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Journal ArticleDOI

Regulation of flagellar motility during biofilm formation

01 Nov 2013-Fems Microbiology Reviews (NIH Public Access)-Vol. 37, Iss: 6, pp 849-871
TL;DR: The regulation of motility during biofilm formation in Bacillus, Pseudomonas, Vibrio, and Escherichia is reviewed, and it is concluded that the motility-to-biofilm transition, if necessary, likely involves two steps.
Abstract: Many bacteria swim in liquid or swarm over solid surfaces by synthesizing rotary flagella The same bacteria that are motile also commonly form nonmotile multicellular aggregates called biofilms Biofilms are an important part of the lifestyle of pathogenic bacteria, and it is assumed that there is a motility-to-biofilm transition wherein the inhibition of motility promotes biofilm formation The transition is largely inferred from regulatory mutants that reveal the opposite regulation of the two phenotypes Here, we review the regulation of motility during biofilm formation in Bacillus, Pseudomonas, Vibrio, and Escherichia, and we conclude that the motility-to-biofilm transition, if necessary, likely involves two steps In the short term, flagella are functionally regulated to either inhibit rotation or modulate the basal flagellar reversal frequency Over the long term, flagellar gene transcription is inhibited and in the absence of de novo synthesis, flagella are diluted to extinction through growth Both short-term and long-term motility inhibition is likely important to stabilize cell aggregates and optimize resource investment We emphasize the newly discovered flagellar functional regulators and speculate that others await discovery in the context of biofilm formation
Citations
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Journal ArticleDOI
TL;DR: The events involved in bacterial biofilm formation are described, the negative and positive aspects associated with bacterial biofilms are listed, the main strategies currently used to regulate establishment of harmful bacterial bioFilms are elaborated as well as certain strategies employed to encourage formation of beneficial bacterialBiofilms.
Abstract: Bacterial biofilms are complex surface attached communities of bacteria held together by self-produced polymer matrixs mainly composed of polysaccharides, secreted proteins, and extracellular DNAs. Bacterial biofilm formation is a complex process and can be described in five main phases: (i) reversible attachment phase, where bacteria non-specifically attach to surfaces; (ii) irreversible attachment phase, which involves interaction between bacterial cells and a surface using bacterial adhesins such as fimbriae and lipopolysaccharide (LPS); (iii) production of extracellular polymeric substances (EPS) by the resident bacterial cells; (iv) biofilm maturation phase, in which bacterial cells synthesize and release signaling molecules to sense the presence of each other, conducing to the formation of microcolony and maturation of biofilms; and (v) dispersal/detachment phase, where the bacterial cells depart biofilms and comeback to independent planktonic lifestyle. Biofilm formation is detrimental in healthcare, drinking water distribution systems, food, and marine industries, etc. As a result, current studies have been focused toward control and prevention of biofilms. In an effort to get rid of harmful biofilms, various techniques and approaches have been employed that interfere with bacterial attachment, bacterial communication systems (quorum sensing, QS), and biofilm matrixs. Biofilms, however, also offer beneficial roles in a variety of fields including applications in plant protection, bioremediation, wastewater treatment, and corrosion inhibition amongst others. Development of beneficial biofilms can be promoted through manipulation of adhesion surfaces, QS and environmental conditions. This review describes the events involved in bacterial biofilm formation, lists the negative and positive aspects associated with bacterial biofilms, elaborates the main strategies currently used to regulate establishment of harmful bacterial biofilms as well as certain strategies employed to encourage formation of beneficial bacterial biofilms, and highlights the future perspectives of bacterial biofilms.

306 citations

Journal ArticleDOI
TL;DR: This review explores six bacterial species as models of flagellar mechanosensing of surfaces to understand the current state of the authors' knowledge and the challenges that lie ahead.

304 citations

Journal ArticleDOI
TL;DR: The bacterial flagellum is an amazingly complex molecular machine with a diversity of roles in pathogenesis including reaching the optimal host site, colonization or invasion, maintenance at the infection site, and post- infected dispersal.

