The sub-seafloor biosphere is the largest prokaryotic habitat on Earth1 but also a habitat with the lowest metabolic rates2. Modelled activity rates are very low, indicating that most prokaryotes may be inactive or have extraordinarily slow metabolism2. Here we present results from two Pacific Ocean sites, margin and open ocean, both of which have deep, subsurface stimulation of prokaryotic processes associated with geochemical and/or sedimentary interfaces. At 90 m depth in the margin site, stimulation was such that prokaryote numbers were higher (about 13-fold) and activity rates higher than or similar to near-surface values. Analysis of high-molecular-mass DNA confirmed the presence of viable prokaryotes and showed changes in biodiversity with depth that were coupled to geochemistry, including a marked community change at the 90-m interface. At the open ocean site, increases in numbers of prokaryotes at depth were more restricted but also corresponded to increased activity; however, this time they were associated with repeating layers of diatom-rich sediments (about 9 Myr old). These results show that deep sedimentary prokaryotes can have high activity, have changing diversity associated with interfaces and are active over geological timescales.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: The unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998)
D'Hondt, S., Rutherford, S. & Spivack, A. J. Metabolic activity of subsurface life in deep-sea sediments. Science 295, 2067–2070 (2002)
Parkes, R. J. & Wellsbury, P. in Microbial Diversity and Bioprospecting (ed. Bull, A. T.) 120–129 (ASM Press, Washington DC, 2004)
Chapelle, F. H. & Lovley, D. R. Rates of microbial-metabolism in deep coastal-plain aquifers. Appl. Environ. Microbiol. 56, 1865–1874 (1990)
Lovley, D. R. & Chapelle, F. H. Deep subsurface microbial processes. Rev. Geophys. 33, 365–381 (1995)
Krumholz, L. R., Mckinley, J. P., Ulrich, G. A. & Suflita, J. M. Confined subsurface microbial communities in Cretaceous rock. Nature 386, 64–66 (1997)
McMahon, P. B., Chapelle, F. H., Falls, W. F. & Bradley, P. M. Role of microbial processes in linking sandstone diagenesis with organic rich clays. J. Sedim. Petrol. 62, 1–10 (1992)
Wellsbury, P. et al. Deep marine biosphere fuelled by increasing organic matter availability during burial and heating. Nature 388, 573–576 (1997)
Parkes, R. J., Cragg, B. A. & Wellsbury, P. Recent studies on bacterial populations and processes in subseafloor sediments: A review. Hydrogeol. J. 8, 11–28 (2000)
Teske, A., Wawer, C., Muyzer, G. & Ramsing, N. B. Distribution of sulfate-reducing bacteria in a stratified Fjord (Mariager Fjord, Denmark) as evaluated by most-probable-number counts and denaturing gradient gel electrophoresis of PCR-amplified ribosomal DNA fragments. Appl. Environ. Microbiol. 62, 1405–1415 (1996)
Coolen, M. J. L., Cypionka, H., Sass, A. M., Sass, H. & Overmann, J. Ongoing modification of Mediterranean Pleistocene sapropels mediated by prokaryotes. Science 296, 2407–2410 (2002)
Inagaki, F. et al. Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl. Environ. Microbiol. 69, 7224–7235 (2003)
D'Hondt, S. et al. Distributions of microbial activities in deep subseafloor sediments. Science 306, 2216–2221 (2004)
Whelan, J. K., Kanyo, Z., Tarafa, M. & McCaffrey, M. A. Organic matter in Peru Upwelling sediments—analysis by pyrolysis, pyrolysis-gas chromatography, and pyrolysis-gas chromatography mass spectrometry. Proc. ODP Sci. Results 112, 573–587 (1990)
Mitterer, R. M. et al. Co-generation of hydrogen sulfide and methane in marine carbonate sediments. Geophys. Res. Lett. 28, 3931–3934 (2001)
Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626 (2000)
