Methanogenesis and sulfate reduction in marine sediments: A new model

Earth and Planetary Science Letters 295 (2010) 358–366

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Earth and Planetary Science Letters j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e p s l

Methanogenesis and sulfate reduction in marine sediments: A new model Richard M. Mitterer Department of Geosciences, University of Texas at Dallas, Richardson, TX 75080 USA

a r t i c l e

i n f o

Article history: Received 30 June 2009 Received in revised form 6 April 2010 Accepted 7 April 2010 Available online 11 May 2010 Editor: M.L. Delaney Keywords: methanogen anaerobic methane oxidation amino acid racemization non-competitive substrate sulfate reduction Ocean Drilling Program

a b s t r a c t A number of studies have shown that methanogens are active in the presence of sulfate under some conditions. This phenomenon is especially exemplified in carbonate sediments of the southern Australian continental margin. Three sites cored during Ocean Drilling Program (ODP) Leg 182 in the Great Australian Bight have high concentrations of microbially-generated methane and hydrogen sulfide throughout almost 500 m of sediments. In these cores, the sulfate-reducing and methanogenic zones overlap completely; that is, the usual sulfate-methane transition zone is absent. Amino acid racemization data show that the gassy sediments consist of younger carbonates than the low-gas sites. High concentrations of the reduced gases also occur in two ODP sites on the margin of the Bahamas platform, both of which have similar sedimentary conditions to those of the high-gas sites of Leg 182. Co-generation of these reduced gases results from an unusual combination of conditions, including: (1) a thick Quaternary sequence of iron-poor carbonate sediments, (2) a sub-seafloor brine, and (3) moderate amounts of organic carbon. The probable explanation for the co-generation of hydrogen sulfide and methane in all these sites, as well as in other reported environments, is that methanogens are utilizing non-competitive substrates to produce methane within the sulfate-reducing zone. Taken together, these results form the basis of a new model for sulfate reduction and methanogenesis in marine sediments. The biogeochemical end-members of the model are: (1) minimal sulfate reduction, (2) complete sulfate reduction followed by methanogenesis, and (3) overlapping sulfate reduction and methanogenesis with no transition zone. © 2010 Elsevier B.V. All rights reserved.

1. Introduction A sequence of microbially-mediated redox reactions occurs in the pore waters of marine sediments with increasing depth below the seafloor. In sediments containing moderate to abundant amounts of organic carbon, the major reactions, after loss of O2, are reduction of manganese, iron, and sulfate, followed by generation of methane (Froelich et al., 1979). Based on thermodynamic calculations and analyses of pore fluids, sulfate reduction (SR) and methanogenesis are generally considered to be mutually exclusive microbially-mediated reactions (Claypool and Kaplan, 1974; Martens and Berner, 1974; Froelich et al., 1979; Sansome and Martens, 1981). Sulfate-reducing bacteria (SRB), in effect, out-compete methanogens for a common organic substrate until all sulfates are depleted. Consequently, significant methane generation in marine sediments occurs only after almost all sulfate has been reduced to sulfide (Jørgensen and Kaster, 2006, and references therein). This relationship leads to the well-known biogeochemical stratification of dissolved constituents in the pore fluids of marine sediments, with the methanogenic zone underlying the sulfate-reducing zone (SRZ). Anaerobic oxidation of methane (AOM) occurs at the interface between the two zones (sulfate-methane transition zone) as methane diffuses upward,

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resulting in consumption of methane within the sediment column. Several recent studies have focused on the biogeochemistry of AOM processes, the marine microorganisms involved in these reactions, and their biomarkers, ecology and energetics (e.g., Hinrichs et al., 1999; Vallentine and Reeburgh, 2000; Orphan et al., 2001; Hinrichs and Boetius, 2002; Orcutt et al., 2005; LaRowe et al., 2008; Moran et al., 2008; also see Whiticar, 1999; Valentine, 2002; Reeburgh, 2007; Caldwell et al., 2008, for recent reviews). The depth in the sediment column for the transition from SR to methane generation is variable and depends primarily on a number of factors including the supply of reactive organic matter and the rates of sediment accumulation and replenishment of sulfate from overlying seawater (Claypool and Kvenvolden, 1983; Borowski et al., 1999; Claypool, 2004; Jørgensen and Kaster, 2006). Reduction of sulfate is typically not completed in sediments with low microbial metabolic activity (D'Hondt et al., 2002). Some exceptions to the prevailing model have been documented. Oremland and Taylor (1978), Oremland and Polcin (1982), and Oremland et al. (1982a,b, 1987) described the generation of methane in the presence of sulfate in sub-tidal carbonates of Florida Bay, Florida, as well as in incubation experiments with salt marsh sediments from San Francisco Bay, California, and with sediments from Big Soda Lake, Nevada, and Mono Lake, California. Significant methane concentrations also occur in the SRZ in some Ocean Drilling Program (ODP) sites (e.g., Sites 1005 and 1009 on the flank of the

