 1983 (circles) as reported by Anderson et al., 1988. The d34SVCDT values of total reduced sulfur (TRS) in the sediments of Framvaren reported by Saelen et al. (1993) are also shown ( ). The horizontal dashed line indicates the depth of 20 m at which sulfide was first detected.
eral, there is good agreement between the d34SSO4 values that we measured in 1993 and those in 1982 by Anderson et al. (1988) (Fig. 2). However, for the deep anoxic waters, the d34SSO4 values measured in 1983 by Anderson et al. (1988) are consistently lower by approximately 10xthan what was measured in either 1982 or 1993 (Fig. 2). Framvaren water column sulfide concentrations measured by Yao and Millero (1995) during the same cruise in 1993 agree well with our data (Table 1). The lowest d34SSH2S value that we measured ( 19.8x) occurred just beneath the interface at 22 m and is 41.2xdepleted in 34S relative to sulfate at that depth (Table 1). Below 24 m, the d34SSH2S values gradually increased with depth to values as high as 3.1xand track similar changes in higher d34SSO4 values (Table 1; Fig. 2). As for sulfate, the d34SSH2S values we measured in the deep anoxic waters are more similar to the values measured for sulfide in samples collected in 1982 versus those collected in 1983 as reported by Anderson et al. (1988) (Fig. 2). In Fig. 3, we plot sulfide versus sulfate concentrations using the 1985 sulfate data from Anderson et
al (1988) and the sulfide data of Yao and Millero (1995) for corresponding depths within the deeper anoxic waters ( z 40 m depth). This results in a straight-line fit with an r2 value of 0.98 and a slope equal to 0.65. If there were no loss of sulfide from this system, such a plot would yield a line with a slope equal to 1 where the decline in sulfate is equally balanced by the increase in sulfide. Instead, we can see from Fig. 3 that approximately 35% of the sulfide produced from reduction has been lost from the water column since the onset of anoxia in Framvaren. Loss of sulfide could occur from diffusion upward and subsequent oxidation near the interface. However, this would not result in significant net loss of sulfide from the system over time as it is recycled near the interface. Furthermore, a sulfur repartitioning process such as this would then produce an excess of sulfate relative to sulfide near the redox interface and an apparent depletion of sulfate relative to sulfide in the deeper anoxic waters. Such a process would then produce in Fig. 3 a linear regression with a slope > 1.0 that would bisect the reference line. Because we do not observe this, and the x-intercept of our plot
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anoxic deep waters of Framvaren have experienced stable and steady-state conditions with respect to sulfate during this time. This is also consistent with previous reports that little water renewal occurs in the bottom waters of Framvaren (Dyrssen et al., 1996; Stigebrandt and Molvaer, 1988). In basins like Framvaren, which have restricted mixing, the d34SSO4 value might be expected to increase with depth as it approximates a Rayleigh distillation effect. If there is a finite amount of available reactant (i.e., sulfate), then the fractionation effect is compounded over time as sulfate reduction proceeds and the sulfide formed is separated from the sulfate. This Rayleigh effect can be described by a simple natural log function: Fig. 3. Sulfide concentrations measured in 1993 (from Table 1 of Yao and Millero, 1995) plotted relative to sulfate concentrations measured in 1985 (from Table 3 of Anderson et al., 1988) for corresponding depths in the water column of Framvaren fjord (40, 50, 70, 100, 110, 130, 150, and 170 m). The measured slope of 0.65 deviates from a slope of 1 by 0.35, suggesting that 35% of the sulfide produced from sulfate reduction has been removed from the water column. The x-intercept, where sulfide concentration is zero, of 18.55 reflects the original sulfate concentration (mM) of Framvaren fjord before anoxia was established (see text).
closely approximates the expected value for the initial sulfate concentration in Framvaren (see following discussion), it seems more reasonable that the greatest loss of sulfide occurs from sedimentation, either as iron sulfides or organic sulfur. In addition, some of the reduced sulfur may exist as Sj or other thiols (Dyrssen et al., 1996). An interesting observation from the regression in Fig. 3 is that the sulfate intercept (i.e., corresponding to null levels of sulfide) is 18.55 mM, which is consistent with the initial sulfate concentration estimated for Framvaren (i.e., prior to removal by sulfate reduction). From the maximum salinity of 22.92 measured by Yao and Millero (1995) for the deepest samples collected at 170 m depth in 1993, we can independently estimate the initial sulfate concentration using a sulfate/salinity ratio of 28.28:35 (Anderson et al., 1988). This results in a similar estimate for the initial sulfate concentration of 18.52 mM. This agreement in estimates, and the internal consistency of our calculation using sulfate data from 1985 and sulfide data from 1993 suggests that the permanently
d34 SSO4 ¼ elnð½Xt =½X0 Þ
ð1Þ
where d34SSO4 is the isotopic composition of the reactant at a certain time of the reaction, which in this case is approximated by the d34SSO4 value at a given depth in the deep anoxic waters where sulfate is progressively removed with depth, epsilon (e) is the isotopic enrichment factor [ = 1000(a 1), where a equals the isotopic fractionation], and [X]0 and [X]t are the concentrations of the reactant at t0 and at any time t, respectively. The ratio [X]t/[X]0 equals F, the fraction of the reactant remaining and is also a measure of the extent of the reaction. If sulfate reduction is primarily a unidirectional process, then Eq. (1) should provide a linear relationship when ln F is plotted against d34S of sulfate, with a slope equal to e (Krouse and Tabatabai, 1986; Mariotti et al., 1981). The value for F plotted in Eq. (1) was estimated as the ratio of the sulfate concentration measured for a given depth to the maximum SO42 concentration of 16.6 mM measured at 24 m depth in 1993 (Table 1). Plotting these results for both the d34S and d18O of sulfate in the anoxic waters ( z 24 m) provides linear relationships (Fig. 4). For comparison, we have also plotted in Fig. 4 the individual data from both 1982 and 1983 of Anderson et al. (1988). Because the isotopic data from 1983 are very distinct from those of 1982 or 1993, we plotted them separately and used the sulfate concentrations measured that year as reported by Anderson et al. (1988). Sulfur isotope enrichment factors (e) of 46.1xand 41.5x estimated for the entire anoxic water column from the
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1982 and 1993 are in good agreement. The value of 41.5xmeasured in 1993 also closely approximates the observed difference in d34S between the sulfate and SH2S measured at the shallowest depth of 22 m (Table 1). However, a sulfur isotope enrichment factor of 17.3xis estimated from the sulfate data of 1983 (Fig. 4), which may indicate non-steady-state conditions in 1983. An oxygen isotope enrichment factor of 9.6xis estimated for sulfate undergoing dissimilatory reduction in Framvaren (Fig. 4). This is approximately 25% of the value estimated for the sulfur isotope enrichment factor. Consequently, a slope of 4.36 is obtained
Fig. 5. The d34SVCDT plotted relative to the d18OVSMOW of sulfate measured in this study from anoxic waters (24 – 150 m) of Framvaren fjord.
