Dataset Information

The iron-dependent regulator fur controls pheromone signaling systems and luminescence in the squid symbiont Vibrio fischeri ES114.

ABSTRACT: Bacteria often use pheromones to coordinate group behaviors in specific environments. While high cell density is required for pheromones to achieve stimulatory levels, environmental cues can also influence pheromone accumulation and signaling. For the squid symbiont Vibrio fischeri ES114, bioluminescence requires pheromone-mediated regulation, and this signaling is induced in the host to a greater extent than in culture, even at an equivalent cell density. Our goal is to better understand this environment-specific control over pheromone signaling and bioluminescence. Previous work with V. fischeri MJ1 showed that iron limitation induces luminescence, and we recently found that ES114 encounters a low-iron environment in its host. Here we show that ES114 induces luminescence at lower cell density and achieves brighter luminescence in low-iron media. This iron-dependent effect on luminescence required ferric uptake regulator (Fur), which we propose influences two pheromone signaling master regulators, LitR and LuxR. Genetic and bioinformatic analyses suggested that under low-iron conditions, Fur-mediated repression of litR is relieved, enabling more LitR to perform its established role as an activator of luxR. Interestingly, Fur may similarly control the LitR homolog SmcR of Vibrio vulnificus. These results reveal an intriguing regulatory link between low-iron conditions, which are often encountered in host tissues, and pheromone-dependent master regulators.

SUBMITTER: Septer AN

PROVIDER: S-EPMC3592230 | biostudies-literature | 2013 Mar

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

The iron-dependent regulator fur controls pheromone signaling systems and luminescence in the squid symbiont Vibrio fischeri ES114.

Septer Alecia N AN Lyell Noreen L NL Stabb Eric V EV

Applied and environmental microbiology 20130111 6

Bacteria often use pheromones to coordinate group behaviors in specific environments. While high cell density is required for pheromones to achieve stimulatory levels, environmental cues can also influence pheromone accumulation and signaling. For the squid symbiont Vibrio fischeri ES114, bioluminescence requires pheromone-mediated regulation, and this signaling is induced in the host to a greater extent than in culture, even at an equivalent cell density. Our goal is to better understand this e ...[more]

PMID: 23315731

Similar Datasets

Project description:UnlabelledVibrio fischeri, the bacterial symbiont of the Hawaiian bobtail squid, Euprymna scolopes, uses quorum sensing to control genes involved in bioluminescence, host colonization, and other biological processes. Previous work has shown that AinS/R-directed quorum sensing also regulates the expression of rpoQ (VF_A1015), a gene annotated as an RpoS-like sigma factor. In this study, we demonstrate using phylogenetics that RpoQ is related to, but distinct from, the stationary-phase sigma factor RpoS. Overexpression of rpoQ results in elevated chitinase activity but decreased motility and luminescence, three activities associated with symbiosis. The reduction in bacterial luminescence associated with the overexpression of rpoQ occurs both in culture and within the light-emitting organ of the squid host. This suppression of bioluminescence is due to the repression of the luxICDABEG promoter. Our results highlight RpoQ as a novel regulatory component, embedded in the quorum-signaling network that controls several biological processes in V. fischeri.ImportanceQuorum signaling is a widely occurring phenomenon that functions in diverse bacterial taxa. It is most often found associated with species that interact with animal or plant hosts, either as mutualists or pathogens, and controls the expression of genes critical to tissue colonization. We present the discovery of rpoQ, which encodes a new regulatory component in the quorum-signaling pathway of Vibrio fischeri. RpoQ is a novel protein in the RpoS family of stationary-phase sigma factors. Unlike many other regulatory proteins involved in the quorum-signaling pathways of the Vibrionaceae, the distribution of RpoQ appears to be restricted to only two closely related species. The role of this regulator is to enhance some quorum-signaling outputs (motility) while suppressing others (luminescence). We propose that RpoQ may be a recently evolved or acquired component in V. fischeri that provides this organism with an additional level of regulation to modulate its existing quorum-signaling pathway.

Project description:Beneficial microbial symbionts are often horizontally acquired by their animal hosts from environmental sources, requiring the symbionts to complete a lifestyle transition from free-living in the environment to association 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 on host mucosa. Extensive work has previously been conducted to isolate the critical factors controlling V. fischeri biofilm formation, yet much remains unknown regarding the full breadth of the biofilm-associated regulon. Here, we probed in vitro models of biofilm formation using transcriptomics, to identify novel regulatory pathways active within biofilms of the V. fischeri type strain ES114. Through comparing the gene-sets which became differentially regulated in multiple biofilm models, we discovered a shared set of 232 genes which demonstrated similar patterns in expression relative to uninduced controls. These genes contained representatives of multiple exopolysaccharide loci, genes involved in flagellar motility, and a diverse collection of other genes. Follow-up analysis suggested that these transcriptomic changes reflected true phenotypic effects, including changes in motility and cyclic-di-GMP production in biofilm-induced backgrounds. Beyond characterizing the shared biofilm response, we additionally profiled the regulatory activity of the sensor kinase RscS. This sensor kinase has previously been characterized to function as a phospho-donor within an established biofilm-inducing phospho-relay, yet our data suggests that RscS moonlights in at least one other phospho-relay that integrates downstream signaling from a homolog of the Vibrio cholerae response regulator VpsR, without a need for its established signaling partners. 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.

Project description:The mutualistic symbiont Vibrio fischeri builds a symbiotic biofilm during colonization of squid hosts. Regulation of the exopolysaccharide component, termed Syp, has been examined in strain ES114, where production is controlled by a phosphorelay that includes the inner membrane hybrid histidine kinase RscS. Most strains that lack RscS or encode divergent RscS proteins cannot colonize a squid host unless RscS from a squid symbiont is heterologously expressed. In this study, we examine V. fischeri isolates worldwide to understand the landscape of biofilm regulation during beneficial colonization. We provide a detailed study of three distinct evolutionary groups of V. fischeri and find that while the RscS-Syp biofilm pathway is required in one of the groups, two other groups of squid symbionts require Syp independent of RscS. Mediterranean squid symbionts, including V. fischeri SR5, colonize without an RscS homolog encoded by their genome. Additionally, group A V. fischeri strains, which form a tightly related clade of Hawaii isolates, have a frameshift in rscS and do not require the gene for squid colonization or competitive fitness. These same strains have a frameshift in sypE, and we provide evidence that this group A sypE allele leads to an upregulation in biofilm activity. Thus, this work describes the central importance of Syp biofilm in colonization of diverse isolates and demonstrates that significant evolutionary transitions correspond to regulatory changes in the syp pathway.IMPORTANCE Biofilms are surface-associated, matrix-encased bacterial aggregates that exhibit enhanced protection to antimicrobial agents. Previous work has established the importance of biofilm formation by a strain of luminous Vibrio fischeri bacteria as the bacteria colonize their host, the Hawaiian bobtail squid. In this study, expansion of this work to many natural isolates revealed that biofilm genes are universally required, yet there has been a shuffling of the regulators of those genes. This work provides evidence that even when bacterial behaviors are conserved, dynamic regulation of those behaviors can underlie evolution of the host colonization phenotype. Furthermore, this work emphasizes the importance of investigating natural diversity as we seek to understand molecular mechanisms in bacteria.

Dataset Information

The iron-dependent regulator fur controls pheromone signaling systems and luminescence in the squid symbiont Vibrio fischeri ES114.

Publications

The iron-dependent regulator fur controls pheromone signaling systems and luminescence in the squid symbiont Vibrio fischeri ES114.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets