Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Analysis
  • Published:

Bacteria and archaea on Earth and their abundance in biofilms

Abstract

Biofilms are a form of collective life with emergent properties that confer many advantages on their inhabitants, and they represent a much higher level of organization than single cells do. However, to date, no global analysis on biofilm abundance exists. We offer a critical discussion of the definition of biofilms and compile current estimates of global cell numbers in major microbial habitats, mindful of the associated uncertainty. Most bacteria and archaea on Earth (1.2 × 1030 cells) exist in the ‘big five’ habitats: deep oceanic subsurface (4 × 1029), upper oceanic sediment (5 × 1028), deep continental subsurface (3 × 1029), soil (3 × 1029) and oceans (1 × 1029). The remaining habitats, including groundwater, the atmosphere, the ocean surface microlayer, humans, animals and the phyllosphere, account for fewer cells by orders of magnitude. Biofilms dominate in all habitats on the surface of the Earth, except in the oceans, accounting for ~80% of bacterial and archaeal cells. In the deep subsurface, however, they cannot always be distinguished from single sessile cells; we estimate that 20–80% of cells in the subsurface exist as biofilms. Hence, overall, 40–80% of cells on Earth reside in biofilms. We conclude that biofilms drive all biogeochemical processes and represent the main way of active bacterial and archaeal life.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Abundance of bacteria and archaea in different habitats on Earth.
Fig. 2: Microbial habitats in fractured suboceanic and continental basaltic rock.
Fig. 3: Interfaces colonized by biofilms in the oceans.
Fig. 4: Biofilms in eukaryotic habitats.

Similar content being viewed by others

References

  1. Costerton, J. W. et al. Bacterial biofilms in nature and disease. Ann. Rev. Microbiol. 41, 435–464 (1987).

    Article  CAS  Google Scholar 

  2. Costerton, J. W. et al. Microbial biofilms. Ann. Rev. Microbiol. 49, 711–745 (1995).

    Article  CAS  Google Scholar 

  3. Lappin-Scott, H. M. & Costerton, J. W. (eds) Microbial Biofilms (Cambridge Univ. Press, 1995).

  4. Stoodley, P., Sauer, K., Davies, D. G. & Costerton, J. W. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56, 187–209 (2002).

    Article  CAS  PubMed  Google Scholar 

  5. Davey, M. E. & O’toole, G. A. Microbial biofilms: from ecology to molecular genetics. Microb. Mol. Biol. Rev. 64, 847–867 (2000).

    Article  CAS  Google Scholar 

  6. Watnick, R. & Kolter, R. Biofilm, city of microbes. J. Bacteriol. 182, 2675–2679 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Donlan, R. M. & Costerton, J. W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167–193 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Krumbein, W. E. et al. in Fossil and Recent Biofilms (eds Krumbein, W. E., Paterson, D. M. & Zavarzin, G. A.) 1–27 (Springer Science & Business Media, 2003).

  9. Costerton, J. W. The Biofilm Primer 169–195 (Springer Science & Business Media, 2007).

  10. Flemming, H.-C. et al. Biofilms: an emergent form of microbial life. Nat. Rev. Microbiol. 14, 563–575 (2016).

    Article  CAS  PubMed  Google Scholar 

  11. Battin, T., Besemer, K., Bengtsson, M. M., Romani, A. & Packman, A. I. The ecology and biogeochemistry of stream biofilms. Nat. Rev. Microbiol. 14, 251–263 (2016).

    Article  CAS  PubMed  Google Scholar 

  12. Tuson, H. H. & Weibel, D. B. Bacteria-surface interactions. Soft Matter 9, 4368–4380 (2013). This study explains the influence of surfaces on attached cells and biofilms — revisited after ZoBell.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Woodcock, S. & Sloan, W. T. Biofilm community succession: a neutral perspective. Microbiology 63, 664–668 (2017).

    Google Scholar 

  14. Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018). This paper takes a comprehensive and thorough approach to assess the biomass on Earth. It is one of the few publications in which the supplementary material is a gold mine of information, particularly on methods of quantification.

    Article  CAS  PubMed  Google Scholar 

  15. Magnabosco, C. et al. The biomass and biodiversity of the continental subsurface. Nat. Geosci. 11, 707–717 (2018). This paper presents a metastudy on 200 publications on continental subsurface cell concentrations, even providing a history of biomass estimates and also providing a highly valuable and comprehensive supplement.

    Article  CAS  Google Scholar 

  16. Conselice, J., Wilkinson, A., Duncan, K. & Mortlock, A. The evolution of galaxy number density AT z >8 and its implications. Astrophys. J. 830, 83 (2016).

    Article  Google Scholar 

  17. Orell, A., Fröls, S. & Albers, S.-V. Archaeal biofilms: the great unexplored. Annu. Rev. Microbiol. 67, 337–354 (2013).

    Article  CAS  PubMed  Google Scholar 

  18. Fröls, S. Archaeal biofilms: widespread and complex. Biochem. Soc. Trans. 41, 393–398 (2013).

    Article  PubMed  CAS  Google Scholar 

  19. Van Wolferen, M., Orell, A. & Albers, S.-V. Archaeal biofilm formation. Nat. Rev. Microbiol. 16, 699–713 (2018).

    Article  PubMed  CAS  Google Scholar 

  20. Pedersen, K. & Ekendahl, S. Incorporation of CO2 and introduced organic compounds by bacterial populations from the deep crystalline bedrock of the Stripa mine. J. Gen. Microbiol. 138, 369–376 (1992).

    Article  CAS  Google Scholar 

  21. McMahon, S. & Parnell, J. Weighing the deep continental biosphere. FEMS Microbiol. Ecol. 87, 113–120 (2013). This study, inspired by Whitman et al. (1998), presents an excellent approach to quantifying cells in the deep subsurface.

    Article  PubMed  CAS  Google Scholar 

  22. Schrenk, M. O., Huber, J. A. & Edwards, K. J. Microbial provinces in the subseafloor. Annu. Rev. Mar. Sci. 2, 279–304 (2010). This paper describes places where microorganisms can live in rocks.

    Article  Google Scholar 

  23. Heberling, C., Lowell, R. P., Liu, L. & Fisk, M. R. Extent of the microbial biosphere in the oceanic crust. Geochem. Geophys. Geosys. 11, Q08003 (2010).