when the d34SSO4 from the anoxic waters is plotted against the corresponding d18OSO4 value (Fig. 5).
4. Discussion 4.1. Interface
Fig. 4. A Rayleigh plot which expresses the changes in the d34SVCDT and d18OVSMOW of sulfate measured in the water column of Framvaren fjord in June 1993 during this study (open squares and circles, respectively) and in 1982 (d34SVCDT, closed squares) and 1983 (d34SVCDT, closed triangles) as a function of ln F, where F is the fraction of sulfate concentration measured in the anoxic waters relative to the maximum concentration of 16.6 mM measured in 1993 at 24 m depth (see Table 1 and text). Therefore, all d34SSO4 values measured at the chemocline in 1982, 1983, and 1993 were assumed to have an initial and maximum sulfate concentration of 16.6 mM, which closely approximates the maximum sulfate concentration of 17.0 mM measured at 22 m by Anderson et al. (1988). Sulfate concentration and d34SSO4 data for 1982 and 1983 were obtained from Tables 1 and 2, respectively, from Anderson et al. (1988). The sulfate concentration of 13.1 mM measured at 50 m in 1982, however, appears conspicuously low when compared to other sulfate measurements made at that depth (J. Skei, unpublished results). Therefore, a value of 15.9 mM was used for this depth which corresponds to the sulfate concentration measured at 50 m in 1985 (see Table 3, Anderson et al., 1988).
The variations in d34SSO4 and d18OSO4 are small near the redox interface. This is to be expected in a marine-influenced system with high sulfate concentrations and because sulfur isotope enrichment factors associated with abiotic and biotic sulfide oxidation are small, generally varying from + 2 to 5x(Fry et al., 1986, 1984; Schoen and Rye, 1970). However, the minima in d34SSO4 of 19.7xat 20 m, where sulfide was first detected, is consistent with the oxidation of sulfide with a low d34S value of f 20x(Table 1). Rates of sulfide oxidation by either phototrophic or chemoautotrophic sulfide-oxidizing bacteria are very high near the interface in Framvaren fjord (Mandernack and Tebo, 1999; Sorensen, 1988). Low d34SSO4 values were also observed in a sharp transition zone of a stratified lake where brackish water overlays bottom seawater and were attributed to oxidation of biogenic sulfide produced in deeper waters (Jeffries et al., 1984).
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Dissolved oxygen has a d18O value of approximately + 26x(Kroopnick and Craig, 1972) and can be incorporated into sulfate from 0xto 87.5% during abiotic or biotic sulfide oxidation, with the remaining oxygen coming from water (Lloyd, 1968; Taylor et al., 1984; Toran and Harris, 1989; Van Everdingen and Krouse, 1985). During abiotic and biotic sulfide oxidation, the isotopic fractionation of dissolved O2 can be as large as 8.7xand 11.1x , respectively, whereas values of eo with respect to water during abiotic and biological sulfide oxidation generally fall within the range of 0xto + 4.1xat earth surface temperatures (Toran and Harris, 1989; Van Stempvoort and Krouse, 1994). Therefore, as a result of sulfide oxidation, the d18OSO4 value may increase, but is more likely to decrease from its average seawater value of + 9.7x(Lloyd, 1967). Dissolved oxygen was undetectable below 18 m depth, and sulfide did not appear until 20 m; therefore, there was no apparent O2 – H2S interface during the time of sampling (Yao and Millero, 1995). Under these conditions, sulfide oxidation may have been coupled to the reduction of iron and/or manganese oxides or mediated by phototrophic bacteria (Mandernack and Tebo, 1999; Millero, 1991), during which incorporation of molecular oxygen (O2) into sulfate would be unlikely. The d18Ovsmow value of water near the interface (19 – 24 m) and at the deepest depths (100 and 150 m) of Framvaren was measured by the CO2 equilibration method to be 3.6 F 0.1x (n = 3) and 3.0 F 0.1x(n = 2), respectively (Mandernack, unpublished results). Consequently, sulfate produced from sulfide oxidation at the interface of Framvaren would probably not be depleted in 18O by more than f 9.1xto 13.2xrelative to seawater sulfate. It appears that sulfide oxidation did not provide enough ‘‘isotopic leverage’’ to significantly decrease the d18O of sulfate at the interface of Framvaren, in contrast to the brine interface of the Orca Basin in the Gulf of Mexico where a 1.5xdepletion in d18OSO4 was observed (Sheu et al., 1988). Disproportionation of SB to sulfate and HS produces sulfate that is enriched in 34S and 18O by f 18xand 17xrelative to Sj and water, respectively (Bo¨ttcher et al., 2001). This fractionation could explain the increase in d34SSO4 and d18OSO4 values from depths of 21.5 to 23 m. These depths also correspond to the suboxic zone where sulfur disproportionation reactions are generally favored due to the
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presence of sufficient oxidizing agents (e.g., iron and manganese oxides) capable of oxidizing HS to sulfur intermediates (Canfield and Thamdrup, 1994). Therefore, d34SSO4 and d18OSO4 values might reflect different sulfur reactions across the redox interface of anoxic basins, although a more thorough analysis at Framvaren is needed to confirm this. 4.2. Deep anoxic waters At depths z 40 m, it appears that sulfate reduction exerts the primary influence on the sulfur and oxygen isotope composition of sulfate (Table 1; Figs. 1 and 4). What is most striking from the combined data sets of this study and those of Anderson et al. (1988) is the consistency in the d34S values of sulfide and sulfate measured in 1982 and 1993 and the contrasting lower values of each measured in 1983 (Fig. 2). Furthermore, estimates of es of 46.1xand 41.5xfor sulfate reduction using the 1982 and 1993 data sets, respectively, are also in closer agreement than the estimate of 17.3xderived from the data collected in 1983 (Fig. 4). The estimated value of es in 1993 is also in good agreement with the observed DH2S – SO4 value of 41.2xmeasured at 22 m in 1993. This DH2S – SO4 value, because it is shallow, represents the instantaneous isotope effect of sulfate reduction rather than the integrated record at depth. This consistency between the two independent estimates when using the 1993 data, however, suggests that the biogeochemical controls of sulfate reduction throughout the anoxic waters of Framvaren have been relatively consistent over time. Slower rates of sulfate reduction can sometimes lead to higher values of es similar to what we have estimated here for Framvaren (Goldhaber and Kaplan, 1975; Kaplan and Rittenberg, 1964). In particular, when organic substrates become limiting to sulfate reduction, this can slow rates of reduction and result in high values of es (Canfield, 2001). However, slower rates of reduction are not necessarily always associated with larger values of es, as recent evidence has indicated (Bolliger et al., 2001; Canfield, 2001; Detmers et al., 2001). The type of organic substrates utilized for sulfate reduction can also affect es. Substrates such as acetate, which can be completely oxidized to CO2 but which provide lower reducing power for sulfate reduction (i.e., less negative DGj value), generally results in higher values of
