Calcium-Responsive Diguanylate Cyclase CasA Drives Cellulose-Dependent Biofilm Formation and Inhibits Motility in Vibrio fischeri

Tischler, Alice H.; Vanek, Michael E; Peterson, Natasha; Visick, Karen L.

doi:10.1128/mbio.02573-21

Cited by 15 publications

(12 citation statements)

References 72 publications

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“…This result may be explained by the shared upregulation of the calcium-induced DGC casA in both models, as overexpression of CasA has previously been linked to increased c-di-GMP synthesis in calcium-supplemented liquid cultures (Fig. S3C) ( 54 ). Overall, both models of biofilm formation appear to be capable of increasing the global levels of c-di-GMP.…”

Section: Resultsmentioning

confidence: 81%

“…SypF has precedent as a sensor kinase with multiple downstream response regulators, affecting both SypE and SypG within the Syp phosphorelay ( 27 , 29 ). Additionally, an increased activity allele of SypF (SypF1) was discovered to increase production of the cellulose exopolysaccharide ( 26 , 54 ). This activity required the gene VF_0454 , which encodes a homolog of the Vibrio cholerae transcriptional regulator VpsR ( 26 , 54 ).…”

Section: Resultsmentioning

confidence: 99%

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Transcriptional pathways across colony biofilm models in the symbiont Vibrio fischeri

Vander Griend,

Isenberg,

Kotla

et al. 2024

mSystems

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Beneficial microbial symbionts that are horizontally acquired by their animal hosts undergo a lifestyle transition from free-living in the environment to associating with host tissues. In the model symbiosis between the Hawaiian bobtail squid and its microbial symbiont Vibrio fischeri , one mechanism used to make this transition during host colonization is the formation of biofilm-like aggregates in host mucosa. Previous work identified factors that are sufficient to induce V. fischeri biofilm formation, yet much remains unknown regarding the breadth of target genes induced by these factors. Here, we probed two widely used in vitro models of biofilm formation to identify novel regulatory pathways in the squid symbiont V. fischeri ES114. We discovered a shared set of 232 genes that demonstrated similar patterns in expression in both models. These genes comprise multiple exopolysaccharide loci that are upregulated and flagellar motility genes that are downregulated, with a consistent decrease in measured swimming motility. Furthermore, we identified genes regulated downstream of the key sensor kinase RscS that are induced independent of the response regulator SypG. Our data suggest that transcriptional regulator VpsR plays a strong role in expression of at least a subset of these genes. Overall, this study adds to our understanding of the genes involved in V. fischeri biofilm regulation while revealing new regulatory pathways branching from previously characterized signaling networks. IMPORTANCE The V. fischeri- squid system provides an opportunity to study biofilm development both in the animal host and in culture-based biofilm models that capture key aspects of in vivo signaling. In this work, we report the results of the transcriptomic profiling of two V. fischeri biofilm models followed by phenotypic validation and examination of novel signaling pathway architecture. Remarkable consistency between the models provides a strong basis for future studies using either approach or both. A subset of the factors identified by the approaches were validated in the work, and the body of transcriptomic data provides a number of leads for future studies in culture and during animal colonization.

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Section: Resultsmentioning

confidence: 81%

Section: Resultsmentioning

confidence: 99%

Transcriptional pathways across colony biofilm models in the symbiont Vibrio fischeri

Vander Griend,

Isenberg,

Kotla

et al. 2024

mSystems

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“…fischeri is regulated by the c-di-GMP-responsive transcriptional regulator VpsR, a homologue of the V. cholerae master regulator of biofilm. ,− This difference in biofilm regulation highlights the complexity and importance of studying the relative biological influence of c-di-GMP-mediated biofilm production in different contexts. To further validate MSI as an effective detection method for c-di-GMP, we applied well-established genetic manipulations to enzymes in the V.…”

Section: Resultsmentioning

confidence: 99%

A Label-Free Approach for Relative Spatial Quantitation of c-di-GMP in Microbial Biofilms

McCaughey,

Trebino,

McAtamney

et al. 2024

Anal. Chem.

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Microbial biofilms represent an important lifestyle for bacteria and are dynamic three-dimensional structures. Cyclic dimeric guanosine monophosphate (c-di-GMP) is a ubiquitous signaling molecule that is known to be tightly regulated with biofilm processes. While measurements of global levels of c-di-GMP have proven valuable toward understanding the genetic control of c-di-GMP production, there is a need for tools to observe the local changes of c-di-GMP production in biofilm processes. We have developed a label-free method for the direct detection of c-di-GMP in microbial colony biofilms using matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI). We applied this method to the enteric pathogen Vibrio cholerae, the marine symbiont V. fischeri, and the opportunistic pathogen Pseudomonas aeruginosa PA14 and detected spatial and temporal changes in c-di-GMP signal that accompanied genetic alterations in factors that synthesize and degrade the compound. We further demonstrated how this method can be simultaneously applied to detect additional metabolites of interest from a single sample.

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“…In E. coli and Salmonella , where cellulose production has been most heavily studied, the second messenger c-di-GMP promotes biofilm formation by binding to and activating cellulose synthase ( 156 , 157 ). V. fischeri likely exerts a similar control over synthase activity but also clearly wields distinct, environmentally responsive regulatory control over bcs transcription ( 158 ).…”

Section: Select V Fischeri Traits Of Interest Beyo...mentioning

confidence: 99%

Lighting the way: how the Vibrio fischeri model microbe reveals the complexity of Earth’s “simplest” life forms

Septer,

Visick

2024

J Bacteriol

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Vibrio ( Aliivibrio ) fischeri ’s initial rise to fame derived from its alluring production of blue-green light. Subsequent studies to probe the mechanisms underlying this bioluminescence helped the field discover the phenomenon now known as quorum sensing. Orthologs of quorum-sensing regulators (i.e., LuxR and LuxI) originally identified in V. fischeri were subsequently uncovered in a plethora of bacterial species, and analogous pathways were found in yet others. Over the past three decades, the study of this microbe has greatly expanded to probe the unique role of V. fischeri as the exclusive symbiont of the light organ of the Hawaiian bobtail squid, Euprymna scolopes . Buoyed by this optically amenable host and by persistent and insightful researchers who have applied novel and cross-disciplinary approaches, V. fischeri has developed into a robust model for microbe-host associations. It has contributed to our understanding of how bacteria experience and respond to specific, often fluxing environmental conditions and the mechanisms by which bacteria impact the development of their host. It has also deepened our understanding of numerous microbial processes such as motility and chemotaxis, biofilm formation and dispersal, and bacterial competition, and of the relevance of specific bacterial genes in the context of colonizing an animal host. Parallels in these processes between this symbiont and bacteria studied as pathogens are readily apparent, demonstrating functional conservation across diverse associations and permitting a reinterpretation of “pathogenesis.” Collectively, these advances built a foundation for microbiome studies and have positioned V. fischeri to continue to expand the frontiers of our understanding of the microbial world inside animals.

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Calcium-Responsive Diguanylate Cyclase CasA Drives Cellulose-Dependent Biofilm Formation and Inhibits Motility in Vibrio fischeri

Cited by 15 publications

References 72 publications

Transcriptional pathways across colony biofilm models in the symbiont Vibrio fischeri

Transcriptional pathways across colony biofilm models in the symbiont Vibrio fischeri

A Label-Free Approach for Relative Spatial Quantitation of c-di-GMP in Microbial Biofilms

Lighting the way: how the Vibrio fischeri model microbe reveals the complexity of Earth’s “simplest” life forms

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