Deep Subseafloor Microbial Communities

Fumio Inagaki, Japan Agency for Marine‐Earth Science and Technology (JAMSTEC), Nankoku, Kochi, Japan

Published online: February 2010

DOI: 10.1002/9780470015902.a0021894

Marine subsurface sediments cover approximately 70% of the Earth surface and harbour a remarkable population of microbial life that comprises one-tenth of all living biota on Earth. Metabolic activity of the subseafloor microbes is generally extremely low due to low flux of nutrient and energy substrates in the habitats. However, the long-term microbial activities play important ecological roles in biogeochemical cycles over geologic time scales. Most subseafloor bacteria and archaea are phylogenetically distinct from known isolates. Hence, the growth characteristics and metabolic activities of each species remain largely unknown.

Key concepts:

  • Significant microbial biomass is present in the deep subseafloor biosphere.
  • Metabolic activity of subseafloor microbes is extraordinary low.
  • Subseafloor microbes play important biogeochemical roles on geologic time scale.
  • Subseafloor microbial communities are mainly composed of uncultivated, hence uncharacterized components.
  • Ecologically significant microbial functions are expected from functional gene surveys and metagenomic analyses.
  • New analytical developments provide new insights into the nature of subseafloor life and the biosphere.

Keywords: deep subseafloor biosphere; phylogenetic diversity; functional genes; Archaea World; biogeochemical cycle