250 citations


Cites background from "Regulation of flagellar motility du..."

  • ...V. cholerae and P. aeruginosa also involve cyclic di-GMP in flagellar motor 319 regulation during biofilm formation and all four systems have been reviewed recently 320 (Guttenplan and Kearns, 2013)....

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  • ...The study of flagellar involvement in biofilm 337 formation is an active research area and several model systems, including Bacillus subtilis, E. 338 coli, P. aeruginosa, V. cholerae and V. parahaemolyticus are being studied and have been 339 recently reviewed (Guttenplan and Kearns, 2013)....

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01 Jan 2012
TL;DR: In this article, BslA (formerly YuaB) was identified as a major contributor to the surface repellency of Bacillus subtilis biofilms, which probably explains the broad-spectrum resistance of the bacteria in these bio-films to antimicrobial agents.
Abstract: Biofilms are surface‐associated bacterial aggregates, in which bacteria are enveloped by polymeric substances known as the biofilm matrix. Bacillus subtilis biofilms display persistent resistance to liquid wetting and gas penetration, which probably explains the broad‐spectrum resistance of the bacteria in these biofilms to antimicrobial agents. In this study, BslA (formerly YuaB) was identified as a major contributor to the surface repellency of B. subtilis biofilms. Disruption of bslA resulted in the loss of surface repellency and altered the biofilm surface microstructure. BslA localized to the biofilm matrix in an exopolysaccharide‐dependent manner. Purified BslA exhibited amphiphilic properties and formed polymers in response to increases in the area of the air–water interface in vitro. Genetic and biochemical analyses showed that the self‐polymerization activity of BslA was essential for its ability to localize to the biofilm matrix. Confocal laser scanning microscopy showed that BslA formed a layer on the biofilm surface. Taken together, we propose that BslA, standing for biofilm‐surface layer protein, is responsible for the hydrophobic layer on the surface of biofilms.

199 citations

Journal ArticleDOI
TL;DR: A review of recent advances in structural biology, cryo-electron tomography, molecular genetics, in vivo imaging, bioinformatics and biophysics aims to integrate these new findings into current knowledge of the evolution, function, regulation and dynamics of the T3SS.
Abstract: The flagellum and the injectisome are two of the most complex and fascinating bacterial nanomachines. At their core, they share a type III secretion system (T3SS), a transmembrane export complex that forms the extracellular appendages, the flagellar filament and the injectisome needle. Recent advances, combining structural biology, cryo-electron tomography, molecular genetics, in vivo imaging, bioinformatics and biophysics, have greatly increased our understanding of the T3SS, especially the structure of its transmembrane and cytosolic components, the transcriptional, post-transcriptional and functional regulation and the remarkable adaptivity of the system. This review aims to integrate these new findings into our current knowledge of the evolution, function, regulation and dynamics of the T3SS, and to highlight commonalities and differences between the two systems, as well as their potential applications.

173 citations

References
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Journal ArticleDOI
TL;DR: The functions, properties and constituents of the EPS matrix that make biofilms the most successful forms of life on earth are described.
Abstract: The microorganisms in biofilms live in a self-produced matrix of hydrated extracellular polymeric substances (EPS) that form their immediate environment. EPS are mainly polysaccharides, proteins, nucleic acids and lipids; they provide the mechanical stability of biofilms, mediate their adhesion to surfaces and form a cohesive, three-dimensional polymer network that interconnects and transiently immobilizes biofilm cells. In addition, the biofilm matrix acts as an external digestive system by keeping extracellular enzymes close to the cells, enabling them to metabolize dissolved, colloidal and solid biopolymers. Here we describe the functions, properties and constituents of the EPS matrix that make biofilms the most successful forms of life on earth.