R.M. Mitterer / Earth and Planetary Science Letters 295 (2010) 358–366

Bahamas platform). More generally, D'Hondt et al. (2002), in their detailed compilation of pore water data from Deep Sea Drilling Project (DSDP) and ODP sites, determined that about one-sixth of all open ocean sites have above background methane and abundant sulfate concentrations. However, the most extreme exceptions to the general biogeochemical profile of a SRZ overlying a methanogenic zone occur in a thick sequence of Quaternary carbonates cored during Leg 182 on the Eucla Margin in the Great Australian Bight (GAB). Three coring sites in this area (Sites 1127, 1129 and 1131), in water depths from about 200 to 480 m, encountered high concentrations of both H2S and methane throughout about 500 m of margin sediments. The results from Leg 182, and other studies noted above, suggest that the general model for SR and methanogenesis may not apply to all marine environments and that some carbonate environments may be exceptions to the prevailing model. The purpose of this study is to: (1) focus on the GAB sediments as a type example of environments exhibiting extensive co-generation of H2S and methane; (2) compare the GAB sites to other marine sites that also exhibit significant methanogenesis in the presence of abundant sulfate; and (3) propose a new model for SR and methanogenesis in marine sediments that incorporates these results. 2. Methods Determination of gas concentrations on the JOIDES Resolution followed the routine headspace method described by Kvenvolden and McDonald (1986). In this procedure, approximately 5 cm3 of sediment was obtained immediately upon core retrieval using a syringe barrel with its tip removed. The sediment was transferred to a vial, sealed and heated at 60 °C for 30 min, after which the gases in the headspace were analyzed by gas chromatography. Gas expansion pockets in the cores, resulting from the decrease in pressure upon core retrieval, were sampled directly through the core liner using a gastight syringe. The constituents of the gas pockets were also analyzed by gas chromatography. Sulfate was determined by ion chromatography on pore-water squeezed from the sediments. See Feary et al. (2000) for additional analytical details. Analytical data from the ODP used in this study are available at www.odp.tamu.edu/database. The headspace method for gas analysis provides for rapid monitoring of hydrocarbons and other gases during drilling to comply with environmental and safety guidelines. Some portion of the gases undoubtedly escapes prior to sampling due to the decrease in pressure and warming experienced by the sediment during core retrieval and subsequent handling. Despite this limitation, the headspace technique provides useful measurements for comparison of gas concentrations between coring sites. The Amino Acid Geochronology Laboratory at Northern Arizona University provided amino acid concentrations and D/L amino acid ratios on samples from ODP Sites 1126 and 1127. In brief, mixed foraminifera, hand-picked from samples displaying minimal evidence of diagenetic effects, were cleaned by sonication and acid-washing prior to dissolving in 6 M HCl. Five foraminiferal separates from each sample were prepared and analyzed independently. Reported values are the average of the five analyses. Kaufman (2006) gives additional details about sample preparation and analyses. 3. Review of Organic Geochemistry Results, ODP Leg 182, Great Australian Bight (GAB) The Eucla Margin in the GAB is the largest modern province of cool-water carbonate sediments (James and von der Borch, 1991). Almost a one km-thick sequence of carbonate sediments has accumulated since the Eocene (Feary and James, 1998). In part of the margin, the Quaternary section has a high accumulation rate (∼ 28 cm/kyr) and comprises about one-half of the sequence (Shipboard Scientific Party, 2000). In contrast to warm-water

