The putative oligosaccharide translocase SypK connects biofilm formation with quorum signaling in
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              <scp>V</scp>
              ibrio fischeri
            </i>

Miyashiro, Tim; Oehlert, Dane; Ray, Valerie A.; Visick, Karen L.; Ruby, Edward G.

doi:10.1002/mbo3.199

Cited by 21 publications

(19 citation statements)

References 57 publications

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“…Bioluminescence assays were performed in LBS medium, as previously reported (23), with the following slight modifications. Each strain was grown in the presence or absence of 120 nM (final concentration) 3-oxo-C 6 HSL, and measurements were taken when the cultures were at an optical density at 600 nm (OD 600 ) of ϳ1.0.…”

Section: Methodsmentioning

confidence: 99%

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Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Sun

LaSota

Cecere

et al. 2016

Appl Environ Microbiol

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Animal development and physiology depend on beneficial interactions with microbial symbionts. In many cases, the microbial symbionts are horizontally transmitted among hosts, thereby making the acquisition of these microbes from the environment an important event within the life history of each host. The light organ symbiosis established between the Hawaiian squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri is a model system for examining how hosts acquire horizontally transmitted microbial symbionts. Recent studies have revealed that the light organ of wild-caught E. scolopes squid contains polyclonal populations of V. fischeri bacteria; however, the function and development of such strain diversity in the symbiosis are unknown. Here, we report our phenotypic and phylogenetic characterizations of FQ-A001, which is a V. fischeri strain isolated directly from the light organ of an E. scolopes individual. Relative to the type strain ES114, FQ-A001 exhibits similar growth in rich medium but displays increased bioluminescence and decreased motility in soft agar. FQ-A001 outcompetes ES114 in colonizing the crypt spaces of the light organs. Remarkably, we find that animals cocolonized with FQ-A001 and ES114 harbor singly colonized crypts, in contrast to the cocolonized crypts observed from competition experiments involving single genotypes. The results with our two-strain system suggest that strain diversity within the squid light organ is a consequence of diversity in the single-strain colonization of individual crypt spaces. IMPORTANCEThe developmental programs and overall physiologies of most animals depend on diverse microbial symbionts that are acquired from the environment. However, the basic principles underlying how microbes colonize their hosts remain poorly understood. Here, we report our findings of bacterial strain competition within the coevolved animal-microbe symbiosis composed of the Hawaiian squid and bioluminescent bacterium Vibrio fischeri. Using fluorescent proteins to differentially label two distinct V. fischeri strains, we find that the strains are unable to coexist in the same niche within the host. Our results suggest that strain competition for distinct colonization sites dictates the strain diversity associated with the host. Our study provides a platform for studying how strain diversity develops within a host. Microbes directly contribute to the physiology, development, and evolution of metazoans (1). Many metazoan-microbe symbioses are established through horizontal transmission, i.e., animals acquire microbial symbionts from their environment (2). Coevolution of host-microbe pairs can result in genetic factors that promote remarkably high specificity between the partners, thereby assisting in the acquisition of symbionts from typically unpredictable environments (3). An important but understudied topic in coevolved metazoan-microbe symbioses is how strain diversity impacts the establishment of these associations.A particularly powerful model system to explo...

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Section: Methodsmentioning

confidence: 99%

“…Fluorescence assays to measure luxI gene expression were performed with liquid cultures, as previously reported (23), with the following slight modifications. Overnight LBS cultures were diluted 1:100 into LBS medium in the presence or absence of 120 nM (final concentration) 3-oxo-C 6 HSL (Sigma-Aldrich, St. Louis, MO, USA).…”

Section: Methodsmentioning

confidence: 99%

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Sun

LaSota

Cecere

et al. 2016

Appl Environ Microbiol

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“…V. fischeri harbors three distinct QS systems (i.e., AinS/AinR, LuxI/LuxR, and LuxS/LuxPQ); however, only the AinS/AinR system is involved in the modulation of the initial steps of surface colonization, and only the AinS/AinR and LuxS/LuxPQ systems are involved in the modulation of subsequent biofilm development (418,419). V. cholerae harbors four distinct QS systems (i.e., CqsA/CqsS, LuxS/ LuxPQ, CqsR, and VpsS), and they all participate in the modulation of surface colonization and biofilm formation (420).…”

Section: Microbial Quorum Sensingmentioning

confidence: 99%

Microbial Surface Colonization and Biofilm Development in Marine Environments

Dang

Lovell

2016

Microbiol Mol Biol Rev

870

636

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SUMMARYBiotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.

