Manganese scavenging and oxidation at hydrothermal vents and in vent plumes

0016-7037/93/$6.00

Geochimica et Cosmochimica Ada Vol. 57, pp. 3907-3923 Copyright 8 1993 Pqamon Press Ltd. Printed in U.S.A.

+ .OO

Manganese scavenging and oxidation at hydrothermal vents tid in vent plumes KEVIN

W. MANDERNACK*

and BRADLEYM. TEBO

University of California, San Diego, ScrippsInstitution of Oceanography, Marine Biology Research Division, La Jolla, CA 92093-0202, USA (Received July 20, 1992; accepted in revisedform March 28, 1993)

Abstract-Hydrothermal vents provide a major source of dissolved Mn(II) to the oceans, where concentrations range from 5 mM within the 35O’C hot smokers to just above ambient seawater concentration in far field vent plumes. The Mn( II)-rich environments within warm vents and vent plumes provide a suitable habitat for Mn( II) oxidizing bacteria. In order to compare rates of scavenging and oxidation of Mn( II) proximally within vent fields (~30 m from venting water and temperatures <16”C) and distally within vent plumes, and to determine the relative contribution of microbes, incubation experiments using “Mn as a radiotmcer were conducted in situ and on collected water samples from three hydrothermal vent locations: the Guaymas basin (GB ) , the Galapagos spreading center (GA), and the Endeavor Ridge of the Juan de Fuca spreading center (JDF). Both the adsorbed and oxidized fractions of the total %Mn scavenged were determined and found to often be significant (as high as 65 and 7496, respectively). Manganese scavenging rates were generally higher in in situ incubations than in incubations conducted on board ship. Inhibition of “Mn scavenging by sodium azide provided evidence for microbially mediated Mn( II) uptake and oxidation in waters both proximal (GA and GB) and distal to the vents (GA and JDF) , even at distances as great as 17 km from the ridge axis at JDF. The highest manganese scavenging rates were observed within the vent fields (up to 2.5 nM/day). The residence times of dissolved Mn( II) were shorter in the GB and GA vent fields (26 and 28 days) than in the JDF vent field ( 1.4 years). This difference may be due to different mechanisms of Mn(I1) precipitation in operation. At the GA vent field Mn( II) precipitation was often strongly inhibited by sodium azide and therefore apparently due to microbial activity. In contrast, Mn( II) scavenging within the JDF vent field was not significantly al&ted by sodium azide. Because 54Mn scavenging in the JDF vent field was dependent on the presence of oxygen and a much larger fraction of the total %Mn scavenged was adsorbed than oxidized, manganese scavenging appears to occur primarily by an abiological mechanism, perhaps coprecipitation with iron oxyhydroxides. In comparison to the vent fields, Mn( II) scavenging rates were lower within the vent plumes (co.6 nM/ day for GA and ~0.2 nM /day for JDF), whereas residence times were not significantly different (as low as 34 days for GA and 1.O years for JDF) . The short residence times (90 and 118 days) and high microbial activity measured in bottom waters beneath the vent plumes at GA and JDF probably resulted from enhanced scavenging by manganate-coated bacteria that settled out from the vent plume and accumulated near the bottom. Therefore, bacteria not only enhance the scavenging of Mn within vent waters, but also facilitate Mn deposition to the sediments. INTRODUCTION

theoretically the energy yield from the reaction is sufficient to support microbial chemoautotrophy; however, this process remains unproven ( NEALSON et al., 1988). At hydrothermal vents reducing hydrothermal fluids rich in Mn(I1) mix with the oxygenated ambient seawater and provide conditions suitable for microbial manganese oxidation. There is a gradient of dissolved Mn( II) from endmember values of l-5 mM in 350°C hot smokers (EDMOND et al., 1982; VON DAMM and BISCHOFF, 1987) to 5-600 nM in vent plumes (BAKER and MASSOTH, 1986; KLINKHAMMER et al., 1985, 1986; KLINKHAMMER and HUDSON, 1986; COALE et al., 1991). In warm lo-20°C vents, such as at Galapagos, the concentrations are around lo-40 PM (JANNASCH and MOTTL, 1985; JOHNSON et al., 1988). Previous reports of Mn (II) scavenging or oxidation within vent fields and therefore evidence for microbial Mn( II) oxidation are lacking. Although measurements of Mn( II) concentrations within and near the Galapagos vent fields were strongly correlated with dissolved silica, suggesting conservative Mn behavior (JOHNSON et al., 1988), transmission electron microscopy of manganate coatings found on shells and rocks in the immediate vicinity of the venting water at GA suggest that bacteria may be catalyzing Mn( II) oxidation

EVIDENCEHAS BEENPRESENTEDin recent years that indicates Mn( II) oxidation in the marine environment is largely microbially catalyzed ( NEALSONet al., 1988). Accelerated rates of microbially catalyzed Mn ( II) oxidation result in residence times of Mn( II) with respect to oxidation that are much lower than expected from chemical mechanisms (EMERSON et al., 1979, 1982). Microbially mediated manganese oxidation is especially evident in reducing environments where Mn(I1) concentrations are elevated, such as near oxic-anoxic interfaces within sediments and in anoxic basins ( EDENBORNet al., 1985; TEBO, 1991; TEBO and EMERSON,1985,1986; TEBO et al., 1984). At the manganese oxidation zone within these environments bacteria rapidly oxidize the soluble reduced Mn(I1) to the more oxidized particulate forms whose oxidation states approach +3.4 (GRILL, 1982; EMERSONet al., 1982; TEBO et al., 1984). This oxidation is exergonic, and

* Present address: Institute of Marine and Coastal Sciences, Division of Pinelands Research,RutgersUniversity,PO Box 23 1, New Brunswick,NJ 08903, USA.

3907

K. W. Mandernackand B. M. Tebo

3908

(JANNASCH and MOTTL, 1985; JANNASCHand WIRSEN, 1981). In addition, EHRLKH (1983, 1985) has isolated Mnoxidizing bacteria from both the Galapagos and 2 1“N East Pacific Rise vent sites. COWEN et al. ( 1986) first reported direct evidence for microbially mediated Mn( II) scavenging within a vent plume at the Southern Juan de Fuca vent site, and electron micrographs made on particulate material collected from the plume revealed the presence of Mn-coated bacteria. Similar observations were made on the hydrothermal plume in the Guaymas Basin, where estimated Mn( II) residence times of 4 days to 2 weeks was thought to be the result of rapid microbial scavenging (CAMPBELL et al., 1988). Using 54Mn( II) as a radiotracer to directly measure the uptake of dissolved Mn( II) into the particulate fraction, we conducted rate measurements of Mn(I1) scavenging and oxidation at hydrothermal vents and in vent plumes. Our measurements were made within the low temperature regime (~16°C) of vent fields, in the buoyant plume, at various distances from the ridge axis within the nonbuoyant portion of the plume (to distances of 17 km at JDF), and in near bottom waters collected beneath the vent plume. Although measurements on each of these environment types could not be completed at every vent site, the extensive geographical sampling of this study permits comparisons of manganese scavenging and oxidation to be made both within and between each vent location. In particular, we report here the first direct measurements of manganese scavenging within the low temperature portion of the vent fields and ascribe the microbial significance of this process. The importance of Mn( II) scavenging proximally within the vent field as it may atfect Mn( II) scavenging and deposition distally throughout the vent plume is discussed.

86”09.21O’W) vent fields, and by hydrocast within the surrounding vent plume at distances
ExperimentalApproach Rate measurements and turnover times for Mn(I1) scavenging and oxidation were made both in situ and on deck by incubating collected water samples with “Mn( II). We define scavenging as the total Mn( II) bound into the particulate phase as a result of all processes, including oxidation, adsorption, coprecipitation with other mineral phases (i.e.. iron oxides or oxyhydroxides), and cellular uptake. Mn( II) adsorption can occur on a variety of charged surfaces, including inorganic (mineral surfaces) or organic (bacteria membranes and cell walls), and thus could contribute significantly to the total Mn( II) uptake within vent environments. Mn(III, IV) manganates themselves also adsorb Mn( II) by virtue of their charged surfaces and high surface area. We have attempted to assess the relative contribution of these processes to the total rate of Mn( II) uptake in vent environments (see the following text) in order to better understand the mechanisms of Mn( II) scavenging.

