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Environmental filtering determines family-level structure of sulfate-reducing microbial communities in subsurface marine sediments


Recent work has shown that subsurface microbial communities assemble by selective survival of surface community members during sediment burial, but it remains unclear to what extent the compositions of the subsurface communities are a product of their founding population at the sediment surface or of the changing geochemical conditions during burial. Here we investigate this question for communities of sulfate-reducing microorganisms (SRMs). We collected marine sediment samples from the upper 3–5 m at four geochemically contrasting sites in the Skagerrak and Baltic Sea and measured SRM abundance (quantitative PCR of dsrB), metabolic activity (radiotracer rate measurements), and community composition (Illumina sequencing of dsrB amplicons). These data showed that SRM abundance, richness, and phylogenetic clustering as determined by the nearest taxon index peaked below the bioturbation zone and above the depth of sulfate depletion. Minimum cell-specific rates of sulfate reduction did not vary substantially between sites. SRM communities at different sites were best distinguished based on their composition of amplicon sequence variants (ASVs), while communities in different geochemical zones were best distinguished based on their composition of SRM families. This demonstrates environmental filtering of SRM communities in sediment while a site-specific fingerprint of the founding community is retained.

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  1. 1.

    Petro C, Starnawski P, Schramm A, Kjeldsen KU. Microbial community assembly in marine sediments. Aquat Microb Ecol. 2017;79:177–95.

  2. 2.

    Starnawski P, Bataillon T, Ettema TJG, Jochum LM, Schreiber L, Chen X, et al. Microbial community assembly and evolution in subseafloor sediment. Proc Natl Acad Sci USA. 2017;114:2940–5.

  3. 3.

    Walsh EA, Kirkpatrick JB, Rutherford SD, Smith DC, Sogin M, D'Hondt S. Bacterial diversity and community composition from seasurface to subseafloor. ISME J. 2016;10:979–89.

  4. 4.

    Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta GT. What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser. 2012;446:285–302.

  5. 5.

    Jørgensen BB, Marshall IPG. Slow microbial life in the seabed. Annu Rev Mar Sci. 2016;8:311–32.

  6. 6.

    Jørgensen BB. Mineralization of organic matter in the sea bed—the role of sulphate reduction. Nature. 1982;296:643–5.

  7. 7.

    Hoehler TM, Jørgensen BB. Microbial life under extreme energy limitation. Nat Rev Microbiol. 2013;11:83–94.

  8. 8.

    Jørgensen BB. A comparison of methods for the quantification of bacterial sulfate reduction in coastal marine sediments. Geomicro J. 1978;1:11–27.

  9. 9.

    Müller AL, Kjeldsen KU, Rattei T, Pester M, Loy A. Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases. ISME J. 2015;9:1152–65.

  10. 10.

    Pelikan C, Herbold CW, Hausmann B, Müller AL, Pester M, Loy A. Diversity analysis of sulfite- and sulfate-reducing microorganisms by multiplex dsrA and dsrB amplicon sequencing using new primers and mock community-optimized bioinformatics. Environ Microbiol. 2016;18:2994–3009.

  11. 11.

    Vigneron A, Cruaud P, Alsop E, Rezende JR, Head IM, Tsesmetzis N. Beyond the tip of the iceberg; a new view of the diversity of sulfite- and sulfate-reducing microorganisms. ISME J. 2018;12:2096–9.

  12. 12.

    Rabus R, Venceslau SS, Whlbrand L, Voordouw G, Wall JD, Pereira IAC. A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes. In: Poole RK, editor. Advances in Microbial Physiology, 1st ed., Vol. 66, pp. 55–321. Cambridge: Elsevier, 2015.

  13. 13.

    Canfield DE, Des Marais DJ. Aerobic sulfate reduction in microbial mats. Science. 1991;251:1471–3.

  14. 14.

    Jørgensen BB, Bak F. Pathways and microbiology of thiosulfate transformations and sulfate reduction in a marine sediment (Kattegat, Denmark). Appl Environ Microbiol. 1991;57:847–56.

  15. 15.

    Cypionka H, Widdel F, Pfennig N. Survival of sulfate-reducing bacteria after oxygen stress, and growth in sulfate-free oxygen-sulfide gradients. FEMS Microbiol Ecol. 1985;31:39–45.

  16. 16.

    Sass H, Cypionka H, Babenzien H-D. Vertical distribution of sulfate-reducing bacteria at the oxic-anoxic interface in sediments of the oligotrophic Lake Stechlin. FEMS Microbiol Ecol. 1997;22:245–55.

  17. 17.

    Minz D, Flax JL, Green SJ, Muyzer G, Cohen Y, Wagner M, et al. Diversity of sulfate-reducing bacteria in oxic and anoxic regions of a microbial mat characterized by comparative analysis of dissimilatory sulfite reductase genes. Appl Environ Microbiol. 1999;65:4666–71.

