The Type II Secretion System Delivers Matrix Proteins for Biofilm Formation by Vibrio cholerae

Johnson, Tanya; Fong, Jiunn C. N.; Rule, Chelsea S.; Rogers, Alisdair; Yildiz, Fitnat H.; Sandkvist, Maria

doi:10.1128/jb.01944-14

Cited by 56 publications

(48 citation statements)

References 55 publications

(62 reference statements)

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“…The T2SS is necessary for proper biofilm development in V. cholerae, in part through secretion of three extracellular proteins (21), and c-di-GMP is similarly essential for biofilm formation (3,6,34). VpsR binds c-di-GMP and upregulates the vpsT and the vps gene clusters in a c-di-GMP-dependent manner (30,39,45).…”

Section: Discussionmentioning

confidence: 99%

“…In addition to cholera toxin, V. cholerae exports, via the T2SS, other extracellular factors, including chitinases, proteases, DNase, and pilin, which aid in its ability to successfully occupy diverse ecological niches (14). The T2SS also secretes the three proteins RbmA, RbmC, and Bap1, which are necessary for robust, shear-resistant biofilm formation (10,(19)(20)(21). Other major bacterial pathogens, such as Escherichia coli and Pseudomonas aeruginosa, secrete virulence factors encoded by genes with considerable similarity to those of V. cholerae through the T2SS (17,(22)(23)(24).…”

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confidence: 99%

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Cyclic Di-GMP and VpsR Induce the Expression of Type II Secretion in Vibrio cholerae

et al. 2017

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Vibrio cholerae is a human pathogen that alternates between growth in environmental reservoirs and infection of human hosts, causing severe diarrhea. The second messenger cyclic di-GMP (c-di-GMP) mediates this transition by controlling a wide range of functions, such as biofilms, virulence, and motility. Here, we report that c-di-GMP induces expression of the extracellular protein secretion (eps) gene cluster, which encodes the type II secretion system (T2SS) in V. cholerae. Analysis of the eps genes confirmed the presence of two promoters located upstream of epsC, the first gene in the operon, one of which is induced by c-di-GMP. This induction is directly mediated by the c-di-GMP-binding transcriptional activator VpsR. Increased expression of the eps operon did not impact secretion of extracellular toxin or biofilm formation but did increase expression of the pseudopilin protein EpsG on the cell surface.IMPORTANCE Type II secretion systems (T2SSs) are the primary molecular machines by which Gram-negative bacteria secrete proteins and protein complexes that are folded and assembled in the periplasm. The substrates of T2SSs include extracellular factors, such as proteases and toxins. Here, we show that the widely conserved second messenger cyclic di-GMP (c-di-GMP) upregulates expression of the eps genes encoding the T2SS in the pathogen V. cholerae via the c-di-GMP-dependent transcription factor VpsR.KEYWORDS Vibrio cholerae, biofilm, VpsR, type II secretion, cyclic di-GMP V ibrio cholerae is a major bacterial pathogen responsible for the diarrheal disease cholera, causing an estimated 2.8 million infections each year resulting in approximately 91,000 deaths (1). V. cholerae is endemic to coastal waterways in tropical countries, where it persists in the environment as a biofilm on chitinous surfaces and periodically causes outbreaks in human populations. V. cholerae can rapidly spread and multiply under favorable environmental conditions, as seen in the recent 2010 Haiti outbreak (2). A fundamental property that allows V. cholerae to cause disease is its ability to transition from environmental reservoirs to human hosts. This transition is in part regulated by the second-messenger molecule cyclic di-GMP (c-di-GMP) (3-5).c-di-GMP is a nearly ubiquitous second-messenger molecule in bacteria that controls a range of physiological functions, including biofilm formation, motility, and virulence factor expression (6). c-di-GMP is synthesized by diguanylate cyclases (DGCs) (7) and degraded by phosphodiesterases (PDEs) (8,9). Together, these enzymes alter the concentration of c-di-GMP in the cell in response to environmental inputs. c-di-GMP has been shown to repress motility and virulence to promote a sessile, biofilmassociated lifestyle by stimulating the production of exopolysaccharide (EPS) matrix substances and adhesins while inhibiting flagellar activity or expression (3, 10-12). Levels of intracellular c-di-GMP have been proposed to be high in environmental

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Cyclic Di-GMP and VpsR Induce the Expression of Type II Secretion in Vibrio cholerae

et al. 2017

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“…These proteins facilitate biofilm formation at particular steps: RbmA is capable of binding the exopolysaccharide VPS and strengthening early cell-cell adhesion, Bap1 facilitates biofilm adhesion and recruits planktonic cells to the surface, and Bap1 and RbmC encase cell clusters that are attached to the surface (467)(468)(469). The type II secretion system (T2SS) delivers these biofilm matrix proteins for biofilm formation in V. cholerae (470). The expression of these biofilm matrix proteins involves regulation by the cyclic AMP (cAMP)-cAMP receptor protein (CRP) complex and the transcriptional regulator VpsR (471,472).…”

Section: Posttranscriptional Regulation By Small Rnasmentioning

confidence: 99%

“…For example, the V. cholerae genome contains Ͼ60 genes predicted to encode distinct c-di-GMP-modulating DGCs and PDEs for a flexible environmental response and high-fidelity signaling (490). The c-di-GMP regulatory pathways are involved in modulating the expression of type IV pili, the exopolysaccharide VPS, and T2SS-facilitated secretion of biofilm matrix proteins, playing important roles in surface colonization and biofilm formation by V. cholerae (470,491). Surface-associated bacteria usually harbor more c-di-GMP regulators than free-living bacteria, presumably as an adaptive strategy (120).…”

Section: Centralized Regulation By Second Messengersmentioning

confidence: 99%

“…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%

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Microbial Surface Colonization and Biofilm Development in Marine Environments

Dang

Lovell

2016

Microbiol Mol Biol Rev

829

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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Biofilm Development and Stress Response in the Cholera Bacterium

Silva

Benítez

2016

Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria

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The Type II Secretion System Delivers Matrix Proteins for Biofilm Formation by Vibrio cholerae

Cited by 56 publications

References 55 publications

Cyclic Di-GMP and VpsR Induce the Expression of Type II Secretion in Vibrio cholerae

Cyclic Di-GMP and VpsR Induce the Expression of Type II Secretion in Vibrio cholerae

Microbial Surface Colonization and Biofilm Development in Marine Environments

Biofilm Development and Stress Response in the Cholera Bacterium

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