Oceanography The Official Magazine of
The Oceanography Society
Volume 32 Issue 01

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Volume 32, No. 1
Pages 212 - 216

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Future Opportunities in Scientific Ocean Drilling: Illuminating Planetary Habitability

By Fumio Inagaki  and Asahiko Taira 
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Article Abstract

Over the past several decades, scientific ocean drilling has significantly expanded our knowledge of life and Earth. The discovery of deep microbial life and its ecosystems beneath the ocean floor suggests that subseafloor microbial ecosystems may have uniquely co-evolved in association with Earth dynamics, and this inevitable interrelationship has shaped planetary habitability for more than 3 billion years. In the future, scientific ocean drilling—from the surface to drilling’s accessible limit in the upper mantle—will permit a better understanding of what is life, why we are here, and what are the possible trajectories of our planet’s habitability and its sustainability as well as that of other celestial bodies in the universe.

Citation

Inagaki, F., and A. Taira. 2019. Future opportunities in scientific ocean drilling: Illuminating planetary habitability. Oceanography 32(1):212–216, https://doi.org/10.5670/oceanog.2019.148.

References

Barnosky, A.D., N. Matzke, S. Tomiya, G.O.U. Wogan, B. Swartz, T.B. Quental, C. Marshall, J.L. McGuire, E.E. Lindsey, K.C. Maguire, and others. 2011. Has the Earth’s sixth mass extinction already arrived? Nature 471(7336):51–57, https://doi.org/10.1038/nature09678.

Bell, E.A., P. Boehnke, T.M. Harrison, and W.L. Mao. 2015. Potentially biogenic carbon preserved in a 4.1 billion-year-old zircon. Proceedings of the National Academy of Sciences of the United States of America 112(47):14,518–14,521, https://doi.org/​10.1073/pnas.1517557112.

Biddle, J.F., J.S. Lipp, M.A. Lever, K.G. Lloyd, K.B. Sørensend, R. Anderson, H.F. Fredricks, M. Elvert, T.J. Kelly, D.P. Schrag, and others. 2006. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proceedings of the National Academy of Sciences of the United States of America 103(10):3,846–3,851, https://doi.org/​10.1073/pnas.0600035103.

Biddle, J.F., S. Fitz-Gibbon, S.C Schuster, J.E. Brenchley, and C.H. House. 2008. Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proceedings of the National Academy of Sciences of the United States of America 105(30):10,583–10,588, https://doi.org/​10.1073/pnas.0709942105.

Bowles, M.W., J.M. Mogollón, S. Kasten, M. Zabel, and K.-U. Hinrichs. 2014. Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities. Science 344(6186):889–891, https://doi.org/10.1126/science.1249213.

Ciobanu, M.-C., G. Burgaud, A. Dufresne, A. Breuker, V. Rédou, S.S. 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(7):1,370–1,380, https://doi.org/10.1038/ismej.2013.250.

Coolen, M.J., W.D. Orsi, C. Balkema, C. Quince, K. Harris, S.P. Sylva, M. Filipova-Marinova, and L. Giosan. 2013. Evolution of the plankton paleome in the Black Sea from the Deglacial to Anthropocene. Proceedings of the National Academy of Sciences of the United States of America 110(21):8,609–8,614, https://doi.org/​10.1073/pnas.1219283110.

D’Hondt, S., S. Rutherford, and A.J. Spivack. 2002. Metabolic activity of subsurface life in deep-sea sediments. Science 295(5562):2,067–2,070, https://doi.org/10.1126/science.1064878.

D’Hondt, S., B.B. Jørgensen, D.J. Miller, A. Batzke, R. Blake, B.A. Cragg, H. Cypionka, G.R. Dickens, T. Ferdelman, K.-U. Hinrichs, and others. 2004. Distributions of microbial activities in deep subseafloor sediments. Science 306(5705):2,216–2,221, https://doi.org/10.1126/science.1101155.

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 seafloor to basement in deep-sea sediment. Nature Geoscience 8:299–304, https://doi.org/​10.1038/ngeo2387.

