13.3: Interactions of the sulfur and oxygen cycles

The sulfur cycle of marine sediments is primarily driven by the dissimilatory sulfate reduction (DSR) to sulfide by anaerobic microorganisms (e.g., Jørgensen and Kasten, 2006). This process links the complex food web of organic matter degradation to the terminal organic carbon oxidation to CO₂. Most of the sulfide is ultimately reoxidized back to sulfate, via diverse sulfur intermediates, by geochemical or microbial reactions that involve oxygen, nitrate, manganese [Mn(IV)], iron [Fe(III)], and other potential oxidants (e.g., Rickard, 2012). A fraction of the sulfide precipitates with iron and other metals or reacts with organic matter and is buried deeply into the seabed. The microbial sulfur transformations affect the isotopic composition of sulfate and sulfides and the resulting isotope fractionation is thereby diagnostic for both process rates and pathways of the sulfur cycle (e.g., Canfield, 2001).

Figure \(\PageIndex{1}\): The biogeochemical sulfur cycle of marine sediments. Arrows indicate fluxes and pathways of biological or chemical processes. For further explanation, see text. (Copyright; Barker Jørgensen, Alyssa J. Findlay and André Pellerin via Frontiers in Microbiology)

Figure \(\PageIndex{1}\) presents the sulfur cycle of marine sediments. The processes include chemical reactions, microbially catalyzed pathways, and a combination of both. Sulfate (SO₄^2-) reduction to sulfide (H₂S + HS^- + S^2-) is driven by the oxidation of buried organic carbon (C_org), supplemented by the anaerobic oxidation of methane (CH₄) at the subsurface sulfate-methane transition (SMT). Manganese and iron reduction are focused toward the surface sediment, but Fe(III) is also buried and acts as an oxidant for sulfide in the deeper sediment layers where it partly binds the produced sulfide as iron sulfide (FeS) and pyrite (FeS₂). Pyrite is the end product of iron-sulfide mineral formation and provides a deep sink for sulfur. Two pathways of pyrite formation are the “polysulfide pathway” (1) and the “H₂S pathway” (2) (Figure \(\PageIndex{1}\)). The sulfidization of buried organic matter provides an additional deep sink for sulfur. Intermediate sulfur species, such as elemental sulfur (S⁰), thiosulfate (S₂O₃^2-), tetrathionate (S₄O₆^2-), and sulfite (SO₃^2-), are formed during the oxidation of sulfide by, for example, buried Fe(III). These intermediates may be reduced back to sulfide, oxidized further to sulfate, or disproportionated to form both sulfide and sulfate. In very sulfidic sediments, a part of the sulfide diffuses up to the surface sediment where it may be oxidized by cable bacteria, by large sulfur bacteria such as Beggiatoa spp., or by other, less conspicuous sulfide oxidizers. The different pathways of sulfide oxidation ultimately depend on oxygen (and less on nitrate) as the ultimate oxidant, and thereby consume a considerable part of the total oxygen uptake of the seabed (Jørgensen, 1982b). The oxygen flux into the sediment is enhanced by bioirrigation (ventillation of burrows) by the benthic macrofauna (e.g., Kristensen et al., 2013).

Sulfate Reduction

Organic Matter Degradation

Organic matter deposited on the seafloor provides food for the benthic communities, either at the sediment surface or upon burial into the sediment layers below. Oxygen is available for respiration and chemical reactions near the surface and through faunal burrows. Beneath this mixed surface zone, marine sediments constitute an anoxic world inhabited by anaerobic microorganisms. These subsurface organisms become increasingly sparse with depth, yet they account for half of all microbial cells in the ocean (Kallmeyer et al., 2012). Their energy source in most of the seabed is the buried organic matter, which they oxidize to CO₂ and inorganic nutrients. Due to the high concentration of sulfate in seawater (28 mM at an ocean salinity of 35), sulfate generally penetrates meters down into the seabed and supplies the sulfate reducing microorganisms (SRM) with an electron acceptor for their respiration. As the sediment ages with increasing burial depth beneath the seafloor, the remaining organic matter becomes steadily more refractory to microbial degradation. The time-course of organic matter degradation in the sediment, and thus of sulfate reduction rates (SRR), can be described by the sum of several exponential decay functions relating to different organic matter components, each of which is being degraded by first-order kinetics (Westrich and Berner, 1984).

