The Novel Sigma Factor-Like Regulator RpoQ Controls Luminescence, Chitinase Activity, and Motility in Vibrio fischeri

Cao, Xiaodan; Studer, Sarah; Wassarman, Karen M.; Zhang, Yuanxing; Ruby, Edward G.; Miyashiro, Tim

doi:10.1128/mbio.00285-11

Cited by 36 publications

(40 citation statements)

References 66 publications

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“…These are annotated as putative lipoproteins, response regulators, a sigma factor, and an antisigma factor antagonist (40). The sigma factor RpoQ (VSAL_II0319) was recently described in V. fischeri and found to be regulated by QS (53). Of the Vibrionaceae, only V. salmonicida and V. fischeri encode this sigma factor, and in both species LitR positively regulates rpoQ expression.…”

Section: Discussionmentioning

confidence: 99%

LitR Is a Repressor of syp Genes and Has a Temperature-Sensitive Regulatory Effect on Biofilm Formation and Colony Morphology in Vibrio (Aliivibrio) salmonicida

Hansen

Bjelland

Ronessen

et al. 2014

Appl Environ Microbiol

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c Vibrio (Aliivibrio) salmonicida is the etiological agent of cold water vibriosis, a disease in farmed Atlantic salmon (Salmo salar) that is kept under control due to an effective vaccine. A seawater temperature below 12°C is normally required for disease development. Quorum sensing (QS) is a cell density-regulated communication system that bacteria use to coordinate activities involved in colonization and pathogenesis, and we have previously shown that inactivation of the QS master regulator LitR attenuates the V. salmonicida strain LFI1238 in a fish model. We show here that strain LFI1238 and a panel of naturally occurring V. salmonicida strains are poor biofilm producers. Inactivation of litR in the LFI1238 strain enhances medium-and temperaturedependent adhesion, rugose colony morphology, and biofilm formation. Chemical treatment and electron microscopy of the biofilm identified an extracellular matrix consisting mainly of a fibrous network, proteins, and polysaccharides. Further, by microarray analysis of planktonic and biofilm cells, we identified a number of genes regulated by LitR and, among these, were homologues of the Vibrio fischeri symbiosis polysaccharide (syp) genes. The syp genes were regulated by LitR in both planktonic and biofilm lifestyle analyses. Disruption of syp genes in the V. salmonicida ⌬litR mutant alleviated adhesion, rugose colony morphology, and biofilm formation. Hence, LitR is a repressor of syp transcription that is necessary for expression of the phenotypes examined. The regulatory effect of LitR on colony morphology and biofilm formation is temperature sensitive and weak or absent at temperatures above the bacterium's upper threshold for pathogenicity.

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Section: Discussionmentioning

confidence: 99%

LitR Is a Repressor of syp Genes and Has a Temperature-Sensitive Regulatory Effect on Biofilm Formation and Colony Morphology in Vibrio (Aliivibrio) salmonicida

Hansen

Bjelland

Ronessen

et al. 2014

Appl Environ Microbiol

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“…Sequential and multitiered quorum sensing regulatory networks have been described for several proteobacterial strains, including Vibrio fischeri, in which quorum sensing is used to modulate intermediate and late symbiotic colonization of the Euprymna scolopes light organ and bioluminescence (12,17,65,66). V. fischeri has two AHL-based quorum sensing systems that synthesize different AHLs at different stages of squid colonization (12,17,65).…”

Section: Discussionmentioning

confidence: 99%

“…V. fischeri has two AHL-based quorum sensing systems that synthesize different AHLs at different stages of squid colonization (12,17,65). Moreover, it has been shown that the response regulator that directly controls bioluminescence (LuxR) can respond to the two AHLs at different binding efficiencies, thus inducing bioluminescence at different cell densities and stages of colonization (67,68).…”

Section: Discussionmentioning

confidence: 99%

Phaeobacter sp. Strain Y4I Utilizes Two Separate Cell-to-Cell Communication Systems To Regulate Production of the Antimicrobial Indigoidine