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es (Detmers et al., 2001). In contrast, substrates such as lactate, which are incompletely oxidized but provide greater reducing power, generally yielded lower values of es (Detmers et al., 2001). Based on the 1982 and 1993 data, the large value of es estimated for sulfate reduction in Framvaren is consistent with lower rates of sulfate reduction resulting from limiting amounts of organic substrates, or they may be the result of organic substrates such as acetate that have lower reducing power to fuel sulfate reduction. An explanation is still required to explain the anomalous low d34SSO4 and d34SSH2S values and small es estimated for sulfate reduction based on the 1983 data of Anderson et al. (1988). Anderson et al. (1988) originally proposed that the low d34S values of sulfate (from + 14.8x to + 18x) measured from depths of 8 to 50 m in 1983 may have resulted from sulfide oxidation due to a major flushing event whereby oxygenated seawater from outside of the fjord spilled over the sill at the entrance to Framvaren and sulfides with a low d34S value were subsequently oxidized. Such a flushing event would also bring in fresh organic material and other nutrients which might also eventually stimulate faster rates of sulfate reduction in the bottom waters after oxygen was consumed during respiration. The lower es estimated using the data of 1983 is consistent with this (Fig. 4). Flushing events in Framvaren have been reported elsewhere, although evidence indicates that they are generally limited to the shallow and intermediate waters and do not penetrate to depths greater than 100 m (Dyrssen et al., 1996; Stigebrandt and Molvaer, 1988). Therefore, for waters sampled near 150 m, it is still difficult to reconcile the shift in d34S values of sulfate from f + 45xin 1982 to f + 30xin 1983 and back to + 42xby 1993 (Fig. 2; Anderson et al., 1988). It is unlikely that the proposed effects of sulfide oxidation at 10– 50 m depth in 1983 could have also lowered the d34SSO4 values in the bottom waters by 10x. To accomplish this, the amount of 34 S-depleted sulfate produced from sulfide oxidation required to lower the d34SSO4 values in the deep water by this amount can be calculated for X by the isotopic mass balance equation below: ðX Þðd34 Soxid:;SO4 Þ þ ð1 X Þðd34 S1982;SO4 Þ ¼ d34 S1983;SO4
d34Soxid.,SO4, d34S1982,SO4, and d34S1983,SO4 correspond to the isotopic signatures of sulfate produced from oxidation, ‘‘background’’ sulfate in the deep waters in 1982, and sulfate in the deep waters in 1983, respectively. This calculation assumes no isotopic fractionation during sulfide oxidation as previous studies have indicated (Fry et al., 1986, 1984; Ku et al., 1999; Schoen and Rye, 1970). Using d34S values of 20x and 3xfor sulfate formed from oxidation, which correspond to the range of d34SSH2S values measured at the interface and deep waters, respectively, we obtain estimates for X of 23% and 31%, respectively. Therefore, sulfate concentrations in the deep waters of Framvaren would have had to increase from 10 to 12.3 – 13.1 mM between 1982 and 1983 to account for the apparent shift in d34SSO4 values. The data of Anderson et al. (1988) in fact indicate that sulfate concentrations at depths z 130 m in Framvaren varied only between 9.55 and 10.04 mM for 1982 and 1983, and therefore do not indicate significant effects of sulfide oxidation. Because evidence presented earlier suggested that sulfate reduction rates (based on observed values of es) appear to have been relatively consistent throughout the water column (Table 1; Fig. 4), it is also difficult to explain a large shift to lower d34SSO4 values as a result of changes in sulfate reduction rates within the deep waters. If a flushing event did occur at some point between the sampling times of 1982 and 1983, it appears from the d34S measurements that the biogeochemical conditions were completely reestablished by the time the fjord was resampled by us in 1993 (Fig. 2). The low and enigmatic d34S values measured in 1983 have important implications regarding the mechanism of iron sulfide formation and the overall sulfur cycle within the water column and sediments of Framvaren as previously discussed by Saelen et al. (1993). Saelen et al. (1993) interpretation of the mechanisms of iron sulfide formation in the sediments of Framvaren was based on a comparison of the d34S values they measured for total reduced sulfur in the sediments (d34STRS), which is dominated by ‘‘FeS’’ and FeS2, with the d34SSH2S values measured in the water column in 1983 by Anderson et al. (1988). These authors propose different scenarios for iron sulfide formation in shallow ( f 25 m), intermediate ( f 100 m), and deep waters ( f 175 m) to explain
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the overall shift toward higher d34SSH2S values with depth and the lower d34STRS values they measured in the sediments when compared by depth to the d34SSH2S values measured in 1983 in the water column (Fig. 2). For the shallow depths, they reasoned that the d34SSH2S values of 19.6xmeasured in the water column by Anderson et al. (1988) may be atypically high and that the average d34STRS value of f 30xthey measured for the sediments may in fact directly reflect the average d34S value of sulfide produced in the water column at that depth. In order to explain a d34S value of reduced sulfur in the intermediate and deep sediments that is lower or similar, respectively, to the d34SSH2S in the water column, Saelen et al. (1993) suggested that the reduced sulfur in the sediments must be a mixture of sulfides formed in the shallow waters (with lower d34S values) with those formed either at intermediate or deep depths (having higher d34S