METHODS Sample Collection and Preparation Description of Study Sites The data presented here were collected during four independent cruises in 1988 to three uniquely different vent locations. The three cruises to the vent fields, which required use of the submersible R/V Alvin for collection of vent water samples and the deployment of in situ devices, were all aboard the R/V Atlantis II. The first expedition was made to the Guaymas Basin (GB; B. Simoneit, Chief Scientist), centered at 27”OO’N, 111”24’W, from Feb. 20-24. Positioned in a basin of high organic productivity, the GB vent site is unique by being blanketed with a thick layer of organic-rich sediments. The interaction of the venting hydrothermal water with these sediments results in the precipitation of Fe and other highly insoluble metal sulfides at depth (VON DAMM et al., 1985b). Consequently, the vent waters emitted at the sediment-water interface are relatively enhanced in metals such as Mn( II) that form more soluble sulfide phases. Mn( II) concentrations of 128-236 pmol/kg have been reported from the hot ( lOO-315“C) vents of GB ( VON DAMM et al., 1985b). A single deployment of our in situ incubator was made 130 m from venting water. In addition, water samples for on deck incubations were collected from the vent fields with Alvin. The second cruise was to the low temperature Galapagos (GA) vent fields durina A~t-i14-Mav 8. 1988 (J. Childress. Chief Scientist j. The relatively low temperat&e.s~ at GA are thought to be the result of extensive subsurface mixing, which promotes the precipitation of Fe and metal sulfides at depth ( EDMONDet al., 1979b). Therefore, as at GB, Mn( II) is enriched relative to other metals within the vented waters, although its concentrations are lower ( 10-40 PM) than at high temperature vents ( JANNASCHand MOTTL, 1985 ) . During the GA cruise, water samples were collected within both the Rose Garden (O0°48.247’N, 86”13.478’W) and Mussel bed (OO”47.894’N.

Although water was sampled in close proximity to the vent fields (sometimes at 1 m above the venting water at GA), due to rapid mixing the temperatures were generally near that of the ambient seawater (2°C). An exception were those collected at moderate temperatures ( 16°C) within the JDF vent field. Vent field samples for on deck incubations were collected by Alvin using 1.7 L Go-flo bottles. At JDF, the vent plume was located with a CT’D-transmissometer and sampled with a rosette of 30-L Go-flo bottles. GA samples were collected with 5-l niskins mounted directly to the hydrowire. At GA no CTD-transmissometer or rosette was available. Consequently, the absolute depth at which the sample was collected is not known. Instead, what has been recorded is the meters at which the sample was collected off the bottom, as determined with a pinger during collection. Plume waters at GA were verified by their enrichment in dissolved manganese relative to ambient seawater. The collected waters were incubated either on deck in 1or 2.5 L acid-washed polycarbonate or polypropylene bottles, or in situ (seethe following text). All on-deck incubations were made in a covered 2°C cooling water bath except for the JDF vent field samples which were incubated at 16-17“C in a refrigerator. Incubation Experiments with “Mn( II) Mn( II) turnover times and scavenging rates were determined by using radioactive 54MnC12as a radiotracer to measure the transformation of dissolved Mn( II) into the particulate phase (as defined by that being trapped on 0.22 pm Nucleopore MF filters). In the literature, the process is variably referred to as particulate manganese formation, Mn( II) binding or uptake, Mn( II) scavenging, or manganese precipitation. In order to assess the microbial importance of

Scavenging and oxidation of Mn in hydrothermal manganese uptake, sodium azide (pH adjusted to 7.6L8.0 with HCI) was added at 10 mM final concentration to a duplicate portion of the water sample 10 min prior to addition of the radiotracer. Sodium azide, a metabolic inhibitor, is a suitable poison for manganese uptake experiments since it interferes little with the solution chemistry of manganese (EMERSONet al., 1982; ROSSONet al., 1984). However, azide may inhibit different strains of Mn-oxidizing bacteria to different extents, and the different mechanisms of microbial manganese oxidation ( NEALSON et al., 1988) may have different sensitivities to azide. All in situ experiments were amended with 5-10 pL of a 0.4 mCi/ mL stock solution of 54MnClz (specific activity 50.65 mCi/mg; New England Nuclear) resulting in a net increase in Mn(I1) concentration of 0.3 f-O.63 nM. The amount of Mnf II) added is insignificant for most of these Mn-enriched vent waters. Amendments of the “Mn stock solution to the 2.4 L JDF and GA plume samples were 0.52 and 1.31 nM 54MnClz, respectively, which may have affected the results for Mn scavenging of certain samples with low Mn concentrations. On-deck incubations of GA and JDF vent water, whose manganese concentrations were much higher, were amended with 1.77-2.25 nM and 9.6 nM “MnClz, respectively. Man8anese concentmtions varied between 60-656 nM within the GA vent held and between 0.4- 1.5pM for JDF. After inoculation of the water samples with “Mn, subsamples at various times were filtered through 0.22 pm Nucleopom MF membrane filters, washed twice with 0.2 hrn prefiltered seawater, and the filters retained for gamma counting. For all incubations made on deck, a sample was filtered at TO, within 5 min after addition of the radiotracer, and the counts were subtracted from the counts of subsequent time points. This corrects for the initial rapid “Mn( II) binding and exchange that occurs. For the experiments, 50-1000 mL subsamples were filtered, usually in duplicate, depending on the availability of the water. The filters were placed into 5 mL gamma vials, to which was added 4 mL of a 0.1% hydroxylamine hydrochloride ( H-HCl) solution. The H-HCl serves to dissolve the particulate manganese on th+ filters and disperse it evenly within the vial to maintain the same geometry for all samples during counting Duplicate 4 mL subsamples of the incubations were also collected in gamma vials at each time point for total counts of mdi~~vity. Fifty microliters of 10% HHCl (0.125% final) was added to these samples prior to counting. The portion of particulate “Mn present on the filters per given period of time was computed as a percent of the total “Mn( II) added (%/ time) and provides an estimated turnover rate.

In Situ Measurements

with the WSD

The water sampling device ( WSD) consists of a pair of 6 L bottles, constructed of PVC and Lucite, mounted to an aluminum frame (Fig. I ). The bottles were kindly loaned to us by M. Mullin of Scripps. The bottles are assembled with stainless steel screws and glued with epoxy and PVC cement. The lids of the bottles are spring loaded with a 3” X M” 3 16 stainless steel spring and operate similarly to a niskin bottle. Upon closure, the lids depress the shaft of a 50 mL PVC/Lucite syringe containing azide and/or the radioisotope, and release the contents into each bottle at depth at the beginning of the incubation, The enclosed cartridge of the syringe was fitted with a small gasket fitted piston which could move in and out in response to water volume changes due to changes in pressure and prevented jamming due to negative pressures that might otherwise develop within the syringe. The aluminum frame consists of a central shaft with another shaft mounted to it crosswise, to which the bottles were hose clamped at each end within hemicylindrical sleeves. The sleeves could be rotated 90” so that the bottles could be oriented either in a horizontal or vertical position. The bottles were positioned vertically during hydrocast use and horizontally during Alvin deployments. To the central shaA was bolted a release mechanism from a 30 L niskin bottle providing an easy means to mount the entire WSD onto a hydrowire or a 30 L rosette (Fig. I), and to which the lanyards of both bottles could be triggered simultaneously during deployment. The aluminum frame with the attached bottles could also be mounted onto an aluminum tripod for Aivin deployments. The bottles were tripped either manually with Alvin, or with a messenger during hydrocast use.

3909

solutions

syringe assembly anmpling tube

FIG. 1. One bottle of the water sampling device for measuring rates of Mn( II) scavenging and oxidation in situ in vent fields and vent plumes. Usually two bottles are mounted on a frame and tripped simultaneously for poisoned and unpoisoned incubations. The frame can be attached to a CTD rosette or hydrowire for hydrocast deployment or deployed on a stand by Alvin. Syringe assembly is shown in the partially open position, Drawing after NAPP ( 1986).

To determine whether pressure affected manganese oxidation within vent environments, at JDF a direct comparison was made between identical water samples incu~t~ in situ vs. on deck. This comparison was accomplished by mounting on the rosette 3-30 L Go-Ilo bottles alternately with each WSD used for in situ experiments permitting replicate samples to he collected at three different depths within the vent plume. Water from the Go-flo samples, however, could not be collected for the on deck incubations until. termination of the in situ incubations and resulted in a IO hour delay before commencement of the on deck experiments. Chemical Mensurements To compute manganese uptake rates from the percentage of “Mn trapped on the filters, dissolved Mn(II) measurements (dMn) were made on 0.2 m filtered subsamples (Nucleopore polycarbonate Iilter) of the incubated water. The water was collected, filtered, and acidified (Ultrex HCI) using clean techniques and acid washed lab ware. Mn( II) measurements were made (with standard additions) by direct injection of the samples into a graphite furnace atomic absorption spectrophotometer. Mn(I1) and.iron concentrations at JDF were obtained by similar techniques, and were provided by Bob Collier and John Sharpe (SHARPE,1991; SHARPEet al., 1993). Determination of Mn( II) Oxidation Rates To estimate the fraction of the total Mn(I1) bound on the filters that was adsorbed vs. oxidized, at certain time points two additional subsamples were collected and treated according to the methods of

K. W. Mandemack and B. M. Tebo

3910

IncuM3 water samples wltll Ml-!%

No oxygen

+ Oxygen

Total Mn-54

Nonexchangeable ml-54

Refractilek&-g4

FIG. 2. Summary of the methods employed to measure Mn(I1) scavenging, adsorption, and oxidation and microbiahy mediated Mn( II) scavenging (MMMS; seetext).