Figure 1. Global microbial biomass in aquatic, soil and subsurface habitats. Data are from Whitman et al. (1998).
Figure 2. Discrimination of cell-derived SYBR Green I fluorescence from background signals using a computer-based image analysis. (a) Spectrum pattern of cell-derived fluorescence and nonspecific binding of SYBR Green I, so-called SYBR-SPAM (SYBR-stainable particulate matter). When SYBR Green I binds to SYBR-SPAM, fluorescent spectra shift to longer wavelengths (red line), whereas fluorescent spectra of cell-derived SYBR-I (blue line) do not shift or shift very little from the original spectrum of SYBR Green I. Green and orange shading areas show the wavelength range of 528/38, 617/73 (nm of centre wavelength/bandwidth) band-pass filters, respectively. (b) to (c) Image analysis to distinguish cell-derived SYBR Green I signals from SYBR-SPAM in heat-sterilized control sediments mixed with E. coli. Fluorescent microscopic images taken using band-pass filters of 528/38 (b) and 617/73 (c). Relative intensity profiles of green/red fluorescence (d) resulted in only cell-derived fluorescent signals without background fluorescence. Bars: 10 m. Data are derived from Morono et al. (2008), with permission from Nature Publishing Group.
Figure 3. Phylogenetic tree of the domains Archaea and Bacteria based on 16S rRNA gene sequences. The red and blue phyla represent archaeal and bacterial groups that include frequently detected 16S rRNA gene sequences from the deep subseafloor sediments, respectively. The subseafloor sediment samples are derived from Peru Margin (ODP Leg 201), Cascadia Margin (ODP Leg 204), Eastern Flank of the Juan de Fuca Ridge (IODP Exp. 301), Northwestern Pacific offshore the Shimokita Peninsula (JAMSTEC CK06-06) and the Nankai Trough seismogenic zone (IODP Exp. 315 and 316). The sequence data were analysed with the ARB software package (Ludwig et al., 2004).
Figure 4. Quantitative analysis of archaeal population in deep marine sediments. (a) Depth profile of total microbial intact polar lipids (IPLs) and the ratio of archaeal IPLs. (b) Archaeal 16S rRNA gene ratios of total microbial 16S rRNA genes evaluated by quantitative-PCR and slot-blot hybridization (SBH) analyses using a new DNA extraction method with physical destruction and multiple displacement amplification (MDA). Data are derived from Lipp et al. (2008), with permission from Nature Publishing Group.
Figure 5. An example of a schematic flow chart of culture-independent molecular ecological and biogeochemical approaches for understanding of eco-physiological functions of the subseafloor ecosystem and subseafloor microbes.
close
 References
    Bach W and Edwards KJ (2003) Iron and sulfide oxidation within the basaltic ocean crust: implications for chemolithoautotrophic microbial biomass production. Geochimica et Cosmochimica Acta 67: 3871–3887.
    Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE and House CH (2008) Metagenomic signatures of the Peru margin subseafloor biosphere show a genetically distinct environment. Proceedings of the National Academy of Sciences of the USA 105: 10583–10588.
    Biddle JF, Lipp JS, Lever MA et al. (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proceedings of the National Academy of Sciences of the USA 103: 3846–3851.
    book Claypool GE and Kaplan IR (1974) "The origin and distribution of methane in marine sediments". In: Kaplan IR (ed.) Natural Gases in Marine Sediments, pp. 99–139. New York: Plenum.
    Colwell FS, Boyd S, Delwiche ME et al. (2008) Estimates of biogenic methane production rates in deep marine sediments at Hydrate ridge, Cascadia margin. Applied and Environmental Microbiology 74: 3444–3452.
    Coolen MJ, Cypionka H, Sass AM, Sass H and Overmann J (2002) Ongoing modification of Mediterranean Pleistocene sapropels mediated by prokaryotes. Science 296: 2407–2410.
    Cowen JP, Giovannoni SJ, Kenig F et al. (2003) Fluids from aging ocean crust that support microbial life. Science 299: 120–123.
    D'Hondt S, Jørgensen BB, Miller DJ et al. (2004) Distributions of microbial activities in deep subseafloor sediments. Science 306: 2116–2121.
    D'Hondt S, Rutherford S and Spivack AJ (2002) Metabolic activity of subsurface life in deep-sea sediments. Science 295: 2067–2070.
    D'Hondt S, Spivack AJ, Pockalny R et al. (2009) Subseafloor sedimentary life in the South Pacific Gyre. Proceedings of the National Academy of Sciences of the USA 106: 11651–11656.
    Edwards KJ, Bach W and Rogers DR (2003) Geomicrobiology of the ocean crust: a role for chemoautotrophic Fe-bacteria. Biological Bulletin 204: 180–185.