The anaerobic degradation of organic matter involves complex microbial food chains, starting with the hydrolysis of macromolecular structures by extracellular enzymes and the formation of organic molecules small enough (generally < ca. 600 dalton, but for polysaccharides possibly larger) to be taken up by bacteria or archaea (Arnosti, 2011; Reintjes et al., 2017). It is this initial hydrolysis of the complex organic material that is rate-limiting for the overall degradation rate of organic matter (Kristensen and Holmer, 2001; Arnosti, 2004; Beulig et al., 2018). Microbial cells, which take up the small organic molecules such as sugars, amino acids, lipids, organic acids etc., conserve energy and grow by multistep fermentation processes that produce a range of volatile fatty acids (VFAs), such as formate, acetate, propionate and butyrate, plus H₂ and CO₂.

Sulfide Oxidation

Mass balance estimates and diffusion gradients of sulfide indicate that a significant fraction of the sulfide produced by sulfate reduction in marine sediments is reoxidized (Jørgensen, 1982b; Canfield et al., 1992; Pellerin et al., 2015b). This reoxidation occurs through diverse biological and geochemical pathways, forming a variety of reactive intermediates (Figure \(\PageIndex{2}\)). The extent of sulfide reoxidation depends upon the quantity and type of available oxidant as well as the presence of microorganisms (e.g., Luther et al., 2011).

Figure \(\PageIndex{2}\): Overview of the processes and major inorganic species of the sulfur cycle. The large black arrow represents sulfate reduction, thin black lines represent oxidation and dotted lines represent disproportionation reactions. The dashed lines represent equilibration to form polysulfides. Schematic adapted from Zopfi et al. (2004). (Copyright; Copyright; Barker Jørgensen, Alyssa J. Findlay and André Pellerin via Frontiers in Microbiologyauthor via source)

Formation of Pyrite

The formation of pyrite (FeS₂) represents the main burial of sulfur, and thereby of reducing potential, in marine sediments, as pyrite is stable over geological timescales under anoxic conditions (Bottrell and Newton, 2006; Fike et al., 2015). Very generally, pyrite forms from the reaction of sulfide with buried ferric iron minerals, initially forming a mixture of elemental sulfur, polysulfides and ferrous iron minerals. Different overall reactions leading to pyrite formation in marine sediments have been proposed over the years, depending upon the initial reacting iron, and sulfur species. However, it has been argued that despite this potential variety only two reaction mechanisms are important: the reaction between FeS and H₂S (“H₂S pathway”; Equation 3) (Rickard and Luther, 1997; Thiel et al., 2019) and the reaction between FeS and polysulfide (“polysulfide pathway”; Equation 4) (Rickard and Luther, 2007).

\[\mathrm{FeS}+\mathrm{H}_2 \mathrm{~S} \rightarrow \mathrm{FeS}_2+\mathrm{H}_2\]
\[\mathrm{FeS}+\mathrm{S}_{\mathrm{x}}^{2-} \rightarrow \mathrm{FeS}_2+\mathrm{S}_{\mathrm{x}-1}{ }^{2-} \]

References

Arnosti, C. (2004). Speed bumps and barricades in the carbon cycle: substrate structural effects on carbon cycling. Mar. Chem. 92, 263–273. doi: 10.1016/j.marchem.2004.06.030

Arnosti, C. (2011). Microbial extracellular enzymes and the marine carbon cycle. Ann. Rev. Mar. Sci. 3, 401–425. doi: 10.1146/annurev-marine-120709-142731

Beulig, F., Røy, H., Glombitza, C., and Jørgensen, B. B. (2018). Control on rate and pathway of anaerobic organic carbon degradation in the seabed. Proc. Natl. Acad. Sci. U.S.A. 115, 367–372. doi: 10.1073/pnas.1715789115

Bottrell, S. H., and Newton, R. J. (2006). Reconstruction of changes in global sulfur cycling from marine sulfate isotopes. Earth Sci. Rev. 75, 59–83. doi: 10.1016/j.earscirev.2005.10.004

Canfield, D. E. (2001). Biogeochemistry of sulfur isotopes. Rev. Mineral. Geochem. 43, 607–636. doi: 10.2138/gsrmg.43.1.607

