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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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Cultivation of unculturable soil bacteria
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Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory
Williamson, K. E., Fuhrmann, J. J., Wommack, K. E., & Radosevich, M. A. (2017) · Annual Review of Virology · doi:10.1146/annurev-virology-101416-041639 · Cited by 442
Vezzulli, L., Grande, C., Reid, P. C., Hélaouët, P., Edwards, M., Höfle, M. G., Brettar, I., Colwell, R. R., & Pruzzo, C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1609157113 · Cited by 457
“Prokaryotes comprise the largest living biomass within the ocean and have a significant impact on the life of the planet, by contributing not only to nutrient element cycling but also to the incidence of human and animal diseases (5).”
BackgroundProkaryotic cells of the deep sub-seafloor biosphere identified as living bacteria
Schippers, A., Neretin, L. N., Kallmeyer, J., Ferdelman, T. G., Cragg, B. A., Parkes, R. J., & Jørgensen, B. B. (2005) · Nature · doi:10.1038/nature03302 · Cited by 436
“Despite the fact that only about 1% of the total marine primary production of organic carbon is available for deep-sea microorganism”
BackgroundThe Macaque Gut Microbiome in Health, Lentiviral Infection, and Chronic Enterocolitis
McKenna, P. M., Hoffmann, C., Minkah, N. K., Aye, P. P., Lackner, A. A., Liu, Z. Z., Lozupone, C., Hamady, M., Knight, R. D., & Bushman, F. D. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.0040020 · Cited by 445
“human nuclear genome by two orders of magnitude [1,2], and these genes contribute many essential metabolic functions to the host.”
BackgroundMapping the niche space of soil microorganisms using taxonomy and traits
Lennon, J. T., Aanderud, Z. T., Lehmkuhl, B. K., & Schoolmaster, D. R. (2012) · Ecology · doi:10.1890/11-1745.1 · Cited by 435
“Although microorganisms are the most abundant and diverse taxa on Earth (cf. Whitman et al. 1998, Curtis et al. 2002) and play an important role in the stability and functioning of managed and natural ecosystems (Hashsham et al. 2000, Bell et al. 2005), ecologists are only beginning to understand…”
BackgroundAn ecological perspective on bacterial biodiversity
Horner‐Devine, M. C., Carney, K. M., & Bohannan, B. J. M. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2549 · Cited by 449
“Perhaps most notably, bacterial cells are estimated to contain, in total, 350–550 Pg of carbon, up to 60–100% of the total carbon found in plants, as well as large amounts of nitrogen and phosphorous (Whitman et al. 1998).”
BackgroundInfluentialMajor viral impact on the functioning of benthic deep-sea ecosystems
Danovaro, R., Dell’Anno, A., Corinaldesi, C., Magagnini, M., Noble, R. T., Tamburini, C., & Weinbauer, M. G. (2008) · Nature · doi:10.1038/nature07268 · Cited by 444
Hill, D. A., Hoffmann, C., Abt, M. C., Du, Y., Kobuley, D. E., Kirn, T. J., Bushman, F. D., & Artis, D. (2009) · Mucosal Immunology · doi:10.1038/mi.2009.132 · Cited by 439
Role of the Gut Microbiome in the Pathogenesis of Obesity and Obesity-Related Metabolic Dysfunction
Bouter, K. E. C., van Raalte, D. H., Groen, A. K., & Nieuwdorp, M. (2017) · Gastroenterology · doi:10.1053/j.gastro.2016.12.048 · Cited by 443
“The gut microbiota, referring to bacteria as well as viruses, fungi, archaea, phages and protozoa residing in the human intestine, [1] equal the amount of all human cells [2] and they have the capability to interact with the host in several ways.”
BackgroundRobust estimation of microbial diversity in theory and in practice
Haegeman, B., Hamelin, J., Moriarty, J., Neal, P. J., Dushoff, J. G., & Weitz, J. S. (2013) · The ISME Journal · doi:10.1038/ismej.2013.10 · Cited by 446
“Moreover, the number of organisms in microbial communities is typically many orders of magnitude larger than the number of organisms in plant or animal communities (Whitman et al., 1998).”
Deep sub-seafloor prokaryotes stimulated at interfaces over geological time
Parkes, R. J., Webster, G., Cragg, B. A., Weightman, A. J., Newberry, C. J., Ferdelman, T. G., Kallmeyer, J., Jørgensen, B. B., Aiello, I. W., & Fry, J. C. (2005) · Nature · doi:10.1038/nature03796 · Cited by 438
Viral and microbial community dynamics in four aquatic environments
Rodriguez-Brito, B., Li, L., Wegley, L., Furlan, M., Angly, F. E., Breitbart, M., Buchanan, J. T., Desnues, C., Dinsdale, E. A., Edwards, R. A., et al. (2010) · The ISME Journal · doi:10.1038/ismej.2010.1 · Cited by 425
Uncultured archaea in deep marine subsurface sediments: have we caught them all?
