Oceanography The Official Magazine of
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Volume 32 Issue 01

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Volume 32, No. 1
Pages 208 - 211

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The Limits of Life and the Biosphere in Earth’s Interior

By Verena B. Heuer , Mark A. Lever, Yuki Morono, and Andreas Teske 
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First Paragraph

Fifty years of scientific ocean drilling have shown that microorganisms are widespread deep inside the ocean floor. Microbial populations exist in both organic-matter-rich and nutrient-​poor sediments (Kallmeyer et al., 2012; D’Hondt et al., 2015), in sediments that are millions of years old and are buried to over a kilometer depth (Roussel et al., 2008; Ciobanu et al., 2014; Inagaki et al., 2015), and deep inside the basaltic oceanic crust (Orcutt et al., 2011; Lever et al., 2013). In these varied environments, metabolic activity is extraordinarily low (D’Hondt et al., 2009; Hoehler and Jørgensen 2013; Lever et al. 2015a), but microbial cells remain physiologically active (Morono et al., 2011) or survive in their dormant phases (Lomstein et al., 2012). The total amount of subsurface biomass is still being debated (Hinrichs and Inagaki, 2012; Kallmeyer et al., 2012; Parkes et al., 2014), and the factors posing ultimate limits to deep life and the habitability of Earth remain to be resolved (Figure 1).

Citation

Heuer, V.B., M.A. Lever, Y. Morono, and A. Teske. 2019. The limits of life and the biosphere in Earth’s interior. Oceanography 32(1):208–211, https://doi.org/10.5670/oceanog.2019.147.

References
    Bach, W., and K.J. Edwards. 2003. Iron and sulfide oxidation within the basaltic ocean crust: Implications for chemolithoautotrophic microbial biomass production. Geochimica et Cosmochimica Acta 67:3,871–3,887, https://doi.org/10.1016/S0016-7037(03)00304-1.
  1. Biddle, J.F., S.P. Jungbluth, M.A. Lever, and M.S. Rappe. 2014. Life in the oceanic crust. Pp. 29–62 in Microbial Life of the Deep Biosphere. J. Kallmeyer and D. Wagner, eds, Walter De Gruyter GmbH, Berlin.
  2. Burggraf, S., H. Fricke, A. Neuner, J. Kristjansson, P. Rouvier, L. Mandelco, C.R. Woese, and K.O. Stetter. 1990. Methanococcus igneus sp. nov., a novel hyperthermophilic methanogen from a shallow submarine hydrothermal system. Systematic and Applied Microbiology 13:263–269, https://doi.org/10.1016/S0723-2020(11)80197-9.
  3. Ciobanu, M.C., G. Burgaud, A. Dufresne, A. Breuker, V. Redou, S. Ben Maamar, F. Gaboyer, O. Vandenabeele-Trambouze, J.S. Lipp, A. Schippers, and others. 2014. Microorganisms persist at record depths in the subseafloor of the Canterbury Basin. The ISME Journal 8:1,370–1,380, https://doi.org/10.1038/ismej.2013.250.
  4. Cowen, J.P., S.J. Giovannoni, F. Kenig, H.P. Johnson, D. Butterfield, M.S. Rappe, M. Hutnak, and P. Lam. 2003. Fluids from aging ocean crust that support microbial life. Science 299:120–123, https://doi.org/​10.1126/science.1075653.
  5. D’Hondt, S., F. Inagaki, C.A. Zarikian, L.J. Abrams, N. Dubois, T. Engelhardt, H. Evans, T. Ferdelman, B. Gribsholt, R.N. Harris, and others. 2015. Presence of oxygen and aerobic communities from sea floor to basement in deep-sea sediments. Nature Geoscience 8:299–304, https://doi.org/​10.1038/ngeo2387.
  6. D’Hondt, S., A.J. Spivack, R. Pockalny, T.G. Ferdelman, J.P. Fischer, J. Kallmeyer, L.J. Abrams, D.C. Smith, D. Graham, F. Hasiuk, and others. 2009. Subseafloor sedimentary life in the South Pacific Gyre. Proceedings of the National Academy of Sciences of the United States of America 106:11,651–11,656, https://doi.org/10.1073/pnas.0811793106.
