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Ecology and evolution of seafloor and subseafloor microbial communities

Nature Reviews Microbiology volume 16, pages 671–683 (2018)Cite this article

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Abstract

Vast regions of the dark ocean have ultra-slow rates of organic matter sedimentation, and their sediments are oxygenated to great depths yet have low levels of organic matter and cells. Primary production in the oxic seabed is supported by ammonia-oxidizing archaea, whereas in anoxic sediments, novel, uncultivated groups have the potential to produce H2 and CH4, which fuel anaerobic carbon fixation. Subseafloor bacteria have very low mutation rates, and their evolution is likely dominated by selection of different pre-adapted subseafloor taxa under oxic and anoxic conditions. In addition, the abundance and activity of viruses indicate that they affect the size, structure and selection of subseafloor communities. This Review highlights how microbial communities survive in the unique, nutrient-poor and energy-starved environment of the seabed, where they have the potential to influence global biochemical cycles.

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Fig. 1: Redox conditions in seafloor and subseafloor ecosystems are linked to sedimentation rate and distance from shore.
Fig. 2: Microbial loops in oxic and anoxic sediments.
Fig. 3: Viruses influence population size and regenerate nutrients for subsisting cells.
Fig. 4: Microbial selection in oxic and anoxic subseafloor sediments.

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References

  1. Kallmeyer, J., Pockalny, R., Adhikari, R., Smith, D. C. & D’Hondt, S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl Acad. Sci. USA 109, 16213–16216 (2012).This work establishes the relationship between sedimentation rate, distance from shore and microbial biomass in subseafloor sediments and estimates that the subseafloor contains 2.9 × 10 29 cells.

    CAS  PubMed  Google Scholar 

  2. Inagaki, F. et al. Exploring deep microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor. Science 349, 420–424 (2015).This study finds that the detection limit of living cells in anoxic subseafloor sediment is likely at depths of ~2.5 km below the seafloor.

    CAS  PubMed  Google Scholar 

  3. D’Hondt, S. et al. Distributions of microbial activities in deep subseafloor sediments. Science 306, 2216–2221 (2004).

    PubMed  Google Scholar 

  4. Biddle, J. F. et al. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc. Natl Acad. Sci. USA 103, 3846–3851 (2006).

    CAS  PubMed  Google Scholar 

  5. Liu, C. H. et al. Exploration of cultivable fungal communities in deep coal-bearing sediments from approximately 1.3 to 2.5 km below the ocean floor. Environ. Microbiol. 19, 803–818 (2017).

    CAS  PubMed  Google Scholar 

  6. Engelhardt, T., Kallmeyer, J., Cypionka, H. & Engelen, B. High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments. ISME J. 8, 1503–1509 (2014).This study makes the discovery that exceptionally high ratios of viruses to cells exist in subseafloor sediments, which are increased in oxic sediment.

    PubMed  PubMed Central  Google Scholar 

  7. Fenchel, T. The ecology of micro- and meiobenthos. Annu. Rev. Ecol. Syst. 9, 99–121 (1978).

    Google Scholar 

  8. Orcutt, B. N., Sylvan, J. B., Knab, N. J. & Edwards, K. J. Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol. Mol. Biol. Rev. 75, 361–422 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. D’Hondt, S. et al. Subseafloor sedimentary life in the South Pacific Gyre. Proc. Natl Acad. Sci. USA 106, 11651–11656 (2009).

    PubMed  Google Scholar 

  10. Hoehler, T. M. & Jorgensen, B. B. Microbial life under extreme energy limitation. Nat. Rev. Microbiol. 11, 83–94 (2013).

    CAS  PubMed  Google Scholar 

  11. Lever, M. A. et al. Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations. FEMS Microbiol. Rev. 39, 688–728 (2015).

    CAS  PubMed  Google Scholar 

  12. Jørgensen, B. Mineralization of organic matter in the sea bed — the role of sulfate reduction. Nature 296, 643–645 (1982).