Dzaugis, M., A.J. Spivack, and S. D’Hondt. Radiolytic H2 production in Martian environments. Astrobiology 18(9):1,137–1,146, https://doi.org/​10.1089/ast.2017.1654.

Engelhardt, T., J. Kallmeyer, H. Cypionka, and B. Engelen. 2014. High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments. The ISME Journal 8:1,503–1,509, https://doi.org/10.1038/ismej.2013.245.

Estes, E.R., R. Pockalny, S. D’Hondt, F. Inagaki, Y. Morono, R.W. Murray, D. Nordlund, A.J. Spivack, S.D. Wankel, N. Xiao, and C.M. Mansel. 2019. Persistent organic matter in oxic subseafloor sediment. Nature Geoscience. 12(2):126–131, https://doi.org/​10.1038/s41561-018-0291-5.

Fry, J.C., R.J. Parkes, B.A. Cragg, A.J. Weightman, and G. Webster. 2008. Prokaryotic biodiversity and activity in the deep subseafloor biosphere. FEMS Microbiology Ecology 66(2):181–196, https://doi.org/​10.1111/j.1574-6941.2008.00566.x.

Hazen, R.M., D. Papineau, W. Bleeker, R.T. Downs, J.M. Ferry, T.J. McCoy, D.A. Sverjensky, and H. Yang. 2008. Mineral evolution. American Mineralogist 93:1,693–1,720, https://doi.org/10.2138/am.2008.2955.

Heuer, V.B., F. Inagaki, Y. Morono, Y. Kubo, L. Maeda, and the Expedition 370 Scientists. 2017. Expedition 370 Preliminary Report: Temperature Limit of the Deep Biosphere off Muroto. International Ocean Discovery Program, College Station, TX, https://doi.org/​10.14379/iodp.pr.370.2017.

Hinrichs, K.-U., and F. Inagaki. 2012. Downsizing the deep biosphere. Science 338(6104):204–205, https://doi.org/10.1126/science.1229296.

Hoehler, T.M., and B.B. Jørgensen. 2013. Microbial life under extreme energy limitation. Nature Reviews Microbiology 11:88–94, https://doi.org/10.1038/nrmicro2939.

Hoshino, T., T. Toki, A. Ijiri, Y. Morono, H. Machiyama, J. Ashi, K. Okamura, and F. Inagaki. 2017. Atribacteria from the subseafloor sedimentary biosphere disperse to the hydrosphere through submarine mud volcanoes. Frontiers in Microbiology 8:1135, https://doi.org/10.3389/fmicb.2017.01135.

Hoshino, T., and F. Inagaki. 2019. Abundance and distribution of Archaea in the subseafloor sedimentary biosphere. The ISME Journal 13:227–231, https://doi.org/​10.1038/s41396-018-0253-3.

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.

Imachi, H., E. Tasumi, Y. Takaki, T. Hoshino, F. Schubotz, S. Gan, T.-H. Tu, Y. Saito, Y. Yamanaka, A. Ijiri, and others. 2019. Cultivable microbial community in 2-km-deep, 20-million-year-old subseafloor coalbeds through ~1000 days anaerobic bioreactor cultivation. Scientific Reports 9:2305, https://doi.org/10.1038/s41598-019-38754-w.

Inagaki, F., T. Nunoura, S. Nakagawa, A. Teske, M. Lever, A. Lauer, M. Suzuki, K. Takai, M. Delwiche, F.S. Colwell, and others. 2006. Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proceedings of the National Academy of Sciences of the United States of America 103(8):2,815–2,820, https://doi.org/10.1073/pnas.0511033103.

Inagaki, F., H. Okada, A.I. Tsapin, and K.H. Nealson. 2012. The paleome: A sedimentary genetic record of past microbial communities. Astrobiology 5(2):141–153, https://doi.org/10.1089/ast.2005.5.141.

Inagaki, F., K.-U. Hinrichs, Y. Kubo, M.W. Bowles, V.B. Heuer, W.-L. Long, 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(6246):420–424, https://doi.org/​10.1126/science.aaa6882.

Jørgensen, B.B., and I.P. Marshall. 2016. Slow microbial life in the seabed. Annual Review of Marine Science 8:311–332, https://doi.org/10.1146/annurev-marine-010814-015535.

