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  • Review Article
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Bacterial adhesion at the single-cell level

Abstract

The formation of multicellular microbial communities, called biofilms, starts from the adhesion of a few planktonic cells to the surface. The transition from a free-living planktonic lifestyle to a sessile, attached state is a multifactorial process that is determined by biological, chemical and physical properties of the environment, the surface and the bacterial cell. The initial weak, reversible interactions between a bacterium and a surface strengthen to yield irreversible adhesion. In this Review, we summarize our understanding of the mechanisms governing bacterial adhesion at the single-cell level, including the physical forces experienced by a cell before reaching the surface, the first contact with a surface and the transition from reversible to permanent adhesion.

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Fig. 1: The impact of flow and solid surfaces on bacterial swimming behaviours.
Fig. 2: Interactions between the surface and the bacterium.

Part Aa adapted with permission from Jeong, H. E., Kim, I., Karam, P., Choi, H. J. & Yang, P. Bacterial recognition of silicon nanowire arrays. Nano letters 13, 2864–2869 (2013). Copyright © 2013 American Chemical Society. Part Ab adapted with permission from Hochbaum, A. I. & Aizenberg, J. Bacteria pattern spontaneously on periodic nanostructure arrays. Nano letters 10, 3717–3721 (2010). Copyright © 2010 American Chemical Society. Part Ac adapted with permission from Díaz, C., Schilardi, P. L., Salvarezza, R. C. & Fernández Lorenzo de Mele, M. Nano/Microscale Order Affects the Early Stages of Biofilm Formation on Metal Surfaces. Langmuir 23, 11206–11210 (2007). Copyright © 2007 American Chemical Society. Parts Ad and Ae adapted with permission from Hizal, F. et al. Nanoengineered superhydrophobic surfaces of aluminum with extremely low bacterial adhesivity. ACS Appl Mat Interfaces 9, 12118–12129 (2017). Copyright © 2017 American Chemical Society.

Fig. 3: The transition from reversible to irreversible attachment.

Part Ba adapted from Ivanov, I. E. et al. Atomic force and super-resolution microscopy support a role for LapA as a cell-surface biofilm adhesin of Pseudomonas fluorescens. Res. Microbiol. (2012) 163, 685–691. Copyright © 2018 Elsevier Masson SAS. All rights reserved. Part Bb adapted with permission from ref.71, Elsevier. Image in part Bc courtesy of C. Berne, Indiana University, USA.

Fig. 4: Production of adhesins in response to surface contact.

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Acknowledgements

The authors thank the members of the Brun laboratory for critical reading of the manuscript. Work in the authors’ laboratory is supported by grants R01GM102841 and R35GM122556 from the National Institutes of Health (to Y.V.B.) and by National Science Foundation fellowship 1342962 (to C.K.E.).

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Nature Reviews Microbiology thanks Y. Dufrene, M. Parsek and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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C.B., C.K.E. and A.D. researched data for the article. Y.V.B., C.B. and C.K.E. made substantial contributions to discussions of the content. C.B. and C.K.E. wrote the article. Y.V.B., C.B. and C.K.E. reviewed and/or edited the manuscript before submission.

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Correspondence to Yves V. Brun.

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Glossary

Shear

The fluctuation developed by particles in movement relative to each other in a liquid environment, reflecting the motion between two adjacent layers of a liquid with flow.

Extracellular appendages

Filamentous structures that are present on the surface of bacteria, including flagella, pili and curli.

Flagella

Filamentous extracellular appendages that are responsible for the active movement of cells in a liquid environment. The bacterial flagellum is composed of three main substructures: the motor that uses proton motive force to generate the torque, the basal body and hook that anchor the flagellum filament to the cell membrane and transmit the motor torque and the flagellar filament, which is composed of flagellin proteins that are arranged in a long, thin filament and functions as a propeller.

Pili

Thin, extracellular protein fibres that are involved in various bacterial behaviours, including attachment, twitching motility, horizontal gene transfer and virulence.

Brownian motion

The continuous movement of micrometre-scale particles that are suspended in liquid as a result of random collisions with each other.

Chemotaxis

A sensing mechanism that enables bacteria to modify their swimming behaviour in the presence of a chemical gradient. Bacteria can sense and swim towards attractants or away from repellents.

Hydrodynamic effects

Different forces that are caused by a liquid in motion.

Psl exopolysaccharide

(Named after the polysaccharide locus). A polysaccharide that is composed of mannose, glucose, rhamnose and possibly galactose residues and is found on the surface of Pseudomonas aeruginosa cells. It is involved in cell–cell and cell–surface interactions, and it is a scaffolding molecule in the biofilm matrix.

cyclic di-GMP

(ci-di-GMP). A second messenger signalling molecule involved in the regulation of various bacterial behaviours, including motility, adhesion, cell cycle progression and virulence.

Stringent response

A stress response in bacteria, whereby starvation induces the production of the small molecule guanosine tetraphosphate and pentaphosphate ((p)ppGpp), which leads to the rapid transcriptional changes and growth arrest.

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Berne, C., Ellison, C.K., Ducret, A. et al. Bacterial adhesion at the single-cell level. Nat Rev Microbiol 16, 616–627 (2018). https://doi.org/10.1038/s41579-018-0057-5

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