    Engelen B, Ziegelmüller K, Wolf L et al. (2008) Fluids from the oceanic crust support microbial activities within the deep biosphere. Geomicrobiolgy Journal 25: 56–66.
    Fisk MR, Giovannoni SJ and Thorseth IH (1998) Alteration of oceanic volcanic glass: textural evidence of microbial activity. Science 281: 978–980.
    Futagami T, Morono Y, Terada T, Kaksonen AH and Inagaki F (2009) Dehalogenation activities and distribution of reductive dehalogenase homologous genes in marine subsurface sediments. Applied and Environmental Microbiology, 75: 6905–6909.
    Heuer VB, Pohlman JW, Torres ME, Elvert M and Hinrichs K-U (2009) The stable carbon isotope biogeochemistry of acetate and other dissolved carbon species in deep subseafloor sediments at the northern Cascadia margin. Geochemica at Cosmochimica Acta 73: 3323–3336.
    Hinrichs K-U, Hayes JM, Bach W et al. (2006) Biological formation of ethane and propane in the deep marine subsurface. Proceedings of the National Academy of Sciences of the USA 103: 14684–14689.
    Inagaki F, Nunoura T, Nakagawa S et al. (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 USA 103: 2815–2820.
    Inagaki F, Suzuki M, Takai K et al. (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Applied and Environmental Microbiology 69: 7224–7235.
    Jørgensen BB and Boetius A (2007) Feast and famine – microbial life in the deep-sea bed. Nature Review of Microbiology 5: 770–781.
    Kendall MM, Liu Y, Sieprawska-Lupa M et al. (2006) Methanococcus aeolicus sp. nov., a mesophilic, methanogenic archaeon from shallow and deep marine sediments. International Journal of Systematic and Evolutionary Microbiology 56: 1525–1529.
    Knittel K and Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annual Review of Microbiology 63: 311–334.
    Lever MA, Heuer VB, Morono Y et al. (2010) Acetogenesis in deep subseafloor sediments of the Juan de Fuca ridge flank: a synthesis of geochemical, thermodynamic, and gene-based evidence. Geomicrobiology Journal, in press.
    Lipp JS, Morono Y, Inagaki F and Hinrichs K-U (2008) Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454: 991–994.
    Ludwig W, Strunk O, Westram R et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32: 1363–1371.
    Marchesi JR, Weightman AJ, Cragg BA, Parkes RJ and Fry JC (2001) Methanogen and bacterial diversity and distribution in deep gas hydrate sediments from the Cascadia margin as revealed by 16S rRNA molecular analysis. FEMS Microbiology Ecology 34: 221–228.
    Masui N, Morono Y and Inagaki F (2008) Microbiological assessment of circulation mud fluids during the first operation of riser drilling by the deep-earth research vessel Chikyu. Geomicrobiology Journal 25: 274–282.
    Meng J, Wang F, Wang F et al. (2009) An uncultivated crenarchaeota contains functional bacteriochlorophyll a synthase. ISME Journal 3: 106–116.
    Mikucki JA, Liu Y, Delwiche M, Colwell FS and Boone DR (2003) Isolation of a methanogen from deep marine sediments that contain methane hydrates, and description of Methanoculleus submarinus sp. nov. Applied and Environmental Microbiology 69: 3311–3316.
    Milkov AV (2004) Global estimates of hydrate-bound gas in marine sediments: how much is really out there? Earth-Science Reviews 66: 183–197.
    Morono Y, Terada T, Masui N and Inagaki F (2008) Discriminative detection and enumeration of microbial life in marine subsurface sediments. ISME Journal 3: 503–511.
    Musat N, Halm H, Winterholler B et al. (2008) A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proceedings of the National Academy of Sciences of the USA 105: 17861–17866.
    Nakagawa S, Inagaki F, Suzuki Y et al., Integrated Ocean Drilling Program Expedition 301 Scientists (2006) Microbial community in black rust exposed to hot ridge flank crustal fluids. Applied and Environmental Microbiology 72: 6789–6799.
    Newberry CJ, Webster G, Cragg BA et al. (2004) Diversity of prokaryotes and methanogenesis in deep subsurface sediments from the Nankai Trough, Ocean Drilling Program Leg 190. Environmental Microbiology 6: 274–287.
    Nunoura T, Soffientino B, Blazejak A et al. (2009) Subseafloor microbial communities associated with rapid turbidite deposition in the Gulf of Mexico continental slope (IODP Expedition 308). FEMS Microbiology Ecology 69: 410–424.
    Pan X, Urban AE, Palejev D et al. (2008) A procedure for highly specific, sensitive, and unbiased whole-genome amplification. Proceedings of the National Academy of Sciences of the USA 105: 15499–15504.