values). They speculated that this may result from iron monosulfides formed in the shallow waters settling to depths where they can react with free sulfide or Sj from intermediate or deeper depths and form FeS2. Therefore, all of the scenarios presented by Saelen et al. (1993) propose that the sedimentary reduced sulfur at all depths is derived from sulfide produced within the water column and does not include in situ production of reduced sulfur within the sediments. Our 1993 measurements of d34SSH2S do not refute the general interpretations of Saelen et al. (1993); however, they do permit additional scenarios that may explain the overall trends observed for d34S of sulfides in the sediments and water column. Our suggestions are based on the 1982 data of Anderson et al. (1988) and the 1993 data presented here. We briefly discuss these scenarios below. What is most apparent from Fig. 2 is that, for a given depth, the d34STRS values in the sediments appears to be consistently lower than d34SH2S measured from the water column, both at the shallow depths just beneath the oxic – anoxic interface and at the deepest depths. This suggests that sulfate reduction has occurred throughout the entire basin and would also explain the parallel trend of increasing d34SSO4 with depth (Fig. 2). Although the lower d34STRS values in the intermediate and deep sediments may result in part from a mixture of sulfide produced at depth with iron sulfides produced in the water
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column at shallower depths (with lower d34S values) and which have subsequently settled to deeper depths, this does not adequately explain the lower d34STRS values of the shallow sediments relative to reduced sulfur in the water column. Furthermore, sulfides collected from a sediment trap at 175 m depth in the water column had a d34S value that was 2.3xheavier than the d34STRS for sediments at this same depth (Saelen et al., 1993). Although this difference is small, these results are nonetheless consistent with our theory that ‘‘isotopically light’’ sulfide is produced in the sediments. However, the relatively similar d34S values could also result if the sediment trap particles were partly derived from sediment resuspension, but might also suggest that most of the sedimentary sulfides are derived from the water column. We provide an alternative interpretation that the general trend of consistently lighter d34STRS values of the sediments may result from sulfide production within the sediments that has a lighter d34S value than that produced in the water column. This proposed mechanism invokes a different rate of sulfate reduction or different mechanism of sulfide production (i.e., sulfur disproportionation) occurring within the sediments versus the water column. Naes et al. (1988) report that sulfate reduction does occur in the deep sediments of Framvaren. This conclusion was based on a single pore water measurement from the deep sediments that indicated elevated alkalinity and sulfide concentration relative to the deep bottom waters. This observation, along with lower d34STRS values measured for the sediments, suggests that sulfate reduction rates in the sediments may be different than that in the water column. Slower cell-specific rates of reduction often result in larger values of es and consequently lower d34SSH2S (Canfield, 2001; Goldhaber and Kaplan, 1975; Kaplan and Rittenberg, 1964). According to the steady-state model of Rees (1973), faster rates lead to less back reaction at each individual step of sulfate reduction and therefore kinetic isotope effects at some steps are not fully expressed. This will consequently diminish the overall fractionation of sulfur isotopes during sulfate reduction. However, more recent evidence indicates that es is not necessarily related to rates of sulfate reduction, nor to temperature or bacterial phylogeny (Bolliger et al., 2001; Canfield, 2001; Detmers et al., 2001). Nonetheless, different rates of sulfate reduction
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(higher or lower), or different biogeochemical conditions within the sediments of Framvaren relative to the water column, could result in the relatively lower d34STRS values of the sediments (Fig. 2). To preserve a sedimentary d34STRS value distinct from that in the overlying water column, however, requires sufficient iron in the sediments to trap the sulfide produced there. Iron concentrations of f 3.5 – 4.0% have been measured in the top 46 cm of sediments collected at a water depth of 184 m in the F-1 basin of Framvaren (J. Skei, unpublished results). Furthermore, 25– 95% (median value f 75%) of the total iron in surface sediments (0 –4 cm) of Framvaren collected at 45 and 175 – 185 m depths is highly reactive, which includes dithionite-extractable Fe (iron oxides and ‘‘FeS’’) and pyrite (Raiswell and Canfield, 1998). If there is sufficient dithioniteextractable Fe in the sediments, this could then preserve a distinct sedimentary d34 S signature. Because dithionite-extractable Fe was not reported separately from the pyrite (Raiswell and Canfield, 1998), it is not currently possible to assess whether sufficient Fe is available in Framvaren sediments to preserve a sedimentary d34S signature. Degree of pyritization (DOP) and ‘‘potential DOP’’ values of 0.2– 0.8 and 0.7– 1.0, respectively, have been reported for these same sediments of Framvaren (Raiswell and Canfield, 1998). However, these measurements were not made below 4 cm sediment depth. Therefore, the DOP values reported for Framvaren sediments also do not provide sufficient evidence to support or refute our theory that diagenetic pyrite formation records the d34S signal of interstitial sulfate reduction occurring in the deep sediments of Framvaren. We are unaware of any sulfate reduction rate measurements having been made in either the water column or sediments of Framvaren that could also test this hypothesis. Based on observed changes in the concentrations of particulate organic matter (POM) collected from sediment traps, Naes et al. (1988) reported that little remineralization of POM occurs in the water column of Framvaren. This would seemingly contradict our suggestion that substantial rates of sulfate reduction occur in the water column of Framvaren where it should result in the mineralization of POM. Naes et al. (1988) indicate that when they sampled at 2-month intervals, from March 15 through November 29, 1983, there was a significant drop in POM from f 70 mg
