Sulfur isotopes of organic matter preserved in 3.45-billion-year-old stromatolites reveal microbial metabolism

Bontognali, Tomaso R. R.; Sessions, Alex L.; Allwood, Abigail; Fischer, Woodward W.; Grotzinger, J. P.; Summons, Roger E.; Eiler, John M.

doi:10.1073/pnas.1207491109

Cited by 141 publications

(86 citation statements)

References 48 publications

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“…The model suggests that this is not because low sulfate levels limited isotopic fractionation (34), but because quantitative reduction of oxidized sulfur species followed by rapid pyrite formation prevented influence of microbial reduction on the isotopic composition of seawater sulfate. This is consistent with large variability in δ 34 S within single samples, indicating that microbial reduction resulted in strong fractionation as early as 3,450 Ma (35).…”

Section: Resultssupporting

confidence: 67%

Production, preservation, and biological processing of mass-independent sulfur isotope fractionation in the Archean surface environment

Halevy

2013

Proc. Natl. Acad. Sci. U.S.A.

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Mass-independent fractionation of sulfur isotopes (S MIF) in Archean and Paleoproterozoic rocks provides strong evidence for an anoxic atmosphere before ∼2,400 Ma. However, the origin of this isotopic anomaly remains unclear, as does the identity of the molecules that carried it from the atmosphere to Earth's surface. Irrespective of the origin of S MIF, processes in the biogeochemical sulfur cycle modify the primary signal and strongly influence the S MIF preserved and observed in the geological record. Here, a detailed model of the marine sulfur cycle is used to propagate and distribute atmospherically derived S MIF from its delivery to the ocean to its preservation in the sediment. Bulk pyrite in most sediments carries weak S MIF because of microbial reduction of most sulfur compounds to form isotopically homogeneous sulfide. Locally, differential incorporation of sulfur compounds into pyrite leads to preservation of S MIF, which is predicted to be most highly variable in nonmarine and shallow-water settings. The Archean ocean is efficient in diluting primary atmospheric S MIF in the marine pools of sulfate and elemental sulfur with inputs from SO 2 and H 2 S, respectively. Preservation of S MIF with the observed range of magnitudes requires the S MIF production mechanism to be moderately fractionating ( ± 20-40‰). Constraints from the marine sulfur cycle allow that either elemental sulfur or organosulfur compounds (or both) carried S MIF to the surface, with opposite sign to S MIF in SO 2 and H 2 SO 4 . Optimal progress requires observations from nonmarine and shallow-water environments and experimental constraints on the reaction of photoexcited SO 2 with atmospheric hydrocarbons.W ith few exceptions, the enrichment or depletion of the rare, stable isotopes of sulfur ( 33 S, 34 S, and 36 S) relative to the abundant isotope ( 32 S) scale as the mass difference between the isotopes (1). Sulfur isotope mass-independent fractionation (S MIF) is defined as a departure from these theoretically derived and empirically observed mass laws, and denoted Δ 33 S and Δ 36 S. S MIF is observed in modern atmospheric sulfate aerosols, as well as in sulfate-bearing layers hosted in glacial ice (2, 3), but is conspicuously absent from the sedimentary record of the last 2,400 My. In contrast, older rocks of the Archean and early Paleoproterozoic eons preserve large and variable S MIF (4, 5). On the basis of experimental SO 2 photolysis and atmospheric chemistry models, the prevailing hypothesis to explain this observation is that the absence of atmospheric oxygen before ∼2,400 Ma allowed both the photochemical production of S MIF and its delivery to the surface in the reduced and oxidized products of sulfur photochemistry (4-7). Thus, S MIF is considered strong geochemical evidence for an anoxic atmosphere before ∼2,400 Ma.Although research converges on atmospheric processes as the source of S MIF, its production mechanism and the identity of its vectors to the surface remain unclear. A focus on photolysis experiments and meas...

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Section: Resultssupporting

confidence: 67%

Production, preservation, and biological processing of mass-independent sulfur isotope fractionation in the Archean surface environment

Halevy

2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Near thermodynamic fractionations appear to be accessible at extremely low sulfate levels (<10 μM), as long as the average respiration rate of a sulfate-reducing population is low enough (79). This feature may neatly unite two conflicting views of S cycling on the Archean earth: large intrasample variability in δ 34 S values (80,81) in the face of low marine sulfate concentrations (6,82).…”

Section: Summary and Natural Extensionsmentioning

confidence: 99%

Intracellular metabolite levels shape sulfur isotope fractionation during microbial sulfate respiration

Wing

Halevy

2014

Proc. Natl. Acad. Sci. U.S.A.

