Transcriptional pathways across colony biofilm models in the symbiontVibrio fischeri

Abstract

ABSTRACTBeneficial microbial symbionts that are horizontally acquired by their animal hosts undergo a lifestyle transition from free-living in the environment to associated with host tissues. In the model symbiosis between the Hawaiian bobtail squid and its microbial symbiontVibrio 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 induceV. fischeribiofilm formation, yet much remains unknown regarding the breadth of target genes induced by these factors. Here, we probed two widely-usedin vitromodels of biofilm formation to identify novel regulatory pathways in the squid symbiontV. fischeriES114. 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 putative response 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 inV. fischeribiofilm regulation, while revealing new regulatory pathways branching from previously characterized signaling networks.IMPORTANCETheV. 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 ofin vivosignaling. In this work, we report the results of the transcriptomic profiling of twoV. fischeribiofilm 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–or both–approaches. 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.