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“…S4B). While previous links have been established between bioluminescence and biofilm formation in V. fischeri (48,49), the fact that the bmp and bal genes appear to comprise an operon yet affect diverse cellular functions was surprising. Furthermore, the impact of the bal genes on luminescence was observed in the absence of sypG (or rscS) overexpression, suggesting that either the level of basal transcription from the SypG-dependent bmp promoter is sufficient for bal expression or there is a second promoter that drives bal expression.…”

Section: Discussionmentioning

confidence: 98%

Identification of a Novel Matrix Protein That Promotes Biofilm Maturation in Vibrio fischeri

Ray¹,

Driks²,

Visick³

2014

J. Bacteriol.

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Bacteria form communities, termed biofilms, in which cells adhere to each other within a matrix, typically comprised of polysaccharides, proteins, and extracellular DNA. Biofilm formation by the marine bacterium Vibrio fischeri requires the Syp polysaccharide, but the involvement of matrix proteins is as yet unknown. Here we identified three genes, termed bmpA, -B, and -C (biofilm maturation protein), with overlapping functions in biofilm maturation. A triple bmpABC mutant, but not single or double mutants, was defective in producing wrinkled colonies, a form of biofilm. Surprisingly, the triple mutant was competent to form pellicles, another biofilm phenotype, but they generally lacked a three-dimensional architecture. Transmission electron microscopy revealed that the extracellular matrix of the bmp mutant contained electron-dense, thread-like structures that were also present in the wild type but lacking in syp mutant strains. We hypothesized that the bmp mutant produces the Syp polysaccharide but fails to produce/export a distinct matrix component. Indeed, a mixture of the bmp and syp mutants produced a wrinkled colony. Finally, BmpA could be detected in cell-free supernatants from disrupted pellicles. Thus, this work identifies a new matrix protein necessary for biofilm maturation by V. fischeri and, based on the conservation of bmp, potentially other microbes. Bacteria can be found as planktonic cells or within sessile communities called biofilms, which are composed of bacterial cells encased in an extracellular matrix (1-3). The matrix is generally self-produced and comprised of polysaccharides, proteins, extracellular DNA, and other bacterial products, such as outer membrane vesicles (OMVs). These matrix components promote adherence of the bacteria to each other and to a variety of surfaces, including host tissues and medical devices, such as catheters (reviewed in reference 4). Furthermore, due at least in part to the protective nature of the matrix, resident cells exhibit increased resistance to predation (5), desiccation (6), host defenses (4), and antibiotics (7). While much is known about the process of biofilm formation and its regulation from the study of a variety of bacteria, we still know little about the constituents of the matrix, in particular the matrix proteins, and their contributions to biofilm formation.Matrix proteins can be anchored to or associated with the cell surface or released into the extracellular space, where they appear to promote cell-matrix, cell-cell, matrix-matrix, and cell-surface interactions. For example, in Pseudomonas aeruginosa, the matrix protein CdrA is both cell associated and secreted and likely promotes cell-matrix and matrix-matrix interactions by binding to the Psl polysaccharide (8), which itself is cell associated and secreted (9). Additionally, the lectins LecA, specific for D-galactose (10), and LecB, specific for L-fucose (11), are thought to promote cell-cell interactions (12) during P. aeruginosa biofilm formation.Perhaps the most is known about the r...

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The putative oligosaccharide translocase SypK connects biofilm formation with quorum signaling in V ibrio fischeri

Cited by 21 publications

References 57 publications

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Microbial Surface Colonization and Biofilm Development in Marine Environments

Identification of a Novel Matrix Protein That Promotes Biofilm Maturation in Vibrio fischeri

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