1932

Abstract

Global microbial cell numbers in the seabed exceed those in the overlying water column, yet these organisms receive less than 1% of the energy fixed as organic matter in the ocean. The microorganisms of this marine deep biosphere subsist as stable and diverse communities with extremely low energy availability. Growth is exceedingly slow, possibly regulated by virus-induced mortality, and the mean generation times are tens to thousands of years. Intermediate substrates such as acetate are maintained at low micromolar concentrations, yet their turnover time may be several hundred years. Owing to slow growth, a cell community may go through only 10,000 generations from the time it is buried beneath the mixed surface layer until it reaches a depth of tens of meters several million years later. We discuss the efficiency of the energy-conserving machinery of subsurface microorganisms and how they may minimize energy consumption through necessary maintenance, repair, and growth.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-010814-015535
2016-01-03
2024-12-04
Loading full text...

Full text loading...

/deliver/fulltext/marine/8/1/annurev-marine-010814-015535.html?itemId=/content/journals/10.1146/annurev-marine-010814-015535&mimeType=html&fmt=ahah

Literature Cited

  1. Ackermann M. 2013. Microbial individuality in the natural environment. ISME J. 7:465–67 [Google Scholar]
  2. Ackermann M, Stearns SC, Jenal U. 2003. Senescence in a bacterium with asymmetric division. Science 300:1920 [Google Scholar]
  3. Aiello IW, Bekins BA. 2010. Milankovitch-scale correlations between deeply buried microbial populations and biogenic ooze lithology. Geology 38:79–82 [Google Scholar]
  4. Andrén T, Jørgensen BB, Cotterill C, Green S. Exped. 347 Sci 2015. Proceedings of the Integrated Ocean Drilling Program 347 Baltic Sea Paleoenvironment Tokyo: Integr. Ocean Drill. Program Manag. Int http://publications.iodp.org/proceedings/347/347title.htm [Google Scholar]
  5. Arndt S, Jørgensen BB, LaRowe DE, Middelburg JJ, Pancost RD, Regnier P. 2013. Quantifying the degradation of organic matter in marine sediments: a review and synthesis. Earth Sci. Rev. 123:53–86 [Google Scholar]
  6. Bada JL. 1982. Racemization of amino acids in nature. Interdiscip. Sci. Rev. 7:30–46 [Google Scholar]
  7. Ballmoos von C, Wiedenmann A, Dimroth P. 2009. Essentials for ATP synthesis by F1F0 ATP synthases. Annu. Rev. Biochem. 78:649–72 [Google Scholar]
  8. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P. et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–12 [Google Scholar]
  9. Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sørensen KB. et al. 2006. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. PNAS 103:3846–51 [Google Scholar]
  10. Borrel G, Colombet J, Robin A, Lehours A-C, Prangishvili D, Sime-Ngando T. 2012. Unexpected and novel putative viruses in the sediments of a deep-dark permantly anoxic freshwater habitat. ISME J. 6:2119–27 [Google Scholar]
  11. Boudreau BP. 1997. Diagenetic Models and Their Implementation: Modelling Transport and Reactions in Aquatic Sediments Berlin: Springer [Google Scholar]
  12. Boudreau BP, Ruddick BR. 1991. On a reactive continuum representation of organic matter diagenesis. Am. J. Sci. 291:507–38 [Google Scholar]
  13. Boyer PD. 1997. The ATP synthase—a splendid molecular machine. Annu. Rev. Biochem. 66:717–49 [Google Scholar]
  14. Breitbart M. 2012. Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4:425–48 [Google Scholar]
  15. Cano RJ, Borucki MK. 1995. Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber. Science 268:1060–64 [Google Scholar]