m 2 day 1 collected in the 40- and 80-m traps relative to f 50 mg m 2 day 1 collected in the 120- and 160m traps. This evidence suggests mineralization of POM between 80 and 120 m and is consistent with the depth range where large increases in alkalinity have been attributed to the activities of sulfate-reducing bacteria (Yao and Millero, 1995). However, during the final 5-month sampling period from November 29, 1983, to May 3, 1984, Naes et al. (1988) reported a steady increase in the amount of POM collected in sediment traps from 40 to 160 m. When the results of this longer sampling period were averaged with the results from the earlier periods, there was no apparent net annual flux of POM throughout the water column and consequently no apparent mineralization of POM (Naes et al., 1988). However, if activities of sulfatereducing bacteria are in fact highest at depths of 80– 120 m, as the alkalinity data of Yao and Millero (1995) suggests, the combined effects of a prolonged sampling period and the absence of any preservative used in the sediment traps might have permitted sulfate-reducing bacteria to decompose the POM collected in the 40- and 80-m traps. Therefore, we suggest that the final sampling period of Naes et al. (1988) may have been anomalous, and consequently, their sediment trap data may in fact support our suggestion that sulfate reduction occurs to a measurable extent within the water column of Framvaren. This could in turn produce sulfide within the water column that has a unique d34S value distinct from that produced in the sediments. Another possible explanation for the low d34S values of reduced sulfur in the sediments is the disproportionation of Sj or other intermediate sulfur compounds (e.g., S2O3, SO3). The bacterial disproportionation of Sj results in sulfide that is enriched in 32 S by 7.3 –8.6x relative to Sj and sulfate that is enriched in 34 S by 12.6 – 15.3x(Canfield and Thamdrup, 1994). This mechanism requires the formation of Sj or other sulfur intermediate. In general, isotopic fractionation associated with the formation of elemental sulfur during bacterial and abiotic oxidation of HS or FeS is small (Kaplan and Rittenberg, 1964; Nakai and Jensen, 1964; Schoen and Rye, 1970), although enrichments in 32S in the Sj product can sometimes be as large as f 5– 6x(Fry et al., 1988; Kaplan and Rittenberg, 1964). If we assume that any Sj that may be present in the water column is formed
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by oxidation of HS and has a similar d34S value as the total reduced sulfur, the observed difference of 9x between d34STRS in the shallow sediments versus d34SSH2S in the water column is consistent with the formation of 34S-depleted sulfide from sulfur disproportionation within the sediments. The formation of Sj during abiotic oxidation of HS is likely to occur in the shallow waters of Framvaren near the chemocline where there is sufficient oxidizing agents such as NO3, Fe(III), or Mn(IV). It is also possible that disproportionation occurs in the intermediate waters during flushing events that carry in dissolved oxygen (Dyrssen et al., 1996). However, it is still questionable whether an alternative oxidant such as reactive iron oxides in the deep waters could generate Sj, because only iron sulfides were detected below 25 m depth at Framvaren (Cutter and Kluckhohn, 1999; Landing and Westerlund, 1988; Skei, 1988; Skei et al., 1996). Furthermore, as will be discussed later, the d34SSO4 and d34OSO4 values in deep waters of Framvaren do not indicate disproportionation at depths z 40 m. Therefore, the lower d34STRS values of the deepest sediments relative to SH2S in the water column at corresponding depths likely results from a mixture of sulfide derived from shallow ( f 20 m) and deep ( z 150 m) waters, as proposed by Saelen et al. (1993), or as we suggest, by different rates of sulfate reduction occurring within the sediments versus the water column. 4.3. Comparisons with the Black sea Recently, Dyrssen (1999) compared the chemistries of the Black Sea and Framvaren fjord. With respect to sulfur, Dyrssen (1999) interpreted the particularly high sulfide concentrations of 8 mM in the bottom waters of Framvaren, compared with concentrations of f 0.35 mM in the bottom waters of the Black Sea, to result primarily from differences in the surface area to volume ratios of 13.4 and 0.78 km 1 for Framvaren and the Black Sea, respectively. Volume-based rates of sulfate reduction in the water column of the Black Sea are several thousand times lower than rates in the sediments (Albert et al., 1995). This presumably results from relatively less terrestrial input and production of organic matter in the Black Sea water column which becomes more diluted, relative to a smaller basin like Framvaren, with a
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much larger water column. Concentrations of particulate organic carbon and nitrogen are approximately one tenth that in Framvaren (Cutter and Kluckhohn, 1999). In earlier studies, slower rates of sulfate reduction occurring in the water column relative to the sediments of the Black Sea had been suggested to explain the overall higher d34SSH2S values in the sediments and bottom waters relative to that in most of the water column (Sweeney and Kaplan, 1980; Vinogradov et al., 1962). However, as will be discussed below, these earlier studies failed to distinguish the causes for the different d34SSH2S values between the microlaminated Unit I sediments and the muddy turbidites of the Black Sea abyssal plain (Lyons, 1997). As previously mentioned, based on measured changes in alkalinity and sulfide concentrations, the depth range where the majority of sulfate reduction appears to occur in the water column of Framvaren is 60– 100 m beneath the oxic – anoxic interface (Yao and Millero, 1995). Consistent with this, rates of sulfate reduction in the water column of the Black Sea were highest 50 – 70 m beneath the depth at which sulfide first appeared (Albert et al., 1995; Fry et al., 1991; Jorgensen et al., 1991). This depth also corresponded with an enrichment in d34SSH2S that may have been the result of faster rates of sulfate reduction or to sulfide oxidation by O2 or MnO2 (Fry et al., 1991). The mean d34S value of 38.6xfor HS just beneath the chemocline depth of the Black Sea (f100 m) is approximately 2xheavier than HS in the deeper anoxic bottom waters and more closely matches d34S values of particulate reduced sulfur collected from mid-water sediment traps and total reduced sulfur in microlaminated surface (0 –26 cm) sediments of Unit I in the deepest off-shore locations of the basin (Calvert et al., 1996; Fry et al., 1991; Lyons, 1997; Muramoto et al., 1991; Sweeney and Kaplan, 1980). This similarity in d34STRS values in the sediments with sulfide just beneath the chemocline and that collected in sediment traps has led several investigators to conclude that sedimentary pyrite in the deep microlaminated sediments of the Black sea forms within the water column (i.e., syngenetically) just below the chemocline (Calvert et al., 1996; Lyons, 1997; Muramoto et al., 1991). Consequently, once the pyrite forms in the water column, it settles