    Parkes RJ, Cragg BA and Wellsbury P (2000) Recent studies on bacterial populations and processes in subseafloor sediments: a review. Hydrogeology Journal 8: 11–28.
    Parkes RJ, Cragg BA, Bale SJ et al. (1994) Deep bacterial biosphere in Pacific Ocean sediments. Nature 371: 410–413.
    Parkes RJ, Webster G, Cragg BA et al. (2005) Deep sub-seafloor prokaryotes stimulated at interfaces over geological time. Nature 436: 390–394.
    Reed DW, Fujita Y, Delwiche ME et al. (2002) Microbial communities from methane hydrate-bearing deep marine sediments in a forearc basin. Applied and Environmental Microbiology 68: 3759–3770.
    Schippers A and Neretin LN (2006) Quantification of microbial communities in near-surface and deeply buried marine sediments on the Peru continental margin using real-time PCR. Environmental Microbiology 8: 1251–1260.
    Schippers A, Neretin LN, Kallmeyer J et al. (2005) Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433: 861–864.
    Smidt H and de Vos WM (2004) Anaerobic microbial dehalogenation. Annual Reviews of Microbiology 58: 105–108.
    Sørensen KB and Teske A (2006) Stratified communities of active Archaea in deep marine subsurface sediments. Applied and Environmental Microbiology 72: 4596–4603.
    Teske A and Sørensen KB (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME Journal 2: 3–18.
    Webster G, Blazejak A, Cragg BA et al. (2009) Subsurface microbiology and biogeochemistry of a deep, cold-water carbonate mound from the Porcupine Seabight (IODP Expedition 307). Environmental Microbiology 11: 239–257.
    Webster G, Parkes RJ, Cragg BA et al. (2006a) Prokaryotic community composition and biogeochemical processes in deep subseafloor sediments from the Peru margin. FEMS Microbiology Ecology 58: 65–85.
    Webster G, Parkes RJ, Fry JC and Weightman AJ (2004) Widespread occurrence of a novel division of bacteria identified by 16S rRNA gene sequences originally found in deep marine sediments. Applied and Environmental Microbiology 70: 5708–5713.
    Webster G, Watt LC, Rinna J et al. (2006b) A comparison of stable-isotope probing of DNA and phospholipid fatty acids to study prokaryotic functional diversity in sulfate-reducing marine sediment enrichment slurries. Environmental Microbiology 8: 1575–1589.
    Wellsbury P, Goodman K, Barth T et al. (1997) Deep marine biosphere fuelled by increasing organic matter availability during burial and heating. Nature 388: 573–576.
    Whitman WB, Coleman DC and Wiebe WJ (1998) Prokaryotes: the unseen majority. Proceedings of the National Academy of Sciences of the USA 95: 6578–6583.
    Woyke T, Xie G, Copeland A et al. (2009) Assembling the marine metagenome, one cell at a time. PLoS ONE 4: e5299.
 Further Reading
    D'Hondt S, Inagaki F, Ferdelman T et al. (2007) Exploring subseafloor life with the Integrated Ocean Drilling Program. Scientific Drilling 5: 26–37.
    DeLong EF (2004) Microbial life breathes deep. Science 306: 2198–2200.
    Edwards K, Bach W and McCollom TM (2005) Geomicrobiology in oceanography: microbe-mineral interactions at and below the seafloor. Trends in Microbiology 13: 449–456.
    Engelen B and Cypionka H (2009) The subsurface of tidal-flat sediments as a model for the deep biosphere. Ocean Dynamics 59: 385–391.
    Hoehler TM (2004) Biological energy requirements as quantitative boundary conditions for life in the subsurface. Geobiology 2: 205–215.
    book Hughes S and Lasken R (2005) Whole Genome Amplification. Oxfordshire, UK: Method Express, Scion Publishing Ltd.
    book Inagaki F and Nakagawa S (2008) "Spatial distribution of the subseafloor life: diversity and biogeography". In: Dilek Y, Furnes H and Muehlenbachs K (eds) Links between Geological Processes, Microbial Activities & Evolution of Life, pp. 135–158. Heidelberg, Germany: Springer Science+Business Media B.V.
    Jørgensen BB and D'Hondt S (2007) A starving majority deep beneath the seafloor. Science 314: 932–934.
    Teske AP (2006) Microbial communities of deep marine subsurface sediments: molecular and cultivation surveys. Geomicrobiology Journal 23: 357–368.
    Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nature Review of Microbiology 5: 316–323.

Related Sub-Topics:

Biomes and Ecosystems | Biogeochemical Cycles | Microbial Interactions and Communities
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Deep Subseafloor Microbial Communities
 
How to Cite close
Inagaki, Fumio(Feb 2010) Deep Subseafloor Microbial Communities. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021894]