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carbonates, with their characteristic coralline-algal predominance, the sediments of the GAB consist largely of skeletal fragments of bryozoans, ostracodes, and planktonic and benthic foraminifera. Numerous large bryozoan-rich mounds occur on shelf regions shallower than 350 m (Shipboard Scientific Party, 2000). As described by Feary et al. (2000), Swart et al. (2000) and Mitterer et al. (2001), three of the nine sites drilled on the Eucla Margin during ODP Leg 182 (Sites 1127, 1129, and 1131) have high concentrations of both H2S and methane. Based on these high-gas concentrations and the sub-seafloor temperature and pressure conditions, Swart et al. (2000) suggested that these sites possess H2S–CH4 clathrates. At the other six sites the two gases are at background levels or at low concentrations. Both H2S and methane appear in the sediments of the three high-gas sites at detectable concentrations within a few tens of meters sub-seafloor, and they occur together at high concentrations throughout the next several hundred meters of sediment. Methane ranges up to 12 000 µL/L and H2S ranges up to 60 000 µL/L in headspace analyses. In addition, heavier hydrocarbon gases (C2 to C6), undoubtedly biogenic in these thermally immature sediments, are present at concentrations up to a few hundred µL/L, although concentrations decrease with increasing carbon number. Individual gas expansion pockets, formed during depressurization as the cores are raised to the surface, have concentrations as high as 245 000 µL/L for methane and as high as 157 000 µL/L for H2S. Carbon isotopic analyses indicate that the methane in these sites is entirely bacterial in origin (Mitterer et al., 2001). A high salinity sub-seafloor brine provides an abundant source of sulfate for the extensive H2S production. Pore-water salinity in eight of the nine sites ranges from 40 to105, or up to almost three times the normal seawater value. Sulfate is present throughout the pore waters in Sites 1129 and 1131. In Site 1127, sulfate is completely reduced between 80 and 170 m below the seafloor, but then is present at greater depths due to the presence of the brine. The lack of reactive iron in these carbonate sediments allows the H2S to accumulate in the three high-gas sites. Fig. 1 illustrates the downhole profiles for sulfate and methane in the three high-gas sites (1127, 1131 and 1129) showing the subseafloor zone of hypersaline pore water and the high methane concentrations throughout. For comparison, Fig. 2 displays the sulfate and methane profiles in one of the low-gas sites (1126), as well as in a site (1229) from another region where sulfate and methane profiles do not overlap significantly. Site 1229, on the Peru margin, represents a typical siliciclastic environment with the methanogenic zone below the SRZ. Further illustrating the usual biogeochemical stratification of sulfate and methane, a sub-seafloor source of sulfate in this site causes inhibition of methanogenesis at greater depths (Fig. 2). Table 1 summarizes the overall pattern for Leg 182 drill sites. Carbonate sediments dominate all nine sites; eight sites have high salinity sub-seafloor pore fluids (except for Site 1128, the deepest at 3874 m); and three sites have high concentrations of H2S and methane throughout most of the cores. The SR and methanogenic zones in these three high-gas cores overlap completely. That is, the usual sulfate-methane transition zone does not exist. 4. Results 4.1. Amino acids in ODP Leg 182 sediments Table 2 and Fig. 3 present new amino acid results from mixed foraminifera for Sites 1126 (low-gas) and 1127 (high-gas) to supplement those reported previously by Mitterer et al. (2001) on bulk sediment. In agreement with the known trend of diagenetic changes displayed by proteins and amino acids in fossil shells with increasing age, the concentrations of selected amino acids (aspartic acid, glutamic acid, and alanine) in the foraminifera decrease systematically down core (Table 2). This decrease is due to a variety

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2 Fig. 1. Profiles of CH4 (open squares) and SO− (solid circles) concentrations in the pore-water of three high-gas sites, ODP Leg 182, Great Australian Bight. Dashed line represents 4 approximate base of Quaternary section. Sediment depth is in meters below the sea floor (mbsf). Data obtained from www-odp.tamu.edu/database.

of reactions, including hydrolysis, decarboxylation and deamination, that convert the proteins to free amino acids and then to other compounds such as amines and organic acids (Mitterer, 1993). Leaching of free amino acids from the skeletal structures also undoubtedly contributes to the decrease in concentrations. The notable difference between these two sites is that the amino acid concentrations are greater at any depth in the sediments at Site 1127 than at a comparable depth in sediments at Site 1126, an indication that the organic constituents of the carbonates at Site 1127 have experienced less diagenetic alteration (Fig. 3). The implication of this result is that the sediments at Site 1127 are younger overall than Site 1126 sediments. The extent of amino acid racemization (i.e., D/L amino acid ratios), another parameter that more directly reflects relative age, increases with increasing depth in sediments of both sites (Table 2; Fig. 3). However, the D/L ratios increase to higher values, indicating older sediments, at a shallower depth at Site 1126 than at Site 1127. The D/L ratios of the three amino acids in Site 1126 sediments approach or reach the equilibrium value (D/L ∼ 1) at sediment depths less than 100 m below the sea floor (mbsf), while the D/L ratios in Site 1127 sediments only reach such high values at depths of about 500 mbsf. These data agree with those obtained previously (Mitterer et al., 2001) and, taken together with the amino acid concentration results above, support the biostratigraphic observation by Feary et al. (2000) that the Quaternary carbonate package in the high-gas sites is much thicker than the Quaternary sediments at the low-gas sites. The data also show that the thick Quaternary sections in the high-gas sites have greater concentrations of skeletally-derived proteins and their diagenetic products (amino acids, amines, etc.) compared to the low-gas sites. The significance of this difference is discussed in Section 5.2.