SUNDA and HUNTSMAN( 1987) prior to filtering (Fig. 2). To one

subsample an excess of “cold” (nonradioactive) MnC& ( IO-50 PM final concentration) was added to exchange adsorbed “Mn( II) with cold Mn(II) for a minimum of 1.5 h. Thus, by comparing these samples with a no treatment control, an estimate of the adsorbed fraction can be made. A~~t~on~ exchange experiments were conducted on vent plume samples collected from JDF, substituting the 10 PM MnClr with 10 NM CuSO, because it had been effective in previous studies and thought to be a more efficient and faster exchange medium ( BROMFIELDand DAVID, 1976; R~SSON and NEALSON, 1982). JDF vent field samples were also incubated in the absence of oxygen to assess by an alternate means the ~n~bution of adsorption towards Mn( II) uptake (see the following text). A second subsample received equimolar additions of ascorbic acid and NaOH (300 PM final concentration) and was filtered after 0.5 h. Ascorbate (pH 78) which does not complex Mn( II), selectively reduces manganese relative to iron oxides releasing both oxidized manganese and Mn(I1) adsorbed on manganese oxides into solution (SUNDA and HUNTSMAN, 1987). Therefore, most of the %Mn tbat remains on the filters after ascorbate treatment has been incorporated intracellularly or coprecipitated with other minerals. Comparison of the ascorbate treated samples with those treated with the cold MnCh provides an estimate of the rate of formation of oxidized manganese, Ascorbate treatment was made on all samples except those collected within the JDF vent field. The times at which the “cold” M&l2 and ascorbate treatments were administered varied between experiments, but are noted for each in the legends to the tables. For some experiments (GA, on deck), these treatments were made for at least three time points, to which a linear regression could be applied. These methods can be summarized as follows: ( 1) T,, - iw,= fraction of Mn(II) a&orbedand (2) M, - A,, = fraction of Mn( II) oxidized, where T,, is the to&I YMn trapped by the filter at time n (corrected for TO) and M, and A,, are the amounts of YMn on the filter after Mn and ascorbate treatments, respectively (Fig. 2). Data Interpret&on

From our 54Mn radiotracer experiments we were able to estimate Mn( II) turnover rates, residence times, scavenging rates, and oxidation rates. The turnover rate is a measure of the percent Mn(I1) bound into the particulate phase per unit time. If the rate at which Mn (II f is scavenged onto particles greatly exceeds the revere rate by which Mnf II) is released from particles, and the initial dissolved %Mn concentration equals the total “Mn concentration, then expression of the turnover rate as a fractional value yields the estimated

k,, the forward rate constant for Mn(IIf scavenging (COWEN et al., 1990). The reciprocal value of k, yields the Mn( II) residence time with respect to scavenging. The manganese scavenging rate can be estimated by multiplying ki by the ambient manganese concentration. Based on our cold Mn and ascorbate treatments we calculate the percentage of the total manganese scavenging rate that is due to oxidation or adsorption. In order to compare results from different experiments, the estimated turnover times from each experiment were extrapolated to 24-h intervals. For time course experiments, this was calculated from the linear regression that was fitted to the data. During the time course incu~tion~ Mn(I1) uptake often became nonlinear and after 20 h approached saturation (Fii 5 and 7). When saturation occutred, the final one or two time points (23 h and greater) were omitted before applying the linear regression. For single time point experiments (10-h incubations of JDF vent plume and all in situ experiments), turnover rates and residence times were estimated from the filtered samples after subtracting the To value (not sub~cting 7’, yields an apparent turnover rate or residence time). As a To sample could not be collected for the in situ experiments, To values measured from similar water samples incubated on deck were subtracted from the in situ measurements. Since sample size and availability was limiting, To filtrations werenot made for the on deck incubations of JDF vent field water. However, subeamples from here were incubated in the absence of oxygen, in order to assess the amount of uptake due to nonoxidative (i.e., adsorptive) processes (TEBO and EMERSON, 1986; TEIKIet al., 1985). The amount of uptake measured during 24-h “no oxygen” incubations closely approximates the T,, values from the other experiments. Therefore, the “no oxygen” value from each JDF vent held sample was subtracted from the total measured uptake. At GA, some of the filters that were retained for gamma counting were accidentally discarded before being counted. However, because these experiments had also been spiked with ‘% as part of a dual label study, the samples had previously been counted on a LKB 12 I9 liquid ~intillation counter. From spectra1 analysis or channel ratio comparisons of the scintillation counts among different experiments and due to the nature of our sampling scheme (ascorbate treated filters remove virtually al1 of the r4Mn signal without affecting that from “Cc), we were able to convert the scintillation counts derived from the 54Mn to gamma counts with a good degree of confidence. While there may be some error with these estimates, resufting in manganese residence times that are low, we believe the error is minimal. Therefore, rather than discarding the results derived from scintillation counting, we present them in the tables designated with a

3911

Scavenging and oxidation of Mn in hydrothermal solutions

In comparison, at the JDF vent field, where inhibition by azide was relatively low ( 20% average), residence times were correspondingly higher (Table 1) . Scavenging rates. Rate measurements were made only within the vent environments at JDF and GA where samples for dissolved manganese measurements were also collected. The results indicate that for both vent locations, higher uptake rates were found within the vent fields as compared to the vent plumes. For four samples collected at JDF, rates varied between 0.37-2.48 nM/day, while five samples collected at GA ranged from 0.14-2.41 nM/day (Table 1; Fig. 8). Although the maximum and minimum rates measured for each location are very similar, the mechanisms of oxidation at each appear to be different. At JDF, where in situ incu~tion temperatures were 16°C and manganese scavenging was weakly inhibited by sodium azide, the process appears to be mostly abiological, In contrast, at GA where temperatures were 2°C high potential for MMMS activity was observed in some of the samples. For example, in the sample from Dive 20 14, a rate of 2.4 1 nM /day (and 70% azide inhibition) was measured (Table I, Fig. 2). These results are significant, since they indicate that Mn(II) scavenging and removal is occurring as the warm water is vented from its source. The particulate manganese phases formed are also carried within the venting water where they can further enhance manganese oxidation by autocatalysis. Oxidation rates. Estimates of the percentage of the par-ticulate manganese formation rate that was due to oxidation and adsorption made using ascorbate and cold manganese treatments are presented as a percentage of the total Mn( II) scavenging rate (Tabie 1). At the GA vent field, values for the percentage of the rate due to oxidation varied from 5% to as high as 68%, while adsorption contributed from 8 to 63% of the total scavenging rate. This high variability would be expected from the heterogeneous nature of vent fields. However, an unexpected result came from sample D.2014, which had the highest microbial activity within the GA vent field, but a relatively low oxidation percentage. Only 34% of

footnote. Inclusion of these results better reveals trends in the data. However, we confine most of our discussion of the upper and lower limits of our measured values to those samples which were gamma counted. RESULTS

Rates and Residence Times of Dissolved Mn in HydrothermalVent Environments

~ve~~/O~ti~ Vent Jields

Residence times. Our rate measurements and estimated residence times for dissolved Mn incorporate all processes accounting for Mn(f1) uptake, including adsorption, oxidation, cop~ipi~tion with other mineral phases, and to a lesser extent, intracellular incorporation into cells. There was a wide range in estimated residence times for samples collected within a given vent en~~nment (Tahle 1). Variations were as great as 28 days-K2 years for the GA vent field, 1.43.3 years at JDF, and ranging from no measurable uptake (data not shown) to 26 days for a single in situ experiment made at GB. The shortest residence times of all of the vent environments sampled within this study were those measured within the GA and GB vent fields (28 and 26 days, respectively ) . Azide inhibition of total particulate 54Mn formation, a qualitative indicator of microbial activity, was observed in all the GA vent field samples when tested (Fig 2 and Table I ). Azide inhibition was as high as 70% when compared to an unpoisoned sample cohected at GA during Alvin dive 2014 to Musselbed, the unpoisoned sample had the shortest measured residence time (28 days) and highest scavenging rate (2.4 1 nM f day, see the following text). In general, samples with high microbial activity also had low residence times and higher rates of scavenging. Although the single in situ experiment conducted at GB was not successfully complemented with an azide-poisoned control, the short residence time measured there (26 days) strongly suggests microbially mediated manganese scavenging ( MMMS ) , in agreement with the results of CAMPBELL et al. ( 1988) for the GB vent plume.

TABLE1. _8 sample

~tJAWA@

summaryof ~~~

Time Mn(ll) (N WV

27.6

tc 0.2014 E 0.2024 0.2027 103 D:202pnb D 2008a’b 31.8

t; ;;

In Vent FWds

%lxue&8to: Residence %azidee time inhibilion adsofption oxidation (%. d-11 InM. d-11 (warn)

Tumrver Sea~&ng

Rate

N.D.

3.79

N.D.

0.1 (26d)

N.D.

26

67 :z

3.59 z

0.1 (28d)

70:

63

666 198

0.03 0:72

2.41 1.36 0.60 0.20 1A3

36fJ E N.D.

4:

ymsb ERDkAVOR Rltk8e 4; 40 41 42 41

Exgmhds

1::; :z

d, o*5P 0.4ii2” d) .