7,041 citations

Journal ArticleDOI
TL;DR: It is evident that biofilm formation is an ancient and integral component of the prokaryotic life cycle, and is a key factor for survival in diverse environments.
Abstract: Biofilms--matrix-enclosed microbial accretions that adhere to biological or non-biological surfaces--represent a significant and incompletely understood mode of growth for bacteria. Biofilm formation appears early in the fossil record (approximately 3.25 billion years ago) and is common throughout a diverse range of organisms in both the Archaea and Bacteria lineages, including the 'living fossils' in the most deeply dividing branches of the phylogenetic tree. It is evident that biofilm formation is an ancient and integral component of the prokaryotic life cycle, and is a key factor for survival in diverse environments. Recent advances show that biofilms are structurally complex, dynamic systems with attributes of both primordial multicellular organisms and multifaceted ecosystems. Biofilm formation represents a protected mode of growth that allows cells to survive in hostile environments and also disperse to colonize new niches. The implications of these survival and propagative mechanisms in the context of both the natural environment and infectious diseases are discussed in this review.

6,170 citations

Journal ArticleDOI
TL;DR: The results reviewed in this article indicate that the formation of biofilms serves as a new model system for the study of microbial development.
Abstract: ▪ Abstract Biofilms can be defined as communities of microorganisms attached to a surface. It is clear that microorganisms undergo profound changes during their transition from planktonic (free-swimming) organisms to cells that are part of a complex, surface-attached community. These changes are reflected in the new phenotypic characteristics developed by biofilm bacteria and occur in response to a variety of environmental signals. Recent genetic and molecular approaches used to study bacterial and fungal biofilms have identified genes and regulatory circuits important for initial cell-surface interactions, biofilm maturation, and the return of biofilm microorganisms to a planktonic mode of growth. Studies to date suggest that the planktonic-biofilm transition is a complex and highly regulated process. The results reviewed in this article indicate that the formation of biofilms serves as a new model system for the study of microbial development.

3,321 citations


"Regulation of flagellar motility du..." refers background in this paper

  • ...Biofilms are multicellular aggregates of bacteria bound by a matrix of extracellular polymers (O’Toole et al., 2000; Kolter & Greenberg, 2006; Monds & O’Toole, 2009)....

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Journal ArticleDOI
TL;DR: The isolation and characterization of mutants of Pseudomonas aeruginosa PA14 defective in the initiation of biofilm formation on an abiotic surface, polyvinylchloride (PVC) plastic are reported and evidence that microcolonies form by aggregation of cells present in the monolayer is presented.
Abstract: The formation of complex bacterial communities known as biofilms begins with the interaction of planktonic cells with a surface in response to appropriate environmental signals. We report the isolation and characterization of mutants of Pseudomonas aeruginosa PA14 defective in the initiation of biofilm formation on an abiotic surface, polyvinylchloride (PVC) plastic. These mutants are designated surface attachment defective (sad ). Two classes of sad mutants were analysed: (i) mutants defective in flagellar-mediated motility and (ii) mutants defective in biogenesis of the polar-localized type IV pili. We followed the development of the biofilm formed by the wild type over 8 h using phase-contrast microscopy. The wild-type strain first formed a monolayer of cells on the abiotic surface, followed by the appearance of microcolonies that were dispersed throughout the monolayer of cells. Using time-lapse microscopy, we present evidence that microcolonies form by aggregation of cells present in the monolayer. As observed with the wild type, strains with mutations in genes required for the synthesis of type IV pili formed a monolayer of cells on the PVC plastic. However, in contrast to the wild-type strain, the type IV pili mutants did not develop microcolonies over the course of the experiments, suggesting that these structures play an important role in microcolony formation. Very few cells of a non-motile strain (carrying a mutation in flgK) attached to PVC even after 8 h of incubation, suggesting a role for flagella and/or motility in the initial cell-to-surface interactions. The phenotype of these mutants thus allows us to initiate the dissection of the developmental pathway leading to biofilm formation.

2,712 citations


"Regulation of flagellar motility du..." refers background in this paper

  • ...Prigent-Combaret et al. (1999) found that cells in a biofilm decrease expression of the flagella filament, fliC....

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