The syp Enhancer Sequence Plays a Key Role in Transcriptional Activation by the  54-Dependent Response Regulator SypG and in Biofilm Formation and Host Colonization by Vibrio fischeri

Ray, Valerie A.; Eddy, Justin L.; Hussa, Elizabeth A.; Misale, Michael; Visick, Karen L.

doi:10.1128/jb.00689-13

Cited by 24 publications

(33 citation statements)

References 41 publications

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“…We previously identified three unlinked two-gene sets (pairs of genes), namely, VF_A1019-VF_A1018, VF_A0120-VF_A0121, and VF_A0550-VF_A0549, as putative members of the SypG regulon (24 (24). To confirm that SypG could also regulate bmpA and bmpC, we generated transcriptional reporter constructs that fuse the promoter regions of these genes to lacZ and introduced the fusions, in single copy, into the chromosome of wild-type V. fischeri at a benign site (the Tn7 site).…”

Section: Resultsmentioning

confidence: 99%

“…9A). Finally, as a control, we collected and examined cell pellets and supernatants from a strain that expresses SypG-FLAG; as a transcription factor (19,24), SypG is expected to be located in the cytoplasm. Indeed, SypG could be found in the cell pellet but not in the supernatant fraction (Fig.…”

Section: Fig 8 Tem Analysis Of Biofilm Mutantsmentioning

confidence: 99%

“…Recently, however, we identified new putative members of the SypG regulon (24). Specifically, three two-gene operons, one of which was immediately adjacent to the syp locus, were identified via bioinformatics based on the presence in their upstream intergenic regions of an SE sequence, indicating a putative SypG binding site, and a predicted 54 binding site (24). Intriguingly, the proteins encoded by the first gene in each operon are similar to each other (27,28), suggesting that they may have overlapping functions.…”

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confidence: 99%

“…Although much is known about the regulatory control over Syp polysaccharide production, important aspects of V. fischeri biofilm formation, including the identities of other matrix components, such as matrix proteins, remain unknown. Recently, however, we identified new putative members of the SypG regulon (24). Specifically, three two-gene operons, one of which was immediately adjacent to the syp locus, were identified via bioinformatics based on the presence in their upstream intergenic regions of an SE sequence, indicating a putative SypG binding site, and a predicted 54 binding site (24).…”

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confidence: 99%

“…1). In its phosphorylated form, SypG serves as the direct transcriptional activator of the syp locus by binding to the syp enhancer (SE), a conserved sequence located upstream of each of four operons within this locus, and promoting transcription in conjunction with RNA polymerase loaded with the alternative sigma factor 54 (19,24). The signal recognized by RscS is unknown, but overexpression of the rscS gene is sufficient to induce syp transcription and promote biofilm phenotypes, including the formation of wrinkled colonies (normally smooth) and pellicles (not normally formed) (17).…”

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confidence: 99%

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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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Section: Resultsmentioning

confidence: 99%

Section: Fig 8 Tem Analysis Of Biofilm Mutantsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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

Ray¹,

Driks²,

Visick³

2014

J. Bacteriol.

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

et al. 2014

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Quorum signaling (QS) describes how bacteria can use small signaling molecules (autoinducers) to coordinate group-level behaviors. In Vibrio fischeri, QS is achieved through a complex regulatory network that ultimately controls bioluminescence, motility, and host colonization. We conducted a genetic screen focused on qrr1, which encodes a small regulatory RNA that is necessary for the core quorum-signaling cascade to transduce autoinducer information into cellular responses. We isolated unique mutants with a transposon inserted into one of two genes within the syp locus, which is involved in biofilm formation. We found that overexpression of sypK, which encodes a putative oligosaccharide translocase, is sufficient to activate qrr1, and, in addition, this effect appears to depend on the kinase activity of the sensor LuxQ. Consistent with the established model for QS in V. fischeri, enhanced expression of qrr1 by the overexpression of sypK resulted in reduced bioluminescence and increased motility. Finally, we found that induction of the syp locus by overexpression of sypG was sufficient to activate qrr1 levels. Together, our results show how conditions that promote biofilm formation impact the quorum-signaling network in V. fischeri, and further highlight the integrated nature of the regulatory circuits involved in complex bacterial behaviors.

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A lasting symbiosis: how Vibrio fischeri finds a squid partner and persists within its natural host

2021

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The syp Enhancer Sequence Plays a Key Role in Transcriptional Activation by the 54-Dependent Response Regulator SypG and in Biofilm Formation and Host Colonization by Vibrio fischeri

Cited by 24 publications

References 41 publications

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

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

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

A lasting symbiosis: how Vibrio fischeri finds a squid partner and persists within its natural host

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