0.24

0.14

1.2

0.06 0.17 0.19 O.li

0.37 2.48 1.60 0.56

3.3 1.6 ::t

N.D.= NotDetem~inad

:: 5

:

;:

49

47

45

z: 26 12

z;

wblwtd@olW~~i~~ncumts s edds itibiabn b6Sedon endpoint detenninalions, not subtracling TOV&MS. ~~~~~~~_~

t~=6~~e~~~on~

74

3:

~28 <73 <30 <39

3912

K. W. Mandemack and B. M. Tebo 3.0 Dive 2014

2.0 -

(b)

I 0

5

10 Time (H)

15

0

5

10

15

0.0

20

(C

-

0

5

15

10

The

The (H)

20

25

:

(H)

FIG. 3. (a, c) Time course of 54Mn(II) removal in Galapagos Vent Field samples incubated on deck at in situ temperatures of 2°C in the presence (m) and absence (0) of sodium azide. The degree of inhibition by azide is a qualitative indicator of the microbial intluence on Mn (II) scavenging. (b) Time course of 54Mn(II) scavenging and oxidation in a Galapagos Vent Field sample. Subsamples were treated with 300 pM tinal ascorbate (m) and excess “cold” non-radioactive Mn( II) (0) at approximately 3- and 8-hour time points. The difference between the untreated sample (0) and the cold Mn( II) treatment reflects the degree of Mn( II) scavenging due to adsorption, while differences between the Mn( II) and ascorbate treated subsamples reveals the amount of Mn( II) removed by oxidation.

the manganese scavenging rate was due to direct oxidation while adsorption alone contributed 63% within this sample (Table I and Fig. 3). A contrasting result was observed at GB, where MMMS activity is believed to be high: 74% of the scavenged manganese within the in situ experiment was due to oxidation and only 26% could be attributed to adsorption. Ascorbate treated samples were not completed on samples collected within the JDF vent field, and therefore the percent rate due to oxidation could not be. calculated as described in the preceding discussion. However, results from the MnClz treated samples indicated that the majority of the uptake was due to adsorption (Fig. 4). For three of the four samples, adsorption accounted for 6 l-72% of the uptake, and only 27% in the fourth (Table 1). This adsorptive driven process is strongly controlled by the presence of 02, since manganese scavenging was greatly retarded when subsamples were incubated under anoxic conditions (Fig. 4). Although the oxidation percentage of Mn(II) appears to be relatively low within the JDF vents, it is conceivable that the oxygen-dependent rates observed there would result in the formation of some newly formed manganese oxides which provide a high surface area for subsequent adsorption. Alternatively, manganese may be coprecipitated with some other oxide phase, possibly iron oxide, which forms in the presence, but not absence, of O2 .Vent Plumes Residence times. MMMS was comparably high within the GA vent plume as within the vent field; the range and average values for the percentage of azide inhibition of Mn ( 11)binding were similar for both environments (Tables 1 and 2). Likewise, short residence times of 34-82 days were measured from the in situ hydrocasts made within the GA vent plume. The on-deck experiments consistently yielded longer residence times, ranging from 1.2-3.3 years. Although there were several samples collected at JDF for which Mn( II) removal was low or not detectable, significant binding occurred in most of them (Table 2 and Fig. 5 ). This

resulted in a wide range of estimated residence times, from I- I5 years (Table 2 ). The variability was greatest in the buoyant portion of the plume immediately above the vent source where both the shortest and longest residence times were measured. While MMMS activity was apparent in samples from all locations within the vent plume, overall it increased with increasing distance from the vent. The average percentage of azide inhibition from all on deck experiments conducted in the O-2 km region was 22% (n = 13), in contrast to corresponding values for the 4-17 km region of 47% (n = 12). Notably high MMMS activity (67-70% azide inhibition) was measured within a sample collected 17 km from

1

-_ 80 70 60 50 40 30 20 10 0

’

no 0,

Mn

’

Azide

treatment n q

above tube worms above microbial mat

B

1m above smoker

q

1 m above smoker

FIG. 4. The effect of excess “cold” Mn( II) and no oxygen treatments on four samples collected from the vent fields at Endeavor Ridge, Juan de Fuca. Results are expressed as a percentage of the control experiments (untreated samples). Experiments were conducted on deck at in situ temperatures of 16°C.

Scavenging and oxidation of Mn in hydrothe~~

3913

solutions

Table 2. Summary of Mng) Scavenging Experiment8 In Veht Plumor &nit Surrounding Waters location

&

Hvdrocast No.

Km fmm v*n$

Depth Imt

.’

Time fH)

‘*

Mn(ll) Turnover Scavenging Residence % a&de % rate due toe TW hhhithnd ad-t& oxidation ink41 Rata Rate - ’ [q&.&1) [o M . d-11 &ears1

GALAPAGOS: “New Vent” ‘: 1.2

1

lAC

1.2

210 310 210 310

mab mab mab mab

l.c.

6? 6:3

16.4 6.8 12.7 11.1

0.00

13.6 15.6 188.1 135.8

36

0.23 i .4a 1.22 0.12 0.21 2.97 2.58

1:: 614:6 234.9

Zt 46 65

ii 43

43 46 ii

Rosa Garden b: t.c : 3 c.e dw ENDEAiOR 12

0.5 0.6 0.6 tx9 RIDGE, iiF: 0

2

0

1

0

4

16 9

0

0

2

6

4

5

4

11

17

10

17

300 168 mab 180 mab 145 mab 2132 2024 1848 2192 2074 2091 1943 1907 2031 1966 1878 2004 2175 2166 2043 1900 1866 2126 2060 2181 2095 1892 2072 2040 1937 2226 2060

6; 7:a

E 20:7 9.1

t.c. t.c.

50.4 65.7

ICE 10:2 t.c. t.c.

6:: 56:6 48.9 73.0 41.4 50.3 48.2 16.0 64.4 51.4 46.3 57.3 52.7 17.9 21.9 32.9 20.2 36.2

1E 13:2 13.4 10.5 10.8 14.4 15.0 15.3 15.0 9.3 9.5 13.7 14.0 14.2 10.3 10.5 10.6 13.6 13.7

2E 23:6 14.6

U.D. 0.05 0.05 0.08 0.02 0.14 0.26 0.08 U.D. U.D. 0.06 E ok4 U.D. 0.03 U.D. 0.04 0.05 0.04 U.D. 0.06 ::: U.D: 0.12 0.04

::

U.D. 3Y.Y 417 51 .O 10.0 70.9 192.0 35.1 E: u”:: U.0: 17.3 U.D. 17.0 U.D. 0.4 16.6 :::. I?:;: U.D: 1::: 5.2

U.D.

NX. 0 0 E 53. -

ii LE U:D: 17 -

ii. -

U;. -

0

so

x U.D.h

tt U.0.h

3s ;$I

46tl $,

U:D:h N-D.’ N.D.’

U:D:! N.D.! N.D.’

1::: BENEATH VENT PLUME: 0.6 t.c. 4.1 1.11 Galapagos, H.C. 5 68 mab 45.3 0.2 (90 d) 42 13.6 JDF. H.C. 5 4 2356 7.1 60.2 0.3 (118 d) 0.65 38 13 4 JDF, H.C. 6’ 2353 9.1 9.1 0.22 34 44 20.3 I.._ 54 : “NewVenl” located at 00°4&15’N. 86”13.2W; plume waters coflected near it were al them dsgme latitude and bngitude. _ Rose Garden lmaled at OO”48.247N. 86”13.478’W; plume walwsmllectednearit wereat thesamedqree lalil!xieandlargilude. s.

dexpeffmnts

conducred in situ e%azideinttibitionitbBsedonttu,encpointoftotalfillarbound~nandisnotmnactedk#To. results obtafned from sdntfffaion counts I Mn scavenging may have been hfgh due lo the settling and enrfchment of particles in sar+e during in sku inoubatfons. “, Bold lace print in the final 2 columns indites samples for which Mn and ascotbaw lmaensnts were very effective, sac text. The cokl Mn and ascorbate treatments signiftcantfy m the partkufate =Mn tn these samples. however,because subtraction of the To resulted in not net measureabfs scavenging. the percentages 01the rates due to adsorption md oxidation couU not be assfgned. i Coid Mn treatment were not performed on these samples and hence they are indiceted as N.D. (not determined). However, Cu was used as a desorbfng agent end it was very effective as was ascotbate. -, Ihe c&f Mn and ascorbate treatma&werenoteifective and thus pmduded rate estknsies mab. melers above bottom t.c.. time course experiments conducted on deck U.D., Undetectable. Based on inspection of Fig.5 and time murse measurements from other vent sites, turnover rates 2 0.02 %@t are delectable ND., Not Di@rmtned

the vent source, corresponding to elevated numbers of a unique assemblage of Mn-coated sheathed bacteria as observed microscopically (J. Baross, pers. comm.). The high IMPS activity at this location p~umably expIains the relatively short (as compared to other JDF plume samples) residence time of 2.3 years measured for the 2226 m sample. In general, where residence times were shortest within a given vent environment, the microbial activity was usually higher, in agreement with our results at Galapagos. This is illustrated in Fig. 6 where the apparent residence time is piotted against the percentage of azide inhibition for samples collected within and beneath the JDF vent plume. The data

are from single time point experiments conducted in situ and on deck. Measurements of percent azide inhibition should be interpreted only as a qualitative measure of microbial activity, since azide will not poison all bacteria equally. While there is considerable scatter in the data ( R2 = OX), the line generated from a simple regression is statistically significant (not shown). A two-tailed 7’-test, measured at the 95% confidence interval, reveals that the slope of this tine is significantly different from zero (P c 0.00 1f . When residence times are corrected for To and plotted against percent azide inhibition, scatter in the data increases (R* = 0.3). This results because the net scavenging (corrected for TO) for many

3914

K. W. Mandemack and B. M. Tebo

.