  7. Edgcomb, V.P., S.J. Molyneaux, S. Boer, C.O. Wirsen, M. Saito, M.S. Atkins, K. Lloyd, and A. Teske. 2007. Survival and growth of two heterotrophic hydrothermal vent archaea, Pyrococcus strain GB-D and Thermococcus fumicolans, under low pH and high sulfide concentrations in combination with high temperature and pressure regimes. Extremophiles 11:329–342, https://doi.org/10.1007/s00792-006-0043-0.
  8. Fisk, M.R., M.C. Storrie-Lombardi, S. Douglas, R. Popa, G. McDonald, and C. Di Meo-Savoie. 2003. Evidence of biological activity in Hawaiian subsurface basalts. Geochemistry, Geophysics, Geosystems 4(12), https://doi.org/​10.1029/2002GC000387.
  9. Glombitza, C., R.R. Adhikari, N. Riedinger, W.P. Gilhooly, K.U. Hinrichs, and F. Inagaki. 2016. Microbial sulfate reduction potential in coal-bearing sediments down to ~2.5 km below the seafloor off Shimokita Peninsula, Japan. Frontiers in Microbiology, https://doi.org/10.3389/fmicb.2016.01576.
  10. Head, I.M., D.M. Jones, and S.R. Larter. 2003. Biological activity in the deep subsurface and the origin of heavy oil. Nature 426:344–352, https://doi.org/10.1038/nature02134.
  11. Heuer, V.B., F. Inagaki, Y. Morono, Y. Kubo, L. Maeda, and the Expedition 370 Scientists. 2016. Temperature Limit of the Deep Biosphere off Muroto. Proceedings of the International Ocean Discovery Program, 370, International Ocean Discovery Program, College Station, TX, https://doi.org/​10.14379/iodp.proc.370.101.2017.
  12. Hinrichs, K.-U., and F. Inagaki. 2012. Downsizing the deep biosphere. Science 338:204–205, https://doi.org/​10.1126/science.1229296.
  13. Hoehler, T.M., and B.B. Jorgensen. 2013. Microbial life under extreme energy limitation. Nature Reviews Microbiology 11:83–94, https://doi.org/10.1038/nrmicro2939.
  14. Holler, T., G. Wegener, H. Niemann, C. Deusner, T.G. Ferdelman, A. Boetius, B. Brunner, and F. Widdel. 2011. Carbon and sulfur back flux during anaerobic microbial oxidation of methane and coupled sulfate reduction. Proceedings of the National Academy of Sciences of the United States of America 108:E1484–E1490, https://doi.org/10.1073/pnas.1106032108.
  15. Horsfield, B., H.J. Schenk, K. Zink, R. Ondrak, V. Dieckmann, J. Kallmeyer, K. Mangelsdorf, R. di Primlo, H. Wilkes, R.J. Parkes, and others. 2006. Living microbial ecosystems within the active zone of catagenesis: Implications for feeding the deep biosphere. Earth and Planetary Science Letters 246:55–69, https://doi.org/10.1016/​j.epsl.2006.03.040.
  16. Ijiri, A., F. Inagaki, Y. Kubo, R.R. Adhikari, S. Hattori, T. Hoshino, H. Imachi, S. Kawagucci, Y. Morono, Y. Ohtomo, and others. 2018. Deep-biosphere methane production stimulated by geofluids in the Nankai accretionary complex. Science Advances 4(6):eaao4631, https://doi.org/10.1126/sciadv.aao4631.
  17. Inagaki, F., K.-U. Hinrichs, Y. Kubo, M.W. Bowles, V.B. Heuer, W.-L. Hong, T. Hoshino, A. Ijiri, H. Imachi, M. Ito, and others. 2015. Exploring deep microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor. Science 349:420–424, https://doi.org/10.1126/science.aaa6882.
  18. Jørgensen, B.B., M.F. Isaksen, and H.W. Jannasch. 1992. Bacterial sulfate reduction above 100°C in deep-sea hydrothermal vent sediments. Science 258:1,756–1,757, https://doi.org/10.1126/science.258.5089.1756.
  19. Jørgensen, B.B., L.X. Zawacki, and H.W. Jannasch. 1990. Thermophilic bacterial sulfate reduction in deep-sea sediments at the Guaymas Basin hydrothermal vent site (Gulf of California). Deep Sea Research Part A 37:695–710, https://doi.org/​10.1016/0198-0149(90)90099-H.
