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Microbial Ecology of Sulfur Cycling in Marine Sediments

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Microbial Ecology of Sulfur Cycling in Marine Sediments Environmental Microbiology Reports (2017) 9(4), 323–344 doi:10.1111/1758-2229.12538 Minireview The life sulfuric: microbial ecology of sulfur cycling in marine sediments Kenneth Wasmund,1,2† Marc Mußmann1† and Introduction Alexander Loy 1,2*† Marine sediments are dynamic environments that are 1Department of Microbiology and Ecosystem Science, shaped by interactions among biotic and abiotic pro- Division of Microbial Ecology, Research Network cesses including the redox reactions by which microor- “ Chemistry meets Microbiology”, University of Vienna, ganisms harness energy (Schrenk et al., 2010). While Althanstrasse 14, Vienna, A-1090, Austria. macrofauna may exist and cause some bioturbation in 2Austrian Polar Research Institute, Vienna, Austria. the most upper sediment layers (Bertics and Ziebis, 2010), the vast diversity and biomass of life at and Summary below the seafloor is predominantly microscopic. Sedi- mentary microorganisms utilise various combinations of Almost the entire seafloor is covered with sediments available electron donors and acceptors for energy con- that can be more than 10 000 m thick and represent a servation, the combinations of which are largely under vast microbial ecosystem that is a major component thermodynamic controls (Jørgensen, 2000) and are also of Earth’s element and energy cycles. Notably, a highly dependent on the amounts, types and rates of significant proportion of microbial life in marine sedi- their respective inputs. Together, these factors manifest ments can exploit energy conserved during transfor- in the depth stratification of marine sediments i.e. a con- mations of sulfur compounds among different redox tinuum of more or less overlapping biogeochemical states. Sulfur cycling, which is primarily driven by zones, whereby each zone is characterised by the pre- sulfate reduction, is tightly interwoven with other vailing electron acceptors (Canfield and Thamdrup, important element cycles (carbon, nitrogen, iron, 2009). In particular, sulfate is an ubiquitous electron manganese) and therefore has profound implications acceptor in marine sediments due to its high concentra- for both cellular- and ecosystem-level processes. tion in seawater (28 mM). Seawater diffuses into sedi- Sulfur-transforming microorganisms have evolved ments and sulfate respiration is thus one of the most diverse genetic, metabolic, and in some cases, pecu- important microbial redox process in marine sediments liar phenotypic features to fill an array of ecological once more energetically favourable electron acceptors niches in marine sediments. Here, we review recent such as oxygen, nitrate/nitrite, and iron and manganese and selected findings on the microbial guilds that are oxides are depleted. involved in the transformation of different sulfur com- On a global scale, recent estimates suggest the remi- pounds in marine sediments and emphasise how neralisation of up to 29% of the organic matter that is these are interlinked and have a major influence on deposited to the seafloor is facilitated by sulfate- ecology and biogeochemistry in the seafloor. Extraor- reducing microorganisms (SRM) (Bowles et al., 2014), dinary discoveries have increased our knowledge on which are conventionally regarded as terminal compo- microbial sulfur cycling, mainly in sulfate-rich sur- nents of anaerobic microbial food webs that coopera- face sediments, yet many questions remain regarding tively degrade organic matter. The activity of SRM is how sulfur redox processes may sustain the deep- particularly important in organic-rich sediments underly- subsurface biosphere and the impact of organic sul- ing the highly productive waters of continental shelves fur compounds on the marine sulfur cycle. and slopes (Jørgensen, 1982; Jørgensen and Kasten, 2006). Global estimates indicate that 11.3 teramoles of sulfate are reduced to hydrogen sulfide in marine sedi- ments every year (Bowles et al., 2014). In turn, hydro- *For correspondence. E-mail [email protected]; Tel. 143 1 4277 76605; Fax 143 1 4277 876605. †All authors contributed gen sulfide and other reduced sulfur compounds serve equally to this review. as electron donors for sulfur-oxidising microorganisms VC 2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 324 K. Wasmund et al. Fig. 1. Conceptual depiction of the sulfur cycle in marine sediments, including main reactions of inorganic and organic sulfur compounds, selected taxa, sulfur oxidation via long-range electron transport by cable