5. Discussion 5.1. Are ODP sites 1127, 1129 and 1131 unique? As noted by many studies, if sufficient organic carbon (TOC) is available, microbial metabolic activity is high and methane is generated in marine sediments following almost complete SR; Site 1229 is an example (Fig. 2). At the opposite extreme, when TOC is a limiting factor, as at Site 1126, microbial metabolic activity is low, SR does not go to completion, and methane is at or close to background levels (Fig. 2). These examples (Sites 1126 and 1229) represent typical end-members of a continuum; as TOC increases, microbial metabolic activity increases, and SR proceeds to completion, followed by methane generation. Ocean Drilling Program Sites 1127, 1129, and 1131, as summarized in Section 3, are exceptions to this model. A few other ODP sites also exhibit significant methane generation in the presence of sulfate. Methane and sulfate concentrations at Site 1005, located on the margin of the Bahamas platform, overlap throughout most of the core length of about 700 m (Fig. 4) (Eberli et al., 1997). Indeed, the methane and sulfate concentration profiles at Site 1005 are similar to those at the high-gas GAB sites (Fig. 1). A second Bahamas margin site (1009; Fig. 4), although only cored to about 220 m, also exhibits an overlap in the sulfate and methane profiles. In both environments, with increasing depth below the sea floor, sulfate initially decreases then increases (Eberli et al., 1997). Even though it reaches the highest concentrations at minimum sulfate concentrations, methane is present at significant levels throughout the SRZ at both Bahamian sites. Interestingly, not every ODP site comprised of a thick section of Quaternary carbonates has overlapping SR and methanogenesis.

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2 Fig. 2. Profiles of CH4 (open squares) and SO− (solid circles) concentrations in the pore-water of ODP Site 1126 (gas-free), Great Australian Bight. For comparison, ODP Site 1229 4 (Peru margin) illustrates these profiles in a dominantly siliciclastic sedimentary environment. Dashed line represents approximate base of Quaternary section for Site 1126; entire profile of Site 1229 is Quaternary. Sediment depth and data source as in Fig. 1.

Despite a thick section of Quaternary carbonates, Site 821, on the continental margin of northeastern Australia, displays the typical biogeochemical zonation of dissolved constituents with a shallow SRZ and a deeper methanogenic zone (Fig. 4). This site, and some of its companion sites cored on ODP Leg 133, resembles those of the GAB and the Bahamas in all but one respect — the Leg 133 sites lack a subseafloor supply of sulfate. Consequently, there is no deep production of H2S in any of these sites and no overlap of the SRZ with the methanogenic zone. That is, even with a thick section of Quaternary carbonates, only methane is generated after the original sulfate is depleted. 5.2. Methanogenesis in carbonate sediments

Table 1 Summary of characteristics for high-gas and low-gas sites, ODP Leg 182, Great Australian Bight. High-gas (eg., Site 1127)

Low-gas (e.g., Site 1126)

Carbonates dominant Hypersaline pore water Deep sulfate present High sedimentation rate Moderate TOC High H2S High CH4

Carbonates dominant Hypersaline pore watera Deep sulfate presenta Low sedimentation rate Low TOC Undetected to low H2S Background to low CH4

Except Site 1128.

Table 2 Concentrations (picomoles/mg) and D/L values for three amino acids in bulk foraminifera from ODP Sites 1126 (low-gas) and 1127 (high-gas), Great Australian Bight. Depth (mbsf)

Methanogenic Archaea do not utilize large organic molecules. Their metabolic diversity is limited to three types of pathways based

a

on their preferred carbon substrates: CO2, acetate, and low molecular weight methylated compounds (Liu and Whitman, 2008). Most methanogens produce methane either by reduction of CO2, with H2 as the primary electron donor, or by reduction of the methyl group of acetate (acetate fermentation). However, SRB out-compete methanogens for both H2 and acetate so that the pathways for CO2 reduction and acetate fermentation by methanogens are inhibited during active

Aspartic acid (pM/mg)

D/L Asp

Glutamic acid (pM/mg)

D/L Glu

Alanine (pM/mg)

D/L Ala

ODP Site 1126 0.1 1245 6.6 772 16.1 482 44.6 454 54.1 438 82.6 366 92.1 359 148.3 253 167.3 274

