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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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Zhao, S., Zettler, E., Amaral‐Zettler, L., & Mincer, T. J. (2020) · The ISME Journal · doi:10.1038/s41396-020-00756-2 · Cited by 97
Microbial oceanography in a sea of opportunity
Bowler, C., Karl, D. M., & Colwell, R. R. (2009) · Nature · doi:10.1038/nature08056 · Cited by 103
Morozova, D., Wandrey, M., Alawi, M., Zimmer, M., Vieth, A., Zettlitzer, M., & Würdemann, H. (2010) · International journal of greenhouse gas control · doi:10.1016/j.ijggc.2009.11.014 · Cited by 103
“Thorough studies of samples from deep boreholes, using a variety of molecular techniques, have shown an active biosphere composed of diverse groups of microorganisms (Parkes at al., 1994; Sahl et al., 2008; Whitman et al., 1998).”
BackgroundResponses of soil microbial community to different concentration of fomesafen
Wu, X., Xu, J., Dong, F., et al. (2014) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2014.03.041 · Cited by 99
Where microorganisms meet rocks in the Earth's Critical Zone
Akob, D. M., & Küsel, K. (2011) · Biogeosciences · doi:10.5194/bg-8-3531-2011 · Cited by 100
“CZ habitats are estimated to harbor an unseen majority of Earth’s biomass with the total carbon in subsurface organisms likely equal to that in all terrestrial and marine plants (Whitman et al., 1998).”
BackgroundThermal force approach to molecular evolution
Braun, D., & Libchaber, A. J. (2004) · Physical Biology · doi:10.1088/1478-3967/1/1/p01 · Cited by 99
A Viable Microbial Community in a Subglacial Volcanic Crater Lake, Iceland
Gaidos, E. J., Lanoil, B., Thorsteinsson, Þ., et al. (2004) · Astrobiology · doi:10.1089/1531107041939529 · Cited by 98
Archaeal transformation of metals in the environment
Bini, E. (2010) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2010.00876.x · Cited by 100
“Marine subsurface sediments are estimated to host 60–90% of the Earth’s prokaryotes (Whitman et al., 1998).”
BackgroundBrigulla, M., & Wackernagel, W. (2010) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-2489-3 · Cited by 104
A model for low‐temperature biogeochemistry of sulfur, carbon, and iron on Europa
Zolotov, M. Y., & Shock, E. L. (2004) · Journal of Geophysical Research Atmospheres · doi:10.1029/2003je002194 · Cited by 100
“The subsurface biosphere has been estimated to contain a significant part (up to 50% [ Whitman et al., 1998 ]) of Earth’s biomass.”
BackgroundGupta, R. S. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuw011 · Cited by 102
Zhang, X., Zhao, S., Song, X., Jia, J., Zhang, Z., Zhou, H., Fu, H., Cui, H., Hu, S., Fang, M., et al. (2018) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2018.03.006 · Cited by 97
Astudillo‐García, C., Hermans, S. M., Stevenson, B., Buckley, H. L., & Lear, G. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-09963-0 · Cited by 101
Translating New Synthetic Biology Advances for Biosensing Into the Earth and Environmental Sciences
Valle, I. D., Fulk, E. M., Kalvapalle, P. B., Silberg, J. J., Masiello, C. A., & Stadler, L. B. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.618373 · Cited by 102
“Biosensors Can Study Spatial Heterogeneity in situ Most microbes on Earth evolved to live in environments with high spatial heterogeneity (Whitman et al., 1998; Kallmeyer et al., 2012).”
BackgroundActivation of cryptic aminoglycoside resistance in Salmonella enterica
Koskiniemi, S., Pränting, M., Gullberg, E., Näsvall, J., & Andersson, D. I. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07657.x · Cited by 96
“These findings also have broader implications with regard to the intrinsic resistome, i.e. the total reservoir of resistance genes present in eubacteria across the globe (Whitman et al., 1998; D’Costa et al., 2006).”
BackgroundCavicchioli, R., Ostrowski, M., Fegatella, F., Goodchild, A., & Guixa-Boixereu, N. (2003) · Microbial Ecology · doi:10.1007/s00248-002-3008-6 · Cited by 99
“more, of the three largest microbial habitats (seawater, soil, and sediment/soil subsurface), the rates of cellular activity and turnover are highest in the open ocean [94].”