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(40):16,213–16,216, https://doi.org/​10.1073/pnas.1203849109.

Karner, M.B., E.F. DeLong, and D.M. Karl. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409(6819):507–510, https://doi.org/10.1038/35054051.

Kirkpatrick, J.B., E.A. Walsh, and S. D’Hondt. 2016. Fossil DNA persistence and decay in marine sediment over hundred-thousand-year to million-year time scales. Geology 44(8):615–618, https://doi.org/​10.1130/G37933.1.

LaRowe, D.E., E. Burwicz, S. Arndt, A.W. Dale, and J.P. Amend. 2017. Temperature and volume of global marine sediments. Geology 45(3):275–278, https://doi.org/10.1130/G38601.1.

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(6125):1,305–1,308, https://doi.org/10.1126/science.1229240.

Lever, M.A., K.L. Rogers, K.G. Lloyd, J. Overmann, B. Schink, R.K. Thauer, T.M. Hoehler, and B.B. Jørgensen. 2015. Life under extreme energy limitation: A synthesis of laboratory- and field-based investigations. FEMS Microbiology Review 39(5):688–728, https://doi.org/10.1093/femsre/fuv020.

Liu, C.-H., X. Huang, T.-N. Xie, N. Duan, Y.-R. Xue, T.-X. Zhao, M.A. Lever, K.-U. Hinrichs, and F. Inagaki. 2017. Exploration of cultivable fungal communities in deep coal-bearing sediments from ~1.3 to 2.5 km below the ocean floor. Environmental Microbiology 19(2):803–818, https://doi.org/​10.1111/1462-2920.13653.

Lipp, J.S., Y. Morono, F. Inagaki, and K.-U. Hinrichs. 2008. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454:991–994, https://doi.org/10.1038/nature07174.

Lloyd, K.G., L. Schreiber, D.G. Petersen, K.U. Kjeldsen, M.A. Lever, A.D. Steen, R. Stepanauskas, M. Richter, S. Kleindienst, S. Lenk, and others. 2013. Predominant archaea in marine sediments degrade detrital proteins. Nature 496(7444):215–218, https://doi.org/10.1038/nature12033.

Lomstein, B.A., A.T. Langerhuus, S. D’Hondt, B.B. Jørgensen, 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.

Lowery, C.M., T.J. Bralower, J.D. Owens, F.J. Rodríguez-Tovar, H. Jones, J. Smit, M.T. Whalen, P. Claeys, K. Farley, S.P.S. Gulick, and others. 2018. Rapid recovery of life at ground zero of the end-Cretaceous mass extinction. Nature 558(7709):288–291, https://doi.org/10.1038/s41586-018-0163-6.

Morono, Y., T. Terada, N. Masui, and F. Inagaki. 2009. Discriminative detection and enumeration of microbial life in marine subsurface sediments. The ISME Journal 3(5):503–511, https://doi.org/10.1038/ismej.2009.1.

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(45):18,295–18,300, https://doi.org/​10.1073/pnas.1107763108.

Orcutt, B.N., C.G. Wheat, O. Rouxel, S. Hulme, K.J. Edwards, and W. Bach. 2012. Oxygen consumption rates in subseafloor basaltic crust derived from a reaction transport model. Nature Communications 4:2539, https://doi.org/10.1038/ncomms3539.

Orsi, W., J.F. Biddle, and V. Edgcomb. 2013. Deep sequencing of subseafloor eukaryotic rRNA reveals active fungi across marine subsurface provinces. PLoS ONE 8(2):e56335, https://doi.org/10.1371/​journal.pone.0056335.

Orsi, W.D., M.J.L. Coolen, C. Wuchter, L. He, K.D. More, X. Irigoien, G. Chust, C. Johnson, J.D. Hemingway, M. Lee, and others. 2017. Climate oscillations reflected within the microbiome of Arabian Sea sediments. Scientific Reports 7:6040, https://doi.org/​10.1038/​s41598-017-05590-9.

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.