0.18 0.41 0.56 0.67 0.72 0.83 0.81 0.82 0.73

561 415 312 284 288 210 230 189 216

0.08 0.20 0.31 0.44 0.52 0.75 0.71 0.74 0.66

671 481 423 342 318 193 241 244 235

0.11 0.37 0.55 0.75 0.83 0.99 1.00 0.97 0.88

ODP Site 1127 0.1 1266 15.5 1092 72.5 879 91.5 767 491.6 270

0.08 0.35 0.51 0.56 0.79

627 547 452 438 209

0.04 0.15 0.25 0.26 0.73

668 595 518 541 225

0.04 0.30 0.46 0.49 0.97

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Fig. 3. Concentrations (picomoles/mg) and D/L ratios of aspartic acid in bulk foraminifera from a gas-free site (ODP Site 1126) and a high-gas site (Site 1127), Great Australian Bight. See Figs. 1 and 2 for approximate base of Quaternary section. Sediment depth as in Fig. 1.

SR (Abram and Nedwell, 1978; Ferry and Lessner, 2008). Only after SR is completed will methanogens be able to utilize CO2 and acetate. The third metabolic pathway for methanogens involves low-carbonnumber methylated compounds such as methanol, methylated amines (mono-, di-, and trimethylamine, and tetramethylammonium), and methylated sulfides (e.g., dimethyl sulfide and metha-

nethiol). SRB do not utilize these molecules, and they therefore serve as “non-competitive” substrates (NCS) for methylotrophic methanogens (Liu and Whitman, 2008). When sufficiently available, these NCS allow methanogens to function actively in the presence of sulfate, as demonstrated in several investigations (Oremland and Taylor, 1978; Oremland and Polcin, 1982; Oremland et al., 1982a,b; Kiene et al.,

2 Fig. 4. Profiles of CH4 (open squares) and SO− (solid circles) concentrations in the pore water of ODP Sites 1005 and 1009, Bahamas margin, and Site 821, northeast Australia 4 margin. Dashed line represents approximate base of Quaternary section for Site 1005; entire profiles of Sites 1009 and 821 are Quaternary. Sediment depth and data source as in Fig. 1.

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1986; Oremland et al., 1987; Oremland et al., 1988; Wang and Lee, 1995). The only explanation, therefore, consistent with known metabolic pathways for the generation of high concentrations of methane in the presence of abundant sulfate and H2S at ODP Sites 1127, 1129, and 1131, and others, is that non-competitive methylated substrates are available for methanogens. Two questions arise from this observation: (1) what are the sources of the NCS, and (2) why are these substrates present in the high-gas sites of the GAB and the Bahamas, but not in the other GAB sites or, for that matter, in most other marine sediments? Based on studies noted above, the two most likely sources for NCS in these marine carbonates are methyl sulfides and methyl amines. Methyl sulfides, such as dimethyl sulfide (DMS) and methanethiol (MeSH), have been demonstrated to serve as NCS for methanogens in incubation experiments using various sediments (Kiene et al., 1986; Oremland et al., 1988). Although these volatile sulfur compounds are produced by organisms in the marine photic zone (e.g., Andreae and Raemdonck, 1983), they may also form abundantly within sediments through secondary reactions due to the high concentration of reactive sulfide. For example, DMS and MeSH may be generated through nucleophilic attack by sulfide on methyl groups in the sedimentary OM. This mechanism would explain why co-generation of methane and H2S occurs in marine sediments such as those of the GAB with a sub-seafloor source of sulfate, but not in sediments lacking a deeper sulfate source, such as those of Leg 133 (northeastern Australia). It would also explain why other GAB sites with a sub-seafloor brine have little or no gas production. The organic carbon content in these low-gas sites is too low for SR, and therefore no sulfide is generated to participate in secondary reactions. Interestingly, methyl sulfides, in addition to serving as substrates for methanogens, may also inhibit AOM. Moran et al., (2008) found that MeSH inhibited AOM while DMS had only a small inhibitory effect on AOM. Thus, methyl sulfides, especially MeSH, may play a dual role, first by enhancing the generation of methane and then by inhibiting anaerobic oxidation of the resulting methane. Methylamines are another documented example of NCS for methanogens (e.g., Oremland et al., 1982a, 1987; Wang and Lee, 1995; Liu and Whitman, 2008). As suggested by Mitterer et al. (2001), a potential source for a variety of methylamines is the protein matrix within biotic carbonate sediments. As this protein is hydrolyzed to smaller peptides and free amino acids during diagenesis (Mitterer, 1993), and some or all of the amino acids are converted to amines, these compounds leach from the carbonate minerals into the pore water where they can be metabolized by methanogens. In addition, sedimentary carbonate mineral surfaces attract extracellular polymeric substances (EPS) (Dupraz et al., 2008) that may be enriched in aminelike components (Carter, 1978; Carter and Mitterer, 1978; Mitterer and Cunningham, 1985). As the carbonate sediments are buried, these EPS as well as dissolved organic matter (DOM) may also undergo diagenetic alteration to simpler compounds, including possibly those favored by methanogens. An ample supply of methylated amine substrates from these sources, biotic carbonates, EPS and DOM, will enable methanogens to generate methane in the presence of active SR. This hypothesis for the source of methylamines would explain why significant co-generation of methane and H2S occurs in the highgas sites but not in low-gas sites. The high-gas sites in the GAB and the Bahamas not only have greater amounts of organic carbon (ranging up to ∼1% TOC) as well as significantly higher carbonate sedimentation rates (∼ 200–400 m/myr) than the low-gas GAB sites (Feary et al., 2000), but also greater amounts of protein products (i.e., amino acids and amines), from the thick section of younger biotic carbonates, to serve as NCS for methanogens (Table 2 and Fig. 3; Mitterer et al., 2001). The low-gas GAB sites have very low sedimentation rates (∼10 m/myr), low organic carbon values (mostly less than 0.4% TOC), and lower amounts of protein products from biotic carbonates. Overall, then, an argument can be made that either methyl sulfides or methylamines, or both, are available as NCS for methanogens in the