  20. Jørgensen, S.L., and R. Zhao. 2016. Microbial inventory of deeply buried oceanic crust from a young ridge flank. Frontiers in Microbiology, https://doi.org/​10.3389/fmicb.2016.00820.
  21. Jungbluth, S.P., J. Grote, H.T. Lin, J.P. Cowen, and M.S. Rappe. 2013. Microbial diversity within basement fluids of the sediment-buried Juan de Fuca Ridge flank. The ISME Journal 7:161–172, https://doi.org/​10.1038/ismej.2012.73.
  22. Kallmeyer, J., R. Pockalny, R.R. Adhikari, D.C. Smith, and S. D’Hondt. 2012. Global distribution of microbial abundance and biomass in subseafloor sediment. Proceedings of the National Academy of Sciences of the United States of America 109:16,213–16,216, https://doi.org/10.1073/pnas.1203849109.
  23. Kallmeyer, J., D.C. Smith, A.J. Spivack, and S. D’Hondt. 2008. New cell extraction procedure applied to deep subsurface sediments. Limnology and Oceanography–Methods 6:236–245, https://doi.org/​10.4319/lom.2008.6.236.
  24. Kashefi, K., and D.R. Lovley. 2003. Extending the upper temperature limit for life. Science 301:934, https://doi.org/10.1126/science.1086823.
  25. Kellermann, M.Y., G. Wegener, M. Elvert, M.Y. Yoshinaga, Y.-S. Lin, T. Holler, X.P. Mollar, K. Knittel, and K.-U. Hinrichs. 2012. Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities. Proceedings of the National Academy of Sciences of the United States of America 109:19,321–19,326, https://doi.org/10.1073/pnas.1208795109.
  26. Labonté, J.M., M.A. Lever, K.J. Edwards, and B.N. Orcutt. 2017. Influence of igneous basement on deep sediment microbial diversity on the eastern Juan de Fuca Ridge flank. Frontiers in Microbiology, https://doi.org/10.3389/fmicb.2017.01434.
  27. LaRowe, D.E., E. Burwicz, S. Arndt, A.W. Dale, and J.P. Amend. 2017. Temperature and volume of global marine sediments. Geology 45:275–278, https://doi.org/10.1130/G38601.1.
  28. Laso-Perez, R., G. Wegener, K. Knittel, F. Widdel, K.J. Harding, V. Krukenberg, D.V. Meier, M. Richter, H.E. Tegetmeyer, D. Riedel, and others. 2016. Thermophilic archaea activate butane via alkyl-​coenzyme M formation. Nature 539:396–401, https://doi.org/10.1038/nature20152.
  29. Lever, M.A., M. Alperin, B. Engelen, F. Inagaki, S. Nakagawa, B.O. Steinsbu, and A. Teske. 2006. Trends in basalt and sediment core contamination during IODP Expedition 301. Geomicrobiology Journal 23:517–530, https://doi.org/​10.1080/​01490450600897245.
  30. Lever, M.A., K.L. Rogers, K.G. Lloyd, J. Overmann, B. Schink, R.K. Thauer, T.M. Hoehler, and B.B. Jorgensen. 2015a. Life under extreme energy limitation: A synthesis of laboratory- and field-based investigations. FEMS Microbiology Review 39:688–728, https://doi.org/10.1093/femsre/fuv020.
  31. Lever, M.A., O. Rouxel, J.C. Alt, N. Shimizu, S. Ono, R.M. Coggon, W.C. Shanks III, L. Lapham, M. Elvert, X. Prieto-Mollar, and others. 2013. Evidence for microbial carbon and sulfur cycling in deeply buried ridge flank basalt. Science 339:1,305–1,308, https://doi.org/10.1126/science.1229240.
  32. Lever, M.A., A. Torti, P. Eickenbusch, A.B. Michaud, T. Santl-Temkiv, and B.B. Jorgensen. 2015b. A modular method for the extraction of DNA and RNA, and the separation of DNA pools from diverse environmental sample types. Frontiers in Microbiology, https://doi.org/10.3389/fmicb.2015.00476.
  33. Lindahl, T., and B. Nyberg. 1972. Rate of depurination of native deoxyribonucleic acid. Biochemistry 11:3,610–3,618, https://doi.org/10.1021/bi00769a018.
