Abstract
The discovery of the marine “deep biosphere”—microorganisms living deep below the seafloor—is one of the most significant and exciting discoveries since the ocean drilling program began more than 40 years ago. Study of the deep biosphere has become a research frontier and a hot spot both for geological and biological sciences. Here, we introduce the history of the discovery of the deep biosphere, and then we describe the types of environments for life below the seafloor, the energy sources for the living creatures, the diversity of organisms within the deep biosphere, and the new tools and technologies used in this research field. We will highlight several recently completed Integrated Ocean Drilling Program Expeditions, which targeted the subseafloor deep biosphere within the crust and sediments. Finally, future research directions and challenges of deep biosphere investigation towards uncovering the roles of subsurface microorganisms will be briefly addressed.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
ZoBell C E, Anderson Q A. Vertical distribution of bacteria in marine sediments. Am Assoc Pet Geol Bull, 1936, 20: 258–269
ZoBell C E, Morita R Y. Barophilic bacteria in some deep sea sediments. J Bacteriol, 1957, 73: 563–568
ZoBell C E. Studies on the bacterial flora of marine bottom sediments. J Sediment Res A Sediment Petrol Process, 1938, 8: 10–18
Corliss J B, Dymond J, Gordon L I, et al. Submarine thermal sprirngs on the Galapagos rift. Science, 1979, 203: 1073–1083
Parkes R J, Cragg B A, Bale S J, et al. Deep bacterial biosphere in Pacific Ocean sediments. Nature, 1994, 371: 410–413
Whitman W B, Coleman D C, Wiebe W J. Prokaryotes: The unseen majority. Proc Natl Acad Sci USA, 1998, 95: 6578–6583
Lipp J S, Morono Y, Inagaki F, et al. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature, 2008, 454: 991–994
Edwards K J, Bach W, McCollom T M. Geomicrobiology in oceanography: microbe-mineral interactions at and below the seafloor. Trends Microbiol, 2005, 13: 449–459
D’Hondt S L, Jorgensen B B, Miller D J, et al. Proc. ODP Init. Repts. 201: College Station, TX (Ocean Drilling Program). 2003
Expedition 331 Scientists. Deep hot biosphere. IODP Prel Rept, 2010, 331. doi: 10.2204/iodp.pr.331.2010
Expedition 329 Scientists. South Pacific Gyre subseafloor life. IODP Prel Rept, 329. 2011, doi: 10.2204/iodp.pr.329.2011
Expedition 336 Scientists. Mid-Atlantic Ridge microbiology: Initiation of long-term coupled microbiological, geochemical, and hydrological experimentation within the seafloor at North Pond, western flank of the Mid-Atlantic Ridge. IODP Prel Rept, 336. 2011, doi: 10.2204/iodp.pr.336.2011
Orcutt B N, Sylvan J B, Knab N J, et al. Microbial ecology of the dark ocean above, at and below the seafloor. Microbiol Mol Biol Rev, 2011, 75: 361–422
Edwards K J, Wheat C G, Sylvan J B. Under the sea: Microbial life in volcanic oceanic crust. Nat Rev Microbiol, 2011, 9: 703–712
Schrenk M O, Huber J A, Edwards K J. Microbial provinces in the subseafloor. Oceanography, 2009, 2: 85–110
Fang J S, Zhang L. Exploring the deep biosphere. Sci China Earth Sci, 2011, 54: 157–165
Fry J C, Parkes R J, Cragg B A, et al. Prokaryotic biodiversity and activity in the deep subseafloor biosphere. FEMS Microbiol Ecol, 2008, 66: 181–196
Santelli C M, Edgcomb V P, Bach W, et al. The diversity and abundance of bacteria inhabiting seafloor lavas positively correlate with rock alteration. Environ Microbiol, 2009, 11: 86–98
Johnson H P, Priuis M J. Fluxes of fluid and heat from the oceanic crustal resevoir. Earth Planet Sci Lett, 2003, 216: 565–574
Fisher A T. Permeability within basaltic oceanic crust. Geol Rev, 1998, 36: 143–182