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high-gas sites of the GAB and Bahamas but not in the low-gas sites. Although the number of high-gas sites from the widely distant regions of the GAB and the Bahamas is only a handful, they have several common denominators. All the sites are dominantly Quaternary carbonates with low concentrations of reactive iron, have sub-seafloor sources of sulfate, have moderate amounts of TOC, lie in relatively deeper water (i.e., below wave base), and have high sedimentation rates; that is, they consist of young carbonate sediments. This combination creates the necessary and sufficient conditions for microbial co-generation of H2S and methane in marine sediments. Fig. 5 illustrates general reaction schemes for the formation of methyl sulfides and methylamines by the pathways described above and their subsequent utilization by methanogens. Although the GAB and Bahamian localities appear to be exceptional examples of sites that lack a sulfate-methane transition zone, many open ocean ODP sites, as noted by D'Hondt et al. (2002), contain relatively low, but above background, methane concentrations, in the range of 10–1000 µL/L, together with abundant sulfate. It is possible therefore that low concentrations of NCS may be present in many marine sediments, including non-carbonates, and the interpretation in the present study may apply to a wider range of marine environments. That is, the extent of methanogenesis within the SRZ of any marine sediment is a function of the availability of NCS. 5.3. Proposed new model for sulfate reduction and methanogenesis in marine sediments Fig. 6 presents a proposed new model for SR and methanogenesis in marine sediments that incorporates the parameters described in Section 5.2. Variables in the model, as outlined in Table 3, are type of substrate, TOC, rate of microbial activity, and pore water salinity. Two end-members (Biogeosystems A and B in Fig. 6 and Table 3) give the parameters for biogeochemical processes in most open marine sediments ranging from minimal microbiological activity, when organic carbon is limiting, to complete SR followed by methanogenesis when organic carbon is more abundant. Biogeosystem C, the third end-member in Fig. 6 and Table 3, extends the range of microbiological activity to include mutual SR and methanogenesis in the presence of NCS and an additional source of sulfate. Biogeosystems A and B apply to siliciclastic as well as carbonate sediments; Biogeosystem C applies only to iron-limited carbonate sediments with significant sources of NCS and sub-seafloor recharge of normal to hypersaline seawater. While the three end-members typify limiting conditions, it should be recognized that a continuum exists within these extremes as emphasized by the ternary diagram (Fig. 6). Biogeosystem A. With low TOC values and low sedimentation rates, Biogeosystem A (Fig. 6 and Table 3) represents the limiting parameters for minimal SR and methanogenesis. In these sediments, typically, sulfate is not completely reduced and methanogenesis does not occur. As noted in Section 5.2, however, D'Hondt et al. (2002) have shown that methane occurs above background levels, albeit at low concentrations, in the SRZ at many ODP sites. In these environments, NCS may be available at concentrations that allow methanogens some limited functionality in the SRZ. In other locations, as at Site 1126, a subseafloor source of sulfate may be present, but due to very low TOC values, little or no SR or methanogenesis occurs. Typical environments for Biogeosystem A occur in low productivity regions of the open ocean or continental margins; ODP Sites 846 (eastern Equatorial Pacific) and 1126 (Great Australian Bight) are representative examples. Biogeosystem B. With increasing TOC, SR goes to completion. As illustrated by Biogeosystem B (Fig. 6 and Table 3), methanogenesis then follows at greater depth with a sulfate-methane transition zone between the two regions. This is the classical model of SR and methanogenesis as described in many previous studies. With no additional source of sub-seafloor sulfate, methanogenic activity does not require the presence of NCS, although some may be available, after