    Google Scholar 

  13. Canfield, D. Sulfate reduction and oxic respiration in marine sediments: implications for organic carbon preservation in euxinic environments. Deep Sea Res. 36, 121–138 632 (1989).

    CAS  Google Scholar 

  14. D’Hondt, S. et al. Presence of oxygen and aerobic communities from seafloor to basement in deep-sea sediments. Nat. Geosci. 8, 299–304 (2015).Together with reference 15, this study integrates oxygen measurements from a high number of sites, together with sedimentation rate models, to estimate the size of the global seabed that contains aerobic microbial communities.

    Google Scholar 

  15. Roy, H. et al. Aerobic microbial respiration in 86-million-year-old deep-sea red clay. Science 336, 922–925 (2012).

    CAS  PubMed  Google Scholar 

  16. Braun, S. et al. Microbial turnover times in the deep seabed studied by amino acid racemization modelling. Sci. Rep. 7, 5680 (2017).

    PubMed  PubMed Central  Google Scholar 

  17. Trembath-Reichert, E. et al. Methyl-compound use and slow growth characterize microbial life in 2-km-deep subseafloor coal and shale beds. Proc. Natl Acad. Sci. USA 114, E9206–E9215 (2017).This study performs a 2.5 year long stable isotope probing experiment from coal and shale beds 2 km below the seafloor, demonstrating that deep biosphere cells have highly variable growth rates, ranging from months to centuries.

    CAS  PubMed  Google Scholar 

  18. Lomstein, B. A., Langerhuus, A. T., D’Hondt, S., Jorgensen, B. B. & Spivack, A. J. Endospore abundance, microbial growth and necromass turnover in deep subseafloor sediment. Nature 484, 101–104 (2012).

    CAS  PubMed  Google Scholar 

  19. Starnawski, P. et al. Microbial community assembly and evolution in subseafloor sediment. Proc. Natl Acad. Sci. USA 114, 2940–2945 (2017).This study uses SNP analysis to show that mutation rates in anoxic subseafloor sediments are extremely low.

    CAS  PubMed  Google Scholar 

  20. Engelhardt, T., Orsi, W. D. & Jorgensen, B. B. Viral activities and life cycles in deep subseafloor sediments. Environ. Microbiol. Rep. 7, 868–873 (2015).

    CAS  PubMed  Google Scholar 

  21. Bowles, M. W., Mogollon, J., Kasten, S., Zabel, M. & Hinrichs, K. U. Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities. Science 344, 889–891 (2014).

    CAS  PubMed  Google Scholar 

  22. Froelich, P. et al. Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim. Cosmochim. Acta 43, 1075–1090 (1979).

    CAS  Google Scholar 

  23. Ziebis, W. et al. Interstitial fluid chemistry of sediments underlying the North Atlantic gyre and the influence of subsurface fluid flow. Earth Planet. Sci. Lett. 323–324, 79–91 (2012).

    Google Scholar 

  24. Meister, P., Prokopenko, M., Skilbeck, C. G., Watson, M. & McKenzie, J. A. in Proc. ODP, Sci. Results 201, 1–20 Proc. ODP, Sci. Results (eds Jørgensen, B. B., D’Hondt, S. & Miller, D. J.) (2005).

  25. Durbin, A. M. & Teske, A. Archaea in organic-lean and organic-rich marine subsurface sediments: an environmental gradient reflected in distinct phylogenetic lineages. Front. Microbiol. 3, 168 (2012).

    PubMed  PubMed Central  Google Scholar 

  26. Breuker, A., Stadler, S. & Schippers, A. Microbial community analysis of deeply buried marine sediments of the New Jersey shallow shelf (IODP Expedition 313). FEMS Microbiol. Ecol. 85, 578–592 (2013).

    CAS  PubMed  Google Scholar 

  27. Danovaro, R., Molari, M., Corinaldesi, C. & Dell’Anno, A. Macroecological drivers of archaea and bacteria in benthic deep-sea ecosystems. Sci. Adv. 2, e1500961 (2016).