  34. Lloyd, K.G., V.P. Edgcomb, S.J. Molyneaux, S. Boer, C.O. Wirsen, M.S. Atkins, and A. Teske. 2005. Effects of dissolved sulfide, pH, and temperature on growth and survival of marine hyperthermophilic archaea. Applied and Environmental Microbiology 71:6,383–6,387, https://doi.org/​10.1128/​AEM.71.10.6383-6387.2005.
  35. Lomstein, B.A., A.T. Langerhuus, S. D’Hondt, B.B. Jorgensen, and A.J. Spivack. 2012. Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484:101–104, https://doi.org/10.1038/nature10905.
  36. McKay, L., V.W. Klokman, H.P. Mendlovitz, D.E. LaRowe, D.R. Hoer, D. Albert, J.P. Amend, and A. Teske. 2016. Thermal and geochemical influences on microbial biogeography in the hydrothermal sediments of Guaymas Basin, Gulf of California. Environmental Microbiology Reports 8:150–161, https://doi.org/10.1111/1758-2229.12365.
  37. Meyer, J.L., U. Jaekel, B.J. Tully, B.T. Glazer, C.G. Wheat, H.T. Lin, C.C. Hsieh, J.P. Cowen, S.M. Hulme, P.R. Girguis, and J.A. Huber. 2016. A distinct and active bacterial community in cold oxygenated fluids circulating beneath the western flank of the Mid-Atlantic Ridge. Scientific Reports 6:22541, https://doi.org/10.1038/srep22541.
  38. Møller, M.H., C.G. Glombitza, M.A. Lever, L. Deng, Y. Morono, F. Inagaki, M. Doll, C.-C. Su, and B.A. Lomstein. 2018. D:L-amino acid modeling reveals fast microbial turnover of days to months in the subsurface hydrothermal sediment of Guaymas Basin. Frontiers in Microbiology 9:967, https://doi.org/​10.3389/​fmicb.2018.00967.
  39. Morono, Y., T. Terada, T. Hoshino, and F. Inagaki. 2014. Hot-alkaline DNA extraction method for deep subseafloor archaeal communities. Applied and Environmental Microbiology 80:1,985–1,994, https://doi.org/10.1128/AEM.04150-13.
  40. Morono, Y., T. Terada, J. Kallmeyer, and F. Inagaki. 2013. An improved cell separation technique for marine subsurface sediments: Applications for high-throughput analysis using flow cytometry and cell sorting. Environmental Microbiology 15:2,841–2,849, https://doi.org/​10.1111/1462-2920.12153.
  41. Morono, Y., T. Terada, M. Nishizawa, M. Ito, F. Hillion, N. Takahata, Y. Sano, and F. Inagaki. 2011. Carbon and nitrogen assimilation in deep subseafloor microbial cells. Proceedings of the National Academy of Sciences of the United States of America 108:18,295–18,300, https://doi.org/10.1073/pnas.1107763108.
  42. Nigro, L.M., K. Harris, B.N. Orcutt, A. Hyde, S. Clayton-Luce, K. Becker, and A. Teske. 2012. Microbial communities at the borehole observatory on the Costa Rica Rift flank (Ocean Drilling Program Hole 896A). Frontiers in Microbiology, https://doi.org/10.3389/fmicb.2012.00232.
  43. Orcutt, B.N., W. Bach, K. Becker, A.T. Fisher, M. Hentscher, B.M. Toner, C.G. Wheat, and K.J. Edwards. 2011. Colonization of subsurface microbial observatories deployed in young ocean crust. The ISME Journal 5:692–703, https://doi.org/​10.1038/​ismej.2010.157.
  44. Orcutt, B., C.G. Wheat, and K.J. Edwards. 2010. Subseafloor ocean crust microbial observatories: Development of FLOCS (FLow-through Osmo Colonization System) and evaluation of borehole construction materials. Geomicrobiology Journal 27:143–157, https://doi.org/​10.1080/​01490450903456772.
  45. Parkes, R.J., B. Cragg, E. Roussel, G. Webster, A. Weightman, and H. Sass. 2014. A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere:geosphere interactions. Marine Geology 352:409–425, https://doi.org/​10.1016/j.margeo.2014.02.009.
  46. Price, P.B., and T. Sowers. 2004. Temperature dependence of metabolic rats for microbial growth, maintenance, and survival. Proceedings of the National Academy of Sciences of the United States of America 101:4,631–4,636, https://doi.org/10.1073/pnas.0400522101.