0.00

0

m

5

u

(a) 8

-

10

15

3

’

10

15

20

-

25

.

m

30

I

35

40

12091 m

0.00

.

0

(b) r

5

1

20

.

25

*

30

.

35

40

Time(H) FIG. 5. Time course of “‘Mn( II) removal in near field vent plume samples collected at 0 km from the ridge axis of Endeavor Ridge, Juan de Fuca. Samples were incubated on deck at in situ temperatures of 2°C in the presence (m) and absence (0) of sodium azide.

samples was often very low or immeasurable. Nevertheless, Fig. 6 suggests that microbes are important for Mn( II) scavenging within the JDF vent plume environments. The result from a sample collected at 1943 m depth in the buoyant portion of the plume (Table 2) suggests that chemical processes alone may influence manganese scavenging. This sample yielded the shortest residence time (and highest scavenging rate) of all JDF vent plume samples ( I year), yet was poorly inhibited by azide (3 1% inhibition ). Manganese may have been coprecipitating with iron oxides in this sample since the total iron content of 198 nmol/kg ( SHARPE,199 1) in this sample was; by far, the highest measured for any of the samples. Furthermore, the total filter-bound 54Mn from this sample was decreased by only 39% following the ascorbate treatment and was unaffected by the excess “cold” Mn(II) and Cu( II) treatments. The precipitation of iron oxides within vent waters, particularly from the hot smokers at JDF, may obscure our estimates of MMMS based on azide inhibition. In sediments azide was ineffective in inhibiting glucose respiration, an observation that was attributed to azide binding to iron oxides ( EDENBORNet al., 1985). Therefore, we examined the relationship between inhibition by azide from each of the experiments and the dissolved (co.4 pm), total (unfiltered), and particulate (>0.4 Km) iron concentrations measured by SHARPE et al. ( 1993). Although there was a weak but significant correlation between particulate iron and inhibition

by azide, they were inversely related (data not shown). This result suggests that MMMS activity is relatively more important where particulate iron is lower, and agrees with our results of increasing relative MMMS activity with increasing distance from the JDF vent. Comparisons of in situ vs. on-deck experiments. Higher apparent microbial activity (78-87% azide inhibition) was observed in in situ as compared to on deck incubations (2854%; Table 3). This result is not surprising given that changes in pressure can affect the viability of certain deep-sea bacteria ( YAYANOS, 1986; YAYANOSet al., 1981) and enhance microbial manganese scavenging rates (COWEN et al., 1990). Some of the shortest residence times (and highest scavenging rates) measured at GA and JDF resulted from the in situ incubations (Tables 2 and 3). This was true for four of the five samples for which this direct comparison was made at JDF (Table 3). Enhanced manganese uptake within the majority of the in situ experiments may be a further indication that Mn-oxidizing bacteria within vent plumes are pressure sensitive ( COWEN, 1989 ), Scavenging rates. At Galapagos, the in situ rates of Mn( II) scavenging ranged from 0.14-0.61 nM/day within the vent plume, whereas samples incubated on deck varied between 9.2-l 5.6 PM/day. Rate calculations for these samples do not include the 1.3 nM Mn added as 54MnC12, since this would have inflated the rate estimates for samples with low Mn( II) concentrations. If the rates are first order with respect to Mn (II) concentration, this would have increased our measured rates proportional to the increase of Mn(I1) added (<16%). For samples collected at JDF for which manganese scavenging was detectable, the rates varied between 2-192 pM/ day (Tables 2 and 3 ). The fastest rates were measured for the Fe-rich sample (HC- 1, 1943 m; 192 PM/day) and two in situ measurements made within the buoyant plume (hydrocast#2;2192m, 172pM/dayand2074m, 107pMlday) where high microbial activity was observed; these samples also showed relatively short residence times (Tables 2 and 3). These results suggest that both iron and microbes may be important scavengers of Mn(I1) in the near field vent

E

2000-

I

OJ . 0

n ’

20

’

.

.

40 60 % Inhibition

-

60

100

FIG. 6. Plot of “apparent” residence time of Mn( II) (not corrected for initial isotope exchange at To) vs. microbial activity (as measured by percent inhibition of Mn(II) binding by azide) for all samples collected in the vent plume at Endeavor Ridge. The residence time plotted here is with respect to particulate manganese formation.

3915

Scavenging and oxidation of Mn in hydrothermal solutions TABLE 3. Coq~~B#~&titt

Distance

U) Bcavengfng w

Yho vent Plume o?

(km)*

Iml

~(11)

:

2074 2192

66.1 56.6

4

2363

2:::

,“s

4

2060 2126

32.9

20

(nM)

insiiu

ondeck

172 107

51 to 2oc 187

In Situ

%inEb&&nby

seavenghlg RRate % (PM.6’1

Depth

ConducM

or Ridge

insilu

ond8ck

insitu

ondebc

-

-

NZ.

ii:

-

z;:

N.D.

54

-

69

ii.

x:,

aDistanmfmmventsource

% azide intWtion based on endpoint&terminations,notsubbciing To values. CMnscavengingmayhavebeenhighckfetascrtl~enden~mentofpartidssfn~ bottomof the Go-flo bottleduffngthe in situinabation snd subsequentretrieval oftflerosett0. -, The cdd Mn and ascofbate treatments were not effectiveand thus precludsd rate esthetes. N.D., Not Detemsined

plume. In the more distant plume ( 4 km or greater), microbes assume this role to a greater degree. Oxidation rates. From the hydrocasts made within the GA vent plume, the estimated percentage of the rate due to oxidation varied from 33-SO%, whereas adsorption contributed from 36-65% (Table 2). The lowest oxidation values were observed from in situ casts 3 and 4 where values were 3334%, and both had high microbial activity (65 and 67% azide inhibition) and short residence times (34 and 39 days). These results are similar to those mentioned previously for the vent iield sample collected during Dive 20 14 (Table 1) which had the highest microbial activity (70%) and shortest residence time (28 days). It appears from these results, that near the vent fields at GA, enhanced adsorption can result when MMMS activity is high. Our methods for determining manganese oxidation rates were not effective in many of the samples collected within the JDF vent plume because the manganese, copper, and ascorbate treatments often did not decrease %Mn filter counts. In general our methods were most successful in the far field vent plume where microbial activity was higher than in the near field plume (Table 2). Generally, copper served as a better “Mn( II) desorption agent within the near field plume, while manganese was better at distances of 4 km or more from the ridge. These distance related trends for our methods may have resulted from changes in the quantity and quality of particles observed between near-field and far-field waters of the vent plume (DYMOND and ROTH, 1988). Based on these results, estimates of the percentage of the rate due to oxidation within the near field plume were made from the copper treatments, while those in the far field (24 km) from the manganese treatments, when these treatments were effective. Sample B-3 ( 1878 m, HC-4, 0 km) was an exception, for which manganese was the better desorbing agent. Values ranged from 17-698 for the nine samples for which these estimates were made (Table 2). The cont~bution by adsorption was sometimes undetectable for these samples, but was as high as 53% in the near field plume and as high as 34% in the far field. Beneath vent plumes Residence times. Three samples (two at JDF and one at GA) were collected in bottom waters (~75 m from bottom) beneath the vent plumes. These samples had relatively low

dissolved manganese levels (
Numerous forms of free-living bacteria have been observed within vent waters. Many of these bacteria are believed to be chemolitho~phs that oxidize reduced inorganic substrates to fuel their metabolic needs (JANNASCH and Morr~, 1985). Sulfur-oxidizing bacteria are believed to be the most abundant chemoli~o~ophs residing at the vents. However, other reduced substrates occur in vent waters, such as Hz, NHf , CH.,, CO, Fe( II), and Mn( II) ( EDMOND et al., 1982; JANNASCH and MOTTL, 1985 ), and autotrophic bacteria that utilize them as energy sources probably exist. Manganese chemoautotrophy, which has never been proven, might be possible in certain vent environments, particularly where high rni~~bi~ly mediated manganese scavenging (MMMS) activity and high Mn( II) scavenging rates are measured. Mnoxidizing bacteria have been isolated from the Galapagos and

3916

K. W. Mandernack and B. M. Tebo

(4 1.0 g r' 0.8 is

0

5

10

15

20

25

30

35

(b)/ 0

5

10

15

’

20

.

’

25

.

’

30

.

’

35

40

Time (H) FIG. 7. Time course of Mn( II) scavenging and oxidation in a sample collected in waters ~75 m from the bottom beneath the vent plume at Galapagos; (a) comparison of azide poisoned (m) and unpoisoned (0) incubations; (b) estimates of the percent manganese scavenged due to oxidation and adsorption as inferred from “cold” Mn (II) (A) and ascorbate (H) amendments.