  16. Chan M, Himes RH, Akagi JM. 1971. Fatty acid composition of thermophilic, mesophilic, and psychrophilic clostridia. J. Bacteriol. 106:876–81 [Google Scholar]
  17. Ciobanu M-C, Burgaud G, Dufresne A, Breuker A, Rédou V. et al. 2014. Microorganisms persist at record depths in the subseafloor of the Canterbury Basin. ISME J. 8:1370–80 [Google Scholar]
  18. Coolen MJL, Cypionka H, Sass AM, Sass H, Overmann J. 2002. Ongoing modification of Mediterranean Pleistocene sapropels mediated by prokaryotes. Science 296:2407–10 [Google Scholar]
  19. Danovaro R, Dell'Anno A, Corinaldesi C, Magagnini M, Noble R. et al. 2008. Major viral impact on the functioning of benthic deep-sea ecosystems. Nature 454:1084–88 [Google Scholar]
  20. D'Hondt S, Inagaki F, Alvarez Zarikian CA. Exped. 329 Sci 2011. Proceedings of the Integrated Ocean Drilling Program 329 South Pacific Gyre Subseafloor Life Tokyo: Integr. Ocean Drill. Program Manag. Int http://publications.iodp.org/proceedings/329/329title.htm [Google Scholar]
  21. D'Hondt S, Inagaki F, Zarikian CA, Abrams LJ, Dubois N. et al. 2015. Presence of oxygen and aerobic communities from sea floor to basement in deep-sea sediments. Nat. Geosci. 8:299–304 [Google Scholar]
  22. D'Hondt S, Jørgensen BB, Miller DJ, Aiello IW, Bekins B. et al. 2003. Proceedings of the Ocean Drilling Program 201 Initial Rep Controls on Microbial Communities in Deeply Buried Sediments, Eastern Equatorial Pacific and Peru Margin College Station: Tex. A&M Univ. Ocean Drill. Program http://www-odp.tamu.edu/publications/201_IR/201ir.htm [Google Scholar]
  23. D'Hondt S, Jørgensen BB, Miller DJ, Batzke A, Blake R. et al. 2004. Distributions of metabolic activities in deep subseafloor sediments. Science 306:2216–21 [Google Scholar]
  24. D'Hondt S, Spivack AJ, Pockalny R, Ferdelman TG, Fischer JP. 2009. Subseafloor sedimentary life in the South Pacific Gyre. PNAS 106:11651–56 [Google Scholar]
  25. D'Hondt S, Wang G, Spivack AJ. 2014. The underground economy (energetic constraints of subseafloor life). See Stein et al. 2014 127–48
  26. Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A. 2011. Marine subsurface eukaryotes: the fungal majority. Environ. Microbiol. 13:172–83 [Google Scholar]
  27. Edwards KJ, Becker K, Colwell F. 2012. The deep, dark energy biosphere: intraterrestrial life on Earth. Annu. Rev. Earth Planet. Sci. 40:551–68 [Google Scholar]
  28. Eloe EA, Fadrosh DW, Novotny M, Allen LZ, Kim M. et al. 2011. Going deeper: metagenome of a hadopelagic microbial community. PLOS ONE 6:e20388 [Google Scholar]
  29. Engelhardt T, Kallmeyer J, Cypionka H, Engelen B. 2014. High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments. ISME J. 8:1503–9 [Google Scholar]
  30. Engelhardt T, Orsi WD, Jørgensen BB. 2015. Viral activities and life-cycles in deep subseafloor sediment. Environ. Microbiol. Rep. In press. doi: 10.1111/1758-2229.12316 [Google Scholar]
  31. Engelhardt T, Sahlberg M, Cypionka H, Engelen B. 2011. Induction of prophages from deep-subseafloor bacteria. Environ. Microbiol. Rep. 3:459–65 [Google Scholar]
  32. Ferdelman TG, Kano A, Williams T, Henriet J-P, Exped. 307 Sci 2006. Proceedings of the Integrated Ocean Drilling Program 307 Modern Carbonate Mounds: Porcupine Drilling. Tokyo: Integr. Ocean Drill. Program Manag. Int http://publications.iodp.org/proceedings/307/307title.htm [Google Scholar]
  33. Finke N, Vandieken V, Jørgensen BB. 2007. Acetate, lactate, propionate, and isobutyrate as electron donors for iron and sulfate reduction in arctic marine sediments, Svalbard. FEMS Microbiol. Ecol. 59:10–22 [Google Scholar]