Parkes, R.J., S. Berlendis, E.G. Roussel, H. Bahruji, G. Webster, A. Oldroyd, A.J. Weightman, M. Bowker, P.R. Davies, and H. Sass. 2019. Rock-crushing derived hydrogen directly supports a methanogenic community: Significance for the deep biosphere. Environmental Microbiology Reports, https://doi.org/10.1111/1758-2229.12723.

Sleep, N.H., D.K. Bird, and E. Pope. 2011. Serpentinite and the dawn of life. Philosophical Transactions of the Royal Society B 366:2,857–2,869, https://doi.org/​10.1098/rstb.2011.0129.

Sleep, N.H., D.K. Bird, and E. Pope. 2012. Paleontology of Earth’s mantle. Annual Review of Earth and Planetary Sciences 40:277–300, https://doi.org/​10.1146/​annurev-​earth-​092611-​090602.

Stamenković, V., L.W. Beegle, K. Zacny, D.D. Arumugam, P. Baglioni, N. Barba, J. Baross, M.-S. Bell, R. Bhartia, J.G. Blank, and others. 2019. The next frontier for planetary and human exploration. Nature Astronomy 3(2):116–120, https://doi.org/​10.1038/s41550-018-0676-9.

Starnawski, P., T. Bataillon, T.J.G. Ettema, L.M. Jochum, L. Schreiber, X. Chena, M.A. Lever, M.F. Polz, B.B. Jørgensen, A. Schramm, and K.U. Kjeldsen. 2017. Microbial community assembly and evolution in subseafloor sediment. Proceedings of the National Academy of Sciences of the United States of America 114(11):2,940–2,945, https://doi.org/​10.1073/​pnas.1614190114.

Steffen, W., W. Broadgate, L. Deutsch, O. Gaffney, and C. Ludwig. 2015. The trajectory of the Anthropocene: The Great Acceleration. The Anthropocene Review 2(1):81–98, https://doi.org/​10.1177/2053019614564785.

Tanikawa, W., O. Tadai, Y. Morono, K.-U. Hinrichs, and F. Inagaki. 2018. Geophysical constraints on microbial biomass in subseafloor sediments and coal seams down to 2.5 km off Shomokita Peninsula, Japan. Progress in Earth and Planetary Science 5:58, https://doi.org/10.1186/s40645-018-0217-2.

Trembath-Reichert, E., Y. Morono, A. Ijiri, T. Hoshino, K.S. Dawson, F. Inagaki, and V.J. Orphan. 2017. Methyl-compound use and slow growth characterize microbial life in 2-km-deep subseafloor coal and shale beds. Proceedings of the National Academy of Sciences of the United States of America 114(44):E9206–E9215, https://doi.org/​10.1073/pnas.1707525114.

Walsh, E.A., J.B. Kirkpatrick, S.D. Rutherford, D.C. Smith, M. Sogin, and S. D’Hondt. 2016. Bacterial diversity and community composition from seasurface to subseafloor. The ISME Journal 10(4):979–989, https://doi.org/10.1038/ismej.2015.175.

Waters, C.N., J. Zalasiewicz, C. Summerhayes, A.D. Barnosky, C. Poirier, A. Gałuszka, A. Cearreta, M. Edgeworth, E.C. Ellis, M. Ellis, and others. 2016. The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351(6269):aad2622, https://doi.org/10.1126/science.aad2622.

Wörmer, L., T. Hoshino, M.W. Bowles, B. Viehweger, R.R. Adhikari, N. Xiao, G.-I. Uramoto, Y. Morono, F. Inagaki, and K.-U. Hinrichs. 2019. Microbial dormancy in the marine subsurface: Global endospore abundance and response to burial. Science Advances 5(2):eaav1024, https://doi.org/10.1126/sciadv.aav1024.

Yung, Y.L., P. Chen, K. Nealson, S. Atreya, P. Beckett, J.G. Blank, B. Ehlmann, J. Eiler, G. Etiope, J.G. Ferry, and others. 2018. Methane on Mars and habitability: Challenges and responses. Astrobiology 18(10):1,221–1,242, https://doi.org/​10.1089/ast.2018.1917.

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