    Google Scholar 

  28. Bienhold, C., Zinger, L., Boetius, A. & Ramette, A. Diversity and biogeography of bathyal and abyssal seafloor bacteria. PLoS ONE 11, e0148016 (2016).

    Google Scholar 

  29. Durbin, A. M. & Teske, A. Microbial diversity and stratification of South Pacific abyssal marine sediments. Environ. Microbiol. 13, 3219–3234 (2011).

    PubMed  Google Scholar 

  30. Walsh, E. A. et al. Bacterial diversity and community composition from seasurface to subseafloor. ISME J. 10, 979–989 (2016).

    PubMed  Google Scholar 

  31. Wasmund, K., Mussmann, M. & Loy, A. The life sulfuric: microbial ecology of sulfur cycling in marine sediments. Environ. Microbiol. Rep. 9, 323–344 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Kaster, A., Blackwell-Mayer, K., Pasarell, B. & Spormann, A. M. Single cell study of Dehalococcoidetes species from deep-sea sediments of the Peruvian Margin. ISME J. 8, 1831–1842 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Kawai, M. et al. High frequency of phylogenetically diverse reductive dehalogenase-homologous genes in deep subseafloor sedimentary metagenomes. Front. Microbiol. 5, 80 (2014).

    PubMed  PubMed Central  Google Scholar 

  34. Nobu, M. K. et al. Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics. ISME J. 10, 273–286 (2016).This genomic analysis characterizes the detailed fermentative metabolism of the ‘ Ca . Atribacteria’, showing that they ferment propionate and can synthesize and store carbohydrates in bacterial microcompartment shell proteins.

    CAS  PubMed  Google Scholar 

  35. Lloyd, K. G. et al. Predominant archaea in marine sediments degrade detrital proteins. Nature 496, 215–218 (2013).

    CAS  PubMed  Google Scholar 

  36. Lazar, C. S. et al. Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ. Microbiol. 18, 1200–1211 (2016).

    CAS  PubMed  Google Scholar 

  37. Petro, C., Starnawski, P., Schramm, A. & Kjeldsen, K. U. Microbial community assembly in marine sediments. Aquat. Microb. Ecol. 79, 177–195 (2017).

    Google Scholar 

  38. Orsi, W., Biddle, J. F. & Edgcomb, V. Deep sequencing of subseafloor eukaryotic rRNA reveals active fungi across marine subsurface provinces. PLoS ONE 8, e56335 (2013).

    Google Scholar 

  39. Orsi, W. D., Richards, T. A. & Francis, W. R. Predicted microbial secretomes and their target substrates in marine sediment. Nat. Microbiol. 3, 32–37 (2018).

    CAS  PubMed  Google Scholar 

  40. Richards, T. A., Jones, M. D., Leonard, G. & Bass, D. Marine fungi: their ecology and molecular diversity. Annu. Rev. Mar. Sci. 4, 495–522 (2012).

    PubMed  Google Scholar 

  41. Russell, J. A., Leon-Zayas, R., Wrighton, K. & Biddle, J. F. Deep subsurface life from north pond: enrichment, isolation, characterization and genomes of heterotrophic bacteria. Front. Microbiol. 7, 678 (2016).

    PubMed  PubMed Central  Google Scholar 

  42. Lauer, A., Sorensen, K. B. & Teske, A. Phylogenetic characterization of marine benthic archaea in organic-poor sediments of the Eastern Equatorial Pacific Ocean (ODP Site 1225). Microorganisms 4, E32 (2016).

    PubMed Central  Google Scholar 

  43. Durbin, A. M. & Teske, A. Sediment-associated microdiversity within the Marine Group I Crenarchaeota. Environ. Microbiol. Rep. 2, 693–703 (2010).This paper reports the discovery that novel benthic clades of Thaumarchaeota dominate the archaeal community in oxic sediments and subsist deep below the seafloor.