  34. Finkel SE. 2006. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat. Rev. Microbiol. 4:113–20 [Google Scholar]
  35. Garlid KD, Beavis AD, Ratkje SK. 1989. On the nature of ion leaks in energy-transducing membranes. Biochim. Biophys. Acta 976:109–20 [Google Scholar]
  36. Hebsgaard MB, Matthew J, Phillips MJ, Willerslev E. 2005. Geologically ancient DNA: fact or artefact?. Trends Microbiol. 13:212–20 [Google Scholar]
  37. Hoehler TM. 2004. Biological energy requirements as quantitative boundary conditions for life in the subsurface. Geobiology 2:205–15 [Google Scholar]
  38. Hoehler TM, Jørgensen BB. 2013. Microbial life under extreme energy limitation. Nat. Rev. Microbiol. 11:83–94 [Google Scholar]
  39. Inagaki F, Hinrichs K-U, Kubo Y, Exped. 337 Sci 2012. Proceedings of the Integrated Ocean Drilling Program 337 Prelim. Rep Deep Coalbed Biosphere Off Shimokita: Microbial Processes and Hydrocarbon System Associated with Deeply Buried Coalbed in the Ocean. Tokyo: Integr. Ocean Drill. Program Manag. Int http://publications.iodp.org/preliminary_report/337/index.html [Google Scholar]
  40. Jiang W, Hermolin J, Fillingame RH. 2001. The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is 10. PNAS 98:4966–71 [Google Scholar]
  41. Johnson SS, Hebsgaard MB, Christensen TR, Mastepanov M, Nielsen R. et al. 2007. Ancient bacteria show evidence of DNA repair. PNAS 104:14401–5 [Google Scholar]
  42. Jørgensen BB, Hondt S, Miller DJ. 2006. Proceedings of the Ocean Drilling Program 201 Sci. Results Controls on Microbial Communities in Deeply Buried Sediments, Eastern Equatorial Pacific and Peru Margin College Station: Tex. A&M Univ. Ocean Drill. Program http://www-odp.tamu.edu/publications/201_IR/201ir.htm [Google Scholar]
  43. Jørgensen BB, Parkes RJ. 2010. Role of sulfate reduction and methane for anaerobic carbon cycling in eutrophic fjord sediments (Limfjorden, Denmark). Limnol. Oceanogr. 55:1338–52 [Google Scholar]
  44. Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D'Hondt S. 2012. Global distribution of microbial abundance and biomass in subseafloor sediment. PNAS 109:16213–16 [Google Scholar]
  45. Kallmeyer J, Smith DC, Spivack A, D'Hondt S. 2008. New cell extraction procedure applied to deep subsurface sediments. Limnol. Oceanogr. Methods 6:236–45 [Google Scholar]
  46. Kallmeyer J, Wagner D. 2014. Microbial Life of the Deep Biosphere Berlin: De Gruyter [Google Scholar]
  47. Kuenen JG, Boonstra J, Schröder HG, Veldkamp H. 1977. Competition for inorganic substrates among chemoorganotrophic and chemolithotrophic bacteria. Microb. Ecol. 3:119–30 [Google Scholar]
  48. Langerhuus AT, Røy H, Lever M, Inagaki F, Morono Y. et al. 2012. Endospore abundance and d:l-amino acid modeling of bacterial turnover in Holocene marine sediment (Aarhus Bay). Geochim. Cosmochim. Acta 99:87–99 [Google Scholar]
  49. LaRowe DE, Amend JP. 2015. Catabolic rates, population sizes and doubling/replacement times of microorganisms in natural settings. Am. J. Sci. 315:167–203 [Google Scholar]
  50. Lennon JT, Jones SE. 2011. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 119:119–30 [Google Scholar]
  51. Lever MA. 2013. Functional gene surveys from ocean drilling expeditions: a review and perspective. FEMS Microbiol. Ecol. 84:1–23 [Google Scholar]
  52. Lever MA, Rogers KL, Lloyd KG, Overmann J, Schink B. 2015. Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations. FEMS Microbiol. Rev. In press. doi: 10.1093/femsre/fuv020 [Google Scholar]
  53. Lipp JS, Morono Y, Inagaki F, Hinrichs K-U. 2008. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454:991–94 [Google Scholar]