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Fig. 5. Proposed reaction schemes for the formation of methyl sulfides and methylamines in marine sediments. Methyl sulfides form by reaction between sulfide and methyl groups of sedimentary organic matter. Methylamines form through diagenesis of the protein within biotic carbonates and leaching of the products into the pore water. TOC — total organic carbon; Q — Quaternary; SRB — sulfate-reducing bacteria; NCS — non-competitive substrates; MOG — methanogenesis; AOM — anaerobic oxidation of methane.

all sulfate is reduced. Typical environments for Biogeosystem B include upwelling areas, productive continental margins, and other regions with moderate to high TOC and sedimentation rates; ODP Sites 821 (northeast Australia margin) and 1229 (Peru margin) are representative examples. Biogeosystem C. As discussed in Section 5.2 and as proposed here, Biogeosystem C (Fig. 6 and Table 3) is unique to carbonate environments with little or no reactive iron, sub-seafloor recharge of normal to hypersaline seawater, moderate to high sedimentation rates, at least moderate levels of TOC, and an adequate supply of noncompetitive methylotrophic substrates for methanogens. Under these conditions, methane and H2S are generated at significant concentrations throughout a large part of the sediment column, and the sulfatemethane transition zone is absent. Type examples for Biogeosystem C are ODP Sites 1005 (Bahamas margin) and 1131 (Great Australian Bight). Fig. 7 summarizes the SR and methanogenic processes occurring in marine sediments with abundant organic carbon in the presence and absence of NCS. The left side of Fig. 7 represents Biogeosystem B in which NCS are absent and methanogenesis occurs only after SR is completed. The right side shows co-generation of H2S and methane when NCS are present, as envisioned in Biogeosystem C.

5.4. Sulfate reduction: which process? An important question raised by the data presented here is: By which metabolic process is SR occurring in the high-gas sites of the GAB and the Bahamas? The two processes by which sulfate is reduced

in marine sediments, both mediated by microbial activity, are: (1) the action of SRB using sedimentary OM as the carbon source and sulfate as the electron acceptor (e.g., Froelich et al., 1979), and (2) AOM by a consortia of archaea using methane as the carbon source instead of other organic compounds, with sulfate also serving as the electron acceptor. Hinrichs and Boetius (2002), Valentine (2002), Reeburgh (2007) and Caldwell et al. (2008) recently reviewed AOM processes. Reactions for SR may be written with HS− or H2S as the product (Caldwell et al., 2008). Summary reactions for production of H2S by SR and AOM are: −

2−

ðSRÞ SO4 þ 2½CH2 O→H2 S þ 2HCO3 2−

þ

ðAOMÞ CH4 þ SO4 þ 2H →H2 S þ CO2 þ 2H2 O

ð1Þ ð2Þ

where [CH2O] represents organic matter. Two possible scenarios for the microbially-mediated reactions leading to extensive co-generation of H2S and methane in carbonate sediments are: (1) SRB and methanogens are mutually active, with the methanogens utilizing NCS. In this simple scenario, SRB and methanogens act independently, all of the H2S is produced by the action of SRB, and AOM is either not occurring or lags methanogenesis. (2) In a more complex scenario, the activity of SRB gradually declines, perhaps due to poisoning by the high levels of H2S (Icgen and Harrison, 2006). Methanogens initially utilize NCS but may utilize both competitive and non-competitive substrates when SRB

Fig. 6. The proposed model for the range of microbial activity in marine sediments based on the variables listed in Table 3 for the three end-members. Additional details are provided in the text. TOC — total organic carbon; NCS — non-competitive substrates.

R.M. Mitterer / Earth and Planetary Science Letters 295 (2010) 358–366 Table 3 Proposed model for sulfate reduction and methanogenesis in marine sediments based on organic carbon substrate, total organic carbon, rate of microbial activity and porewater salinity. Microbial reactions