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f 2100 m to the bottom with relatively little change in its sulfur isotope composition. Analysis of size distributions of sedimentary pyritic framboids also indicates that pyrite in the more recent and uppermost sediments have an origin within the water column (Wilkin et al., 1997). Furthermore, there appears to be little additional pyrite formation in these offshore laminated sediments (i.e., relatively minor diagenetic pyrite) as evidenced by little change in either the DOP or d34STRS values throughout the top 26 cm (Lyons, 1997; Lyons and Berner, 1992). In contrast to the deep offshore laminated sediments of the Black Sea, acid volatile sulfur (AVS) and pyritic sulfur in near-shore sediments collected at a depth of 198 m had higher d34S values of f 25x and f 27.6x , respectively, relative to sulfide in the water column (Lyons, 1997). In addition, the d34S values of pyrite and AVS showed a small but steady increase with sediment depth, evidence for pyrite formation within the sediments as a result of interstitial sulfate reduction (Lyons, 1997). We propose that these shallower sediments of the Black Sea mimic conditions in sediments of Framvaren where interstitial sulfate reduction also occurs. Considering basic differences in surface area to volume ratios between the Black Sea and Framvaren (Dyrssen, 1999), it seems reasonable to predict that the deepest and most offshore sediments of Framvaren could still experience conditions similar to the near-shore sediments of the Black Sea sampled at 198m depth. However, in contrast to the shallow sediments of the Black Sea, at all depths of Framvaren, the d34STRS values are consistently lower in the sediments relative to d34SSH2S in the water column (Fig. 2). Nonetheless, considering recent evidence that suggests sulfate reduction rates cannot always be correlated with d34SSH2S values (Canfield, 2001; Detmers et al., 2001), the lower d34STRS values in Framvaren sediments could still reflect different rates of sulfate reduction occurring in the sediments relative to the water column, as suggested for the shallow Black Sea sediments (Lyons, 1997). 4.4. Biogeochemical controls of d34SSO4 and d18OSO4 values Early field and laboratory studies with enrichment cultures of marine sulfate-reducing bacteria revealed
that the enrichment factor for sulfur in sulfate, es, was approximately four times that of the enrichment factor for oxygen in sulfate, eo (Mizutani and Rafter, 1969; Rafter and Mizutani, 1967). Consequently, when the d34S was plotted relative to the d18O value of the sulfate, this yielded a slope of f 4. However, similar experiments by these authors subsequently revealed that differences in the d18O value of water used in the microbiological media resulted in changes in the measured value of eo, which generally resulted in a slope less than 4 when the d34S was plotted relative to the d18O value (Mizutani and Rafter, 1973). It was suggested by these authors that this effect resulted from isotopic exchange between sulfate and water via sulfite or an unknown metabolic intermediate of the sulfate reduction pathway. Fritz et al. (1989) conducted experiments similar to Mizutani and Rafter (1973) with freshwater lake sediments amended with a pure culture of Desulfovibrio desulfuricans to initiate sulfate reduction. These authors observed that with increased reduction, the d18O values of the residual sulfate trended towards d18O values predicted for equilibrium oxygen isotope exchange between sulfate and water at the respective temperatures the experiments were conducted. They further speculated that there was rapid equilibrium isotope exchange, which is typically very slow for sulfate and water at earth surface temperatures (Lloyd, 1968), which resulted from a SO42 enzyme complex rather than a sulfite intermediate. Based on these earlier studies discussed above, it has been proposed, and a model presented, that the 4:1 ratio of es to eo that sometimes occurs during sulfate reduction may reflect the 1:4 stoichiometric ratio of sulfur to oxygen atoms in the sulfate molecule (Grinenko and Ustinov, 1990). According to this model, the 4:1 ratio of es to eo could result from purely kinetic effects controlled by the bacterial reduction pathway when rates are sufficiently fast to not permit oxygen isotopic exchange between water and an intermediate (e.g., SO32 or a SO42 enzyme complex) of sulfate reduction. Under these conditions, a slope of f 4 will result when d34SSO4 is plotted relative to the d18OSO4 value. However, at slower rates of sulfate reduction, varying degrees of oxygen isotopic exchange can occur between intermediates of sulfate reduction and water, which will subsequently affect the final d18OSO4 value of the residual sulfate and generally