BackgroundNew perspectives in benthic deep-sea microbial ecology
Corinaldesi, C. (2015) · Frontiers in Marine Science · doi:10.3389/fmars.2015.00017 · Cited by 106
“…in the oceans, from the surface to subsurface sediments, revealed that deep-sea microbes represent the " hidden majority " of all life forms, comprising between 50 and >80% of the Earth's total microbial biomass and between 10 and 30% of the Earth's total living biomass (Whitman et al., 1998).”
BackgroundCommunity history affects the predictability of microbial ecosystem development
Pagaling, E., Strathdee, F., Spears, B. M., Cates, M. E., Allen, R. J., & Free, A. (2013) · The ISME Journal · doi:10.1038/ismej.2013.150 · Cited by 96
“This need is especially acute for microbial communities, which are key drivers of the Earth’s biogeochemical cycles (Whitman et al., 1998), industrial processes including wastewater treatment, and human gut health (Palmer et al., 2007) and are the subject of ever increasing data sets generated by…”
BackgroundDurbin, A. M., & Teske, A. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00168 · Cited by 94
“The Domain Archaea accounts for a large portion, perhaps the majority, of deep-subsurface prokaryotic cells and biomass (Biddle et al., 2006; Lipp et al., 2008), and by implication, global biomass (Parkes et al., 1994; Whitman et al., 1998).”
BackgroundKobayashi, T., Koide, O., Mori, K., et al. (2008) · Extremophiles · doi:10.1007/s00792-008-0157-7 · Cited by 96
Kennedy, P. G., Hortal, S., Bergemann, S. E., & Bruns, T. D. (2007) · Journal of Ecology · doi:10.1111/j.1365-2745.2007.01306.x · Cited by 96
“topic have focused on plant and animal assemblages, but the high richness of microbial organisms in numerous habitats is being increasingly recognized (Whitham et al. 1998; Hawksworth 2001).”
BackgroundSexual dimorphism of cardiometabolic dysfunction: Gut microbiome in the play?
Cross, T.-W. L., Kasahara, K., & Rey, F. E. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.05.016 · Cited by 87
“Humans harbor over 100 trillion microbes, with the gastrointestinal tract being the most densely populated body habitat [1,2].”
BackgroundNeon identifies two billion year old fluid component in Kaapvaal Craton
Lippmann‐Pipke, J., Lollar, B. S., Niedermann, S., Stroncik, N. A., Naumann, R., van Heerden, E., & Onstott, T. C. (2011) · Chemical Geology · doi:10.1016/j.chemgeo.2011.01.028 · Cited by 96
“…of such occurrences will be significant both in terms of defining the limits of life in the earth's deep crust and for evaluating the proportion of the earth's biomass attributable to the deep biosphere — estimated by some to equal that of the planet's total surface biomass (Whitman et al., 1998).”
BackgroundThen and now: a systematic review of the systematics of prokaryotes in the last 80 years
Oren, A., & Garrity, G. M. (2013) · Antonie van Leeuwenhoek · doi:10.1007/s10482-013-0084-1 · Cited by 95
“terrestrial subsurface (Whitman et al. 1998).”
BackgroundKirpich, I., Petrosino, J. F., Ajami, N. J., Feng, W., Wang, Y., Liu, Y., Beier, J. I., Barve, S. S., Yin, X., Wei, X., et al. (2016) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.11.017 · Cited by 96
Arndt, S., Brumsack, H., & Wirtz, K. (2005) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2005.09.010 · Cited by 95
Süß, J., Engelen, B., Cypionka, H., & Sass, H. (2004) · FEMS Microbiology Ecology · doi:10.1016/j.femsec.2004.07.010 · Cited by 96
Inagaki, F., Sakihama, Y., Inoue, A., Kato, C., & Horikoshi, K. (2002) · Environmental Microbiology · doi:10.1046/j.1462-2920.2002.00294.x · Cited by 95
Aging and the mucosal immune system in the intestine
Mabbott, N. A., Kobayashi, A., Sehgal, A., Bradford, B. M., Pattison, M., & Donaldson, D. S. (2015) · Biogerontology · doi:10.1007/s10522-014-9498-z · Cited by 95
“The lumen of the mammalian lower intestine contains an enormous burden of commensal microorganisms which is estimated to comprise ~10 12 bacteria/g of contents (Whitman et al. 1998).”