    CAS  PubMed  Google Scholar 

  44. Lloyd, K. G., May, M. K., Kevorkian, R. T. & Steen, A. D. Meta-analysis of quantification methods shows that archaea and bacteria have similar abundances in the subseafloor. Appl. Environ. Microbiol. 79, 7790–7799 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Tully, B. J. & Heidelberg, J. F. Potential mechanisms for microbial energy acquisition in oxic deep-sea sediments. Appl. Environ. Microbiol. 82, 4232–4243 (2016).This metagenomic analysis in oxic sediments suggested that remineralization of ammonia from necromass via secreted extracellular proteases supports a syntrophic relationship between ammonia oxidizing Thaumarchaeota and heterotrophic Proteobacteria.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Molari, M., Manini, E. & Dell’Anno, A. Dark inorganic carbon fixation sustains the functioning of benthic deep-sea ecosystems. Global Biogeochem. Cycles 27, 212–221 (2013).This study provides the first experimental evidence that Thaumarchaeota perform autotrophy and mixotrophy in abyssal deep-sea oxic sediments.

    CAS  Google Scholar 

  47. Qin, W. et al. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc. Natl Acad. Sci. USA 111, 12504–12509 (2014).

    CAS  PubMed  Google Scholar 

  48. Bradley, J. A., Amend, J. P. & LaRowe, D. E. Necromass as a limited source of energy for microorganisms in marine sediments. Biogeosciences 123, 577–590 (2018).

    Article  Google Scholar 

  49. Wankel, S. D., Buchwald, C., Ziebis, W., Wenk, C. B. & Lehmann, M. F. Nitrogen cycling in the deep sedimentary biosphere: nitrate isotopes in porewaters underlying the oligotrophic North Atlantic. Biogeosciences 12, 7483–7502 (2015).

    CAS  Google Scholar 

  50. Blair, C. C., D’Hondt, S., Spivack, A. J. & Kingsley, R. H. Radiolytic hydrogen and microbial respiration in subsurface sediments. Astrobiology 7, 951–970 (2007).

    CAS  PubMed  Google Scholar 

  51. Mussmann, M. et al. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc. Natl Acad. Sci. USA 108, 16771–16776 (2011).

    CAS  PubMed  Google Scholar 

  52. Sewell, H. L., Kaster, A. K. & Spormann, A. M. Homoacetogenesis in deep-sea Chloroflexi, as inferred by single-cell genomics, provides a link to reductive dehalogenation in terrestrial Dehalococcoidetes. mBio 8, e02022–17 (2017).

    PubMed  PubMed Central  Google Scholar 

  53. Vandieken, V., Marshall, I. P. G., Niemann, H., Engelen, B. & Cypionka, H. Labilibaculum manganireducens gen. nov., sp. nov. and Labilibaculum filiforme sp. nov., novel bacteroidetes isolated from subsurface sediments of the Baltic Sea. Front. Microbiol. 8, 2614 (2017).

    PubMed  Google Scholar 

  54. Valentine, D. L. Microbiology: intraterrestrial lifestyles. Nature 496, 176–177 (2013).

    CAS  PubMed  Google Scholar 

  55. Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).

    CAS  Google Scholar 

  56. Beulig, F., Roy, H., Glombitza, C. & Jorgensen, B. B. Control on rate and pathway of anaerobic organic carbon degradation in the seabed. Proc. Natl Acad. Sci. USA 115, 367–372 (2018).

    CAS  PubMed  Google Scholar 

  57. Scheller, S., Yu, H., Chadwick, G. L., McGlynn, S. E. & Orphan, V. J. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351, 703–707 (2016).This study provides strong experimental data showing that anaerobic methane-oxidizing archaea can use ferric iron and humic acids as TEAs, independently of syntrophy with sulfate-reducing bacteria.

    CAS  PubMed  Google Scholar 

  58. McGlynn, S. E., Chadwick, G. L., Kempes, C. P. & Orphan, V. J. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526, 531–535 (2015).

    CAS  PubMed  Google Scholar 

  59. Wegener, G., Krukenberg, V., Riedel, D., Tegetmeyer, H. E. & Boetius, A. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526, 587–590 (2015).