    Article  Google Scholar 

  24. Menez, B., Pasini, V. & Brunelli, D. Life in the hydrated suboceanic mantle. Nat. Geosci. 5, 133–137 (2012).

    Article  CAS  Google Scholar 

  25. Edwards, K. J., Wheat, C. G. & Sylvain, J. B. Under the sea: microbial life in the volcanic crust. Nat. Rev. Microbiol. 9, 703–712 (2011). This paper is a very well-written treatise on life below the ocean.

    Article  CAS  PubMed  Google Scholar 

  26. Johnson, H. P. & Pruis, M. J. Fluxes of fluid and heat from the oceanic crustal reservoir. Earth Planet. Sci. Lett. 216, 565–574 (2003).

    Article  CAS  Google Scholar 

  27. Lloyd, K. G., May, M. K., Kevorkian, R. T. & Steen, A. D. Meta-analysis of quantification methods shows that archaea and bacteria have similar abundances in the subseafloor. Appl. Environ. Microbiol. 79, 7790–7799 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Danovaro, R., Corinaldesi, C., Rastelli, E. & Dell Anno, A. Towards a better quantitative assessment of the relevance of deep-sea viruses, Bacteria and Archaea in the functioning of the ocean seafloor. Aquat. Microb. Ecol. 75, (81–90 (2015).

    Google Scholar 

  29. Lipp, J. S., Morono, Y., Inagaki, F. & Hinrichs, K.-U. Significant contribution of Archaea to extent biomass in marine subsurface sediments. Nature 454, 991–994 (2008).

    Article  CAS  PubMed  Google Scholar 

  30. Justice, N. B. et al. Heterotrophic archaea contribute to carbon cycling in low-pH, suboxic biofilm communities. Appl. Environ. Microbiol. 78, 8321–8330 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Xie, S., Lipp, J. S., Wegener, G., Ferdelman, T. G. & Hinrichs, K.-U. Turnover of microbial lipids in the deep biosphere and growth of benthic archaeal populations. Proc. Natl Acad. Sci. USA 110, 6010–6014 (2013).

    Article  CAS  PubMed  Google Scholar 

  32. Griebler, C., Mindl, B., Slezak, D. & Geiger-Kaiser, M. Distribution patterns of attached and suspended bacteria in pristine and contaminated shallow aquifers studied with an in situ sediment exposure microcosm. Aquat. Microb. Ecol. 28, 117–129 (2002).

    Article  Google Scholar 

  33. Biddle, J., Jungbluth, S. P., Lever, M. A. & Rappe, M. S. in Microbial Life of the Deep Biosphere (eds Kallmeyer, J. & Wagner, D.) 29–62 (De Gruyter, Berlin, 2014).

  34. Morono, Y. & Inagaki, F. Analysis of low-biomass microbial communities in the deep biosphere. Adv. Appl. Microbiol. 95, 149–178 (2016). This paper presents a comprehensive overview of methods to determine biomass in the subsurface.

    Article  CAS  PubMed  Google Scholar 

  35. Jørgensen, B. B. & Boetius, A. Feast and famine — microbial life in the deep-sea bed. Nat. Rev. Microbiol. 5, 770–781 (2007).

    Article  PubMed  CAS  Google Scholar 

  36. Santelli, C. M. et al. Abundance and diversity of microbial life in the ocean crust. Nature 453, 653–656 (2008).

    Article  CAS  PubMed  Google Scholar 

  37. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998). This paper, the classic on the global census of microorganisms, reflects the fun the authors must have had while writing it.

    Article  CAS  PubMed  Google Scholar 

  38. Kallmeyer, J., Pockalny, R., Adhikari, R. R., Smith, D. C. & D’Hondt, S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl Acad. Sci. USA 109, 16213–16216 (2012). This study is a thoughtful and complex revisit of numbers from Whitman et al. (1998) that is based on their own measurements.

    Article  Google Scholar 

  39. Parkes, R. J. et al. A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere:geosphere interactions. Mar. Geol. 352, 409–425 (2014). This paper presents an excellent review on how deeply buried prokaryotes influence the surface processes on Earth.

    Article  CAS  Google Scholar 

  40. Colwell, F. S. & D’Hondt, S. Nature and extent of the deep biosphere. Rev. Miner. Geochem. 75, 547–574 (2013).

    Article  CAS  Google Scholar 

  41. Pedersen, K. Exploration of deep intraterrestrial microbial life: current perspectives. FEMS Microbiol. Lett. 185, 9–16 (2000).

    Article  CAS  PubMed  Google Scholar 

  42. Thorseth, I. H. et al. Diversity of life in ocean floor basalt. Earth Planet. Sci. Lett. 194, 31–37 (2001).

    Article  CAS  Google Scholar 

  43. Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626 (2001).

    Article  Google Scholar 

  44. Trembath-Reichert, E. et al. Methyl-compound use and slow growth characterize microbial life in 2-km-deep subseafloor coal and shale beds. Prod. Natl Acad. Sci. USA 114, E9206–E9215 (2017).

    Article  CAS  Google Scholar 

  45. Gerbersdorf, S. & Wieprecht, S. Biostabilization of cohesive sediments: revisiting the role of abiotic conditions, physiology and diversity of microbes, polymeric secretion, and biofilm architecture. Geobiology 15, 68–97 (2017).

    Google Scholar 

  46. Schippers, A. et al. Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433, 861–864 (2017).

    Article  CAS  Google Scholar 

  47. Orsi, W. D. Ecology and evolution of seafloor and subseafloor microbial communities. Nat. Rev. Microbiol. 16, 671–683 (2018). This paper presents a valuable resource about various paths of microbial metabolism in the subsurface.

    Article  CAS  PubMed  Google Scholar 

  48. Ramirez-Llodra, E. et al. Deep, diverse and definitely different: unique attributes of the world’s largest ecosystem. Biogeosciences 7, 2851–2899 (2010).

    Article  Google Scholar 

  49. Hoehler, T. & Jørgensen, B. B. Microbial life under extreme energy limitation. Nat. Rev. Microbiol. 11, 83–94 (2013). This paper presents in-depth considerations of the ways of life and survival in the deep subsurface.

    Article  CAS  PubMed  Google Scholar 

  50. Røy, H. et al. Aerobic microbial respiration in 86-million-year-old deep-sea red clay. Science 336, 922–925 (2012).

    Article  PubMed  CAS  Google Scholar 

  51. Edwards, K. J., Bach, W. & McCollom, T. M. Geomicrobiology in oceanography: microbe-mineral interactions at and below the seafloor. Trends Microbiol. 13, 449–456 (2005). This paper presents a view on the microbial traffic between the deep subsurface and the sea floor.