Wheat C G, McManus J, Mottl M J, et al. Oceanic phosphorous imbalance: Magnitude of the mid-ocean ridge flank hydrothermal sink. Geophys Res Lett, 2003, 30: 1895
D’Hondt S L, Spivack A J, Pockalnya R, et al. Subseafloor sedimentary life in the South Pacific gyre. Proc Natl Acad Sci USA, 2009, 106: 11651–11656
Pollack H N, Hurter S J, Johnson J R. Heat flow from the Earth’s interior: Analysis of the global data set. Rev Geophys, 1993, 31: 267–280
Detrick R S. Portrait of a magma chamber. Nature, 2000, 406: 578–579
Fisk M R, Giovannoni S J, Thoreth I H. Alteration of oceanic volcanic glass: Textural evidence of microbial activity. Science, 1998, 281: 978–980
Reysenbach A L, Banta A B, Boone D R, et al. Microbial essentials at hydrothermal vents. Nature, 2000, 404: 835
Wang F P, Zhou H Y, Meng J, et al. GeoChip-based analysis of metabolic diversity of microbial communities at the Juan de Fuca Ridge hydrothermal vent. Proc Natl Acad Sci USA, 2009, 106: 4840
Huber J A, Butterfield D A, Baross J A. Temporal changes in archaeal diversity and chemistry in a mid-ocean ridge subseafloor habitat. Appl Environ Microbiol, 2002, 68: 1585–1594
Page A, Tivey M K, Stakes D S, et al. Temporal and spatial archaeal colonization of hydrothermal vent deposits. Environ Microbiol, 2008, 10: 874–884
Flores G E, Campbell J H, Kirshtein J D, et al. Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. Environ Microbiol, 2011, 13: 2158–2171
Deming J W, Baross J A. Deep-sea smokers: Windows to a subsurface biosphere? Geochim Cosmochim Acta, 1993, 57: 3219–3230
Kelley D S, Baross J A, Delaney J R. Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Annu Rev Earth Planet Sci, 2002, 30: 385–491
Takai K, Gamo T, Tsunogai U, et al. Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field. Extremophiles, 2004, 8: 269–282
Cowen J. Fluids from aging ocean crust that support microbial life. Science, 2003, 299: 120–123
Embley R W, Hobart M A, Anderson R N, et al. Anomalous heat flow in the Northwest Atlantic: A case for continued hydrothermal circulation in 80-M.Y. Crust. J Geophys Res, 1983, 88: 1067–1074
Moyer C L, Tiedje J M, Dobbs F C, et al. Diversity of deep-sea hydrothermal vent Archaea from Loihi Seamount, Hawaii. Deep Sea Res Part II, 1998, 45: 303–317
Kelley D S, Karson J A, Blackman D K, et al. An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30°N. Nature, 2001, 412: 145
Kelley D S. A serpentinite-hosted ecosystem: The lost city hydrothermal field. Science, 2005, 307: 1428–1434
Wheat C G, Elderfield H, Mottl M J, et al. Chemical composition of basement fluids within an oceanic ridge flank: Implications for along-strike and across-strike hydrothermal circulation. J Geophys Res, 2000, 105: 13437–13447
Bach W, Edwards K J. Iron and sulfide oxidation within the basaltic ocean crust: Implications for chemolithoautotrophic microbial biomass production. Geochim Cosmochim Acta, 2003, 67: 3871–3887
Furnes H, Staudigel H, Thorseth I H, et al. Bioalteration of basaltic glass in the oceanic crust. Geochem Geophys Geosys, 2001, 2: 1049
Cande S C, Kent D V. Revised calibration of the geomagnetic polarity timescale for the Late Cretaceous and Cenozoic. J Geophys Res, 1995, 100: 6093–6095
Shipboard Scientific Party. Juan de Fuca hydrogeology: The hydrogeologic architecture of basaltic oceanic crust: compartmentalization, anisotropy, microbiology, and crustal-scale properties on the eastern flank of Juan de Fuca Ridge, eastern Pacific Ocean. IODP Prel Rept, 301. 2004, doi: 10.2204/iodp.pr.301.2004.
Expedition 327 Scientists. Juan de Fuca Ridge-flank hydrogeology: The hydrogeologic architecture of basaltic oceanic crust: Compartmentalization, anisotropy, microbiology, and crustal-scale properties on the eastern flank of Juan de Fuca Ridge, eastern Pacific Ocean. IODP Prel Rept, 327. 2010, doi: 10.2204/iodp.pr.327.2010.