East Pacific Rise vent fields ( DURAND et al., 1990; EHRLICH, 1983, 1985 ) and from the Endeavor segment of JDF (WILDE and TEBO, 1989; B. M. Tebo, unpubl. data). However, all of these organisms appear to be organotrophs although some may be able to generate ATP at the expense of manganese oxidation (EHRLICHand SALERNO,1990). At GA, these Mnoxidizing bacteria leave their mark in the near surrounding environment, coating shells and rocks with dark deposits of manganese minerals ( JANNA~CH and MOTTL, 1985; JANNASCH and WIRSEN, 198 1). Galapagos (GA) and Guaymas basins (GB) High MMMS activity, fast Mn( II) turnover times (short residence times, as low as 28 days), and some of the highest Mn( II) scavenging rates (2.4 nM/day) were measured in the GA vent field (Table 1; Fig. 8). A short residence time of 26 days measured from our in situ experiment within the GB

vent field is also suggestive of high MMMS activity. Thus, the GA and GB vent fields appear to be particularly suitable environments for MMMS activity. These results Seem to contradict the results of JOHNSONet al. ( 1988), who observed linear relationships between dissolved manganese and silicate concentrations at the GA vent fields, indicating conservative behavior of Mn( II). The reason(s) for this discrepancy is unclear, although it may relate to differences in the sensitivity of the methods employed, to environmental variability, or to the presence of reduced chemical species (e.g., hydrogen sulfide or Fe( II)) that would rapidly reduce any oxidized manganese that may form and hence make it appear to behave conservatively. In the surrounding bottom waters and within the vent plume at GA, Mn( II) turnover rates were consistently high for virtually all samples coliected (Table 2; Fig. 8). A range of relatively short Mn( II) scavenging residence times of 34483 days was observed for seven of the nine samples. All of the residence times measured at GA are shorter than one would expect from abiological oxidation and much shorter than the estimate of 50 years for total dissolvable Mn (TDM) in the plume (WEISS, 1977 ). Minimum measured Mn( II) residence times of 4 weeks within the GA and GB vent fields are similar to model estimates of OS-2 weeks made for the vent plume at Guaymas Basin (CAMPBELLet al., 1988). These residence times determined by entirely different methods are in remarkable agreement considering our estimates were based on point measurements in an area characterized by high chemical heterogeneity. Because GA and GB each contain warm water vents ( < I OO’C), whose temperatures are not too extreme for microbial growth, they can support dense populations of mesophilic and thermophilic bacteria ( HUBER et al., 1989, 1990; JANNASCHand WIRSEN, 1979; KARL, 1985; STETTER et al., 1987 ). Therefore, the warm vent waters at GA and GB may be a source of either bacteria or organic substrates for subsequent bacterial growth in the colder vent plumes. The elevated levels of organics within the waters of GB and the entire Gulf of California ( CALVERT, 1966; VAN ANDEL, 1964) may further enhance microbial growth and help sustain the population of Mn-oxidizing bacteria that have been identified within the GB vent plume (CAMPBELLet al., 1988). In addition to temperature and nutrient availability, the geochemical milieu may also be a significant factor contributing to the microbes enhanced turnover of manganese at GA and GB. The effluent waters at each of these vent sites is noted for having an unusually high Mn/Fe ratio (EDMOND et al., 1979a.b; VON DAMM et al., 1985a,b). At GA Fe(I1) is precipitated at depth as iron sulfides due to extensive subsurface mixing of the hydrothermal fluids, while at GB it is suggested that iron sulfides are trapped within the overlying thick sediment layer ( EDMOND et al., 1979b; VON DAMM et al., 1985b), thus allowing manganese to become relatively enriched. In Mn-em-iched warm water vents as these, manganese should not be removed as quickly from the region of venting by physicochemical means (for example, rapid advection or coprecipitation with Fe oxides and other minerals). Therefore, manganese may be more available to the microbes residing there. Even the suspended matter within the hydrothermal plume at GA is enriched with weak acid soluble manganese relative to iron ( BOLGERet al., 1978).

Scavenging and oxidation of Mn in hydrothermal

solutions

5km

3917 20 km

200

.. 100

Galapagos

20km

5Om

Endeavor Ridge, Juan de Fuca

FIG. 8. Illustration summarizing measured microbial activities, residence times (with respect to particulate manganese formation), and scavenging rates in samples collezted during this study from the vent fields, vent plumes, and surrounding waters of the Galapagos and Endeavor Ridge, Juan de Fuca hydrothermal vents.

Endeavor Ridge, Juan de Fuca Unlike GA, the hot smoker environment of Endeavor Ridge, Juan de Fuca is characterized by hot vent fluids with a lower Mn/ Fe ratio (inferred from reports by BAKER and MASSOTH, 1986; KADKO et al., 1990), and generally lower MMMS activity in the vent field and near field plume (O-2 km) (Tables 1 and 2, Fig. 8). At JDF, Mn(II) turnover rates were generally slower than those measured at GA (Tables 1 and 2 ) . These results are in agreement with previous reports of the conservative nature of manganese within the proximal portions of the plume arising from high temperature vents such as Southern Juan de Fuca segment (COWEN et al., 1990), the Endeavor Ridge ( KADKO et al., 1990), the TAG hydrothermal field on the mid Atlantic ridge ( TROCINE and TREFRY, 1988), and 21’N on the East Pacific Rise (MOT-K and

MCCONACHY, 1990). The cumulative results from these studies are also consistent with sediment trap data at Endeavor Ridge that showed marked depletion in the percentage of manganese within particulates collected from a near vent field trap when compared to a far field trap ( DYMOND and ROTH, 1988). Smoker environments may be too hot and reducing for Mn-oxidizing bacteria to reside and may account for the relatively low MMMS activity we observed at the JDF vent field. However, turnover rates measured in this study were still relatively fast within the JDF vent field (residence times of 1.4-3.3 years), and occasionally in the near field plume directly over the vent (Tables 1 and 2, Fig. 8). The results from these samples imply that a abiological mechanism for this rapid precipitation might prevail in the vent field and within the near field plume, perhaps coprecipitation with or adsorption to iron oxyhydroxides as suggested by CAMPBELL

3918

K. W. Mandemack and B. M. Tebo

et al. ( 1988) for the East Pacific Rise. Consistent with this hypothesis, much of the manganese scavenging in the JDF vent field samples is exchangeable (i.e., adsorbed), is not strongly inhibited by sodium azide (i.e., not microbially precipitated), not ascorbate reducible (i.e., not oxidized manganese), and dependent on O2 (suggesting an oxide phase other than manganese). MOTTL and MCCONACHY( 1990) report that the residence time of plume water within 25 m of its source at 2 1ON is only a few minutes. Collection of this dynamically buoyant vent plume water with Go-flo or niskin bottles may impose artificially static conditions on it, which may induce unusual post sampling reactions, such as precipitation, that do not normally occur in situ. It is conceivable that such reactions could result from prolonged entrapment of vent plume water having exceptionally high concentrations of hydrothermally derived elements, and that the Mn(I1) might coprecipitate “artificially” with different mineral phases. While this might explain the high manganese scavenging rates measured in the JDF vent field (Table 1 ), in situ measurements by hydrocast (HC-2) in the buoyant portion of the JDF plume at Endeavor Ridge gave similar results (Table 3 ) . The CTD data from this cast showed pulses of emitted vent water having exceptionally high temperature and light transmission anomalies (>O.l7”C and a 5% decrease in light transmission), indicative of the buoyant plume. Residence times of 1. 1- 1.4 years were estimated for the two deepest samples collected at 25 and 143 m off the bottom (Table 3). These samples also revealed high MMMS activity, in contrast to results from the vent field (Table 1) and in the near field plume at the Southern Juan de Fuca Ridge (COWEN et al., 1990). Although some artifactual (co)precipitation of Mn( II) with iron oxyhydroxides or with sulfides may occur as a result of closed bottle incubations, the short residence times and high microbial activity suggest that some Mn( II) scavenging may occur in the buoyant portions of the plume, whether it be by chemical or microbiological means (Tables 1 and 3). Although direct rate measurements by COWENet al. ( 1986, 1990) at the Southern Juan de Fuca Ridge (SJDR) did not indicate chemical or microbiological manganese scavenging in the buoyant plume (results which also argue against artifactual precipitation ) , FEELEY et al. ( 1987 ) report the presence of iron and manganese oxyhydroxide plume particles 100 m above the vent source at SJDR. Similar results were reported by BAKERand MASSOTH( 1986) at Endeavor Ridge, where iron and manganese were observed in plume particles collected by a sediment trap in the near field. In addition, although MOTTL and MCCONACHY ( 1990) conclude that manganese behaves conservatively in the buoyant plume at 21 “N, one of their samples ( 1155-l ) examined from this region revealed particulates with a relatively high manganese (and iron) content, suggestive of manganese coprecipitation with iron. The 1155-I sample had the highest wt % of iron within the particulates, a high Fe/Mn ratio within the filtrate, and relatively low dissolved Mn (co.45 PM). Differences between the measured vs. estimated concentrations of manganese in this sample if it behaved conservatively (based on dilution of lithium, a conservative tracer) suggest that >53% of the manganese (and 93% of the iron) could have been removed from solution ( MOTTL and MCCONACHY, 1990).