  54. Lloyd KG, May MK, Kevorkian RT, Steen AD. 2013. Meta-analysis of quantification methods shows that archaea and bacteria have similar abundances in the subseafloor. Appl. Environ. Microbiol. 79:7790–99 [Google Scholar]
  55. Lolkema JS, Speelmans G, Konings WN. 1994. Na+-coupled versus H+-coupled energy transduction in bacteria. Biochim. Biophys. Acta 1187:211–15 [Google Scholar]
  56. Lomstein BAa, Langerhuus AT, D'Hondt S, Jørgensen BB, Spivack A. 2012. Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484:101–4 [Google Scholar]
  57. Mayer F, Müller V. 2014. Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol. Rev. 38:449–72 [Google Scholar]
  58. McCollom TM, Amend JP. 2005. A thermodynamic assessment of energy requirements for biomass synthesis by chemolithoautotrophic micro-organisms in oxic and anoxic environments. Geobiology 3:135–44 [Google Scholar]
  59. McCollom TM, Bach W. 2009. Thermodynamic constraints on hydrogen generation during serpentinization of ultramafic rocks. Geochim. Cosmochim. Acta 73:856–75 [Google Scholar]
  60. McInerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJM. et al. 2008. Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann. N.Y. Acad. Sci. 1125:58–72 [Google Scholar]
  61. Meier T, Krah A, Bond PJ, Pogoryelov D, Diederichs K, Faraldo-Gómez JD. 2009. Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases. J. Mol. Biol. 391:498–507 [Google Scholar]
  62. Meier T, Morgner N, Matthies D, Pogoryelov D, Keis S. et al. 2007. A tridecameric c ring of the adenosine triphosphate (ATP) synthase from the thermoalkaliphilic Bacillus sp. strain TA2.A1 facilitates ATP synthesis at low electrochemical proton potential. Mol. Microbiol. 65:1181–92 [Google Scholar]
  63. Meister P, Prokopenko M, Skilbeck CG, Watson M, McKenzie JA. 2006. Data report: compilation of total organic and inorganic carbon data from Peru margin and eastern equatorial Pacific drill sites (ODP Legs 112, 138, and 201. See Jørgensen et al. 2006, chap. 105, http://www-odp.tamu.edu/publications/201_SR/105/105.htm
  64. Middelboe M, Glud RN, Filippini M. 2011. Viral abundance and activity in the deep sub-seafloor biosphere. Aquat. Microb. Ecol. 63:1–8 [Google Scholar]
  65. Middelboe M, Holmfeldt K, Riemann L, Nybroe O, Haaber J. 2009. Bacteriophages drive strain diversification in a marine Flavobacterium: implications for phage resistance and physiological properties. Environ. Microbiol. 11:1971–82 [Google Scholar]
  66. Middelburg JJ. 1989. A simple rate model for organic matter decomposition in marine sediments. Geochim. Cosmochim. Acta 53:1577–81 [Google Scholar]
  67. Mikada H, Moore GF, Taira A, Becker K, Moore JC, Klaus A. 2005. Proceedings of the Ocean Drilling Program 190/196 Sci. Results Deformation and Fluid Flow Processes of the Nankai Trough Accretionary Prism: Coring, Logging While Drilling, and Advanced CORKs College Station: Tex. A&M Univ. Ocean Drill. Program http://www-odp.tamu.edu/publications/190196SR/190196sr.htm [Google Scholar]
  68. Mitchell P. 1961. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–48 [Google Scholar]
  69. Morono Y, Terada T, Kallmeyer J, Inagaki F. 2013. An improved cell separation technique for marine subsurface sediments: applications for high-throughput analysis using flow cytometry and cell sorting. Environ. Microbiol. 15:2841–49 [Google Scholar]
  70. Morono Y, Terada T, Nishizawa M, Ito M, Hillion F. et al. 2011. Carbon and nitrogen assimilation in deep subseafloor microbial cells. PNAS 108:18295–300 [Google Scholar]
  71. Mulkidjanian AY, Galperin MY, Makarova KS, Wolf YI, Koonin EV. 2008. Evolutionary primacy of sodium bioenergetics. Biol. Direct 3:13 [Google Scholar]