Teske, A., & Sørensen, K. B. (2007) · The ISME Journal · doi:10.1038/ismej.2007.90 · Cited by 446
“The microbial cells of subseafloor sediments have been estimated to constitute 1/2–5/6 of Earth’s microbial biomass (Whitman et al., 1998) and 1/10–1/3 of Earth’s total living biomass (Whitman et al.”
BackgroundImportant Metabolic Pathways and Biological Processes Expressed by Chicken Cecal Microbiota
Polanský, O., Sekelová, Z., Faldynová, M., Šebková, A., Šišák, F., & Rychlı́k, I. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.03473-15 · Cited by 440
“It is not surprising that it is occupied with billions of microorganisms, which collectively comprise the gut microbiota (1).”
BackgroundToward a census of bacteria in soil
Schloss, P. D., & Handelsman, J. (2006) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020092 · Cited by 429
“Although a complete census of a country is theoretically possible, it is currently impractical to survey all 10(9) bacterial cells in a gram of soil [1], making a sample-based census the best option for estimating richness—the number of bacterial taxa in soil.”
BackgroundThe biodiversity hypothesis and allergic disease: world allergy organization position statement
Haahtela, T., Holgate, S., Pawankar, R., Akdis, C. A., Benjaponpitak, S., Caraballo, L., Demain, J., Portnoy, J., & von Hertzen, L. (2013) · World Allergy Organization Journal · doi:10.1186/1939-4551-6-3 · Cited by 426
“Although the Convention of Biological Diversity [15] is primarily concerned with plants and animals, biodiversity also includes micro-organisms, which are less visible but comprise the bulk of living matter on our Earth [18].”
BackgroundMicrobial communities and their relevance for ecosystem models: Decomposition as a case study
McGuire, K. L., & Treseder, K. K. (2009) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2009.11.016 · Cited by 420
“Soil microbial communities are many times more diverse than their associated plant and animal communities (Whitman et al., 1998; Hawksworth, 2001), and less than 5% of all microbes have been identified and described (Schleifer, 2004).”
BackgroundLu, L., Luo, T., Zhao, Y., Cai, C., Fu, Z., & Jin, Y. (2019) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2019.02.380 · Cited by 431
Zeglin, L. H. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00454 · Cited by 413
“Surface-attached and bed sediment-entrained cells are not always accounted for in broad views of microbial life in aquatic ecosystems (Whitman et al., 1998), yet their activity drives biogeochemical processes at reach, watershed and continental scales (Likens et al., 1970; Mulholland et al., 2008;…”
BackgroundEcosystem function and services provided by the deep sea
Thurber, A. R., Sweetman, A. K., Narayanaswamy, B. E., Jones, D. O. B., Ingels, J., & Hansman, R. L. (2014) · Biogeosciences · doi:10.5194/bg-11-3941-2014 · Cited by 451
“The pelagic deep sea below 200 m comprises∼ 95 % of the volume of the ocean and harbors on the order of 1028 prokaryotes (Whitman et al., 1998), a great diversity of fish, and large pelagics such as the infamous giant squid (Architeuthis spp.).”
BackgroundDeep Sequencing of the Oral Microbiome Reveals Signatures of Periodontal Disease
Liu, B., Faller, L. L., Klitgord, N., Mazumdar, V., Ghodsi, M., Sommer, D. D., Gibbons, T. R., Treangen, T. J., Chang, Y.-C., Li, S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037919 · Cited by 411
“Our body harbors an enormous amount of microbial cells, estimated to exceed the number of human cells by an order of magnitude [5].”
BackgroundDarmon, E., & Leach, D. R. F. (2014) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00035-13 · Cited by 437
Microbial Extremophiles at the Limits of Life
Pikuta, E. V., Hoover, R. B., & Tang, J. (2007) · Critical Reviews in Microbiology · doi:10.1080/10408410701451948 · Cited by 424
“It is predicted that the largest number of prokaryotes in the biosphere occurs under ground (Whitman et al. 1998).”
BackgroundPomeroy, L. R., Williams, P. J. L., Azam, F., & Hobbie, J. E. (2007) · Oceanography · doi:10.5670/oceanog.2007.45 · Cited by 408
A comprehensive repertoire of prokaryotic species identified in human beings
Hugon, P., Dufour, J.-C., Colson, P., Fournier, P., Sallah, K., & Raoult, D. (2015) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(15)00293-5 · Cited by 424
Marine viruses and global climate change
Danovaro, R., Corinaldesi, C., Dell’Anno, A., Fuhrman, J. A., Middelburg, J. J., Noble, R. T., & Suttle, C. A. (2010) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2010.00258.x · Cited by 428
“…in global ecosystems, and comprise 1030 particles in the world’s oceans (Suttle, 2005, 2007), or about 10-fold greater than prokaryotic abundance (Whitman et al., 1998; Karner et al., 2001), and equivalent to the carbon in 75 million blue whales ( 10% of prokaryotic carbon by weight; Suttle,…”
BackgroundPresent state and future prospects for groundwater ecosystems
Danielopol, D. L., Griebler, C., Gunatilaka, A., & Notenboom, J. (2003) · Environmental Conservation · doi:10.1017/s0376892903000109 · Cited by 409
“The biomass of GW-dwelling prokaryotes in the unconsolidated subsurface domain accounts for about 6–40% of the earth’s total microbial biomass; this is a minimum estimate, based on unconsolidated sediments representing only 20% of the terrestrial subsurface, yet these sediments may be much more extensive (Whitman et a…”
BackgroundS-layers: principles and applications
Sleytr, U. B., Schuster, B., Egelseer, E.-M., & Pum, D. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12063 · Cited by 408
“Moreover, as the biomass of prokaryotic organisms surpasses the biomass of eukaryotic organism (Whitman et al., 1998), S-layer proteins can be considered as one of the most abundant biopolymers on our planet.”
