Key Points
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Bacterial biofilms can be considered to be an emergent form of bacterial life, in which communal life is completely different from bacteria that live as free-living cells.
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Emergent properties of bacterial biofilms include social cooperation, resource capture and enhanced survival following exposure to antimicrobials, and cannot be understood and predicted through the study of free-living bacterial cells.
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The physical scaffold of biofilm life is the matrix of extracellular polymeric substances (EPS) that keeps cells in the biofilm together and attaches them to substrata when colonizing surfaces. The matrix underlies the emergent properties of biofilms.
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The emergent properties of the biofilm are the reason for the evolutionary success of biofilms and underlie the role of biofilms as global habitat formers.
Abstract
Bacterial biofilms are formed by communities that are embedded in a self-produced matrix of extracellular polymeric substances (EPS). Importantly, bacteria in biofilms exhibit a set of 'emergent properties' that differ substantially from free-living bacterial cells. In this Review, we consider the fundamental role of the biofilm matrix in establishing the emergent properties of biofilms, describing how the characteristic features of biofilms — such as social cooperation, resource capture and enhanced survival of exposure to antimicrobials — all rely on the structural and functional properties of the matrix. Finally, we highlight the value of an ecological perspective in the study of the emergent properties of biofilms, which enables an appreciation of the ecological success of biofilms as habitat formers and, more generally, as a bacterial lifestyle.
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Acknowledgements
H.-C.F., S.K., S.R. and P.S. gratefully acknowledge the influence of the inspiring and motivating atmosphere during the Singapore Centre on Environmental Life Sciences Engineering (SCELSE) Summer Course while preparing this Review article. The authors thank J. Froesler for assistance with the figures. H.-C.F. appreciates the long-term support of the IWW Water Centre (Muelheim, Germany) to his work, and the support of P. Wilderer, his first mentor. The authors also thank SCELSE for supporting this work.
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Glossary
- Grazing
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A form of predation, such as when protozoa feed on bacteria.
- Macrophytes
-
Aquatic photosynthetic organisms that are visible to the naked eye. In marine systems, 'macrophytes' is often used as a general term that includes macroalgae, such as kelps, and coastal plants, such as seagrasses or mangroves.
- Bromeliads
-
A family of flowering plants that has leaves that often form in such a way so as to enable the persistence of pools of water that form distinct habitats and ecological communities.
- Microrheology
-
The study of the rheological properties of a material at the micrometre scale.
- Desiccation tolerance
-
The ability to survive water limitation.
- Nanowires
-
Electrically conductive structures that are produced by microorganisms.
- Rheologocial
-
Pertaining to the study of the flow of matter, primarily in a liquid state but also as 'soft solids' or solids under conditions in which they respond to an applied force with plastic flow rather than elastic deformation.
- Ecomechanics
-
The biomechanical mechanisms by which organisms interact with their environment.
- Electrogenic
-
Capable of generating an electric current.
- Microbial mats
-
A coherent, layered organization of microorganisms with complementary metabolic capacities. Microbial mats are typically found in aquatic environments, anchored to a surface.
- Mass transfer
-
The net movement of compounds or chemical species from one position to another.
- Streamers
-
Portions of the biofilm extracellular polymeric substances (EPS) that extend out from the biofilm surface into the liquid flow.
- Sorption
-
Adsorption or absorption, or a combination of both processes.
- Oligotrophic
-
An environment that is characterized by low nutrient concentrations.
- Lithification
-
A process in which sediments compact under pressure and gradually become solid rock. The biogenesis of carbonate can support this process.
- Activated sludge
-
The microbial biomass in the aerobic portion of a wastewater treatment system.
- Carbon cloth
-
A soft, flexible cloth-like material made from carbon fibre.
- Planktonic cells
-
Free-living cells (that is, not in a biofilm) in the liquid phase.
- Humic substances
-
The combination of compounds, generally humic acids, that make up the organic components of soils, peat and coal.
- Molecular modelling
-
Methods that encompass theoretical methods and computational techniques that are used to model or mimic the behaviour of molecules.
- Copiotrophic
-
An environment that is characterized by high nutrient concentrations.
- Heterotrophic
-
Refers to the use of organic compounds for nutrition.
- Type VI secretion systems
-
Multiprotein complexes that use a one-step mechanism to inject effector proteins, such as virulence factors, from the interior of a bacterial cell into a target cell. These systems have been found in a quarter of all proteobacterial genomes, including those that encode animal, plant and human pathogens, as well as soil, environmental and marine bacteria.
- Aminoglycosides
-
A class of antibiotics that typically have a cyclohexane ring and amino sugars.
- Stationary phase
-
A slow or non-growth phase of the bacterial growth cycle that typically results from a lack of electron donors or acceptors.
- Viable-but-nonculturable state
-
(VBNC state). A state of dormancy that is defined by failure of an organism to be cultured on media that normally supports its growth, while retaining measurable indications of viability, such as respiratory activity, the presence of rRNA and integrity of the cell membrane.
- Plasmid conjugation
-
The transfer of a specialized type of plasmid from one cell to another by a pilus that is encoded within the plasmid genome.
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Flemming, HC., Wingender, J., Szewzyk, U. et al. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14, 563–575 (2016). https://doi.org/10.1038/nrmicro.2016.94
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DOI: https://doi.org/10.1038/nrmicro.2016.94
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