  72. Novitsky JA, Morita RY. 1976. Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine vibrio. Appl. Environ. Microbiol. 32:617–22 [Google Scholar]
  73. Onstott TC, Magnabosco C, Aubrey AD, Burton AS, Dworkin JP. et al. 2014. Does aspartic acid racemization constrain the depth limit of the subsurface biosphere?. Geobiology 12:1–19 [Google Scholar]
  74. Orcutt BN, Sylvan JB, Knab NJ, Edwards KJ. 2011. Microbial ecology of the dark ocean above, at and below the seafloor. Microbiol. Mol. Biol. Rev. 72:361–422 [Google Scholar]
  75. Orsi WD, Biddle JF, Edgcomb V. 2013a. Deep sequencing of subseafloor eukaryotic rRNA reveals active fungi across marine subsurface provinces. PLOS ONE 8:e56335 [Google Scholar]
  76. Orsi WD, Edgcomb VP, Christman GD, Biddle JF. 2013b. Gene expression in the deep biosphere. Nature 499:205–11 [Google Scholar]
  77. Park JS, Vreeland RH, Cho BC, Lowenstein TK, Timofeeff MN. et al. 2009. Haloarchaeal diversity in 23, 121, and 419 MYA salts. Geobiology 7:515–23 [Google Scholar]
  78. Parkes RJ, Cragg B, Roussel E, Webster G, Weightman A, Sass H. 2014. A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere:geosphere interactions. Mar. Geol. 352:409–25 [Google Scholar]
  79. Parkes RJ, Webster G, Cragg BA, Weightman AJ, Newberry CJ. et al. 2005. Deep sub-seafloor prokaryotes stimulated at interfaces over geological time. Nature 436:390–94 [Google Scholar]
  80. Pogoryelov D, Krah A, Langer JD, Yildiz Ö, Faraldo-Gómez JD, Meier T. 2010. Microscopic rotary mechanism of ion translocation in the Fo complex of ATP synthases. Nat. Chem. Biol. 6:891–99 [Google Scholar]
  81. Rang CU, Peng AY, Chao L. 2011. Temporal dynamics of bacterial aging and rejuvenation. Curr. Biol. 21:1813–16 [Google Scholar]
  82. Rebata-Landa V, Santamarina JC. 2006. Mechanical limits to microbial activity in deep sediments. Geochem. Geophys. Geosyst. 7:Q11006 [Google Scholar]
  83. Roussel EG, Bonavita M-AC, Querellou J, Cragg BA, Webster G. et al. 2008. Extending the sub-sea-floor biosphere. Science 320:1046 [Google Scholar]
  84. Røy H, Kallmeyer J, Adhikar RR, Pockalny R, Jørgensen BB. et al. 2012. Aerobic microbial respiration in 86-million-year-old deep-sea red clay. Science 336:922–25 [Google Scholar]
  85. Røy H, Weber HS, Tarpgaard IH, Ferdelman TG, Jørgensen BB. 2014. Sulfate reduction rate measurement in marine sediment using 35S-tracer. Limnol. Oceanogr. Methods 12:196–211 [Google Scholar]
  86. Russell NJ, Fukunaga N. 1990. A comparison of thermal adaptation of membrane lipids in psychrophilic and thermophilic bacteria. FEMS Microbiol. Rev. 75:171–82 [Google Scholar]
  87. Schink B. 1997. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61:262–80 [Google Scholar]
  88. Schippers A, Neretin LN, Kallmeyer J, Ferdelman TG, Cragg BA. et al. 2005. Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433:861–64 [Google Scholar]
  89. Schleifer KH, Kandler O. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bact. Rev. 36:407–77 [Google Scholar]
  90. Seyfried B, Schink B. 1990. Fermentative degradation of dipicolinic acid (pyridine-2,6-dicarboxylic acid) by a defined coculture of strictly anaerobic bacteria. Biodegradation 1:1–7 [Google Scholar]
  91. Sinninghe Damste JS, Rijpstra WIC, Hopmans EC, Weijers JWH, Foesel BU. et al. 2011. 13,16-Dimethyl octacosanedioic acid (iso-diabolic acid), a common membrane-spanning lipid of acidobacteria subdivisions 1 and 3. Appl. Environ. Microbiol. 77:4147–54 [Google Scholar]
  92. Sørensen J, Christensen D, Jørgensen BB. 1981. Volatile fatty acids and hydrogen as substrates for sulfate-reducing bacteria in anaerobic marine sediment. Appl. Environ. Microbiol. 42:5–11 [Google Scholar]
