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Prokaryotes: The unseen majority
Open accessAbstract
The number of prokaryotes and the total amount of their cellular carbon on earth are estimated to be 4–6 × 10 30 cells and 350–550 Pg of C (1 Pg = 10 15 g), respectively. Thus, the total amount of prokaryotic carbon is 60–100% of the estimated total carbon in plants, and inclusion of prokaryotic carbon in global models will almost double estimates of the amount of carbon stored in living organisms. In addition, the earth’s prokaryotes contain 85–130 Pg of N and 9–14 Pg of P, or about 10-fold more of these nutrients than do plants, and represent the largest pool of these nutrients in living organisms. Most of the earth’s prokaryotes occur in the open ocean, in soil, and in oceanic and terrestrial subsurfaces, where the numbers of cells are 1.2 × 10 29 , 2.6 × 10 29 , 3.5 × 10 30 , and 0.25–2.5 × 10 30 , respectively. The numbers of heterotrophic prokaryotes in the upper 200 m of the open ocean, the ocean below 200 m, and soil are consistent with average turnover times of 6–25 days, 0.8 yr, and 2.5 yr, respectively. Although subject to a great deal of uncertainty, the estimate for the average turnover time of prokaryotes in the subsurface is on the order of 1–2 × 10 3 yr. The cellular production rate for all prokaryotes on earth is estimated at 1.7 × 10 30 cells/yr and is highest in the open ocean. The large population size and rapid growth of prokaryotes provides an enormous capacity for genetic diversity.
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“However, the majority of astrobiological research is focused on the possible existence and detection of microbial life, which is the simplest, most robust, and most abundant form of life on our own planet (Whitman et al., 1998) and therefore is considered to be the most likely form of life to exist on other planets and moons.”
From The Astrobiology Primer v2.0 (2016) · cites this paper as Whitman et al., 1998
In the citing paper
“Given that there are estimated to be greater than 1030 prokaryotes on earth (Whitman et al., 1998), the vast majority of which are yet unstudied, there are likely to be more PFAS‐metabolizing bacteria uncovered.”
From Nothing lasts forever: understanding microbial biodegradation of polyfluorinated compounds and perfluorinated alkyl substances (2022) · cites this paper as Whitman et al., 1998
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BackgroundNostrand, J. D. V., Wu, W., Wu, L., et al. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.01986.x · Cited by 111
“However, one of the major challenges in examining microbial communities is that only an estimated 1% of all microbes are cultivated (Whitman et al., 1998).”
BackgroundSangal, V., Goodfellow, M., Jones, A. L., Schwalbe, E. C., Blom, J., Hoskisson, P. A., & Sutcliffe, I. C. (2016) · Scientific Reports · doi:10.1038/srep38392 · Cited by 111
Restoration of dysbiotic human gut microbiome for homeostasis
Dixit, K. K., Chaudhari, D. S., Dhotre, D. P., Shouche, Y. S., & Saroj, S. D. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119622 · Cited by 116
Molecular approaches: advantages and artifacts in assessing bacterial diversity
Pontes, D. S., Lima-Bittencourt, C. I., Chartone‐Souza, E., & Nascimento, A. M. A. (2007) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-007-0219-3 · Cited by 111
“Currently, it is estimated that there are about 4–6 £ 10(30) diVerent prokaryotic cells, exceeding, by various orders of magnitude, all plant and animal diversity [124].”
BackgroundIdentifying microorganisms responsible for ecologically significant biogeochemical processes
Madsen, E. L. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1151 · Cited by 111
“Microorganisms are the primary agents of geochemical change, and the global biomass of prokaryotes is approximately equal to that of all other (eukaryotic) life form”
BackgroundGeomicrobiology of deep, low organic carbon sediments in the Woodlark Basin, Pacific Ocean
Wellsbury, P., Mather, I. D., & Parkes, R. J. (2002) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2002.tb00995.x · Cited by 114
“Deep marine sediments have been estimated to contain a bacterial biomass equivalent to V10% of living carbon in the surface biosphere [1] and possibly much more [2,3].”
