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.

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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.

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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.

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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.

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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.

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Correspondence to Hans-Curt Flemming or Stefan Wuertz.

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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.

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Flemming, H., 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

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