    Article  CAS  PubMed  Google Scholar 

  52. Colwell, F. S. & Smith, R. P. in The Subseafloor Biosphere at Mid-Ocean Ridges Vol. 144 (eds Wilcock, W. S. D., Delong, E. F., Kelley, D. S., Baross, J. A. & Cary, S. C.) 355–367 (2013).

  53. Sharma, A. et al. Microbial activity at gigapascal pressures. Science 295, 1514–1516 (2002).

    Article  CAS  PubMed  Google Scholar 

  54. Siliakus, M. F., van der Oost, J. & Kengen, S. W. M. Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure. Extremophiles 21, 651–670 (2017).

    Article  CAS  Google Scholar 

  55. Fang, J. et al. Predominance of viable spore-forming piezophilic bacteria in high-pressure enrichment cultures from ~1.5 to 2.4 km-deep coal-bearing sediments below the ocean floor. Front. Microbiol. 8, 137 (2017).

    PubMed  PubMed Central  Google Scholar 

  56. Starnawski, P. et al. Microbial community assembly and evolution in subseafloor sediment. Proc. Natl Acad. Sci. USA 114, 2940–2945 (2017).

    Article  CAS  PubMed  Google Scholar 

  57. Brazelton, W. J., Morrill, P. L., Szponar, N. & Schrenk, M. O. Bacterial communities associated with subsurface geochemical processes in continental serpentinite springs. Appl. Environ. Microbiol. 79, 3906–3916 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. D’Hondt, S. et al. Distribution of microbial activities in deep seafloor sediments. Science 306, 2216–2221 (2004).

    Article  PubMed  CAS  Google Scholar 

  59. Parkes, R. J. et al. Deep sub-seafloor prokaryotes stimulated at interfaces over geological time. Nature 436, 390–394 (2005).

    Article  CAS  PubMed  Google Scholar 

  60. Ciobanu, M.-C. et al. Microorganisms persist at record depths in the subseafloor of the Canterbury Basin. ISME J. 8, 1370–1380 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Morono, Y. et al. Carbon and nitrogen assimilation in deep subseafloor microbial cells. Proc. Natl Acad. Sci. USA 108, 18925–18300 (2011).

    Article  Google Scholar 

  62. Johnson, S. S. et al. Ancient bacteria show evidence of DNA repair. Proc. Natl Acad. Sci. USA 104, 14401–14405 (2007).

    Article  CAS  PubMed  Google Scholar 

  63. Marshall, K. C. Bacterial adhesion in oligotrophic habitats. Microbiol. Sci. 2, 321–326 (1985).

    CAS  PubMed  Google Scholar 

  64. Lever, M. A. et al. Life under extreme energy limitation: a synthesis of laboratory and field-based investigations. FEMS Microbiol. Rev. 39, 688–728 (2015).

    Article  CAS  PubMed  Google Scholar 

  65. Dang, H. & Lovell, C. R. Microbial surface colonization and biofilm development in marine environments. Microbiol. Mol. Biol. Rev. 80, 91–138 (2016). This paper presents an excellent overview of interfaces with cell aggregates in the ocean.

    Article  CAS  PubMed  Google Scholar 

  66. Orcutt, B. N. et al. Microbial activity in the marine deep biosphere: progress and prospects. Front. Microbiol. 4, 189 (2013). This paper presents a compilation of ample evidence that the deep marine biosphere is alive.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Orcutt, B. N., Sylvan, J. B., Knab, N. J. & Edwards, K. J. Microbial ecology of the dark ocean above, at, and below the seafloor. Microb. Mol. Biol. Rev. 75, 361–422 (2011). This paper presents a comprehensive overview of life in the deep ocean biosphere.

    Article  CAS  Google Scholar 

  68. Teske, A. P. The deep subsurface biosphere is alive and well. Trends Microbiol. 13, 402–404 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Gold, T. The deep, hot biosphere. Proc. Natl Acad. Sci. USA 89, 6045–6049 (1992). This seminal, strongly argued and visionary paper turns the attention to the borders of life in the deep depths.

    Article  CAS  PubMed  Google Scholar 

  70. Kieft, T. L. in Their World: A Diversity of Microbial Environments (ed. Hurst, C. J.) 225–253 (Springer Int. Publ., Switzerland, 2016).

  71. Ehrlich, H. L., Newman, D. K. & Kappler, A. (eds) Ehrlich’s Geomicrobiology 6th edn (CRC Press, Boca Raton, 2015).

  72. Beatty, J. T. et al. An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc. Natl Acad. Sci. USA 102, 9306–9310 (2005).

    Article  CAS  PubMed  Google Scholar 

  73. Osburn, M. R., LaRowe, D. E., Momper, L. M. & Amend, J. P. Chemolithotrophy in the continental deep subsurface: Sanford Underground Research Facility (SURF), USA. Front. Microbiol. 5, 610 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Ehrlich, H. L. Microbes as geologic agents: their role in mineral formation. Geomicrobiol. J. 16, 135–153 (1999).

    Article  Google Scholar 

  75. Pedersen, K. Microbial life in deep granitic rock. FEMS Microbiol. Rev. 20, 399–414 (1997).

    Article  CAS  Google Scholar 

  76. Douglas, S. Mineralogical footprints of microbial life. Am. J. Sci. 305, 503–525 (2005).

    Article  CAS  Google Scholar 

  77. Tuck, V. A. et al. Biologically induced clay formation in subsurface granitic environments. J. Geochem. Explor. 90, 123–133 (2006).

    Article  CAS  Google Scholar 

  78. Anderson, C., James, R. E., Fru, E. C., Kennedy, C. B. & Pedersen, K. In-situ ecological development of a bacteriogenic iron oxide producing microbial community from a subsurface granitic rock environment. Geobiology 4, 29–42 (2006).

    Article  CAS  Google Scholar 

  79. Stevens, T. O. & McKinley, J. P. Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270, 450–454 (1995).

    Article  CAS  Google Scholar 

  80. Fredrickson, J. K. & Balkwill, D. L. Geomicrobial processes and biodiversity in the deep terrestrial subsurface. Geomicrobiol. J. 23, 345–356 (2006).

    Article  CAS  Google Scholar 

  81. Albrechtsen, H.-J. Distribution of bacteria, estimated by a viable count method, and heterotrophic activity in different size fractions of aquifer sediment. Geomicrobiol. J. 12, 253–264 (1994).