  93. Steen AD, Jørgensen BB, Lomstein BAa. 2013. Abiotic racemization kinetics of amino acids in marine sediments. PLOS ONE 8:e71648 [Google Scholar]
  94. Stein R, Blackman DK, Inagaki F, Larsen H-C. 2014. Earth and Life Processes Discovered from Subseafloor Environments Dev. Mar. Biol. Vol. 7 Amsterdam: Elsevier [Google Scholar]
  95. Stewart EJ, Madden R, Paul G, Taddei F. 2005. Aging and death in an organism that reproduces by morphologically symmetric division. PLOS Biol. 3:e45 [Google Scholar]
  96. Suess E, von Huene R, Emeis K-C, Bourgois J, Cruzado Castañeda JDC. et al. 1988. Proceedings of the Ocean Drilling Program 112 Initial Rep Peru Continental Margin College Station: Tex. A&M Univ. Ocean Drill. Program http://www-odp.tamu.edu/publications/112_IR/112ir.htm [Google Scholar]
  97. Suttle CA. 2007. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5:801–12 [Google Scholar]
  98. Teske A. 2013. Marine deep sediment microbial communities. The Prokaryotes: Prokaryotic Communities and Ecophysiology E Rosenberg, EF DeLong, S Lory, E Stackebrandt, F Thompson 123–38 Berlin: Springer [Google Scholar]
  99. Teske A, Biddle JF, Lever MA. 2014. Genetic evidence of subseafloor microbial communities. See Stein et al. 2014 85–125
  100. Tréhu AM, Bohrmann G, Torres ME, Colwell FS. 2006. Proceedings of the Ocean Drilling Program 204 Sci. Results Drilling Gas Hydrates on Hydrate Ridge, Cascadia Continental Margin College Station: Tex. A&M Univ. Ocean Drill. Program http://www-odp.tamu.edu/publications/204_SR/204sr.htm [Google Scholar]
  101. Valentine DL. 2007. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat. Rev. Microbiol. 5:316–23 [Google Scholar]
  102. van Bodegom P. 2005. Microbial maintenance: a critical review of its quantification. Microb. Ecol. 53:513–23 [Google Scholar]
  103. van de Vossenberg JLCM, Driessen AJM, Konings WN. 1998. The essence of being extremophilic: the role of the unique archaeal membrane lipids. Extremophiles 2:163–70 [Google Scholar]
  104. Velimirov B. 2001. Nanobacteria, ultramicrobacteria, and starvation forms: a search for the smallest metabolizing bacterium. Microbes Environ. 16:67–77 [Google Scholar]
  105. Vreeland RH, Rosenzweig WD, Powers DW. 2000. Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature 407:897–900 [Google Scholar]
  106. Wang G, Spivack AJ, D'Hondt S. 2010. Gibbs energies of reaction and microbial mutualism in anaerobic deep subseafloor sediments of ODP Site 1226. Geochim. Cosmochim. Acta 74:3938–47 [Google Scholar]
  107. Wegener G, Bausch M, Holler T, Thang NM, Mollar XP. et al. 2012. Assessing sub-seafloor microbial activity by combined stable isotope probing with deuterated water and 13C-bicarbonate. Environ. Microbiol. 14:1517–27 [Google Scholar]
  108. Weijers JWH, Schouten S, Hopmans EC, Geenevasen JAJ, David ORP. et al. 2006. Membrane lipids of mesophilic anaerobic bacteria thriving in peats have typical archaeal traits. Environ. Microbiol. 8:648–57 [Google Scholar]
  109. Weinbauer MG, Rassoulzadegan F. 2004. Are viruses driving microbial diversification and diversity?. Environ. Microbiol. 6:1–11 [Google Scholar]
  110. Whitman WB, Coleman DC, Wiebe WJ. 1998. Prokaryotes: the unseen majority. PNAS 95:6578–83 [Google Scholar]
  111. Wilhelms A, Larter SR, Head I, Farrimond P, di-Primio R. et al. 2001. Biodegradation of oil in uplifted basins prevented by deep-burial sterilization. Nature 411:1034–37 [Google Scholar]
/content/journals/10.1146/annurev-marine-010814-015535
Loading
/content/journals/10.1146/annurev-marine-010814-015535
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error