    CAS  PubMed  Google Scholar 

  60. Timmers, P. H. et al. Reverse methanogenesis and respiration in methanotrophic archaea. Archaea 2017, 1654237 (2017).

    PubMed  PubMed Central  Google Scholar 

  61. Treude, T. et al. Anaerobic oxidation of methane and sulfate reduction along the Chilean continental margin. Geochim. Cosmochim. Acta 69, 2767–2779 (2005).

    CAS  Google Scholar 

  62. Lloyd, K. G., Alperin, M. J. & Teske, A. Environmental evidence for net methane production and oxidation in putative ANaerobic MEthanotrophic (ANME) archaea. Environ. Microbiol. 13, 2548–2564 (2011).

    CAS  PubMed  Google Scholar 

  63. Stewart, E. J., Madden, R., Paul, G. & Taddei, F. Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol. 3, e45 (2005).

    Google Scholar 

  64. Morono, Y. et al. Carbon and nitrogen assimilation in deep subseafloor microbial cells. Proc. Natl Acad. Sci. USA 108, 18295–18300 (2011).

    CAS  PubMed  Google Scholar 

  65. Visick, J. E. & Clarke, S. Repair, refold, recycle: how bacteria can deal with spontaneous and environmental damage to proteins. Mol. Microbiol. 16, 835–845 (1995).

    CAS  PubMed  Google Scholar 

  66. Orsi, W. D., Barker Jorgensen, B. & Biddle, J. F. Transcriptional analysis of sulfate reducing and chemolithoautotrophic sulfur oxidizing bacteria in the deep subseafloor. Environ. Microbiol. Rep. 8, 452–460 (2016).

    CAS  PubMed  Google Scholar 

  67. Orsi, W. D., Richards, T. A. & Santoro, A. E. Cellular maintenance processes that potentially underpin the survival of subseafloor fungi over geological timescales. Estuar. Coast. Shelf Sci. 164, A1–A9 (2015).

    CAS  Google Scholar 

  68. Dell’Anno, A., Corinaldesi, C. & Danovaro, R. Virus decomposition provides an important contribution to benthic deep-sea ecosystem functioning. Proc. Natl Acad. Sci. USA 112, E2014–E2019 (2015).This study tests a large number of samples to show that extracellular enzymes hydrolyse viral capsid proteins that are released after cell lysis. Living microorganisms then use these proteins as a carbon and energy source in abyssal marine sediments.

    PubMed  Google Scholar 

  69. Danovaro, R., Corinaldesi, C., Rastelli, E. & Dell’Anno, A. Towards a better quantitative assessment of the relevance of deep-sea viruses, Bacteria, and Archaea in the functioning of the ocean seafloor. Aquat. Microb. Ecol. 75, 81–90 (2015).

    Google Scholar 

  70. Preuß, F. The impact of viruses on the marine deep biosphere. Ph.D Thesis, Carl von Ossietzky Universität Oldenburg (2016).

  71. Finkel, S. E. & Kolter, R. DNA as a nutrient: novel role for bacterial competence gene homologs. J. Bacteriol. 183, 6288–6293 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Engelhardt, T., Sahlberg, M., Cypionka, H. & Engelen, B. Induction of prophages from deep-subseafloor bacteria. Environ. Microbiol. Rep. 3, 459–465 (2011).

    PubMed  Google Scholar 

  73. Engelhardt, T., Sahlberg, M., Cypionka, H. & Engelen, B. Biogeography of Rhizobium radiobacter and distribution of associated temperate phages in deep subseafloor sediments. ISME J. 7, 199–209 (2013).

    CAS  PubMed  Google Scholar 

  74. Kleber, M., Sollins, P. & Sutton, R. A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry 85, 9–24 (2007).

    Google Scholar 

  75. Kallmeyer, J. Contamination control for scientific drilling operations. Adv. Appl. Microbiol. 98, 61–91 (2017).

    CAS  PubMed  Google Scholar 

  76. Johansen, K. S. Lytic polysaccharide monooxygenases: the microbial power tool for lignocellulose degradation. Trends Plant Sci. 21, 926–936 (2016).