  47. Robador, A., S.P. Jungbluth, D.E. LaRowe, R.M. Bowers, M.S. Rappe, J.P. Amend, and J.P. Cowen. 2015. Activity and phylogenetic diversity of sulfate-reducing microorganisms in low-​temperature subsurface fluids within the upper oceanic crust. Frontiers in Microbiology 5:748, https://doi.org/​10.3389/​fmicb.2014.00748.
  48. Röling, W.F.M., I.M. Head, and S.R. Larter. 2003. The microbiology of hydrocarbon degradation in subsurface petroleum reservoirs: Perspectives and prospects. Research in Microbiology 154:321–328, https://doi.org/10.1016/S0923-2508(03)00086-X.
  49. Roussel, E.G., M.-A.C. Bonavita, J. Querellou, B.A. Cragg, G. Webster, D. Prieur, and R.J. Parkes. 2008. Extending the sub-sea-floor biosphere. Science 320:1,046, https://doi.org/10.1126/science.1154545.
  50. Rueter, P., R. Rabus, H. Wilkes, F. Aeckersberg, F.A. Rainey, H.W. Jannasch, and F. Widdel. 1994. Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphate-reducing bacteria. Nature 372:455–458, https://doi.org/​10.1038/372455a0.
  51. Santelli, C.M., N. Banerjee, W. Bach, and K.J. Edwards. 2010. Tapping the subsurface ocean crust biosphere: Low biomass and drilling-related contamination calls for improved quality controls. Geomicrobiology Journal 27:158–169, https://doi.org/​10.1080/01490450903456780.
  52. Steen, A.D., B.B. Jorgensen, and B.A. Lomstein. 2013. Abiotic racemization kinetics of amino acids in marine sediments. PLoS One 10(4):e0123837, https://doi.org/10.1371/journal.pone.0071648.
  53. Takai, K., K. Nakamura, T. Toki, U. Tsunogai, M. Miyazaki, J. Miyazaki, H. Hirayama, S. Nakagawa, T. Nunoura, and K. Horikoshi. 2008. Cell proliferation at 122°C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proceedings of the National Academy of Sciences of the United States of America 105:10,949–10,954, https://doi.org/​10.1073/​pnas.0712334105.
  54. Teske, A., V. Edgcomb, A.R. Rivers, J.R. Thompson, A.D. Gomez, S.J. Molyneaux, and C.O. Wirsen. 2009. A molecular and physiological survey of a diverse collection of hydrothermal vent Thermococcus and Pyrococcus isolates. Extremophiles 13:905–915, https://doi.org/10.1007/s00792-009-0278-7.
  55. Tully, B.J., C.G. Wheat, B.T. Glazer, and J.A. Huber. 2018. A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer. The ISME Journal 12:1–16, https://doi.org/​10.1038/ismej.2017.187.
  56. Wellsbury, P., K. Goodman, T. Barth, B.A. Cragg, S.P. Barnes, and R.J. Parkes. 1997. Deep marine biosphere fuelled by increasing organic matter availability during burial and heating. Nature 388:573–576, https://doi.org/10.1038/41544.
  57. Wheat, C.G., H.W. Jannasch, A.T. Fisher, K. Becker, J. Sharkey, and S. Hulme. 2010. Subseafloor seawater-​basalt-microbe reactions: Continuous sampling of borehole fluids in a ridge flank environment. Geochemistry, Geophysics, Geosystems 11(7), https://doi.org/​10.1029/​2010GC003057.
  58. Wilhelms, A., S.R. Larter, I. Head, P. Farrimond, R. di-Primio, and C. Zwach. 2001. Biodegradation of oil in uplifted basins prevented by deep-burial sterilization. Nature 411:1,034–1,037, https://doi.org/​10.1038/35082535.
  59. Wolfenden, R., X.D. Lu, and G. Young. 1998. Spontaneous hydrolysis of glycosides. Journal of the American Chemical Society 120:6,814–6,815, https://doi.org/10.1021/ja9813055.
  60. Yanagawa, K., A. Ijiri, A. Breuker, S. Sakai, Y. Miyoshi, S. Kawagucci, T. Noguchi, M. Hirai, A. Schippers, J. Ishibashi, and others. 2017. Defining boundaries for the distribution of microbial communities beneath the sediment-buried, hydrothermally active seafloor. The ISME Journal 11:529–542, https://doi.org/10.1038/ismej.2016.119.
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