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

• Published in: Angewandte Chemie International Edition 2021-07, Vol.60 (29), p.15891-15898
• Main Authors: Ióca, Laura P., Dai, Yitao, Kunakom, Sylvia, Diaz‐Espinosa, Jennifer, Krunic, Aleksej, Crnkovic, Camila M., Orjala, Jimmy, Sanchez, Laura M., Ferreira, Antonio G., Berlinck, Roberto G. S., Eustáquio, Alessandra S.
• Format: Article
• Language: English
• Subjects: Animals; Bacteria; bacterial metabolites; biofilm formation; Biofilms; Biofilms - drug effects; Colonization; Genetics; Genomes; Insects; Lipopeptides; Mass spectrometry; Mass spectroscopy; Metabolites; Microbiomes; Motility; Multigene Family; natural products; Peptide Synthases - genetics; Peptide Synthases - metabolism; Peptides; Peptides - chemistry; Peptides - metabolism; Peptides - pharmacology; Pollutants; Polyketide synthase; Porifera - microbiology; Pseudovibrio; Sponges; Surfactants; Swarming
• ISSN: 1433-7851; 1521-3773; 1521-3773
• DOI: 10.1002/anie.202017320

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. Pseudovibrio are α‐proteobacteria proposed to contribute to marine sponge health. Lack of reverse genetics have hindered exploration of the ecological and biotechnological potential of Pseudovibrio. Here we describe reverse genetics methods that enabled identification of 12 pseudovibriamides, which we show affect motility and biofilm behavior of Pseudovibrio.