    CAS  PubMed  Google Scholar 

  77. Shraddha, Shekher, R., Sehgal, S., Kamthania, M. & Kumar, A. Laccase: microbial sources, production, purification, and potential biotechnological applications. Enzyme Res. 2011, 217861 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Arnosti, C. Microbial extracellular enzymes and the marine carbon cycle. Annu. Rev. Mar. Sci. 3, 401–425 (2011).

    PubMed  Google Scholar 

  79. Xie, S., Lipp, J. S., Wegener, G., Ferdelman, T. G. & Hinrichs, K. U. Turnover of microbial lipids in the deep biosphere and growth of benthic archaeal populations. Proc. Natl Acad. Sci. USA 110, 6010–6014 (2013).

    CAS  PubMed  Google Scholar 

  80. Artzi, L., Bayer, E. A. & Morais, S. Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides. Nat. Rev. Microbiol. 15, 83–95 (2017).

    CAS  PubMed  Google Scholar 

  81. Baker, B. J. et al. Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea. Nat. Microbiol. 1, 16002 (2016).

    CAS  PubMed  Google Scholar 

  82. Treseder, K. K. & Lennon, J. T. Fungal traits that drive ecosystem dynamics on land. Microbiol. Mol. Biol. Rev. 79, 243–262 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Burgaud, G. et al. Deciphering the presence and activity of fungal communities in marine sediments using a model estuarine system. Aquat. Microb. Ecol. 70, 45–62 (2013).

    Google Scholar 

  84. Xu, W., Pang, K. L. & Luo, Z. H. High fungal diversity and abundance recovered in the deep-sea sediments of the Pacific Ocean. Microb. Ecol. 68, 688–698 (2014).

    CAS  PubMed  Google Scholar 

  85. Malik, A. A. et al. Soil fungal:bacterial ratios are linked to altered carbon cycling. Front. Microbiol. 7, 1247 (2016).

    PubMed  PubMed Central  Google Scholar 

  86. Kracher, D. et al. Extracellular electron transfer systems fuel cellulose oxidative degradation. Science 352, 1098–1101 (2016).

    CAS  PubMed  Google Scholar 

  87. Harms, H., Schlosser, D. & Wick, L. Y. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat. Rev. Microbiol. 9, 177–192 (2011).

    CAS  PubMed  Google Scholar 

  88. Nissilä, M. E., Lay, C. H. & Puhakka, J. A. Dark fermentative hydrogen production from lignocellulosic hydrolyzates — a review. Biomass Bioenergy 67, 145–159 (2014).

    Google Scholar 

  89. Cordero, O. X. & Polz, M. F. Explaining microbial genomic diversity in light of evolutionary ecology. Nat. Rev. Microbiol. 12, 263–273 (2014).

    CAS  PubMed  Google Scholar 

  90. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).

    CAS  Google Scholar 

  91. Hoshino, T. et al. Atribacteria from the subseafloor sedimentary biosphere disperse to the hydrosphere through submarine mud volcanoes. Front. Microbiol. 8, 1135 (2017).

    PubMed  PubMed Central  Google Scholar 

  92. Biddle, J. F. et al. Prospects for the study of evolution in the deep biosphere. Front. Microbiol. 2, 285 (2012).

    PubMed  PubMed Central  Google Scholar 

  93. Morris, J. J., Lenski, R. E. & Zinser, E. R. The Black Queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 3, e00036-12 (2012).

    PubMed  PubMed Central  Google Scholar 

  94. Coolen, M. J., Cypionka, H., Sass, A. M., Sass, H. & Overmann, J. Ongoing modification of Mediterranean Pleistocene sapropels mediated by prokaryotes. Science 296, 2407–2410 (2002).

    CAS  PubMed  Google Scholar 

  95. Swan, B. K. et al. Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proc. Natl Acad. Sci. USA 110, 11463–11468 (2013).