Edwards K J, Fisher A T, Wheat C G. The deep subsurface biosphere in igneous ocean crust: Frontier habitats for microbiological exploration. Front Microbiol, 2012, 3: 8
McCollom T M. Geochemical constraints on primary productivity in submarine hydrothermal vent plumes. Deep Sea Res Part I, 2000, 47: 85–101
Lomstein B A, Langerhuus A T, D’Hondt S, et al. Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature, 2012, 484: 101–104
Nauhaus K, Boetius A, Krüger M, et al. In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ Microbiol, 2002, 4: 296–305
Nauhaus K, Treude T, Boetius A, et al. Environmental regulation of the anaerobic oxidation of methane: A comparison of ANME-I and ANME-II communities. Environ Microbiol, 2005, 7: 98–106
Knittel K, Boetius A. Anaerobic oxidation of methane: Progress with an unknown process. Annu Rev Microbiol, 2009, 63: 311–334
House C H, Orphan V J, Turk K A, et al. Extensive carbon isotopic heterogeneity among methane seep microbiota. Environ Microbiol, 2009, 11: 2207–2215
Dekas A E, Poretsky R S, Orphan V J. Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science, 2009, 326: 422–426
Beal E J, House C H, Orphan V J. Manganese- and iron-dependent marine methane oxidation. Science, 2009, 325: 184–187
Biddle J F, Lipp J S, Lever M A, et al. Heterotrophic archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA, 2006, 103: 3846–3851
Inagaki F, Nunoura T, Nakagawa S, et al. Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proc Natl Acad Sci USA, 2006, 103: 2815–2820
Meng J, Wang F P, Wang F, et al. An uncultivated crenarchaeota contains functional bacteriochlorophyll a synthase. ISME J, 2009, 3: 106–116
Chapelle F H, O’Neill K, Bradley P M, et al. A hydrogen-based subsurface microbial community dominated by methanogens. Nature, 2002, 415: 312–315
Mason O U, Di Meo-Savoie C A, Van Nostrand J D, et al. Prokaryotic diversity, distribution, and insights into their role in biogeochemical cycling in marine basalts. ISME J, 2009, 3: 231–242
Santelli C M, Orcutt B N, Banning E, et al. Abundance and diversity of microbial life in ocean crust. Nature, 2008, 453: 653–657
Orcutt B N, Bach W, Becker K, et al. Colonization of subsurface microbial observatories deployed in young ocean crust. ISME J, 2010, 5: 692–703
Lysnes K, Thorseth I H, Steinsbu B O, et al. Microbial community diversity in seafloor basalt from the Arctic spreading ridges. FEMS Microbiol Ecol, 2004, 50: 213–230
Emerson D, Rentz J A, Lilburn T G, et al. A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS one, 2007, 2: e667
Expedition 330 Scientists. Louisville Seamount Trail: Implications for geodynamic mantle flow models and the geochemical evolution of primary hotspots. IODP Prel Rept, 330. 2011, doi: 10.2204/iodp.pr.330.2011
Einen J, Thorseth I H, Ovreas L. Enumeration of archaea and bacteria in seafloor basalt using real-time quantitative PCR and fluorescence microscopy. FEMS Microbiol Lett, 2008, 282: 182–187
Auguet J C, Barberan A, Casamayor E O. Global ecological patterns in uncultured Archaea. ISME J, 2009, 4: 182–190
Takai K, Nakamura K. Archaeal diversity and community development in deep-sea hydrothermal vents. Curr Opin Microbiol, 2011, 14: 282–291
Xie W, Wang F P, Guo L, et al. Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries. ISME J, 2011, 5: 414
Davis E E, Becker K, Pettigrew T L, et al. Proc. ODP Init. Repts. 139: College Station, TX (Ocean Drilling Program). 1992
Fisher A T, Wheat C G, Becker K, et al. Scientific and technical design and deployment of longterm, subseafloor observatories for hydrogeologic and related experiments, IODP Expedition 301, eastern flank of Juan de Fuca Ridge. 301: College Station, TX Integrated Ocean Drilling Program Management International, Inc. 2005
Expedition 332 Scientists. NanTroSEIZE Stage 2: Riserless observatory. IODP Prel Rept, 332. 2011, doi: 10.2204/iodp.pr.332.2011
State Key Laboratory of Marine Geology. Under Water Observatories: The Combination of Science and Technology (in Chinese). Shanghai: Tongji University Press, 2011