The data here and elsewhere suggests that manganese may not always behave conservatively in the near-field vent plume and may either coprecipitate with other minerals, or be scavenged by bacteria. Recently, COALE et al. ( 199 1) reported unusually low Mn:Q (Q = excess heat anomaly) ratios in vent plume waters of the Southern Juan de Fuca; rapid scavenging of manganese was dismissed by the authors as a viable explanation for these low ratios due to lack of evidence for chemical or biological Mn(I1) scavenging in the buoyant plume. COALE et al. ( 199 1) concluded that the low Mn:Q resulted from mixing of high and low Mn:Q discharge from different vent sources. We suggest that microbial or chemical Mn( II) scavenging in the near-field plume may at times be high, and perhaps contributes to low Mn:Q values in vent plume waters. Microbial biomass is enriched within vent plumes (STRAUEE et al., 1990; WINN et al., 1986). STRAUBE et al. ( 1990) suggest that a unique microbial population must be residing in the buoyant portions of the plume at Endeavor Ridge as entrainment of seawater alone could not account for the elevated levels of particulate DNA measured. Furthermore, these authors found a wide heterogeneity in particulate DNA and bacterial abundance within the vent plume, perhaps a reflection of turbulent mixing in this environment or simply a response of bacterial growth. This heterogeneity in microbial density agrees well with our observations of heterogeneous MMMS activity in the near field plume at JDF. Although manganese may sometimes appear to behave conservatively within the proximal portions of the buoyant plume and vent fields at JDF, this does not necessarily imply that it is unreactive. Precipitation of metal sulfides and redox reactions occur rapidly within the buoyant plume. These processes may interact with manganates that have recently formed in the proximal regions of the vent plume and thus inhibit their initial accumulation. Oxidized manganese can be reduced by reactions with sulfide ( ALLERand RUDE, 1988; BURDIGE and NEALSON, 1986), reduced iron (Fe( II)), (MYERS and NEALSON, 1988b; POSTMA, 1985), and by microbial activities ( LOVLEY and PHILLIPS, 1988; MYERS and NEALSON, 1988a,b; TEBO et al., 1991). Thus, there is a good possibility that manganese oxidation is quite rapid in these environments but Mn( 111,IV) manganates do not accumulate because they are highly reactive. For example, TEBO et al. ( 1991) have demonstrated that in the Black Sea both manganese oxidation and reduction could occur simultaneously as long as O2 was present. The process of iron or sulfur oxidation and manganese reduction may extend even farther than the most proximal portions of the buoyant plume. Sulfides of copper and zinc, and more importantly, a variety of iron sulfides such as pyrite, pyrrhotite, and marcasite, have been identified within smoker particulates at Endeavor Ridge ( FEELYet al., 1987 ) . Following precipitation, these particles can dissolve during their transit within the vent plume and further react with manganates. The minerals marcasite and pyrrhotite may be especiahy reactive since they are soluble and rapidly dissolve. Assuming an average plume particle size of 2 pm in the more distal reaches of the plume (WALKER and BAKER, 1988), residence times of 23 and 11 days were estimated, respectively, for marcasite and pyrrhotite particles of this size (FEELY et

Scavenging and oxidation of Mn in hydmth~al

al., 1987). This process may extend even further within the plume, as more resistant pyrite particles of < 10 pm size have been identified in sediment traps 4 km from their source (FEELYet al., 1987). The presence of higher sulfide in the vent waters at Endeavor may explain the slower Mn(I1) turnover rates observed there in the far-field plume when compared to those estimated by COWEN et ai. ( 1990) at the SJDR. We calculated average residence times in the far-field plume (>3 km), where MMMS activity was highest, at both locations (Table 4). A mean k, value for each vent site was calculated by averaging the estimated k, values from individual samples; the reciprocal of the mean k, yields the average residence time. We have assumed that our estimated turnover rates closely approximate k, values in the far field portions of the plume ( COWEN et al., 1990). Furthermore, this calculation assumes random sample collection at both vent sites that was representative of mean conditions throughout the distal portions of the vent plume. We included samples for which no measurable manganese scavenging was measured in our average residence times, by assigning these samples a forward scavenging rate constant of 0. We excluded samples collected beneath the vent plume at Endeavor Ridge, since they may represent anomalously high values. Because the results of COWEN et al. ( 1990) for the SJDR were not corrected for the initial rapid binding and exchange of the s4Mn to particulates after addition of the radioisotope (J. Cowen, pers. commun.) , we applied a correction for SJDR k, values from a linear regression of a plot of corrected vs. uncorrected k, values at Endeavor. This correction increased the estimated residence time for SJDR by 30%. The average residence times within the far field plumes at Endeavor and SJDR were 8.0 and I .3 year, respectively (Table 4, see the following discussion ) . Differences between scavenging residence times estimated for Endeavor Ridge (our results) and the Southern Juan de Fuca segment ( COWEN et al., 1990) may reflect slight differences in the methods used to measure and compute the times, or they may reflect actual differences in vent environments. In the studies at the SJDR the water samples were incubated at in situ pressures on deck (COWEN et al., 1990), since a previous report indicated a positive pressure affect on manganese oxidation within the vent plume environment ( COWEN, 1989). This pressure affect, however, was most evident only when long incubation times (3 weeks) were used, the effect was much smaller for short incubation times ( 15 h). Although we also observed a positive pressure effect of 3.4-10.7X on manganese scavenging rates in the near field,

solutions

the effect was less in the t&r field (<2.3X; Table 3). Thus, it is unlikely that incubations under pressure could account for the higher rate constants for SJDR vs. the Endeavor Ridge, and thus the difference appears to be real. Our observation of higher MMMS activity with increasing distance within the plume agrees well with observations at the Southern Juan de Fuca Ridge (COWEN et al., 1990). However, we did not observe a corresponding trend of higher rate constants with increasing distance as reported by COWEN et al. ( 1990). This may be because we occasionally observed high MMMS activity in the near-field plume. However, at the 17 km station, where a unique assemblage of filamentous sheathed Mn-oxidizing bacteria were observed and bacterial numbers were also elevated ( lO’/mL) (J. Baross, unpubl. results), relatively fast turnover rates were measured. Mn( II) Oxidation and Mn( II) Adsorption From thermodynamic considerations, manganese autotrophic bacteria, if they exist, should fully oxidize the Mn (II) they scavenge in order to optimize the energetic yield from this reaction. If manganese autotrophy occurs in the environment, then, in addition to high MMMS activity, one might also expect a high percentage of the scavenging to be due to oxidation. Mechanistically, however, this may not be possible. EHRLICH (1984) has reported that some Mn(II)-oxidizing bacteria require preformed manganate before they oxidize Mn( II). The adsorption of Mn( II) ions on the preformed manganate is believed to reduce the activation energy for oxidation (EHRLICH, 1984). Whatever the mechanism of microbial Mn(II) oxidation, rapid formation of oxidized manganese could conceivably be followed by enhanced Mn( II) adsorption as well. Within our study, some of the highest oxidation percentages were observed within the GA and GB vent fields. For example, samples D.2024 of GA and the single in situ experiment at GB, 68 and 74%, respectively, was attributed to oxidation as manganates (Table I). Although it was not extraordinarily high, MMMS activity was also observed in the GA sample. The high Mn( II) concentration (243 nM) measured translates to a very high rate of manganate formation. This suggests that the high accumulation rates of relatively pure man~nat~ forming near the GA vent fields (MOURE and VOCT, 1976) can result from microbial activity. Comparison of results from our in situ and corresponding on-deck experiments illustrate the importance of time for the formation and a~umulation of manganates within the JDF vent plume (Table 3 ) . The ascorbate and excess cold Mn( II)

Tnble 4. Mn(li)AeekienceThee InHydrethem~l Vent Plmos

ventLcoatbn Gueymw EWn(O+km) Galapqos SpreadingCenter (0-1.2km)

ScuIhemJuande FuceRkQe (35-20 km) EndeavorRidge,JDF (4-17km) a average residence time ND., NotDetermined

3919

Avera kt(v p”1 ND.