    CAS  PubMed  Google Scholar 

  96. Reintjes, G., Arnosti, C., Fuchs, B. M. & Amann, R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 11, 1640–1650 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Valentine, D. L. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat. Rev. Microbiol. 5, 316–323 (2007).

    CAS  PubMed  Google Scholar 

  98. Orsi, W. D., Edgcomb, V. P., Christman, G. D. & Biddle, J. F. Gene expression in the deep biosphere. Nature 499, 205–208 (2013).

    CAS  PubMed  Google Scholar 

  99. Ruff, S. E. et al. Global dispersion and local diversification of the methane seep microbiome. Proc. Natl Acad. Sci. USA 112, 4015–4020 (2015).

    CAS  PubMed  Google Scholar 

  100. Pasulka, A. L. et al. Colonial tube-dwelling ciliates influence methane cycling an microbial diversity within methane seep ecosystems. Front. Mar. Sci. 3, 276 (2017).

    Google Scholar 

  101. Orsi, W. D. et al. Climate oscillations reflected within the microbiome of Arabian Sea sediments. Sci. Rep. 7, 6040 (2017).

    PubMed  PubMed Central  Google Scholar 

  102. Zinke, L. A. et al. Thriving or surviving? Evaluating active microbial guilds in Baltic Sea sediment. Environ. Microbiol. Rep. 9, 528–536 (2017).

    CAS  PubMed  Google Scholar 

  103. Marshall, I. P. G., Karst, S. M., Nielsen, P. H. & Jorgensen, B. B. Metagenomes from deep Baltic Sea sediments reveal how past and present environmental conditions determine microbial community composition. Mar. Genomics 37, 58–68 (2018).

    PubMed  Google Scholar 

  104. Contreras, S. et al. Cyclic 100-ka (glacial-interglacial) migration of subseafloor redox zonation on the Peruvian shelf. Proc. Natl Acad. Sci. USA 110, 18098–18103 (2013).

    CAS  PubMed  Google Scholar 

  105. Hubert, C. et al. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. Science 325, 1541–1544 (2009).

    CAS  PubMed  Google Scholar 

  106. Dekas, A. E., Connon, S. A., Chadwick, G. L., Trembath-Reichert, E. & Orphan, V. J. Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses. ISME J. 10, 678–692 (2016).

    CAS  PubMed  Google Scholar 

  107. Shapiro, B. J. et al. Population genomics of early events in the ecological differentiation of bacteria. Science 336, 48–51 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Overkamp, W. et al. Physiological and cell morphology adaptation of Bacillus subtilis at near-zero specific growth rates: a transcriptome analysis. Environ. Microbiol. 17, 346–363 (2015).

    PubMed  Google Scholar 

  109. Vuillemin, A. et al. Microbial community composition along a 50,000 year lacustrine sediment sequence. FEMS Microbiol. Ecol. 94, fiy029 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Inagaki, F., Okada, H., Tsapin, A. I. & Nealson, K. H. Microbial survival: the paleome: a sedimentary genetic record of past microbial communities. Astrobiology 5, 141–153 (2005).

    CAS  PubMed  Google Scholar 

  111. Friese, A. et al. A simple and inexpensive technique for assessing contamination during drilling operations. Limnol. Oceanogr. Methods 15, 200–211 (2017).

    CAS  Google Scholar 

  112. Tully, B. J., Wheat, C. G., Glazer, B. T. & Huber, J. A. A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer. ISME J. 12, 1–16 (2018).

    CAS  PubMed  Google Scholar 

  113. Jungbluth, S. P., Amend, J. P. & Rappe, M. S. Metagenome sequencing and 98 microbial genomes from Juan de Fuca Ridge flank subsurface fluids. Sci. Data 4, 170037 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Riederer-Henderson, M. A. & Wilson, P. W. Nitrogen fixation by sulphate-reducing bacteria. J. Gen. Microbiol. 61, 27–31 (1970).