220

266

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We present a quantitative model for sulfur isotope fractionation accompanying bacterial and archaeal dissimilatory sulfate respiration. By incorporating independently available biochemical data, the model can reproduce a large number of recent experimental fractionation measurements with only three free parameters: (i) the sulfur isotope selectivity of sulfate uptake into the cytoplasm, (ii) the ratio of reduced to oxidized electron carriers supporting the respiration pathway, and (iii) the ratio of in vitro to in vivo levels of respiratory enzyme activity. Fractionation is influenced by all steps in the dissimilatory pathway, which means that environmental sulfate and sulfide levels control sulfur isotope fractionation through the proximate influence of intracellular metabolites. Although sulfur isotope fractionation is a phenotypic trait that appears to be strain specific, we show that it converges on near-thermodynamic behavior, even at micromolar sulfate levels, as long as intracellular sulfate reduction rates are low enough (<<1 fmol H 2 S·cellissimilatory sulfate reduction is a respiratory process used by some bacteria and archaea to generate energy under anaerobic conditions. Aqueous sulfate serves as the terminal electron acceptor in this process, leading to the oxidation of organic carbon compounds and sometimes hydrogen and to the production of aqueous sulfide (1). Dissimilatory sulfate respiration was one of the first microbial metabolisms to be isotopically characterized through culture experiments (2), with 32 S-bearing sulfate shown to be consumed preferentially to 34 S-bearing sulfate. Early experiments identified two critical features of this dissimilatory sulfur isotope fractionation: Its magnitude correlates inversely with the sulfate reduction rate of an individual cell but correlates directly with extracellular sulfate concentrations (3-5).Through careful regulation of the environmental controls on respiration, more recent experiments have precisely calibrated these relationships and suggest that their particular form may be strain specific (6-11). All experiments, however, show a nonlinear response, where sulfur isotope fractionation increases rapidly with decreasing rate. At the low-rate limit, sulfur isotope fractionation appears to approach levels defined by thermodynamic equilibrium between aqueous sulfate and sulfide (8, 12), the initial reactant and final waste product in the respiratory processing chain.In parallel with experimental studies, theoretical work has built a broad foundation for understanding the net sulfur isotope fractionation expressed during sulfate respiration (13-17). These efforts initially dealt with sulfur flow through simplified metabolic networks (13) (Fig. 1A) and have expanded to incorporate, for example, electron supply to the reaction cycles of individual respiratory enzymes (17). The reversibility of an individual enzymatic reaction is a central theoretical concept behind these approaches, as it carries the isotopic memory of downstream steps in the pathway...

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“…Such zones may have two isotopically distinct populations of pyrite and TOS, corresponding to the upper and lower SMT fringe. Techniques such as sulfur isotope analyses using SIMS have the potential to reveal such variations and clustering of isotope signatures that remain undetected in a bulk sample (Xiao et al, 2010;Bontognali et al, 2012;Farquhar et al, 2013;Fischer et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Sulfur Cycling in an Iron Oxide-Dominated, Dynamic Marine Depositional System: The Argentine Continental Margin

Riedinger

Brunner

Krastel³

et al. 2017

Front. Earth Sci.

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The interplay between sediment deposition patterns, organic matter type and the quantity and quality of reactive mineral phases determines the accumulation, speciation, and isotope composition of pore water and solid phase sulfur constituents in marine sediments. Here, we present the sulfur geochemistry of siliciclastic sediments from two sites along the Argentine continental slope-a system characterized by dynamic deposition and reworking, which result in non-steady state conditions. The two investigated sites have different depositional histories but have in common that reactive iron phases are abundant and that organic matter is refractory-conditions that result in low organoclastic sulfate reduction rates (SRR). Deposition of reworked, isotopically light pyrite and sulfurized organic matter appear to be important contributors to the sulfur inventory, with only minor addition of pyrite from organoclastic sulfate reduction above the sulfate-methane transition (SMT). Pore-water sulfide is limited to a narrow zone at the SMT. The core of that zone is dominated by pyrite accumulation. Iron monosulfide and elemental sulfur accumulate above and below this zone. Iron monosulfide precipitation is driven by the reaction of low amounts of hydrogen sulfide with ferrous iron and is in competition with the oxidation of sulfide by iron (oxyhydr)oxides to form elemental sulfur. The intervals marked by precipitation of intermediate sulfur phases at the margin of the zone with free sulfide are bordered by two distinct peaks in total organic sulfur (TOS).Organic matter sulfurization appears to precede pyrite formation in the iron-dominated margins of the sulfide zone, potentially linked to the presence of polysulfides formed by reaction between dissolved sulfide and elemental sulfur. Thus, SMTs can be hotspots for organic matter sulfurization in sulfide-limited, reactive iron-rich marine sedimentary systems. Furthermore, existence of elemental sulfur and iron monosulfide phases meters below the SMT demonstrates that in sulfide-limited systems metastable sulfur constituents are not readily converted to pyrite but can be buried to deeper Riedinger et al.Non-steady State Subsurface Sulfur Cycling sediment depths. Our data show that in non-steady state systems, redox zones do not occur in sequence but can reappear or proceed in inverse sequence throughout the sediment column, causing similar mineral alteration processes to occur at the same time at different sediment depths.

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Sulfur isotopes of organic matter preserved in 3.45-billion-year-old stromatolites reveal microbial metabolism

Cited by 141 publications

References 48 publications

Production, preservation, and biological processing of mass-independent sulfur isotope fractionation in the Archean surface environment

Production, preservation, and biological processing of mass-independent sulfur isotope fractionation in the Archean surface environment

Intracellular metabolite levels shape sulfur isotope fractionation during microbial sulfate respiration

Sulfur Cycling in an Iron Oxide-Dominated, Dynamic Marine Depositional System: The Argentine Continental Margin

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