Dale, A. W., Regnier, P. A. G., & Cappellen, P. V. (2006) · American Journal of Science · doi:10.2475/ajs.306.4.246 · Cited by 111
Factors Affecting the Performance of Single-Chamber Soil Microbial Fuel Cells for Power Generation
Deng, H., Yi-Cheng, W. U., Zhang, F., HUANG, Z.-C., Zheng, C. H. E. N., Xu, H., & Zhao, F. (2014) · Pedosphere · doi:10.1016/s1002-0160(14)60019-9 · Cited by 112
“Soil generally has a bacterial population of approximately 109 cells g−1 (Whitman et al., 1998) and organic matter content of within 100 mg g−1 (Bot and Benites, 2005), in spite of the variation between different soil types, e.g., in organic soil, the abundance of bacteria and organic matter can be…”
BackgroundMicroorganisms persist at record depths in the subseafloor of the Canterbury Basin
Ciobanu, M., Burgaud, G., Dufresne, A., Breuker, A., Rédou, V., Maamar, S. B., Gaboyer, F., Vandenabeele‐Trambouze, O., Lipp, J. S., Schippers, A., et al. (2014) · The ISME Journal · doi:10.1038/ismej.2013.250 · Cited by 110
“Considering these levels of contamination, mean cell counts of 5 10(5) cellsml in surface waters in the ocean (Whitman et al., 1998) and average densities of 1.”
BackgroundInfluentialGat, D., Tsesarsky, M., Shamir, D., & Ronen, Z. (2014) · Biogeosciences · doi:10.5194/bg-11-2561-2014 · Cited by 114
“Prokaryotes comprise the major part of the biomass in all major soil types, with an estimated average of 2.2·108 cells per cm3 of soil in the top 10 m (Whitman et al., 1998).”
BackgroundInfluentialEvidence of biological activity in Hawaiian subsurface basalts
Fisk, M. R., Storrie‐Lombardi, M. C., Douglas, S., Popa, R., McDonald, G. D., & Meo-Savoie, C. A. D. (2003) · Geochemistry Geophysics Geosystems · doi:10.1029/2002gc000387 · Cited by 110
“[2] Microorganisms in subsurface environments may comprise a significant fraction of the Earth’s biomass with estimates varying from 5% to 50% [Parkes et al., 1994; Gold, 1992; Whitman et al., 1998].”
Miteva, V. I., Teacher, C. E., Sowers, T., & Brenchley, J. E. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01835.x · Cited by 110
“The aerial dispersal of dust across the globe is estimated to be 2.2 ¥ 109 tons per year (Goudie and Middleton, 2001) with 1 g of soil containing approximately 1 ¥ 109 cells (Whitman et al., 1998).”
BackgroundInfluentialCultivating the uncultivated: a community genomics perspective
Tyson, G. W., & Banfield, J. F. (2005) · Trends in Microbiology · doi:10.1016/j.tim.2005.07.003 · Cited by 111
In situ monitoring of antibiotic susceptibility of bacterial biofilms in a microfluidic device
Kim, K. P., Kim, Y., Choi, C., et al. (2010) · Lab on a Chip · doi:10.1039/c0lc00154f · Cited by 110
Zhang, X., Tang, G.-L., Xu, X., Nong, X., & Qi, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109118 · Cited by 109
“[2] reported that deep-sea-derived microbial communities, mainly composed of bacteria and archaea, accounted for a total cellular carbon content of approximately 3610(17) g.”