Cude

Prevatte

Hadden

et al. 2015

Appl Environ Microbiol

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The marine roseobacter Phaeobacter sp. strain Y4I synthesizes the blue antimicrobial secondary metabolite indigoidine when grown in a biofilm or on agar plates. Prior studies suggested that indigoidine production may be, in part, regulated by cell-to-cell communication systems. Phaeobacter sp. strain Y4I possesses two luxR and luxI homologous N-acyl-L-homoserine lactone (AHL)-mediated cell-to-cell communication systems, designated pgaRI and phaRI. We show here that Y4I produces two dominant AHLs, the novel monounsaturated N-(3-hydroxydodecenoyl)-L-homoserine lactone (3OHC 12:1 -HSL) and the relatively common N-octanoyl-L-homoserine lactone (C 8 -HSL), and provide evidence that they are synthesized by PhaI and PgaI, respectively. A Tn5 insertional mutation in either genetic locus results in the abolishment (pgaR::Tn5) or reduction (phaR::Tn5) of pigment production. Motility defects and denser biofilms were also observed in these mutant backgrounds, suggesting an overlap in the functional roles of these systems. Production of the AHLs occurs at distinct points during growth on an agar surface and was determined by isotope dilution high-performance liquid chromatography-tandem mass spectrometry (ID-HPLC-MS/MS) analysis. Within 2 h of surface inoculation, only 3OHC 12:1 -HSL was detected in agar extracts. As surface-attached cells became established (at ϳ10 h), the concentration of 3OHC 12:1 -HSL decreased, and the concentration of C 8 -HSL increased rapidly over 14 h. After longer (>24-h) establishment periods, the concentrations of the two AHLs increased to and stabilized at ϳ15 nM and ϳ600 nM for 3OHC 12:1 -HSL and C 8 -HSL, respectively. In contrast, the total amount of indigoidine increased steadily from undetectable to 642 M by 48 h. Gene expression profiles of the AHL and indigoidine synthases (pgaI, phaI, and igiD) were consistent with their metabolite profiles. These data provide evidence that pgaRI and phaRI play overlapping roles in the regulation of indigoidine biosynthesis, and it is postulated that this allows Phaeobacter sp. strain Y4I to coordinate production of indigoidine with different growth-phase-dependent physiologies. Bacteria are in constant competition for niches in the environment, and the ability to coordinate gene expression may provide a competitive advantage (1). Some bacteria are able to synchronize gene expression in a cell-density-dependent manner by sensing and responding to small diffusible molecules synthesized by individuals; in proteobacteria, members of the broadly distributed and chemically diverse class of N-acyl-L-homoserine lactones (AHLs) are among the best-characterized signaling molecules (2). Proteobacterial AHL synthases are fairly well conserved and form the LuxI protein family. Members of the LuxR protein family are cytoplasmic transcriptional regulators that can modulate gene expression, most typically when bound to the corresponding cognate AHL (3-7). It has been shown that luxI-luxR (luxIR) pairs are frequently colocalized within chromosomes and constitutively exp...

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“…The utilization of chitin by vibrios involves multiple levels of gene regulation that govern motility, chemotaxis, extracellular polysaccharide and biofilm matrix protein synthesis and secretion, type IV pilus production, chitin-binding protein secretion, chitin surface attachment, biofilm formation, extracellular chitinase secretion, chitoporin expression, and competence (166,338,470,(520)(521)(522)(523). Association with insoluble materials may be the preferred lifestyle of vibrios, including deep-sea hydrothermal vent species (15,403,524), and regulatory systems involving TCSs, chemotaxis, QS, sRNAs, cAMP, c-di-GMP, alternative sigma factors, and the stringent response enable vibrios to optimize resource utilization and survival (Fig.…”

Section: An Example Of Microbial Interaction With Surfaces: Vibrio Chmentioning

confidence: 99%

Microbial Surface Colonization and Biofilm Development in Marine Environments

Dang

Lovell

2016

Microbiol Mol Biol Rev

837

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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The Novel Sigma Factor-Like Regulator RpoQ Controls Luminescence, Chitinase Activity, and Motility in Vibrio fischeri

Cited by 36 publications

References 66 publications

LitR Is a Repressor of syp Genes and Has a Temperature-Sensitive Regulatory Effect on Biofilm Formation and Colony Morphology in Vibrio (Aliivibrio) salmonicida

LitR Is a Repressor of syp Genes and Has a Temperature-Sensitive Regulatory Effect on Biofilm Formation and Colony Morphology in Vibrio (Aliivibrio) salmonicida

Phaeobacter sp. Strain Y4I Utilizes Two Separate Cell-to-Cell Communication Systems To Regulate Production of the Antimicrobial Indigoidine

Microbial Surface Colonization and Biofilm Development in Marine Environments

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