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result in a slope less than 4 when d34SSO4 is plotted relative to the d18OSO4 value. Therefore, the effects of oxygen isotopic exchange with water can complicate interpretations of measured d34SSO4 versus d18OSO4 values derived from anoxic environments. Additional complexities in interpreting d34SSO4 and d18OSO4 values in anoxic environments can result from reoxidation of sulfide or from sulfur disproportionation. Although sulfate produced from bacterial Sj disproportionation is enriched in 18O by f 17xrelative to water, for most marine environments, this will decrease the slope when d34SSO4 is plotted relative to d18OSO4 (Bo¨ttcher et al., 2001). Reoxidation of sulfide in pore waters of anoxic marine carbonate sediments also had a similar effect on this slope (Ku et al., 1999). 4.5. d34S versus d18O values of sulfate in anoxic marine systems Few studies of anoxic marine systems have measured both the d34SSO4 and d18OSO4 values in either interstitial pore waters (Aharon and Fu, 2000; Bo¨ttcher et al., 1999; Bottrell et al., 2000; Ku et al., 1999; Zak et al., 1980) or in the water column (Jeffries et al., 1984). In all of these studies except one (Ku et al., 1999), an increase in both d34SSO4 and d18OSO4 was measured when sulfate concentrations became depleted, and in most cases when d34SSO4 was plotted versus d18OSO 4, a slope of < 3 was measured. Recently, Aharon and Fu (2000) measured d34SSO4 and d18OSO4 collected from pore waters in sediments of oil and gas seeps of the Gulf of Mexico. Relative to non-seep (‘‘reference’’) sediments at the same location, seep sediments had much higher rates of sulfate reduction, as estimated from pore water sulfate profiles. Aharon and Fu (2000) also observed that the fractionation effects for oxygen and sulfur in sulfate were lower when the rates of reduction were highest. For instance, for gas seep, oil seep, and reference sediments, sulfate reduction rates were 2.000, 0.090, and 0.004 Amol SO42 cm 3 day 1, respectively, whereas the corresponding values of es were estimated to be 8.6x, 18.0x, and 27.2x. When d34SSO4 was plotted relative to d18OSO4 from each of these environments, they observed slopes of 3.5, 2.8, and 1.4, respectively (r2>0.9 for each). The authors concluded from these observations that the
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d34S versus d18O ratio of sulfate might be largely controlled by the rates of dissimilatory sulfate reduction, in agreement with Grinenko and Ustinov’s (1990) model. Aharon and Fu (2000) hypothesized that when sulfate reduction rates are highest and fractionation effects small, such as at the gas seeps, kinetic isotope effects, rather than oxygen isotopic exchange with water, are largely responsible for the d34SSO4 and d18OSO4 values. Under these conditions, a plot of d34SSO4 versus d18OSO4 will yield a slope closer to 4. Conversely, Aharon and Fu (2000) speculated that during slow rates of reduction, more oxygen isotope exchange between a sulfate intermediate and water will occur and thus lower this slope. 4.6. d34S versus d18O values of sulfate in the anoxic bottom waters of Framvaren The hypotheses of Aharon and Fu (2000) regarding the kinetic controls of d18OSO4 values during dissimilatory sulfate reduction are insightful; however, they do not completely explain our observations of the deep anoxic waters of Framvaren. Here, we measured a relatively large value of es for sulfate reduction of 41.5xand still observe a slope close to 4 for d34SSO4 versus d18OSO4 (Fig. 5). Based on the results of Aharon and Fu (2000) and other studies (Canfield, 2001; Goldhaber and Kaplan, 1975; Kaplan and Rittenberg, 1964), this large value of es could suggest a slow rate of sulfate reduction. According to Aharon and Fu’s hypothesis, a slow rate would not yield a slope close to 4 as we observe (Fig. 5). However, as previously discussed, the relative availability and type of organic substrates also have important effects on es for sulfate reduction, and es may not always be correlated with sulfate reduction rates (Canfield, 2001; Detmers et al., 2001). As mentioned earlier, we know of no reports of measured rates of sulfate reduction within the sediments or water column of Framvaren fjord. It is possible that the generalizations made by Aharon and Fu (2000) regarding sulfate reduction rates and associated isotope effects may only apply for a given environment where all other parameters (depth, temperature, type of organic matter, water column versus sedimentary environments) are essentially the same. Therefore, we hypothesize that under conditions where dissimilatory sulfate reduction is
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more unidirectional, which would include faster rates, there will be relatively less back reaction at each biochemical step of reduction and consequently less opportunity for oxygen isotopic exchange between reaction intermediates and water. Consequently, during these conditions, a plot of d34SSO4 versus d18OSO4 could have a slope near 4.0. However, unidirectionality of a biochemical reaction is not necessarily restricted to conditions of fast rates. Detmers et al. (2001) suggest that sulfate reduction will be more unidirectional when it is coupled to oxidation of organic substrates that yield a more negative DGj value. These substrates were observed to generally produce a lower value of es for sulfate reduction (Detmers et al., 2001). Low temperatures generally decrease rates of sulfate reduction. However, Canfield (2001) observed smaller values of es for sulfate reduction at lower temperatures. Canfield (2001) proposes that the first step of sulfate reduction, the entry of sulfate into the cell, might become more unidirectional at low temperatures and thus explain this lower value of es. In fact, the relative degree of concurrent forward and back reactions during biochemical reactions represents a major means of regulatory control (Stryer, 1995). The concurrent small changes in the rates of the forward or backward reaction can generate rapid changes in the net forward reaction rate. This is best explained with examples (see below). We simplify our examples by considering only one of the first steps in sulfate reduction, the binding of sulfate to the sulfate reductase enzyme. However, we could have considered any step in the pathway that involves reaction of the oxygen in sulfate
Example A 15 (forward reaction) SO4 X SO4 – enzyme 10 (back reaction) Net reaction: 5
Example B 20 (forward) SO4 X SO4 – enzyme 10 (back) Net reaction: 10
Example C 10 (forward) SO4 X SO4 – enzyme 5 (back) Net reaction: 5
In examples A and B shown, the numbers correspond to arbitrary rates of the forward and reverse reaction. As seen by comparing example A with B, a 33% increase in the gross forward reaction can result in a 100% increase in the net rate of a reaction. Similar changes can also be elicited by lowering the