  18. 18.

    Fukami T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol S. 2015;46:1–23.

  19. 19.

    Vass M, Langenheder S. The legacy of the past: effects of historical processes on microbial metacommunities. Aquat Microb Ecol. 2017;79:13–9.

  20. 20.

    Marshall IPG, Karst SM, Nielsen PH, Jørgensen BB. Metagenomes from deep Baltic Sea sediments reveal how past and present environmental conditions determine microbial community composition. Mar Genomics. 2018;37:58–68.

  21. 21.

    Orsi WD, Coolen MJL, Wuchter C, He L, More KD, Irigoien X, et al. Climate oscillations reflected within the microbiome of Arabian Sea sediments. Sci Rep. 2017;7:619.

  22. 22.

    Lyra C, Sinkko H, Rantanen M, Paulin L, Kotilainen A. Sediment bacterial communities reflect the history of a sea basin. PLoS ONE. 2013;8:e54326.

  23. 23.

    Louca S, Parfrey LW, Doebeli M. Decoupling function and taxonomy in the global ocean microbiome. Science. 2016;353:1272–7.

  24. 24.

    Emerson BC, Gillespie RG. Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol Evol. 2008;23:619–30.

  25. 25.

    Webb CO. Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat. 2000;156:145–55.

  26. 26.

    Stegen JC, Lin X, Konopka AE, Fredrickson JK. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J. 2012;6:1653–64.

  27. 27.

    Zhou J, Ning D. Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev. 2017;81:e00002–17.

  28. 28.

    Shen C, Ni Y, Liang W, Wang J, Chu H. Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra. Front Micro. 2015;6:582.

  29. 29.

    Tripathi BM, Kim M, Kim Y, Byun E, Yang J-W, Ahn J, et al. Variations in bacterial and archaeal communities along depth profiles of Alaskan soil cores. Sci Rep. 2018;8:504.

  30. 30.

    DeAngelis KM, Firestone MK. Phylogenetic clustering of soil microbial communities by 16S rRNA but not 16S rRNA genes. Appl Environ Microbiol. 2012;78:2459–61.

  31. 31.

    Boyd ES, Hamilton TL, Spear JR, Lavin M, Peters JW. [FeFe]-hydrogenase in Yellowstone National Park: evidence for dispersal limitation and phylogenetic niche conservatism. ISME J. 2010;4:1485–95.

  32. 32.

    Hu W, Zhang Q, Tian T, Li D, Cheng G, Mu J, et al. Relative roles of deterministic and stochastic processes in driving the vertical distribution of bacterial communities in a permafrost core from the Qinghai-Tibet Plateau, China. PLoS ONE. 2015;10:e0145747.

  33. 33.

    Nemergut DR, Knelman JE, Ferrenberg S, Bilinski T, Melbourne B, Jiang L, et al. Decreases in average bacterial community rRNA operon copy number during succession. ISME J. 2016;10:1147–56.

  34. 34.

    Martiny JBH, Jones SE, Lennon JT, Martiny AC. Microbiomes in light of traits: a phylogenetic perspective. Science. 2015;350:aac9323.

  35. 35.

    Martiny AC, Treseder K, Pusch G. Phylogenetic conservatism of functional traits in microorganisms. ISME J. 2013;7:830–8.

  36. 36.

    Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017;11:2639–43.

  37. 37.

    Kristensen E, Røy H, Debrabant K, Valdemarsen T. Carbon oxidation and bioirrigation in sediments along a Skagerrak-Kattegat-Belt Sea depth transect. Mar Ecol Prog Ser. 2018;604:33–50.

  38. 38.

    Flury S, Røy H, Dale AW, Fossing H, Tóth Z, Spiess V, et al. Controls on subsurface methane fluxes and shallow gas formation in Baltic Sea sediment (Aarhus Bay, Denmark). Geochim Cosmochim Act. 2016;188:297–309.

  39. 39.

    Jochum LM, Chen X, Lever MA, Loy A, Jørgensen BB, Schramm A, et al. Depth distribution and assembly of sulfate-reducing microbial communities in marine sediments of Aarhus Bay. Appl Environ Microbiol. 2017;83:e01547–17.

  40. 40.

    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.

  41. 41.

    McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.

  42. 42.

    Canfield DE, Jørgensen BB, Fossing H, Glud R, Gundersen J, Ramsing NB, et al. Pathways of organic carbon oxidation in three continental margin sediments. Mar Geol. 1993;113:27–40.

  43. 43.

    Canfield DE, Thamdrup B, Hansen JW. The anaerobic degradation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction. Geochim Cosmochim Act. 1993;57:3867–83.