Canfield, D. E., Raiswell, R., and Bottrell, S. (1992). The reactivity of sedimentary iron minerals toward sulfide. Am. J. Sci. 292, 659–683. doi: 10.2475/ajs.292.9.659

Fike, D. A., Bradley, A. S., and Rose, C. V. (2015). Rethinking the ancient sulfur cycle. Annu. Rev. Earth Planet. Sci. 43, 593–622. doi: 10.1146/annurev-earth-060313-054802

Jørgensen, B. B. (1982b). Mineralization of organic matter in the sea bed - the role of sulfate reduction. Nature 296, 643–645. doi: 10.1038/296643a0:

Jørgensen, B. B., and Kasten, S. (2006). “Sulfur cycling and methane oxidation,” in Marine Geochemistry, eds H. D. Schulz and M. Zabel (Berlin: Springer), 271–309. doi: 10.1007/3-540-32144-6_8:

Kallmeyer, J., Pockalny, R., Adhikari, R. R., Smith, D. C., and D’Hondt, S. (2012). Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl. Acad. Sci. U.S.A. 109, 16213–16216. doi: 10.1073/pnas.1203849109

Kristensen, E., Haese, R. R., and Kostka, J. E. (2013). Interactions between Macro and Microorganisms in Marine Sediments, Coastal and Estuarine Studies, Vol. 60. Washington, DC: American Geophysical Union. doi: 10.1007/bf00413135

Luther, G. W. III, Findlay, A. J., MacDonald, D. J., Owings, S. M., Hanson, T. E., Beinart, R. A., et al. (2011). Thermodynamics and kinetics of sulfide oxidation by oxygen: a look at inorganically controlled reactions and biologically mediated processes in the environment. Front. Microbiol. 2:62. doi: 10.3389/fmicb.2011.00062

Pellerin, A., Bui, T. H., Rough, M., Mucci, A., Canfield, D. E., and Wing, B. A. (2015b). Mass-dependent sulfur isotope fractionation during reoxidative sulfur cycling: a case study from Mangrove Lake, Bermuda. Geochim. Cosmochim. Acta 149, 152–164. doi: 10.1016/j.gca.2014.11.007

Reintjes, G., Arnosti, C., Fuchs, B. M., and Amann, R. (2017). An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 11, 1640–1650. doi: 10.1038/ismej.2017.26

Rickard, D. (2012). Sulfidic Sediments and Sedimentary Rocks. Developments in Sedimentology, Vol. 65. Amsterdam: Elsevier. doi: 10.1126/science.207.4437.1355:

Rickard, D., and Luther, G. W. III (1997). Kinetics of pyrite formation by the H2S oxidation of iron (II) monosulfide in aqueous solutions between 25 and 125°C: The mechanism. Geochim. Cosmochim. Acta 61, 135–147. doi: 10.1016/s0016-7037(96)00322-5

Rickard, D., and Luther, G. W. III (2007). Chemistry of iron sulfides. Chem. Rev. 107, 514–562. doi: 10.1021/cr0503658

Thiel, J., Byrne, J. M., Kappler, A., Schink, B., and Pester, M. (2019). Pyrite formation from FeS and H₂S is mediated through microbial redox activity. Proc. Natl. Acad. Sci. U.S.A 116, 6897–6902. doi: 10.1073/pnas.1814412116

Westrich, J. T., and Berner, R. A. (1984). The role of sedimentary organic matter in bacterial sulfate reduction - the G model tested. Limnol. Oceanogr. 29, 236–249. doi: 10.4319/lo.1984.29.2.0236

Zopfi, J., Ferdelman, T. G., and Fossing, H. (2004). “Distribution and fate of sulfur intermediates - sulfite, tetrathionate, thiosulfate, and elemental sulfur - in marine sediments,” in Sulfur Biogeochemistry—Past and Present, Vol. 379, eds J. P. Amend, K. J. Edwards, and T. W. Lyons (Boulder, CO: Geological Society of America), 97–116. doi: 10.1130/0-8137-2379-5.97

Excerpted from:

Jørgensen, B. B., Findlay, A. J., & Pellerin, A. (2019). The biogeochemical sulfur cycle of marine sediments. Frontiers in microbiology, 10, 849. Accessed December 2023 at https://www.frontiersin.org/articles/10.3389/fmicb.2019.00849/full. CC-BY-4.0