Girguis P R, Cozen A E, DeLong E F. dynamics of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria in a continuous-clow bioreactor. Appl Environ Microbiol, 2005, 71: 3725–3733
Deusner C, Meyer V, Ferdelman T G. High-pressure systems for gas-phase free continuous incubation of enriched marine microbial communities performing anaerobic oxidation of methane. Biosens Bioelectron, 2009, 105: 524–533
Jagersma G C, Meulepas R J W, Heikamp J I, et al. Microbial diversity and community structure of a highly active anaerobic methane-oxidizing sulfate-reducing enrichment. Environ Microbiol, 2009, 11: 3223–3232
Zhang Y, Arends J B A, Van de Wiele T, et al. Bioreactor technology in marine microbiology: From design to future application. Biotechnol Adv, 2011, 29: 312–321
Grossart H P, Gust G. Hydrostatic pressure affects physiology and community structure of marine bacteria during settling to 4000 m: An experimental approach. Mar Ecol Prog Ser, 2009, 390: 97–104
Jannasch H W, Wirsen C O, Doherty K W. A pressurized chemostat for the study of marine barophilic and oligotrophic bacteria. Appl Environ Microbiol, 1996, 62: 1593
Parkes R J, Sellek G, Webster G, et al. Culturable prokaryotic diversity of deep, gas hydrate sediments: First use of a continuous high-pressure, anaerobic, enrichment and isolation system for subseafloor sediments (DeepIsoBUG). Environ Microbiol, 2009, 11: 3140–3153
Zhang Y, Henriet J P, Bursens J, et al. Stimulation of in vitro anaerobic oxidation of methane rate in a continuous high-pressure bioreactor. Bioresour Technol, 2010, 101: 3132–3138
Zhang Y, Maignien L, Zhao X X, et al. Enrichment of a microbial community performing anaerobic oxidation of methane in a continuous high-pressure bioreactor. BMC Microbiol, 2011, 11: 137
Zeng X, Birrien J L, Fouquet Y, et al. Pyrococcus CH1, an obligate piezophilic hyperthermophile: Extending the upper pressure-temperature limits for life. ISME J, 2009, 3: 873–876
Imachi H, Aoi K, Tasumi E, et al. Cultivation of methanogenic community from subseafloor sediments using a continuous-flow bioreactor. ISME J, 2011, 5: 1913–1925
Takano Y, Chikaraishi Y, Ogawa N O, et al. Sedimentary membrane lipids recycled by deep-sea benthic archaea. Nat Geosci, 2010, 3: 858–861
Lasken R S. Single-cell genomic sequencing using multiple displacement amplification. Curr Opin Microbiol, 2007, 10: 510–516
Behrens S, Loesekann T, Pett-Ridge J, et al. Linking microbial phylogeny to metabolic activity at the single-cell level by using enhanced element labeling-catalyzed reporter deposition fluorescence in situ hybridization (EL-FISH) and NanoSIMS. Appl Environ Microbiol, 2008, 74: 3143–3150
Nunoura T, Takaki Y, Kakuta J, et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res, 2011, 39: 3204–3223
Hallam S J, Mincer T J, Schleper C, et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol, 2006, 4: 520–536
Illuminating earth through subseafloor sampling, observation, and experimentation: The international ocean discovery program, science plan for 2013–2023. Washington DC: IWG Supporting Office, 2010
Xie S, Yang H, Luo G, et al. Geomicrobial functional groups: A window on the interaction between life and environments. Chin Sci Bull, 2012, 57: 2–19
Author information
Authors and Affiliations
Corresponding authors
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
This article is published under an open access license. Please check the 'Copyright Information' section either on this page or in the PDF for details of this license and what re-use is permitted. If your intended use exceeds what is permitted by the license or if you are unable to locate the licence and re-use information, please contact the Rights and Permissions team.
About this article
Cite this article
Wang, F., Lu, S., Orcutt, B.N. et al. Discovering the roles of subsurface microorganisms: Progress and future of deep biosphere investigation. Chin. Sci. Bull. 58, 456–467 (2013). https://doi.org/10.1007/s11434-012-5358-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11434-012-5358-x