BackgroundFOCUS: an alignment-free model to identify organisms in metagenomes using non-negative least squares
Silva, G. G. Z., Cuevas, D., Dutilh, B. E., & Edwards, R. A. (2014) · PeerJ · doi:10.7717/peerj.425 · Cited by 106
Buried Alive: Microbes from Ancient Halite
Jaakkola, S., Ravantti, J., Oksanen, H. M., & Bamford, D. H. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2015.12.002 · Cited by 109
A multidimensional perspective on microbial interactions
Pacheco, A. R., & Segrè, D. (2019) · FEMS Microbiology Letters · doi:10.1093/femsle/fnz125 · Cited by 108
Cell/Bacteria‐Based Bioactive Materials for Cancer Immune Modulation and Precision Therapy
Pan, H., Zheng, M., Ma, A.-Q., Liu, L., & Cai, L. (2021) · Advanced Materials · doi:10.1002/adma.202100241 · Cited by 109
Real-time analysis of gut flora in Entamoeba histolytica infected patients of Northern India
Verma, A. K., Verma, R. P., Ahuja, V., & Paul, J. (2012) · BMC Microbiology · doi:10.1186/1471-2180-12-183 · Cited by 105
“The vast majority reside in our colon where densities approach 10(11) - 10(12) cells/ml, the highest density recorded for any microbial habitat [3].”
BackgroundKatz, B. G., Griffin, D. W., & Davis, J. H. (2009) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2009.01.022 · Cited by 114
“…a barrier to the subsurface environment is the 10 million to 1 billion bacterial cells composed of approximately 10 thousand bacterial types found in the average gram of soil located in the top few centimeters of most surface environments (Whitman et al., 1998, Torsvik et al., 2002).”
BackgroundThe Role of Microbiota on the Gut Immunology
Min, Y. W., & Rhee, P. (2015) · Clinical Therapeutics · doi:10.1016/j.clinthera.2015.03.009 · Cited by 124
“] 2015 10(11) to 10(12) cells/mL.(1,2) The gut microbiota plays an important role in health and disease in humans.”
BackgroundNatural attenuation: What does the subsurface have in store?
Röling, W. F. M., & van Verseveld, H. W. (2002) · Biodegradation · doi:10.1023/a:1016310519957 · Cited by 109
“01 h−1 (Whitman et al. 1998), the amount of rRNA is merely indicative of presence, but not activity.”
BackgroundInfluentialAdvancements toward a systems level understanding of the human oral microbiome
McLean, J. S. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00098 · Cited by 108
Niches of the pre‐photosynthetic biosphere and geologic preservation of Earth's earliest ecology
SLEEP, N. H., & BIRD, D. K. (2007) · Geobiology · doi:10.1111/j.1472-4669.2007.00105.x · Cited by 117
“Evidence for an extensive subsurface biosphere within modern (Gold, 1992; Pedersen, 1993; Fyfe, 1996; Whitman et al ., 1998; Krumholz, 2000; Takai et al ., 2004b) and early (Canfield, 2006; Ueno et al ., 2006) Earth suggests that the upper crust, to depths exceeding several kilometers or more, is a…”
BackgroundRomick‐Rosendale, L. E., Goodpaster, A. M., Hanwright, P. J., Patel, N. B., Wheeler, E. T., Chona, D. L., & Kennedy, M. A. (2009) · Magnetic Resonance in Chemistry · doi:10.1002/mrc.2511 · Cited by 107
Garel, M., Bonin, P., Martini, S., Guasco, S., Roumagnac, M., Bhairy, N., Armougom, F., & Tamburini, C. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00453 · Cited by 108
“Despite the deep sea, being the largest ecosystem of the ocean (mean depth of about 3,500m, i.e., 35 MPa), with the greatest reservoir of microbes (Whitman et al., 1998), it still hasn’t been sampled or studied adequately under in situ conditions.”