rate of the back reaction or changing the relative rates of both the forward and back reactions. In example C, the forward and back reactions are each halved with respect to example B, which results in a 50% reduction in the net reaction rate. Although the net rates of sulfate reduction in B and C are clearly different, the relative balance between the forward and back reactions is the same. We hypothesize that these two conditions might result in similar kinetic isotope effects for oxygen and sulfur being preserved in the residual sulfate and may therefore result in a similar slope when d34SSO4 is plotted relative to d18OSO4 during sulfate reduction. Different values of es and eo could still be expressed from shifts in the rate limiting steps of sulfate reduction. Environmental parameters specific to a given site could presumably influence the relative balance of the forward and back reactions of sulfate reduction, the rate limiting steps, and consequently the d18OSO4 and d34SSO4 values. Evidence to support the above hypothesis comes from a recent study by Mandernack et al. (2000b). They observed that the microbial reduction of gaseous N2O to N2 during a soil incubation resulted in a slope of f 0.5 when the d15N value of the residual N2O was plotted relative to the d18O. In this case, the oxygen isotope effect was twice that of the nitrogen and presumably reflects the 1:2 atom ratio of oxygen to nitrogen in the N2O molecule. The reduction of N2O to N2 is a type of anaerobic respiration that is analogous to sulfate reduction, although the reactants and products are gaseous and therefore there is less opportunity for oxygen isotope exchange with water. It appears that N2O reduction is a unidirectional process, perhaps due in part to the chemical stability of the N2 product, which may minimize back reactions from occurring and subsequent oxygen isotopic exchange between the N2O (or N2O – enzyme complex) and water. We hypothesize that a similar phenomena occurs during dissimilatory sulfate reduction when it occurs unidirectionally, including conditions that favor fast rates of sulfate reduction. During these conditions, sulfate reduction will yield a slope near 4.0 when d34SSO4 is plotted relative to d18OSO4, as we observed for the deep anoxic water of Framvaren. If our above hypothesis is correct, it would imply that processes such as Sj disproportionation or reoxidation of sulfide, which would both decrease the slope of d34SSO4 versus d18OSO4 to values < 4
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(Bo¨ttcher et al., 2001; Ku et al., 1999), were not significant within the deep anoxic waters of Framvaren. Therefore, d34SSO4 and d18OSO4 values of sulfate deposits precipitated from euxinic environments and preserved in the geological record might similarly reflect a system where sulfate reduction was a dominant and unidirectional process (m = f 4.0), or where reoxidation of sulfide, sulfur disproportionation, and/ or oxygen isotope exchange reactions with water during (non-unidirectional) sulfate reduction also occurred (m < 4.0).
5. Conclusions Variations in the d34SSO4 and d18OSO4 values are relatively small across the oxic – anoxic interface of Framvaren fjord, although a distinct minimum in d34SSO4 was observed at 20 m depth, consistent with sulfide oxidation, and small enrichments in d34SSO4 and d18OSO4 3 m beneath this depth are consistent with possible sulfur disproportionation. At water depths >24 m, the d34SSO4 and d18OSO4 values steadily increased with depth in response to dissimilatory sulfate reduction. Estimates for es and eo of 41.5xand 9.8x, respectively, for sulfate reduction were obtained from Rayleigh plots. The value for es closely approximates the observed difference between the d34SSO4 and d34SSH2S values near the oxic –anoxic interface. Therefore, a closed system model appears to provide a good approximation of sulfate behavior in the deeper anoxic waters of Framvaren. Consequently, for the deep waters of Framvaren, it is difficult to reconcile our 1993 d34SSO4 data and the 1982 d34SSO4 data of Anderson et al. (1988) with the 1983 d34SSO4 measurements of Anderson et al. (1988). The 1983 d34SSO4 measurements are approximately 10xdepleted relative to both the 1982 and 1993 data. Oxidation of sulfide in the deep bottom waters between 1982 and 1983 does not adequately explain this 10xdepletion. From our measurements made in 1993, a plot of d34SSO4 versus d18OSO4 from water depths >24 m provided a linear relationship with a slope of f 4.4. We hypothesize that this slope results from kinetic isotope effects associated with sulfate reduction, which proceeds unidirectionally in the deeper anoxic waters of Framvaren, and approximates the 4:1 ratio
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of oxygen to sulfur in the residual sulfate. Plots of d34SSO4 versus d18OSO4 from ancient euxinic deposits might provide similar information regarding the biogeochemical controls of sulfur cycling in the geological past. For comparable water depths, the d34STRS of the sediments in Framvaren are consistently lower by f9xthan the d34SSH2S of the water column. As originally proposed by Saelen et al. (1993), the low d34STRS values for the deep sediments could be derived from a mixture of sulfide derived from shallow and deep waters with lower and higher d34SSH2S values, respectively. However, this does not adequately explain the lighter d34STRS values in the shallow sediments relative to d34SSH2S in the water column. Sulfur disproportionation reactions, which can produce sulfide that is very depleted in 34S, in the shallower sediments just beneath the chemocline might provide an alternative explanation, although these reactions are not likely to occur in the deeper sediments of Framvaren. Additionally, we hypothesize that different rates of sulfate reduction, both interstitially in the sediments and within the water column, may explain the consistent depth-dependent offset between sedimentary d34STRS and water column d34SSH2S values. Acknowledgements We thank Drs. Wayne, C. (Pat) Shanks and Vladimir Grinenko for their insightful comments regarding this manuscript; for resources provided by Dr. Mark Morgan, and Maria Mihailescu, Jesusa Overend-Pontoy, and Nenita Lozano for stable isotopic analyses. The authors are also grateful for the helpful comments of Dr. Robert Raiswell, Dr. Timothy Lyons, and an anonymous reviewer. [EO] References Adams, C.A., Warnes, G.M., Nicholas, D.J.D., 1971. A sulphitedependent nitrate reductase from Thiobacillus denitrificans. Biochim. Biophys. Acta 235, 398 – 405. Aharon, P., Fu, B., 2000. Microbial sulfate reduction rates and sulfur and oxygen isotope fractionations at oil and gas seeps in deepwater Gulf of Mexico. Geochim. Cosmochim. Acta 64, 233 – 246. Albert, D.B., Taylor, C., Martens, C.S., 1995. Sulfate reduction rates and low molecular weight fatty acid concentrations in
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