Iversen, N. & Jorgensen, B. B. Anaerobic methane oxidation rates at the sulfate-methane transition in marine sediments from Kattegat and Skagerrak (Denmark). Limnol. Oceanogr. 30, 944–955 (1985)
Wellsbury, P., Goodman, K., Cragg, B. A. & Parkes, R. J. The geomicrobiology of deep marine sediments from Blake Ridge containing methane hydrate (Sites 994, 995 and 997). Proc. ODP Sci. Results 164, 379–391 (2000)
Wellsbury, P., Herbert, R. A. & Parkes, R. J. Incorporation of [methyl-3H]thymidine by obligate and facultative anaerobic bacteria when grown under defined culture conditions. FEMS Microbiol. Ecol. 12, 87–95 (1993)
Webster, G., Newberry, C. J., Fry, J. C. & Weightman, A. J. Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J. Microbiol. Methods 55, 155–164 (2003)
Newberry, C. J. et al. Diversity of prokaryotes and methanogenesis in deep subsurface sediments from the Nankai Trough, Ocean Drilling Program Leg 190. Environ. Microbiol. 6, 274–287 (2004)
Webster, G., Parkes, R. J., Fry, J. C. & Weightman, A. J. Widespread occurrence of a novel division of bacteria identified by 16S rRNA gene sequences originally found in deep marine sediments. Appl. Environ. Microbiol. 70, 5708–5713 (2004)
Schippers, A. et al. Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433, 861–864 (2005)
Ibarki, M. Eocene through Pleistocene planktonic Foraminifers off Peru, Leg 112—Biostratigraphy and Paleoceanography. Proc. ODP Sci Results 112, 239–262 (1990)
Parkes, R. J., Cragg, B. A., Fry, J. C., Herbert, R. A. & Wimpenny, J. W. T. Bacterial biomass and activity in deep sediment layers from the Peru Margin. Phil. Trans. R. Soc. Lond. A 331, 139–153 (1990)
Marchesi, J. R., Weightman, A. J., Cragg, B. A., Parkes, R. J. & Fry, J. C. Methanogen and bacterial diversity and distribution in deep gas hydrate sediments from the Cascadia Margin as revealed by 16S rRNA molecular analysis. FEMS Microbiol. Ecol. 34, 221–228 (2001)
Kemp, P. F. & Aller, J. Y. Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol. Ecol. 47, 161–177 (2004)
Leloup, J., Quillet, L., Oger, C., Boust, D. & Petit, F. Molecular quantification of sulfate-reducing microorganisms (carrying dsrAB genes) by competitive PCR in estuarine sediments. FEMS Microbiol. Ecol. 47, 207–214 (2004)
Shipboard Scientific Party, Controls on microbial communities in deeply buried sediments, eastern Equatorial Pacific and Peru Margin sites 1225–1231, 27 January – 29 March 2002. Proc. ODP Init. Rep. 201, 1–81 (2003)
Kallmeyer, J., Ferdelman, T. G., Weber, A., Fossing, H. & Jørgensen, B. B. A cold chromium distillation procedure for radiolabeled sulfide applied to sulfate reduction measurements. Limnol. Oceanogr. Methods 2, 171–180 (2004)
We thank members of the Leg 201 cruise for assistance in obtaining and processing samples, and T. Daniell for assistance with DNA sequencing. This research used samples and data provided by the ODP. The ODP is sponsored by the US National Science Foundation (NSF) and participating countries under the management of Joint Oceanographic Institutions (JOI), Inc. We thank the European Union and the Natural Environment Research Council (Marine and Freshwater Microbial Biodiversity Programme) for supporting this research financially.
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
About this article
Cite this article
Parkes, R., Webster, G., Cragg, B. et al. Deep sub-seafloor prokaryotes stimulated at interfaces over geological time. Nature 436, 390–394 (2005) doi:10.1038/nature03796
Nature Reviews Microbiology (2019)
Seawater recirculation through subducting sediments sustains a deeply buried population of sulfate-reducing bacteria
Journal of Oceanology and Limnology (2019)
Marine Geology (2019)
Lateral variations and vertical structure of the microbial methane cycle in the sediment of Lake Onego (Russia)
Inland Waters (2019)