    Article  Google Scholar 

  82. Jägevall, S., Rabe, L. & Pedersen, K. Abundance and diversity of biofilms in natural and artificial aquifers of the Äspö Hard Rock Laboratory, Sweden. Microb. Ecol. 61, 410–422 (2011).

    Article  PubMed  Google Scholar 

  83. Itävaraa, M. et al. Characterization of bacterial diversity to a depth of 1500m in the Outokumpu deep borehole, Fennoscandian Shield. FEMS Microbiol. Ecol. 77, 295–309 (2011).

    Article  CAS  Google Scholar 

  84. Sakurai, K. & Yoshikawa, H. Isolation and identification of bacteria able to form biofilms from deep subsurface environments. J. Nucl. Sci. Technol. 49, 287–292 (2012).

    Article  CAS  Google Scholar 

  85. Wanger, G., Southam, G. & Onstott, T. C. Structural and chemical characterization of natural fracture surface from 2.8 km below land surface: biofilms in the deep subsurface. Geomicrobiol. J. 23, 443–452 (2006).

    Article  CAS  Google Scholar 

  86. Escudero, C., Vera, M., Oggerin, M. & Amils, R. Active microbial biofilms in deep poor porous continental subsurface rocks. Sci. Rep. 8, 1538 (2018). This paper presents evidence from CARD–FISH and fluorescent lectin-binding assays for biofilm existence in the deep underground.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Gantner, S. et al. In-situ quantification of the spatial scale of calling distances and population density-independent N-acylhomoserine-lactone-mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiol. Ecol. 56, 188–194 (2006). This elegant study determines the calling distance of microbial aggregates.

    Article  CAS  PubMed  Google Scholar 

  88. Amano, Y., Iwatsuki, T. & Naganuma, T. Characteristics of naturally grown biofilms in deep groundwaters and their heavy metal sorption property in a deep subsurface environment. Geomicrobiol. J. 34, 769–783 (2017).

    Article  CAS  Google Scholar 

  89. Leon-Morales, C. F., Leis, A. P., Strathmann, M. & Flemming, H.-C. Interactions between laponite and microbial biofilms in porous media: implications for colloid transport and biofilm stability. Water Res. 38, 3614–3626 (2004).

    Article  CAS  PubMed  Google Scholar 

  90. Coombs, P. et al. The role of biofilms in subsurface transport processes. Q. J. Eng. Geol. Hydrogeol. 43, 131–139 (2010).

    Article  CAS  Google Scholar 

  91. Nazina, T. N. et al. Microbiology of formation waters from the deep repository of liquid radioactive wastes Severnyi. FEMS Microbiol. Ecol. 49, 97–107 (2004).

    Article  CAS  PubMed  Google Scholar 

  92. Onstott, T. C., Colwell, F. S., Kieft, T. L., Murdoch, L. & Phelps, T. J. New horizons for deep surface microbiology. Microbe 11, 499–505 (2009).

    Google Scholar 

  93. Meyer-Reil, L. A. Microbial life in sedimentary biofilms — the challenge to microbial ecologists. Mar. Ecol. Prog. Ser. 112, 303–311 (1994).

    Article  Google Scholar 

  94. Petro, C., Starnawski, P., Schramm, A. & Kjeldsen, K. U. Microbial community assembly in marine sediments. Aquat. Microb. Ecol. 79, 177–195 (2017).

    Article  Google Scholar 

  95. Glud, R. et al. High rates of microbial turnover in sediments in the deepest oceanic trench on Earth. Nat. Geosci. 6, 284–288 (2013).

    Article  CAS  Google Scholar 

  96. Bowles, M. W., Mogollon, J., Kasten, S., Zabel, M. & Hinrichs, K. U. Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities. Science 344, 889–891 (2014).

    Article  CAS  PubMed  Google Scholar 

  97. D’Hondt, S. et al. Presence of oxygen and aerobic communities from seafloor to basement in deep-sea sediments. Nat. Geosci. 8, 299–304 (2015).

    Article  CAS  Google Scholar 

  98. Probandt, D. et al. Microbial life on a sand grain. ISME J. 12, 623–633 (2018).

    Article  PubMed  Google Scholar 

  99. Balzer, M., Witt, N., Flemming, H.-C. & Wingender, J. Accumulation of fecal indicator bacteria in river biofilms. Water Sci. Technol. 61, 1106–1111 (2010).

    Article  CAS  Google Scholar 

  100. Weise, W. & Rheinheimer, G. Scanning electron microscopy and epifluorescence investigation of bacterial colonization of marine sand sediments. Microb. Ecol. 4, 175–188 (1978).

    Article  Google Scholar 

  101. Chen, X. D. et al. Stabilizing effects of biofilms: EPS penetration and re-distribution of bed stability down the sediment profile. J. Geophys. Res. Biogeosci. 122, 3113–3125 (2017).

    Article  Google Scholar 

  102. Chen, X. D. et al. Hindered erosion: The biological mediation of noncohesive sediment behaviour. Water Resour. Res. 53, 4787–4801 (2017).

    Article  Google Scholar 

  103. Spadafora, A., Perri, E., McKenzie, J. & Vasconcelos, C. Microbial biomineralization process forming modern Ca:Mg carbonate stromatolites. Sedimentology 57, 27–40 (2010).

    Article  CAS  Google Scholar 

  104. Bontognali, T. R. R. et al. Dolomite formation within microbial mats in the coastal sabkha of Abu Dhabi (United Arab Emirates). Sedimentology 57, 824–844 (2010).

    Article  CAS  Google Scholar 

  105. Fierer, N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15, 579–590 (2017).

    Article  CAS  PubMed  Google Scholar 

  106. Raynaud, X. & Nunan, N. Spatial ecology of bacteria at the microscale in soil. PLOS ONE 9, e87217 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Wei, C.-L. et al. Global patterns and predictions of seafloor biomass using random forests. PLOS ONE 5, e15323 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Ranjard, L. & Richaume, A. Quantitative and qualitative distribution of bacteria in soil. Res. Microbiol. 152, 707–716 (2001).

    Article  CAS  PubMed  Google Scholar 

  109. Kuzyakov, Y. & Blagodatskaya, L. Microbial hotspots and hot moments in soil: concept and review. Soil Biol. Biochem. 83, 184–199 (2015).

    Article  CAS  Google Scholar 

  110. Young, I. M., Crawford, J. W., Nunan, N., Otten, W. & Spiers, A. Microbial distribution in soils: physics and scaling. Adv. Agronom. 100, 81–121 (2008). This is an excellent overview of soil microbiology.