Biogeosystem A

Biogeosystem B

Biogeosystem C

No sulfate reduction or methanogenesis

Complete sulfate reduction; deeper methanogenesis

Sulfate reduction with methanogenesis

Substrate

Mostly competitive Low Low

Mostly competitive Moderate to high High

Mostly noncompetitive Moderate to high High

Possible

Absent

Present

Low

Moderate to high

Moderate to high

Variable Open ocean; low productivity margins ODP Sites 846, 1126

Variable High productivity margins

Carbonate High productivity margins

ODP Sites 821, 1229

ODP Sites 1005, 1131

TOC Microbial activity Sub-seafloor sulfate source Sedimentation rate Lithology Typical environments Type examples

become less active. At some point, AOM begins and, with sulfate serving as the electron acceptor, leads to further production of H2S. The concentration of methane is maintained at a balance between generation and reduction by the microbial processes of methanogenesis and anaerobic oxidation, although the rate of AOM must be less than the rate of methanogenesis. Stable carbon isotopes do not inform if AOM is occurring in the GAB sites. The usual evidence for AOM is a very low carbon isotopic composition (δ13C b − 50%o) for dissolved inorganic carbon or carbonate cements, the oxidation products of biogenic methane (e.g., Reeburgh, 2007). Carbonate sediments in the GAB sites, however, dominate the carbon isotopic values in this environment, overwhelming any possible isotopic signal due to methane oxidation (Mitterer, et al., 2001). The lack of carbon isotopic evidence does not preclude the occurrence of AOM in these sites, only that it cannot be demonstrated. In fact, neither of the two scenarios above can be ruled out, and both are possible explanations for co-generation of H2S and methane. The second option is the preferred choice on the basis that AOM is inferred to be the main process for methane consumption and SR when both sulfate and methane are available.

Fig. 7. Overview of sulfate reduction and methanogenesis in organic carbon-rich marine sediments in the presence and absence of non-competitive substrates for methanogens. The left side corresponds to the microbial reactions occurring in Biogeosystem B, while the right side illustrates the reactions occurring in Biogeosystem C. SOM – sedimentary organic matter; AOM – anaerobic oxidation of methane; NCS – non-competitive substrates.

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6. Significance to the global carbon cycle The model presented here is relevant to the global carbon cycle and climate. With no sulfate-methane transition zone, and with incomplete consumption of H2S and methane, the high concentrations of these reduced gases in thick sequences of carbonates may lead to the formation of clathrate structures, containing both methane and H2S, as possibly occur in GAB sediments (Swart et al., 2000). Whether or not clathrates form, the reduced gases, if present as free gas, may escape into the water column. Accordingly, continental margin carbonate sediments may be a previously unrecognized source of these reduced gases to the oceanic water column and, potentially, to the atmosphere. The only currently known locations of possible gas escape from marine carbonates are the sediments of the GAB and the Bahamas margin, described here; neither of these regions are sufficiently extensive to be major sources of methane or H2S to the water column. During previous times of widespread carbonate– evaporite deposition, however, methane produced in carbonatedominated margin sediments may have been a significant contributor to the global greenhouse. Depending on the depth and temperature of the sea floor in these regions, methane and H2S may have diffused continuously from the sediments or may have been temporarily stored in clathrates that were periodically destabilized. Methane and H2S would also have contributed to oxygen demand in the ocean–atmosphere system leading to a partial drawdown of O2 as the reduced gases were oxidized (Dickens, 2001); the decrease in O2, and the presence of H2S, in turn, would have had a severe impact on animal life. 7. Summary and conclusions Marine sediments display a greater range of biogeochemical variability than previously recognized. In addition to the wellknown relationship of a SRZ above the methanogenic zone, documented in numerous studies, some marine environments exhibit completely overlapping SR and methanogenic zones and an absence of the sulfate-methane transition zone. This latter relationship is best seen in carbonate sediments with high concentrations of H2S and methane located on the southern margin of Australia and the margin of the Bahamas platform. Methanogens are known to utilize non-competitive substrates such as methylamines and methyl sulfides, and several previous investigations have shown that methanogens are active during sulfate reduction when these substrates are available. Methylamines may be derived from the organic matrix of biotic carbonates, and methyl sulfides may be generated by high concentrations of H2S acting on sedimentary OM. The optimum conditions for co-generation of high concentrations of methane and H2S appear to be rapidly accumulating, iron-poor carbonate sediments, a sub-seafloor supply of sulfate, and sufficient TOC levels. These results are incorporated in a new model for SR and methanogenesis in marine sediments. The end-members in this ternary model are: (1) minimal SR and methanogenesis, (2) complete SR followed by methanogenesis, with a sulfate-methane transition zone, and (3) overlapping SR and methanogenesis, with no transition zone. The focus of previous research has been on the usual biogeochemical model of a SRZ and an underlying methanogenic zone, with a sulfate-methane transition zone at the interface of the two. Future studies should address the exceptions to the prevailing model described here and whether these exceptions are anomalies or whether they provide further insight into deep marine microbial processes. Neither of the two high-gas environments described here is contributing significant H2S or methane to the ocean–atmosphere system at present. However, during previous times of extensive carbonate deposition, these gases may have been generated in

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