BackgroundAn Estimate of the Total DNA in the Biosphere
Landenmark, H., Forgan, D. H., & Cockell, C. S. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002168 · Cited by 98
“8 Gt of carbon [5], 520 Gt of carbon [7], 1,841 Gt biomass [8], and 890 Gt biomass [9], was converted to the number of cells, assuming carbon content is 50% of dry weight and using a plant cell mass of 2 × 10 g [10] and, lastly, converted to a total amount of DNA of 3.”
BackgroundMethodInfluentialMetaproteomic data analysis at a glance: advances in computational microbial community proteomics
Muth, T., Renard, B. Y., & Martens, L. (2016) · Expert Review of Proteomics · doi:10.1080/14789450.2016.1209418 · Cited by 92
“In this context, the enormous size of prokaryotic populations [3], the limited culturability for the majority of single bacterial strains [4], and the growing comprehension of entire multi-species assemblages [5] required the development of holistic analysis approaches for microbial community…”
BackgroundThe valuation of ecosystem services
Barbier, E. B., Baumgärtner, S., Chopra, K., Costello, C., Duraiappah, A. K., Hassan, R., Kinzig, A. P., Lehman, M., Pascual, U., Polasky, S., et al. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199547951.003.0018 · Cited by 98
Blazejak, A., & Schippers, A. (2010) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2010.00838.x · Cited by 96
“Previous studies have shown that microbial life in this environment is widespread and represents one-tenth to one-third of all prokaryotic biomass on Earth (Whitman et al., 1998; Jørgensen & Boetius, 2007; Fry et al., 2008).”
BackgroundSmith, M. C. M., Burns, R. N., Wilson, S. E., et al. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.10.2145 · Cited by 94
Xavier, J. C., Patil, K. R., & Rocha, I. (2016) · Metabolic Engineering · doi:10.1016/j.ymben.2016.12.002 · Cited by 94
“…lack of standardized protocols (both experimental and computational) and multi-species comparative assays in determining (quantitative and qualitatively) which components make up the cell's biomass, in contrast with the advanced picture in terms of the elemental composition (Whitman et al., 1998).”
BackgroundFrost, F., Weiß, F. U., Sendler, M., Kacprowski, T., Rühlemann, M. C., Bang, C., Franke, A., Völker, U., Völzke, H., Lamprecht, G., et al. (2020) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000232 · Cited by 98
Psychrotrophic Strain of Janthinobacterium lividum from a Cold Alaskan Soil Produces Prodigiosin
Schloss, P. D., Allen, H. K., Klimowicz, A. K., et al. (2010) · DNA and Cell Biology · doi:10.1089/dna.2010.1020 · Cited by 93
“A single gram of soil may contain 10 9 to 10 11 bacteria distributed among thousands of species, which play a significant role in biogeochemical cycling, bioremediation, and the production of antimicrobials and industrially useful small molecules and enzymes (Whitman et al. , 1998; Janssen, 2006).”
Basso, O., Lascourrèges, J., Borgne, F. L., et al. (2008) · Research in Microbiology · doi:10.1016/j.resmic.2008.10.010 · Cited by 93
Bacterial, archaeal, and eukaryal diversity in the intestines of Korean people
Nam, Y., Chang, H.-W., Kim, K., Roh, S. W., Kim, M., Jung, M., Lee, S., Kim, J.-Y., Yoon, J., & Bae, J. (2008) · The Journal of Microbiology · doi:10.1007/s12275-008-0199-7 · Cited by 93
Individual-based Modelling: An Essential Tool for Microbiology
Ferrer, J., Prats, C., & López, D. (2008) · Journal of Biological Physics · doi:10.1007/s10867-008-9082-3 · Cited by 93
“Bacteria alone are estimated to contain up to 60–100% of the carbon found in plants, accounting for 50% of the total biomass of carbon, and they are, by far, the largest pool of organic bound nitrogen and phosphorus [1].”
BackgroundLin, B., Hyacinthe, C., Bonneville, S., Braster, M., Cappellen, P. V., & Röling, W. F. M. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01312.x · Cited by 94
“Microorganisms generally grow with doubling times ranging from days to months under limiting substrate concentrations in the marine environment (Whitman et al., 1998).”
BackgroundBatzke, A., Engelen, B., Sass, H., & Cypionka, H. (2007) · Geomicrobiology Journal · doi:10.1080/01490450701456453 · Cited by 95
“Although the prokaryotes in the deep marine biosphere play a dominant role in global biogeochemical processes and have been estimated to comprise one-tenth to one-third of the world’s living biomass (Whitman et al. 1998; Parkes et al. 2000), little is known about them.”
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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