BackgroundCommunity-level respiration of prokaryotic microbes may rise with global warming
Smith, T., Thomas, T. J. H., García‐Carreras, B., Sal, S., Yvon‐Durocher, G., Bell, T., & Pawar, S. S. (2019) · Nature Communications · doi:10.1038/s41467-019-13109-1 · Cited by 106
Aerobic microbial life persists in oxic marine sediment as old as 101.5 million years
Morono, Y., Ito, M., Hoshino, T., Terada, T., Hori, T., Ikehara, M., D'Hondt, S. L., & Inagaki, F. (2020) · Nature Communications · doi:10.1038/s41467-020-17330-1 · Cited by 107
Seager, S., Petkowski, J. J., Gao, P., Bains, W., Bryan, N. C., Ranjan, S., & Greaves, J. (2020) · Astrobiology · doi:10.1089/ast.2020.2244 · Cited by 108
“For the context, Earth is estimated to have more than 10 30 free-living single-celled microbes (Whitman et al. , 1998; Bar-On et al. , 2018), with a rough estimate of 10 24 total cells in Earth’s aerial biosphere (Bryan et al. , 2019).”
Waldron, P. J., Petsch, S. T., Martini, A. M., & Nüsslein, K. R. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01459-07 · Cited by 108
“Subsurface sedimentary environments contain an estimated 1/10 to 1/3 of all living biomass on Earth, and the activity of subsurface microorganisms plays an important role in biogeochemical cycling of elements and the global carbon cycle (38, 51, 57).”
More, smaller bacteria in response to ocean's warming?
Morán, X. A. G., Alonso‐Sáez, L., Nogueira, E., Ducklow, H. W., González, N., López‐Urrutia, Á., Díaz‐Pérez, L., Calvo‐Díaz, A., Arandia‐Gorostidi, N., & Huete‐Stauffer, T. M. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.0371 · Cited by 110
Shi, Z. J., Yin, H., Nostrand, J. D. V., Voordeckers, J. W., Tu, Q., Deng, Y., Yuan, M., Zhou, A., Zhang, P., Xiao, N., et al. (2019) · mSystems · doi:10.1128/msystems.00296-19 · Cited by 107
Wright, G. D. (2010) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2010.497535 · Cited by 117
“There are an estimated 5 10(30) prokaryotes across the globe [25] and only a very small fraction is associated with human disease.”
BackgroundKing, G. M. (2010) · Trends in Microbiology · doi:10.1016/j.tim.2010.11.006 · Cited by 109
Parkes, R. J., Sellek, G. A., Webster, G., Martin, D., Anders, E., Weightman, A. J., & Sass, H. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02018.x · Cited by 107
“90% (Whitman et al., 1998), with the dominant habitat being marine sediments (Parkes et al.”
BackgroundResultInfluentialMeynet, P., Hale, S. E., Davenport, R. J., et al. (2012) · Environmental Science & Technology · doi:10.1021/es2043905 · Cited by 107
Klaassens, E. S., Boesten, R. J., Haarman, M., Knol, J., Schuren, F. H. J., Vaughan, E. E., & de Vos, W. M. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02492-08 · Cited by 107
“The vast majority reside in the colon, where densities approach 10(11) to 10(12) cells per gram, the highest recorded for any microbial habitat (66).”
Background
Metadata
- Authors
- Whitman, W. B., Coleman, D. C., & Wiebe, W. J.
- Affiliations
- University of Georgia (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1998-06-09
- Volume
- 95
- Issue
- 12
- Pages
- 6578-6583
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC33863
- OpenAlex
- W2118001436
- Semantic Scholar
- 321e4c5e6031364c39db3cfdb151dcc2deaac1ba
- Cited by
- 4,871
- References
- 92
- Citations by year
- 2026: 86 · 2025: 134 · 2024: 159 · 2023: 220 · 2022: 190 · 2021: 252 · 2020: 223 · 2019: 238 · 2018: 273 · 2017: 251 · 2016: 281 · 2015: 282 · 2014: 311 · 2013: 252 · 2012: 238
- FWCI
- 6.26
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Plankton and Biogeochemistry
- Keywords
- prokaryotes, nitrogen, phosphorus, open ocean, soil, subsurface environments, genetic diversity
- MeSH terms
- Prokaryotic Cells
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