    Google Scholar 

  111. Chotte, J. L., Ladd, J. N. & Amato, N. Sites of microbial assimilation, and turnover of soluble and particulate 14C-labelled substrates decomposing in clay soil. Soil Biol. Biochem. 30, 205–218 (1998).

    Article  CAS  Google Scholar 

  112. Flemming, H.-C. & Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633 (2010).

    Article  CAS  PubMed  Google Scholar 

  113. Davis, C. A. et al. Microbial-induced heterogeneity in the acoustic properties of porous media. Geophys. Res. Let. 36, L21405 (2009).

    Article  Google Scholar 

  114. Tang, J., Mo, Y., Zhang, J. & Zhang, R. Influence of biological aggregating agents associated with microbial population on soil aggregate stability. Appl. Soil. Ecol. 47, 153–159 (2011).

    Article  Google Scholar 

  115. Cunliffe, M. et al. Sea surface microlayers: a unified physicochemical and biological perspective of the ocean-air interface. Prog. Oceanogr. 109, 104–116 (2013).

    Article  Google Scholar 

  116. Engel, A. et al. The ocean’s vital skin: toward an integrated understanding of the sea surface microlayer. Front. Mar. Sci. 4, 165 (2017).

    Article  Google Scholar 

  117. Aller, J. Y., Kusnetzova, M. R., Jahns, C. J. & Kemp, P. The sea surface microlayer as a source of viral and bacterial enrichment in marine aerosols. J. Aerosol Sci. 36, 801–812 (2005).

    Article  CAS  Google Scholar 

  118. Wurl, O. & Cunliffe, M. in The Perfect Slime: Microbial Extracellular Polymeric Substances (EPS) (eds Flemming, H.-C., Neu, T. R., Wingender, J.) 249–268 (IWA Publishing, London, 2016).

  119. Franklin, R. B. et al. Bacterial diversity in the bacterioneuston (sea surface microlayer): the bacterioneuston through the looking glass. Environ. Microbiol. 7, 723–736 (2005).

    Article  CAS  PubMed  Google Scholar 

  120. Wurl, O. & Holmes, M. The gelatinous nature of the sea-surface microlayer. Mar. Chem. 110, 89–97 (2008).

    Article  CAS  Google Scholar 

  121. Rahlff, J. et al. High wind speeds prevent formation of a distinct bacterioneuston community in the sea-surface microlayer. FEMS Microb. Ecol. 93, fix041 (2017).

    Article  CAS  Google Scholar 

  122. Wurl, O., Ekau, W., Landing, W. M. & Zappa, C. J. Sea surface layer in a changing ocean — a perspective. Elem. Sci. Anth. 5, 31 (2017). This paper presents a very good overview of the neuston microbial community.

    Article  Google Scholar 

  123. Barberàn, A., Henley, J., Fierer, N. & Casamayor, E. O. Structure, inter-annual recurrence and global-scale connectivity of airborne microbial communities. Sci. Total Environ. 487, 187–195 (2014).

    Article  PubMed  CAS  Google Scholar 

  124. Hardy, J. T. The sea surface microlayer: biology, chemistry and anthropogenic enrichment. Prog. Oceanog. 11, 307–328 (1982).

    Article  Google Scholar 

  125. Upstill-Goddard, R. C., Frost, T. & Henry, G. R. Bacterioneuston control of air-water methane exchanged determined with a laboratory gas exchange tank. Glob. Biogeochem. Cycles 17, 1108 (2003).

    Article  CAS  Google Scholar 

  126. Hörtnagl, P., Pérez, M. R. & Sommaruga, P. Living at the border: a community and single-cell assessment of lake bacterioneuston activity. Limnol. Oceanogr. 55, 1134–1144 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Arístegui, J., Gasol, J. M., Duarte, C. M. & Herndl, G. J. Microbial Oceanography of the dark ocean’s pelagic realm. Limnol. Oceanogr. 54, 1501–1529 (2009).

    Article  Google Scholar 

  128. Buitenhuis, E. T. et al. Picoheterotroph (Bacteria and Archaea) biomass distribution in the global ocean. Earth Syst. Sci. Data 4, 101–106 (2012).

    Google Scholar 

  129. Buitenhuis, E. T. et al. Picophytoplankton biomass distribution in the global ocean. Earth Syst. Sci. Data 4, 37–46 (2012). References 128 and 129 present gold mines of marine microbiological data.

    Google Scholar 

  130. Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–809 (2002).

    Article  CAS  PubMed  Google Scholar 

  131. Giovannoni, S. J. SAR11 bacteria: the most abundant plankton in the Oceans. Annu. Rev. Mar. Sci. 9, 231–255 (2017).

    Google Scholar 

  132. Flombaum, P. et al. Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl Acad. Sci. USA 110, 9824–9829 (2013).

    Article  CAS  PubMed  Google Scholar 

  133. Giovannoni, S. J. et al. Genome streamlining in a cosmopolitan oeanic bacterium. Science 309, 1242–1245 (2005).

    Article  CAS  PubMed  Google Scholar 

  134. Lauro, F. et al. The genomic basis of trophic strategy in marine bacteria. Proc. Natl Acad. Sci. USA 106, 15527–15533 (2009).

    Article  CAS  PubMed  Google Scholar 

  135. Morris, J. J., Johnson, Z. I., Szul, M. J., Keller, M. & Zinser, E. R. Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the Ocean’s surface. PLOS ONE 6, e16805 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Becker, S., Singh, A. K., Postius, C., Böger, P. & Ernst, A. Genetic diversity and distribution of periphytic Synechococcus spp. in biofilms and picoplankton of Lake Constance. FEMS Microbiol. Ecol. 49, 181–190 (2004).

    Article  CAS  PubMed  Google Scholar 

  137. Ghiglione, J.-F., Conan, P. & Pujo-Pay, M. Diversity of total and active free-living versus particle-attached bacteria in the euphotic zone of the NW Mediterranean Sea. FEMS Microbiol. Lett. 299, 9–21 (2009).

    Article  CAS  PubMed  Google Scholar 

  138. Moeseneder, M. M., Winter, C. & Herndl, G. J. Horizontal and vertical complexity of attached and free-living bacteria of the eastern Mediterranean Sea, determined by 16s rDNA and 16s rRNA fingerprints. Limnol. Oceanogr. 46, 95–107 (2001).