    CAS  PubMed  Google Scholar 

  115. Dekas, A. E., Chadwick, G. L., Bowles, M. W., Joye, S. B. & Orphan, V. J. Spatial distribution of nitrogen fixation in methane seep sediment and the role of the ANME archaea. Environ. Microbiol. 16, 3012–3029 (2014).

    CAS  PubMed  Google Scholar 

  116. Dekas, A. E., Poretsky, R. S. & Orphan, V. J. Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326, 422–426 (2009).

    CAS  PubMed  Google Scholar 

  117. Schulz, H. D. & Zabel, M. Marine Geochemistry. Second Edition (Spring-Verlag, 2006).

  118. Yang, W. H., Weber, K. A. & Silver, W. L. Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction. Nat. Geosci. 5, 538–541 (2012).

    CAS  Google Scholar 

  119. Richter, K., Schicklberger, M. & Gescher, J. Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl. Environ. Microbiol. 78, 913–921 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Jorgensen, S. L. et al. Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge. Proc. Natl Acad. Sci. USA 109, E2846–E2855 (2012).

    CAS  Google Scholar 

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Acknowledgements

This work was supported by the Deutsche Forschungsgemeinschaft (DFG) Project OR 417/1-1 granted to W.D.O. The author thanks A. Vuillemin and T. Hohmann for their comments and discussions. The author acknowledges the Center for Dark Energy Biosphere Investigations (C-DEBI), which has supported many of the studies discussed here, as well as the comments and suggestions from the three reviewers, which helped to greatly improve the article.

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Nature Reviews Microbiology thanks Andreas Schramm, Alfred Spormann and Andreas Teske for their contribution to the peer review of this work.

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  1. Department of Earth and Environmental Sciences, Paleontology and Geobiology and GeoBio-Center LMU, Ludwig-Maximilians-Universität München, Munich, Germany

    William D. Orsi

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Glossary

Benthos

The community of organisms living in surface sediments.

Hydrothermal vents

Submarine volcanoes that expel heated fluids that are rich in sulfur, hydrogen and metals.

Cold seeps

Regions in which methane gas bubbles out of the seafloor into the overlying seawater.

Chemosynthetic communities

Ecosystems that are supported by microbial autotrophy in the absence of sunlight.

Terminal electron acceptors

(TEAs). Substrates, such as oxygen, nitrate and sulfate, that are reduced at the end of the electron transport chain during cellular respiration and directly support ATP production.

Abyssal plain

A vast expanse of the ocean floor ranging between 3,000 and 6,000 m water depth.

Oligotrophic

An ecosystem in which primary production is limited by low levels of nutrients.

Horizontal gene transfer

(HGT). The transfer of genetic material between cells by a mechanism other than vertical inheritance, including transformation, transduction and conjugation.

Continental shelf

A broad, flat, sand-covered and mud-covered platform representing a shallow submerged part of a continent.

Remineralization

A process in which microbial metabolism converts organic matter to an inorganic form, for example, CO2.

Dissimilatory reduction

Energy-yielding reduction of terminal electron acceptors during cellular respiration.

Heterotrophs

Organisms that use organic matter as their primary carbon source.

Chemolithoautotrophic

Involving biological carbon fixation that is fuelled by inorganic energy sources other than sunlight.

Pelagic

Belonging to the water column of the ocean.

Mixotrophically

Using both CO2 and organic carbon as major substrates for growth.

Necromass

Non-living cellular material.

Stickland-type reaction

Microbial fermentation of amino acids.

Diagenesis

Chemical alterations of organic matter in sediments during burial.

Dark biomass fermentation

Anaerobic fermentation of dead biomass in the absence of light under anoxic conditions.

Transduction

DNA transfer mediated by a virus.

Transformation

Free DNA from one cell is taken up by another.

Conjugation

DNA transfer that involves contact between cells and a conjugative plasmid in the donor cell.

Flexible genome

The set of genes that are present only in a fraction of a clade or population.

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Orsi, W.D. Ecology and evolution of seafloor and subseafloor microbial communities. Nat Rev Microbiol 16, 671–683 (2018). https://doi.org/10.1038/s41579-018-0046-8

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