bacteria, sulfate-dependent anaerobic methane oxidation, and trans- formations of sulfur compounds of intermediate oxidation states (sulfur cycle intermediates, SCI). Blue lines depict biologically-mediated sulfur transformations that can also be components of disproportionation reactions. Orange lines depict abiotic reactions. Inorganic sulfur compounds are depicted within yellow eclipses. Other electron acceptors are depicted within orange ellipses, and electron donors are depicted within blue ellipses. OSM 5 organo-sulfur molecules, Corg 5 organic matter. DIET 5 direct-interspecies electron transport. ANME 5 anaerobic methane- oxidising. (SOM) or are abiotically oxidised. Sulfate reduction is improved considerably during recent years. Yet, there thereby the primary driver of the biogeochemical cycling still remain significant questions regarding the biology of of sulfur in marine sediments (Fig. 1). Sulfur cycling is a microorganisms and factors that control the turnover of major determinant of the biogeochemistry and microbial sulfur compounds in marine sediments. For example, lit- ecology in sulfate-rich surface sediments and the under- erally only the (sediment) surface of the species rich- lying sulfate-methane transition zone (SMTZ). Interest- ness of sulfur-transforming microorganisms in the ingly, the discovery of cryptic sulfur cycling i.e. the rapid subseafloor realm, which is one of the largest microbial recycling of sulfur species at low sulfate concentrations biomes on Earth, has been explored. Cycling between (Holmkvist et al., 2011; Brunner et al., 2016) and contin- the most oxidised (16, sulfate) and most reduced (–2, uous detection of functional genes of SRM (Leloup sulfide) states of sulfur involves several inorganic sulfur et al., 2007; Leloup et al., 2009; Blazejak and Schippers, compounds of intermediate oxidation states (i.e. sulfur 2011; Aoki et al., 2015) in sulfate-poor sediment zones cycle intermediates, SCI) that allow for (i) sulfur metabo- deep below the SMTZ revealed that the impact of micro- lite handoff to other microorganisms and (ii) shortcuts in bial sulfur metabolism extends to biogeochemical zones the sulfur cycle (Fig. 1) (Jørgensen, 1990). The extent that were traditionally viewed as largely fermentative by which sulfur cycling in the different biogeochemical and methanogenic (Bowles et al., 2014; Glombitza sediment horizons is mediated by ‘sulfur compound syn- et al., 2016). trophy’, i.e. the interspecies transfer of SCI, and the Our understanding of sulfur cycling processes and the interplay between generalists that utilise diverse sulfur biology of microorganisms that catalyse them has compounds of various oxidation states and specialists VC 2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 9, 323–344 Microbial sulfur cycling in marine sediments 325 that utilise only selected sulfur compounds, is unknown. variety of other substrates including longer fatty acids, Additionally, previous research has concentrated on alkanes, and aromatic compounds, some of which allow cycling of inorganic sulfur compounds, leaving the these organisms to thrive at natural hydrocarbon seeps impact of organic sulfur compounds on life in the sea- (Kleindienst et al., 2014; Na et al., 2015; Dorries et al., floor largely unexplored. Furthermore, individual microor- 2016b). Detailed proteomic-genomic analyses of cul- ganisms have evolved various, sometimes seemingly tured representatives of the marine Desulfobacteraceae redundant enzyme systems to catalyse the many possi- indicated their flexibility and ecological success is ble conversions of sulfur compounds between different afforded by a combination of physiological mechanisms oxidation states. While progress in the biochemical char- (Dorries et al., 2016a,b). These include multiple oxygen acterisation of these enzymes is continuously made defence systems, various signal transduction pathways (Denger et al., 2014; Felux et al., 2015; Santos et al., for sensing different environmental cues such a sub- 2015; Johnston et al., 2016), some sulfur pathways and strate availability, as well as abundant and constitutively sulfur-converting enzymes are yet to be discovered and/ expressed membrane-bound redox complexes that are or functionally characterised (Milucka et al., 2012). important for linking electron flows from the catabolism In this review, we highlight recent and selected find- of different substrates to respiration. Recent studies sug- ings in marine sediment sulfur cycle microbiology and gest that members of the uncultured Sva0081 clade of address knowledge gaps that might become emphases the Desulfobacteraceae are particularly abundant in for
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