    Article  CAS  Google Scholar 

  139. Lee, S. W., Lee, C. W., Bong, C. W., Narayanan, K. & Sim, E. U. The dynamics of attached and free-living bacterial population in tropical coastal waters. Mar. Freshw. Res. 66, 701–710 (2015).

    Article  CAS  Google Scholar 

  140. Milici, M. et al. Diversity and community composition of particle-associated and free-living bacteria in mesopelagic and bathypelagic Southern Ocean water masses: Evidence of dispersal limitation in the Bransfield Strait. Limnol. Oceanogr. 62, 1080–1095 (2017).

    Article  Google Scholar 

  141. Mestre, M., Borrull, E., Sala, M. M. & Gasol, J. M. Patterns of bacterial diversity in the marine planktonic particulate matter continuum. ISME J. 11, 999–1010 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  142. Zettler, E. R., Mincer, T. J. & Amaral-Zettler, L. A. Life in the ‘plastisphere’: microbial communities on plastic marine debris. Environ. Sci. Technol. 47, 7137–7148 (2013).

    Article  CAS  PubMed  Google Scholar 

  143. Harrison, J. P., Schratzberger, M., Sapp, M. & Osborn, A. M. Rapid bacterial colonization of low-density polyethylene microplastics in coastal sediment microcosms. BMC Microbiol. 14, 232 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  144. Lapoussière, A., Michel, C., Starr, M., Gosselin, M. & Poulin, M. Role of free-living and particle-attached bacteria in the recycling and export of organic material in the Hudson Bay system. J. Mar. Syst. 88, 434–455 (2011).

    Article  Google Scholar 

  145. Bruckner, C. G., Bahulikar, R., Rahalkar, M., Schink, B. & Kroth, P. Bacteria associated with benthic diatoms from Lake Constance: phylogeny and influences on diatom growth and secretion of extracellular polymeric substances. Appl. Environ. Microbiol. 74, 7740–7749 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Wahl, M., Goecke, F., Labes, A., Dobretsov, S. & Weinberger, F. The second skin: ecological role of epibiotic biofilms on marine organisms. Front. Microbiol. 3, 292 (2012). This study comprehensively highlights the role of eukaryotes as substrata for marine biofilms.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Eriksen, M. et al. Plastic pollution in the world’s oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLOS ONE 9, e111913 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  148. Cózar, A. et al. Plastic debris in the open ocean. Proc. Nat. Acad. Sci. USA 111, 10239–10244 (2014).

    Article  CAS  Google Scholar 

  149. Kooi, M., van Nes, E. H., Scheffer, M. & Koelmans, A. A. Ups and downs in the oceans: effect of biofouling on vertical transport of microplastics. Environ. Sci. Technol. 51, 7963–7971 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Ahmed, T. et al. Biodegradation of plastics: current scenario and future prospects for environmental safety. Environ. Sci. Pollut. Res. 25, 7287–7298 (2018).

    Article  CAS  Google Scholar 

  151. Galloway, T. S., Cole, M. & Lewis, C. Interactions of microplastic debris throughout the marine ecosystem. Nat. Ecol. Evol. 1, 0116 (2017).

    Article  Google Scholar 

  152. Kirstein, I. V. et al. Dangerous hitchhikers? Evidence for pathogenic Vibrio spp. on microplastic particles. Mar. Environ. Res. 120, 1–8 (2016).

    Article  CAS  PubMed  Google Scholar 

  153. Alldredge, A. L. & Silver, M. W. Characteristics, dynamics and significance of marine snow. Prog. Oceanog. 20, 41–82 (1988).

    Article  Google Scholar 

  154. Neu, T. In situ cell and glycoconjugate distribution in river snow studied by confocal laser scanning microscopy. Aquat. Microb. Ecol. 21, 85–95 (2000).

    Article  Google Scholar 

  155. Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791 (2007). This paper presents a visionary look at microorganisms and oceans.

    Article  CAS  PubMed  Google Scholar 

  156. Thiele, S., Fuchs, B. M., Ammann, R. & Iversen, M. H. Colonization in the photic zone and subsequent changes during sinking determine bacerial community composition in marine snow. Appl. Environ. Microbiol. 81, 1463–1471 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  157. Gram, L., Grossart, H.-P., Schlinghoff, A. & Kiorboe, T. Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl. Environ. Microbiol. 68, 4111–4116 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Eloe, E. A. et al. Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep-ocean environment. Environ. Microbiol. Rep. 3, 449–458 (2011).

    Article  PubMed  Google Scholar 

  159. Yooseph, S. et al. Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468, 60–67 (2010).

    Article  CAS  PubMed  Google Scholar 

  160. Busch, K. et al. Bacterial colonization and vertical distribution of marine gel particles (TEP and CSP) in the Arctic Fram strait. Front. Microbiol. 4, 166 (2017).

    Google Scholar 

  161. Zäncker, B., Cunliffe, M. & Engel, A. Bacterial community composition in the sea surface microlayer off the Peruvian coast. Front. Microbiol. 9, 2699 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  162. Decho, A. & Guiterrez, T. Microbial extracellular substances (EPSs) in Ocean systems. Front. Microbiol. 8, 922 (2017). This study sheds light on the importance of the biofilm matrix in ocean processes.

    Article  PubMed  PubMed Central  Google Scholar 

  163. Oberbeckmann, S., Löder, M. G. & Labrenz, M. Marine microplastic-associated biofilms — a review. Environ. Chem. 12, 551–562 (2015). This paper provides an excellent overview on microplastic as an emerging habitat for microbial biofilms.

    Article  CAS  Google Scholar 

  164. DeLeon-Rodriguez, N. et al. Microbiome of the upper troposphere: species comoposition and prevalence, effects of tropical storms and atmospheric implications. Prod. Natl Acad. Sci. USA 110, 2575–2580 (2013).

    Article  CAS  Google Scholar 

  165. Jones, A. M. & Harrison, R. M. The effects of meteorological factors on atmospheric bioaerosol concentrations — a review. Sci. Total Environ. 326, 151–180 (2004).

    Article  CAS  PubMed  Google Scholar 

  166. Marks, R., Kruczalak, K., Jankowska, K. & Michalska, M. Bacteria and fungi in air over the Gulf of Gdansk and Baltic sea. J. Aerosol Sci. 32, 237–250 (2001).

    Article  CAS  Google Scholar 

  167. Morris, C. E., Georgakopoulos, D. & Sands, D. Ice nucleation active bacteria and their potential role in precipitation. J. Phys. IV France 121, 87–103 (2004).