  44. 44.

    Canfield DE, Thamdrup B. Towards a consistent classification scheme for geochemical environments, or, why we wish the term “suboxic” would go away. Geobiology. 2009;7:385–92.

  45. 45.

    Ramette A. Multivariate analyses in microbial ecology. FEMS Microbiol Ecol. 2007;62:142–60.

  46. 46.

    Plugge CM, Zhang W, Scholten JCM, Stams AJM. Metabolic flexibility of sulfate-reducing bacteria. Front Micro. 2011;2:81.

  47. 47.

    Beulig F, Røy H, Glombitza C, Jørgensen BB. Control on rate and pathway of anaerobic organic carbon degradation in the seabed. Proc Natl Acad Sci USA. 2018;115:367–72.

  48. 48.

    Holmkvist L, Ferdelman T, Jørgensen B. A cryptic sulfur cycle driven by iron in the methane zone of marine sediment (Aarhus Bay, Denmark). Geochim Cosmochim Act. 2011;75:3581–99.

  49. 49.

    Jaussi M. Microbial metabolism in the deep biosphere. PhD dissertation. Aarhus: Aarhus University; 2017.

  50. 50.

    Petro C. Assembly and activity of microbial communities in marine sediments. PhD dissertation. Aarhus: Aarhus University; 2018.

  51. 51.

    Chen X, Andersen TJ, Morono Y, Inagaki F, Jørgensen BB, Lever MA. Bioturbation as a key driver behind the dominance of Bacteria over Archaea in near-surface sediment. Sci Rep. 2017;7:2400.

  52. 52.

    Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol. 2012;10:497–1093.

  53. 53.

    Goldford JE, Lu N, Bajić D, Estrela S, Tikhonov M, Sanchez-Gorostiaga A, et al. Emergent simplicity in microbial community assembly. Science. 2018;361:469–74.

  54. 54.

    Tanaka K, Stackebrandt E, Tohyama S, Eguchi T. Desulfovirga adipica gen. nov., sp. nov., an adipate-degrading, gram-negative, sulfate-reducing bacterium. Int J Syst Evol Microbiol. 2000;50(Pt 2):639–44.

  55. 55.

    Sievert SM, Kuever J. Desulfacinum hydrothermale sp. nov., a thermophilic, sulfate-reducing bacterium from geothermally heated sediments near Milos Island (Greece). Int J Syst Evol Microbiol. 2000;50(Pt 3):1239–46.

  56. 56.

    Davidova IA, Duncan KE, Choi OK, Suflita JM. Desulfoglaeba alkanexedens gen. nov., sp. nov., an n-alkane-degrading, sulfate-reducing bacterium. Int J Syst Evol Microbiol. 2006;56(Pt 12):2737–42.

  57. 57.

    Oude Elferink SJ, Maas RN, Harmsen HJ, Stams AJ. Desulforhabdus amnigenus gen. nov. sp. nov., a sulfate reducer isolated from anaerobic granular sludge. Arch Microbiol. 1995;164:119–24.

  58. 58.

    Baena S, Perdomo N, Carvajal C, Díaz C, Patel BKC. Desulfosoma caldarium gen. nov., sp. nov., a thermophilic sulfate-reducing bacterium from a terrestrial hot spring. Int J Syst Evol Microbiol. 2011;61(Pt 4):732–6.

  59. 59.

    Cypionka H. Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol. 2000;54:827–48.

  60. 60.

    Suzuki D, Li Z, Cui X, Zhang C, Katayama A. Reclassification of Desulfobacterium anilini as Desulfatiglans anilini comb. nov. within Desulfatiglans gen. nov., and description of a 4-chlorophenol-degrading sulfate-reducing bacterium, Desulfatiglans parachlorophenolica sp. nov. Int J Syst Evol Microbiol. 2014;64(Pt 9):3081–6.

  61. 61.

    Jochum LM, Schreiber L, Marshall IPG, Jørgensen BB, Schramm A, Kjeldsen KU. Single-cell genomics reveals a diverse metabolic potential of uncultivated Desulfatiglans-related Deltaproteobacteria widely distributed in marine sediment. Front Micro. 2018;9:2038.

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We thank all participants and crew in the Aurora SKA cruise, 2014, and Britta Poulsen, Jeanette Johansen, Karina Bomholt Oest and Susanne Nielsen for excellent technical assistance in the lab. The work was supported by the Danish National Research Foundation (grant no DNRF104); the ERC Advanced Grant MICROENERGY [grant no 294200], and the VILLUM Experiment project “FISHing for the ancestors of the eukaryotic cell”. The sampling cruise was supported by the Danish Center for Marine Research.

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The authors declare that they have no conflict of interest.

Correspondence to Ian P. G. Marshall.

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