0.52 weeks

Campbellelal., 1966

4.457

11.7weeks

ThisShMy

0.769

1.3 years

Cowenet& 1990

0.125

6.0 yeers

mrsstudv

Timea

Reference

3920

K. W. Mandernack and B. M. Tebo

treatments indicated that little of the manganese precipitation during the in situ experiments resulted in the formation of manganates, and therefore the manganese must have been incorporated into or adsorbed to other minerals. This may also explain our observation that many ofthe near-field samples indicated significant particulate manganese formation, but resulted in no apparent formation of manganates. In contrast, manganese scavenging could be attributed to manganate formation for the ondeck experiments at the 4 km station. It appears that the additional time that had lapsed (during the in situ incubation) before processing the on-deck experiments was sufficient to permit manganates to accumulate. In agreement with this, the “cold” Mn(II) and ascorbate treatments also proved more effective in the more distal portions of the plume (>3 km), where MMMS activity was higher, and the formation of manganates expected. In summary, formation of Mn( III, IV) manganates is less apparent in the near-field and buoyant portions of the JDF vent plume; an abundance of Fe*+ and sulfide in dissolved and particulate forms may control the fate of manganese by reducing its oxidized forms. The formation and accumulation of manganate is more significant in the far-field portions of the plume, where high MMMS activity (>49% inhibition by azide) is observed (Fig. 8). These results are in overall agreement with previous reports at Endeavor Ridge and other hot smoker environments (BAKER and MASSOTH, 1986; COWEN et al., 1990; DYMOND and ROTH, 1988; MOTTL and MCCONACHY, 1990). In contrast, microbially mediated manganate formation is sometimes very high within the GA vent field, where residence times are significantly shorter than those measured within the JDF vent field (Fig. 8). MMMS activity and oxidation percentages remain relatively high in the GA vent plume and surrounding waters. Beneath Hydrothermal Vent Plumes: The Role of Bacteria in Removing Manganese and other Particulates from the Plume Fast turnover rates (short residence times) and high MMMS activity were observed in a few select samples collected in the Mn-poor bottom waters (~75 mab) beneath the vent plumes at Galapagos (Fig. 7a) and JDF (Table 2, Fig. 8). We propose that the accelerated uptake in these samples results from the flux of Mn-oxidizing bacteria to the bottom waters from the overlying vent plume. Extracellular deposits of manganese might burden the bacteria and hasten their settling. As the Mn-coated bacteria settle into the Mnpoor waters, an increase in both the apparent microbial activity and manganese particulate levels should occur in the bottom waters. Both high MMMS activity (Table 2), and elevated particulate manganese concentrations (3.5-4 nM; SHARPE, 1991; SHARPE et al., 1993) were observed in the two JDF samples. This is also consistent with water column profiles of particulate manganese from a variety of vent plume locations that indicated a steady increase with depth beneath the vent plume ( BOLGERet al., 1978; CAMPBELLet al., 1988; COWENet al., 1990). In addition, at GA, BOLGERet al. ( 1978) showed a steady increase in the Mn/Fe ratio of suspended material with depth beneath the vent plume. High Mn/Fe ratios were also noted for some of the sediments collected

near the spreading axis. We also attribute this depth-related increase in Mn/Fe to Mn-coated bacteria settling from the plume and propose that this might result in relatively pure manganese oxide deposits that have previously been reported near the GA rift (CORLISSet al., 1978; MOORE and VOGT, 1976). CORLISSet al. ( 1978) suggested that manganese deposits of the GA hydrothermal mounds were precipitated near the seawater sediment surface, but they could not explain the mechanism since measurements of total dissolvable manganese ( TDM ) in the bottom waters near GA increased with depth ( KLINKHAMMERet al., 1977), suggesting a flux of manganese from the sediments (CORLISSet al., 1978). We suggest a mechanism of selective microbial manganese scavenging after the vent fluids are emitted. Mn-oxidizing bacteria within the plume selectively scavenge and oxidize Mn( II). As they become coated with manganese oxides they settle and further scavenge manganese during their transport to the sediments. Comparison of Manganese Residence Times with Manganese Deposition Rates at Vent Sites From this study and others it seems apparent that bacteria are important agents in manganese cycling in hydrothermal vent environments. They are active in Mn(II) scavenging and oxidation and subsequent transport to the metalliferous sediments that form near the ridge crests. Comparison of the average Mn( II) residence times (with respect to scavenging and oxidation) at GA and JDF (Endeavor Ridge) from this study can be made with those estimated at GB (CAMPBELL et al., 1988) and the Southern Juan de Fuca Ridge (COWEN et al., 1990) (Table 4). At GA, where mixing is extensive from strong tidal currents near the spreading center ( LONSDALE, 1976). an average residence time was calculated from all samples (excluding the 103 hour in situ incubation within the vent field) collected in the vent field, vent plume, and surrounding waters. At Endeavor Ridge and at SJDR the average residence time is for vent plume waters >3 km from the axial valley, where microbial scavenging seems to be most pronounced and Mn( II) residence times are lower. Our JDF estimate does not include a correction for a possible pressure affect; however, pressure effects in the distal portions of the plume were not great enough to change the order and relative differences between the vents sites. The differences in Mn(II) residence times, and rates of manganese deposition to the sediments, estimated for the various vent sites may reflect different biogeochemical influences at each location. The numerous variables that control manganese scavenging ultimately control the deposition and formation of manganese oxide deposits in these vent environments. Comparisons of the Mn( II) residence times at the different vent sites should mirror accumulation rates of manganese in the underlying sediments, although the Mn( II) residence times we report are with respect to scavenging and oxidation and not necessarily to particle settling. The total flux of manganese from each vent site will also influence manganese accumulation rates within the adjacent sediments. However, dissolved manganese concentrations within the different vent plumes are less variable than are the residence times. Because the Mn( II) turnover rate (- 1/residence time)

Scavenging and oxidation of Mn in hydrothermal solutions at GA exceeded that at Endeavor

by 36X, we predict that the manganese accumulation rate to the sediments at these vent sites could also differ by a proportional amount. Unfortunately, there are no reports of estimated manganese accumulation rates at locations near our study sites. However, estimates made by the “?h method for manganese oxide deposits collected 1100 km from Rose Garden (MOORE and VOGT, 1976 ) , and those for Fe/ Mn deposits at the ridge crest of the East Pacific Rise (EPR; DYMOND and VEEH, 1975), indicate that manganese is accumulating 20-100X faster at the GA site that at the EPR. The relatively fast turnover rates we measured at GA corroborates the high manganese accumulation rates measured by MOORE and VOGT ( 1976 ) . The rate at which Mn( II) is (microbially ) scavenged and oxidii into particulate manganese within vent waters may directly control the rate at which it precipitates to the sediments. CONCLUSIONS Distinct differences in microbially mediated manganese scavenging (MMMS) activity exist between the low temperature vents at Galapagos (GA) and the high temperature vents at Endeavor Ridge, Juan de Fuca (JDF) (Fig. 8). MMMS activity was high in the GA vent field and remained high throughout the vent plume. High MMMS activity at GA resulted in low Mn (II) residence times (with respect to scavenging and oxidation) and high manganese scavenging and oxidation rates both within the vent field and vent plume. These results may explain the occurrence of relatively pure manganese oxide deposits reported in the local vicinity of the GA vents (CORLISS et al., 1978; MOORE and VOGT, 1976). In contrast to GA, MMMS activity was’low within the JDF vent field, which is reflected by longer Mn( II) residence times. However, compared to the JDF vent plume, the residence times were relatively low and scavenging rates were high in the JDF vent field. Chemical processes, such as coprecipitation or adsorption with other minerals (possibly iron oxyhydroxides), may explain this, since the percentage of Mn( II) scavenging due to oxidation was low within the JDF vent field and in the near-field plume. In general, MMMS activity was higher at more distal locations (>3 km) within the JDF vent plume, where manganese scavenging was more frequently attributed to oxidation. The high temperatures of the venting fluids at JDF and the presence of higher levels of sulfide and other reduced compounds may create conditions whereby microbial manganese scavenging is limited, or the accumulation of manganates impeded, in the proximal regions of the JDF vent. We also present evidence that microbes may be important for the transport of particulate manganese to the sediments after it is scavenged within the vent plume. We observed high MMMS activity, and exceptionally low Mn(I1) residence times, within bottom waters (~75 m from bottom) beneath the vent plumes at GA and JDF. The high Mn( II) turnover rates and MMMS activity we measured in the vent fields and plumes at GA may explain the high manganese accumulation rates that have been measured for manganese oxide deposits collected at other GA sites (MOORE and VCK~T,1976). Acknowledgments-This work required contributions from numerous sources and people to whom we are grateful. We thank the following

3921

individuals for their generous support: Chief Scientists, Marvin LiIley,

John Baross, Jim Childress, and Bemd Simoneit; the Captains and crews of the RV’s Atlantis II/Alvin and Melville, with special thanks to Chief Alvin pilot Ralph Hollis and Engineer Steve Bean of the Atlantis II who provided personal assistance to the deployments of the in situ WSD, Mike Mullin of SIO who kindly loaned us the Bottles for the in situ WSD, Bob Ranf and Dennis Long of the SIO Support Shops whose thrifty and inventive ways led to economical and efficient designs for the WSD, David Wirth of SIO for equipment provisions; Bob Collier and John Sharpe for iron and manganese measurements at JDF. Personal and technical assisnmce was provided by the following individuals: Doug Nelson, Art Yayanos, Russe.1Vetter, Bob Hessler, Joris Gieskes, Mike Troutman, Michel Boudrias, Scott France, Chris Maclsaac, and Deeanne Edwards. We thank Ed Baker and two anonymous reviewers for their constructive reviews of the manuscript. This work was supported by grants from the National Science Foundation (GCE86-20289) and the Office of Naval Research (NOOO14-87-K-0532and NOOOl4-90-J-1097).

Editorial handling: R. A. Schmitt

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