    Google Scholar 

  168. Carotenuto, F. et al. Measurements and modelling of surface-atmosphere exchange of microorganism in Mediterranean grassland. Atmos. Chem. Phys. 17, 14919–14936 (2017).

    Article  CAS  Google Scholar 

  169. Després, V. et al. Primary biological aerosol particles in the atmosphere: a review. Tellus B Chem. Phys. Meteorol. 64, 15598 (2012).

    Article  Google Scholar 

  170. Amato, P. et al. Microbial population in cloud water at the Puy de Drôme: Implications for the chemistry of clouds. Atmos. Environ. 39, 4143–4153 (2005).

    Article  CAS  Google Scholar 

  171. Deguillaume, L. et al. Microbiology and atmospheric processes: Chemical interactions of primary biological aerosols. Biogeosci. Discuss. 5, 1073–1084 (2008).

    Article  CAS  Google Scholar 

  172. Sattler, B., Puxbaum, H. & Psenner, R. Bacterial growth in supercooled cloud droplets. Geophys. Res. Let. 28, 239–242 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Carpenter, E. J., Lin, S. & Capone, D. G. Bacterial activity in South Pole snow. Appl. Environ. Microbiol. 66, 4514–4517 (2000).

    Article  Google Scholar 

  174. Wainwright, M., Wickramasinghe, N. C., Narlikar, J. V. & Rajaratnam, P. Microorganisms cultured from stratospheric air samples obtained at 41 km. FEMS Microbiol. Lett. 218, 161–165 (2003).

    Article  CAS  PubMed  Google Scholar 

  175. Imshenetsky, A. A., Lysenko, S. V. & Kazakov, G. A. Upper boundary of the biosphere. Appl. Environ. Microbiol. 35, 1–5 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  176. Burrows, S. M., Elbert, W., Lawrence, M. G. & Pöschl, U. Bacteria in the global atmosphere – part 1: review and synthesis of literature data for different ecosystems. Atmos. Chem. Phys. 9, 9263–9280 (2009).

    Article  CAS  Google Scholar 

  177. Morris, C. E. & Monier, J.-M. The ecological significance of biofilm formation by plant-associated bacteria. Annu. Rev. Phytopathol. 41, 429–453 (2003).

    Article  CAS  PubMed  Google Scholar 

  178. Ruinen, J. The phyllosphere: I. An ecologically neglected milieu. Plant Soil 15, 81–109 (1961).

    Article  Google Scholar 

  179. Bringel, F. & Couée, I. Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front. Microbiol. 6, 486 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  180. Baldotto, L. E. B. & Olivares, F. L. Phylloepiphytic interaction between bacteria and different plant species in a tropical agricultural system. Can. J. Microbiol. 54, 918–931 (2008).

    Article  CAS  PubMed  Google Scholar 

  181. Vorholt, J. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828–840 (2012).

    Article  CAS  PubMed  Google Scholar 

  182. Vacher, C. et al. The phyllosphere: microbial jungle at the plant-climate interface. Ann. Rev. Ecol. Evol. Syst. 47, 1–24 (2016). This paper is a comprehensive and well-written overview of the complex interactions between plant surfaces and the atmosphere.

    Article  Google Scholar 

  183. Lebeis, S. Greater than the sum of their parts: characterizing plant microbiomes at the community level. Curr. Opin. Plant Biol. 24, 82–86 (2015).

    Article  CAS  PubMed  Google Scholar 

  184. Morris, C. E. & Kinkel, L. L. in Phyllosphere Microbiology (eds Lindow, S. E., Hecht-Poinar, E. I. & Elliott, V. J.) 365–375 (APS Press, 2002).

  185. De Nys, R. et al. Broad spectrum effects of secondary metabolites from the red alga delisea pulchra in antifouling assays. Biofouling 8, 259–271 (1995).

    Article  Google Scholar 

  186. De Vos, W. Microbial biofilms and the human intestinal microbiome. NPJ Biofilms Microbiomes 1, 15005 (2015). This study explains why the human gut can be considered a biofilm.

    Article  PubMed  PubMed Central  Google Scholar 

  187. Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLOS Biol. 14, e1002533 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  188. Luckey, T. Introduction to intestinal microecology. Am. J. Clin. Nutr. 25, 1292–1294 (1972).

    Article  CAS  PubMed  Google Scholar 

  189. Ma, L. et al. Rapid quantification of bacteria and viruses in influent, settled water, activated sludge and effluent from a wastewater treatment plant using flow cytometry. Water Sci. Technol. 68, 1763–1769 (2013).

    Article  CAS  PubMed  Google Scholar 

  190. Mateo-Sagasta, J., Raschid-Sally, L. & Thebo, A. in Wastewater: Economic Asset in Urbanizing World (eds Drechsel, P., Qadir, M. & Wichelns, D.) 15–24 (Springer, Netherlands, 2015).

  191. Schultz, J. E. & Breznak, J. A. Heterotrophic bacteria present in hindguts of wood-eating Termites [Reticulitermes flavipes (Kollar)]. Appl. Environ. Microbiol. 35, 930–936 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  192. Brune, A. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12, 168–180 (2014).

    Article  CAS  PubMed  Google Scholar 

  193. ZoBell, C. The effect of solid surfaces upon bacterial activity. J. Bact. 46, 39–56 (1943).

    CAS  PubMed  Google Scholar 

  194. Marshall, K. C., Stout, R. & Mitchell, R. Mechanisms of the initial events in the sorption of marine bacteria to surfaces. J. Gen. Microbiol. 68, 337–348 (1971).

    Article  CAS  Google Scholar 

  195. Fletcher, M. M. & Floodgate, G. D. An electron-microscopic demonstration of an acidic polysaccahride involved in the adhesion of a marine bacterium to solid surfaces. J. Gen. Microbiol. 74, 325–334 (1973).

    Article  CAS  Google Scholar 

  196. Characklis, W. G. Attached microbial growths – I. Attachment and growth. Water Res. 7, 1113–1127 (1973).

    Article  CAS  Google Scholar 

  197. Geesey, G. G., Mutch, R. & Costerton, J. W. Sessile bacteria: an important component of the microbial population in small mountain streams. Limnol. Oceanogr. 23, 1214–1224 (1978). This paper introduces the view that biofilms are the place where most bacteria live.

    Article  CAS  Google Scholar 

  198. Corning, P. A. The re-emergence of “emergence”: a venerable concept in search of a theory. Complexity 7, 18–30 (2002).

