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A Family of Nonribosomal Peptides Modulate Collective Behavior in Pseudovibrio Bacteria Isolated from Marine Sponges*.

ABSTRACT: Although swarming motility and biofilms are opposed collective behaviors, both contribute to bacterial survival and host colonization. Pseudovibrio bacteria have attracted attention because they are part of the microbiome of healthy marine sponges. Two-thirds of Pseudovibrio genomes contain a member of a nonribosomal peptide synthetase-polyketide synthase gene cluster family, which is also found sporadically in Pseudomonas pathogens of insects and plants. After developing reverse genetics for Pseudovibrio, we isolated heptapeptides with an ureido linkage and related nonadepsipeptides we termed pseudovibriamides A and B, respectively. A combination of genetics and imaging mass spectrometry experiments showed heptapetides were excreted, promoting motility and reducing biofilm formation. In contrast to lipopeptides widely known to affect motility/biofilms, pseudovibriamides are not surfactants. Our results expand current knowledge on metabolites mediating bacterial collective behavior.

SUBMITTER: Ioca LP

PROVIDER: S-EPMC8269750 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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A Family of Nonribosomal Peptides Modulate Collective Behavior in Pseudovibrio Bacteria Isolated from Marine Sponges*.

Ióca Laura P LP Dai Yitao Y Kunakom Sylvia S Diaz-Espinosa Jennifer J Krunic Aleksej A Crnkovic Camila M CM Orjala Jimmy J Sanchez Laura M LM Ferreira Antonio G AG Berlinck Roberto G S RGS Eustáquio Alessandra S AS

Angewandte Chemie (International ed. in English) 20210617 29

Although swarming motility and biofilms are opposed collective behaviors, both contribute to bacterial survival and host colonization. Pseudovibrio bacteria have attracted attention because they are part of the microbiome of healthy marine sponges. Two-thirds of Pseudovibrio genomes contain a member of a nonribosomal peptide synthetase-polyketide synthase gene cluster family, which is also found sporadically in Pseudomonas pathogens of insects and plants. After developing reverse genetics for Ps ...[more]

PMID: 33961724

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Project description:Pseudovibrio α-Proteobacteria have been repeatedly isolated from marine sponges and proposed to be beneficial to the host. Bacterial motility is known to contribute to host colonization. We have previously identified pseudovibriamides A and B, produced in culture by Pseudovibrio brasiliensis Ab134, and shown that pseudovibriamide A promotes flagellar motility. Pseudovibriamides are encoded in a hybrid nonribosomal peptide synthetase-polyketide synthase gene cluster that also includes several accessory genes. Pseudovibriamide A is a linear heptapeptide and pseudovibriamide B is a nonadepsipeptide derived from pseudovibriamide A. Here, we define the borders of the pseudovibriamides gene cluster, assign function to biosynthetic genes using reverse genetics, and test the hypothesis that pseudovibriamides impact motility by modulating gene transcription. RNA-sequencing transcriptomic analyses of strains having different compositions of pseudovibriamides suggested that both pseudovibriamides A and B affect genes potentially involved in motility, and that a compensatory mechanism is at play in mutants that produce only pseudovibriamide A, resulting in comparable flagellar motility as the wild type. The data gathered suggest that pseudovibriamides A and B have opposite roles in modulating a subset of genes, with pseudovibriamide B having a primary effect in gene activation, and pseudovibriamide A on inhibition. Finally, we observed many differentially expressed genes (up to 29% of the total gene number) indicating that pseudovibriamides have a global effect on transcription that goes beyond motility.IMPORTANCEMarine sponges are found throughout the oceans from tropical coral reefs to polar sea floors, playing crucial roles in marine ecosystems. Pseudovibrio bacteria have been proposed to contribute to sponge health. We have previously shown that pseudovibriamides produced by Pseudovibrio brasiliensis promote bacterial motility, a behavior that is beneficial to bacterial survival and host colonization. The gene cluster that encodes pseudovibriamide biosynthesis is found in two-thirds of Pseudovibrio genomes. This gene cluster is also present in Pseudomonas bacteria that interact with terrestrial plants and animals. Here, we first assign functions to pseudovibriamide biosynthetic genes using reverse genetics. We then show that pseudovibriamides play a major role in transcriptional regulation, affecting up to 29% of P. brasiliensis genes, including motility genes. Thus, this work gives insights into pseudovibriamide biosynthesis and provides evidence that they are signaling molecules relevant to bacterial motility and to other yet-to-be-identified phenotypes.

Dataset Information

A Family of Nonribosomal Peptides Modulate Collective Behavior in Pseudovibrio Bacteria Isolated from Marine Sponges*.

Publications

A Family of Nonribosomal Peptides Modulate Collective Behavior in Pseudovibrio Bacteria Isolated from Marine Sponges*.

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