BackgroundThe Origins of Eukaryotic Gene Structure
Lynch, M. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj050 · Cited by 391
“The goal of this paper is to expand on these previous results to demonstrate the plausibility of the hypothesis that many of the unique complexities of the eukaryotic gene arose by semi-neutral processes with little, if any, direct involvement of positive selection.”
BackgroundResultEmergence of a Habitable Planet
Zahnle, K., Arndt, N., Cockell, C., Halliday, A., Nisbet, E., Selsis, F., & Sleep, N. H. (2007) · Space Science Reviews · doi:10.1007/s11214-007-9225-z · Cited by 380
“8.4 Transient Environmental Effects of Impacts Today, the total number of prokaryotes on Earth is estimated to be 4–6 ×1030 cells (Whitman et al. 1998).”
BackgroundInfluentialRummel, J. D., Beaty, D. W., Jones, M. A., Bakermans, C., Barlow, N. G., Boston, P. J., Chevrier, V. F., Clark, B. C., Vera, J.-P. P. D., Gough, R. V., et al. (2014) · Astrobiology · doi:10.1089/ast.2014.1227 · Cited by 395
“Approximately 50% of Earth’s total biomass exists as subsurface prokaryotic life, much of which is found within unconsolidated sediments and groundwater (Whitman et al., 1998).”
Rice, S. A., Tan, C. H., Mikkelsen, P. J., Kung, V. L., Woo, J. K. K., Tay, M., Hauser, A. R., McDougald, D., Webb, J. S., & Kjelleberg, S. J. (2008) · The ISME Journal · doi:10.1038/ismej.2008.109 · Cited by 376
“Bacteriophage have been suggested to be one of the most abundant biological agents on the planet, estimated at a total of 1 10(31) (Rohwer and Edwards, 2002), compared with 2–6 10(30) bacterial cells (Whitman et al., 1998), outnumbering prokaryotes by approximately 10:1.”
BackgroundInfectious plant diseases: etiology, current status, problems and prospects in plant protection
Nazarov, P. A., Baleev, D. N., Ivanova, M. I., Sokolova, L. M., & Karakozova, M. V. (2020) · Acta Naturae · doi:10.32607/actanaturae.11026 · Cited by 418
“Blooming” in the gut: how dysbiosis might contribute to pathogen evolution.
Stecher, B., Maier, L., & Hardt, W.-D. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2989 · Cited by 378
Extracellular DNA Plays a Key Role in Deep-Sea Ecosystem Functioning
Dell’Anno, A., & Danovaro, R. (2005) · Science · doi:10.1126/science.1117475 · Cited by 378
Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review
Valentine, D. L. (2002) · Antonie van Leeuwenhoek · doi:10.1023/a:1020587206351 · Cited by 377
“Below Earth’s solid surface exists a microbiallydominated biosphere (Whitman et al. 1998).”
BackgroundHatfull, G. F. (2008) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.09.004 · Cited by 374
Exploration of deep intraterrestrial microbial life: current perspectives.
Pedersen, K. (2000) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2000.tb09033.x · Cited by 367
“An attempt to estimate the total carbon in terrestrial and intraterrestrial environments was recently made [13].”
BackgroundLooft, T. P., Allen, H. K., Cantarel, B. L., Levine, U. Y., Bayles, D. O., Alt, D. P., Henrissat, B., & Stanton, T. B. (2014) · The ISME Journal · doi:10.1038/ismej.2014.12 · Cited by 378
“The human colon may harbor as many as 1000 bacterial species, with 10(11) cells per gram of feces (Whitman et al., 1998), whereas small intestinal bacterial communities show much lower diversity (species richness and abundance) and cell densities (Booijink et al.”
BackgroundMetagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community
Hemme, C. L., Deng, Y., Gentry, T. J., Fields, M. W., Wu, L., Barua, S., Barry, K., Tringe, S. G., Watson, D. B., He, Z., et al. (2010) · The ISME Journal · doi:10.1038/ismej.2009.154 · Cited by 373
Fish immune system. A crossroads between innate and adaptive responses
Tort, L., & MacKenzie, S. A. (2003) · Cited by 370
Phillips, V. T. J., DeMott, P. J., & Andronache, C. (2008) · Journal of the Atmospheric Sciences · doi:10.1175/2007jas2546.1 · Cited by 372
“2001) to counts of culturable cells (Bovallius et al. 1978; Mandrioli et al. 1984; Shaffer and Lighthart 1997; Whitman et al. 1998; Andreeva et al. 2001).”
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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