Redox-driven regulation of microbial community morphogenesis

Okegbe, Chinweike; Price-Whelan, Alexa; Dietrich, Lars E. P.

doi:10.1016/j.mib.2014.01.006

Cited by 70 publications

(70 citation statements)

References 51 publications

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“…Furthermore, the availability of electron acceptors, including oxygen, can drive structuring of biofilm morphology, as has been shown for Pseudomonas aeruginosa (35,36). Therefore, these findings expand the role that oxygen gradients can play in biofilm formation by highlighting an ability to modulate protein function.…”

Section: (31)supporting

confidence: 58%

Bifunctionality of a biofilm matrix protein controlled by redox state

Arnaouteli

Ferreira

Schor

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Biofilms are communities of microbial cells that are encapsulated within a self-produced polymeric matrix. The matrix is critical to the success of biofilms in diverse habitats; however, many details of the composition, structure, and function remain enigmatic. Biofilms formed by the Gram-positive bacteriumBacillus subtilisdepend on the production of the secreted film-forming protein BslA. Here, we show that a gradient of electron acceptor availability through the depth of the biofilm gives rise to two distinct functional roles for BslA and that these roles can be genetically separated through targeted amino acid substitutions. We establish that monomeric BslA is necessary and sufficient to give rise to complex biofilm architecture, whereas dimerization of BslA is required to render the community hydrophobic. Dimerization of BslA, mediated by disulfide bond formation, depends on two conserved cysteine residues located in the C-terminal region. Our findings demonstrate that bacteria have evolved multiple uses for limited elements in the matrix, allowing for alternative responses in a complex, changing environment.

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Section: (31)supporting

confidence: 58%

Bifunctionality of a biofilm matrix protein controlled by redox state

Arnaouteli

Ferreira

Schor

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In both of these systems, Pel has the effect of increasing O 2 availability, although the physical basis of this effect differs in the two regimes. In colonies, increased access to O 2 results from the increased colony surface area of a wrinkled morphology compared to a smooth one, which exposes a higher proportion of resident cells to the atmosphere (49). In pellicles, increased access to O 2 is achieved because the formation of the floating biofilm retains cells at the air-liquid interface in physical proximity to the atmosphere.…”

Section: Discussionmentioning

confidence: 99%

Facultative Control of Matrix Production Optimizes Competitive Fitness in Pseudomonas aeruginosa PA14 Biofilm Models

Madsen

Lin

Squyres

et al. 2015

Appl Environ Microbiol

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cAs biofilms grow, resident cells inevitably face the challenge of resource limitation. In the opportunistic pathogen Pseudomonas aeruginosa PA14, electron acceptor availability affects matrix production and, as a result, biofilm morphogenesis. The secreted matrix polysaccharide Pel is required for pellicle formation and for colony wrinkling, two activities that promote access to O 2 . We examined the exploitability and evolvability of Pel production at the air-liquid interface (during pellicle formation) and on solid surfaces (during colony formation). Although Pel contributes to the developmental response to electron acceptor limitation in both biofilm formation regimes, we found variation in the exploitability of its production and necessity for competitive fitness between the two systems. The wild type showed a competitive advantage against a non-Pel-producing mutant in pellicles but no advantage in colonies. Adaptation to the pellicle environment selected for mutants with a competitive advantage against the wild type in pellicles but also caused a severe disadvantage in colonies, even in wrinkled colony centers. Evolution in the colony center produced divergent phenotypes, while adaptation to the colony edge produced mutants with clear competitive advantages against the wild type in this O 2 -replete niche. In general, the structurally heterogeneous colony environment promoted more diversification than the more homogeneous pellicle. These results suggest that the role of Pel in community structure formation in response to electron acceptor limitation is unique to specific biofilm models and that the facultative control of Pel production is required for PA14 to maintain optimum benefit in different types of communities. Most bacteria form multicellular communities called biofilms by producing and encasing themselves in matrices of secreted polymers (1). The National Institutes of Health has estimated that more than half of all bacterial infections involve such biofilm formation, a feature that complicates treatment due to a variety of associated mechanisms that confer increased antibiotic resistance and tolerance in these communities (2). Steep chemical gradients that form within cellular aggregates give rise to microenvironmental heterogeneity; consequently, cells in biofilms exist in diverse physiological states, at least some of which are unique to this lifestyle. For example, in the opportunistic pathogen Pseudomonas aeruginosa PA14, some genes expressed specifically in biofilms are critical for the establishment of lung infections in a mouse model (3). A better understanding of the physiology of biofilm development is required for rational approaches to new therapies for many types of bacterial infections.Using a colony biofilm model, we have found that a primary factor influencing P. aeruginosa PA14 community morphology is the availability of electron acceptors (4-6). As colonies increase in thickness, the formation of O 2 gradients renders the community anoxic at depth and leads to an increase in intr...

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“…For instance, when motile bacteria, such as Escherichia coli, adhere to a substratum (33,82,83), motility ceases, cell multiplication continues (84)(85)(86)(87), and early biofilm-related genes are upregulated, including those that encode additional adhesins (88)(89)(90). Although Karatan and Watnick (91) suggested that bacteria at this point can form either an adherent monolayer biofilm or a multilayer biofilm, the former is not sufficient to encompass some of the main characteristics of a complex biofilm, most notably the formation of ECM and a three-dimensional, controlled microenvironment that facilitates biofilm growth, nutrient acquisition, control of gas and pH, and cell-cell signaling (92)(93)(94)(95)(96)(97). It therefore may not be legitimate to consider an adhering cell monolayer lacking ECM a bona fide biofilm.…”

Section: Defining a C Albicans Biofilm: Lessons From Bacteriamentioning

confidence: 99%

Plasticity of Candida albicans Biofilms

Soll

Daniels

2016

Microbiol Mol Biol Rev

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SUMMARYCandida albicans, the most pervasive fungal pathogen that colonizes humans, forms biofilms that are architecturally complex. They consist of a basal yeast cell polylayer and an upper region of hyphae encapsulated in extracellular matrix. However, biofilms formedin vitrovary as a result of the different conditions employed in models, the methods used to assess biofilm formation, strain differences, and, in a most dramatic fashion, the configuration of the mating type locus (MTL). Therefore, integrating data from different studies can lead to problems of interpretation if such variability is not taken into account. Here we review the conditions and factors that cause biofilm variation, with the goal of engendering awareness that more attention must be paid to the strains employed, the methods used to assess biofilm development, every aspect of the model employed, and the configuration of theMTLlocus. We end by posing a set of questions that may be asked in comparing the results of different studies and developing protocols for new ones. This review should engender the notion that not all biofilms are created equal.

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Redox-driven regulation of microbial community morphogenesis

Cited by 70 publications

References 51 publications

Bifunctionality of a biofilm matrix protein controlled by redox state

Bifunctionality of a biofilm matrix protein controlled by redox state

Facultative Control of Matrix Production Optimizes Competitive Fitness in Pseudomonas aeruginosa PA14 Biofilm Models

Plasticity of Candida albicans Biofilms

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