    Article  Google Scholar 

  199. Characklis, W. G. & Wilderer, P. A. (eds) Structure and Function of Biofilms (John Wiley, New York, 1989).

  200. Characklis, W. G. & Marshall, K. C. (eds) Biofilms 3–15 (John Wiley & Sons, New York, NY, 1990).

  201. Vert, M. et al. Terminology for biorelated polymers and applications (IUPAC Recommendations 2012). Pure Appl. Chem. 84, 377–410 (2012).

    Article  CAS  Google Scholar 

  202. Fisk, M. R. et al. Evidence of biological activity in Hawaiian subsurface basalts. Geochem. Geophys. Geosyst. 4, 1103 (2003).

    Article  CAS  Google Scholar 

  203. Fry, J. C. et al. Prokaryotic populations and activities in an interbedded coal deposit, including a previously deeply buried section (1.6–2.3 km) above ~150 Ma basement rock. Geomicrobiol. J. 26, 163–178 (2009).

    Article  CAS  Google Scholar 

  204. United Nations. UN World Water Development Report 2017: Wastewater: the Untapped Resource. United Nations Educational, Scientific and Cultural Organization, Paris, France. http://www.unesco.org/new/en/natural-sciences/environment/water/wwap/wwdr/2017-wastewater-the-untapped-resource/ (2017).

Download references

Acknowledgements

Many colleagues responded to requests for bacterial numbers or were ready to discuss them, which was highly appreciated: A. Boetius, R. Colwell, A. Decho, R. Gerlach, R. Glud, B. B. Jørgensen, K. Kjeldsen, S. Kjelleberg, F. Lauro, H. Lesch, R. Meckenstock, L. Melo, L. A. Meyer-Reil, J. Parkes, K. Pedersen, H. Peter, P. Rettberg, B. Schink, U. Schreiber, S. Schuster, P. Stoodley, W. Streit, S. Swarup, U. Szewzyk, M. Vera, G. Wolfaardt, O. Wurl and, above all, J. Wingender. Special thanks to K. Peter for help with figure drafts. Furthermore, the authors are very thankful to the reviewers whose thorough work helped to improve this Analysis.

Reviewer information

Nature Reviews Microbiology thanks Y. M. Bar-On, R. Milo, P. Stoodley and I. Wagner-Döbler for their contribution to the peer review of this work.

Author information

Authors and Affiliations

Authors

Contributions

H.-C.F. did the data research and drafted the manuscript and figures; S.W. provided the idea to this work, substantially contributed to discussion of content and performed and edited the calculations.

Corresponding authors

Correspondence to Hans-Curt Flemming or Stefan Wuertz.

Ethics declarations

Competing interests

The authors declare no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Glossary

Basalt

The most common type of solidified lava; a fine-grained igneous rock.

Dike

A rock sheet formed in crevices and fractures of an already existing rock body.

Gabbroid rock

A compact, dark, coarse-grained magmatic rock, chemically equivalent to basalt, that forms when molten magma is trapped in the subsurface, slowly cools and forms a crystalline mass.

Gyre

A large system of circulating ocean currents, caused by the Coriolis effect, involved with large wind movements. The five most notable gyres are the Indian Ocean gyre, the North Atlantic gyre, the North Pacific gyre, the South Atlantic gyre and the South Pacific gyre.

Emergent properties

The characteristics of a community not identifiable by analysing the component organisms in isolation, including novel and coherent structures, patterns and properties arising during the process of self-organization in complex systems — the whole is more than the sum of its parts.

Substratum

A solid surface on which organisms adhere and grow.

Diagenesis

All processes that happen during the transformation of a sediment to its final lithification. It is a low-pressure, low-temperature process that can involve microbial biofilms, owing to their extracellular polymeric substances, as opposed to metamorphism, a rock alteration process that occurs at high temperatures and pressures.

Igneous

A type of crystalline rock that forms directly from the cooling of magma.

Serpentinization

The hydrothermal transformation of primary ferromagnesian minerals producing fluids rich in hydrogen and various secondary minerals. The hydrogen can reduce carbon dioxide and initiate an inorganic pathway for organic compounds.

Canterbury basin

The sedimentary basin around the South Island of New Zealand.

Stable isotope incubation

The exposure of microbial communities to stable isotopes (for example, 13C- or 15N-labelled glucose, pyruvate and amino acids) to determine the incorporation and thus the metabolic activity of microorganisms.

Nanometre-scale secondary ion mass spectroscopy

(Nano-SIMS). A type of imaging with secondary ion mass spectroscopy with nanoscopic-scale resolution.

CARD–FISH

Fluorescence in situ hybridization (FISH) with horseradish-peroxidase-labelled oligonucleotide probes and tyramide signal amplification, also known as catalysed reporter deposition (CARD).

Chasmoendoliths

Organisms growing in fissures of rocks.

Cryptoendoliths

Organisms growing in deep cavities or crevices within rock.

Euendoliths

Organisms growing in cracks and pits actively penetrating the mineral material.

Extracellular polymeric substances

(EPS). Mainly polysaccharides, proteins, nucleic acids and lipids; they provide the mechanical stability of biofilms, mediate adhesion to surfaces and form a cohesive, 3D polymer network that interconnects and transiently immobilizes biofilm cells. In addition, the biofilm matrix functions as an external digestive system by retaining extracellular enzymes in close proximity to the cells that solubilize colloidal and solid biopolymers and thus make them bioavailable.

Quorum sensing

The sensing of microbial population density. This mechanism can regulate gene expression in response to fluctuations of cell-population density. It is based on the production and release of small soluble molecules named ‘autoinducers’ because they act not only on other cells but also on the producing ones once a threshold concentration is reached.

Conchoidal breakage sites

The locations of breakages that are characteristic of the way in which brittle materials break or fracture if they do not follow any natural planes of separation. Quartz, flint, quartzite, jasper and other fine-grained or amorphous materials, such as pure silica, obsidian and window glass, are among the materials that break in this way.

Plastisphere

The microbial community of heterotrophs, autotrophs, predators and symbionts living on plastic debris in oceans, fresh water, soils and sediments.

Troposphere

The lowest and densest part of the atmosphere, which extends up to ~11 km in altitude. It is where most of the weather changes occur and where the vast majority of microbial and abiotic aerosols are found.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Flemming, HC., Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol 17, 247–260 (2019). https://doi.org/10.1038/s41579-019-0158-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-019-0158-9

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing