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Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae

Laura Louise Lindqvist Orcid Logo, Scott A. Jarmusch Orcid Logo, Eva C. Sonnenschein Orcid Logo, Mikael Lenz Strube Orcid Logo, Janie Kim Orcid Logo, Maike Wennekers Nielsen, Paul J. Kempen Orcid Logo, Erwin M. Schoof Orcid Logo, Sheng-Da Zhang Orcid Logo, Lone Gram Orcid Logo

mSphere, Volume: 8, Issue: 1

Swansea University Author: Eva C. Sonnenschein Orcid Logo

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Abstract

In the marine environment, surface-associated bacteria often produce an array of antimicrobial secondary metabolites, which have predominantly been perceived as competition molecules. However, they may also affect other hallmarks of surface-associated living, such as motility and biofilm formation....

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Published in: mSphere
ISSN: 2379-5042
Published: American Society for Microbiology 2023
Online Access: Check full text

URI: https://cronfa.swan.ac.uk/Record/cronfa62315
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Abstract: In the marine environment, surface-associated bacteria often produce an array of antimicrobial secondary metabolites, which have predominantly been perceived as competition molecules. However, they may also affect other hallmarks of surface-associated living, such as motility and biofilm formation. Here, we investigate the ecological significance of an antibiotic secondary metabolite, tropodithietic acid (TDA), in the producing bacterium, Phaeobacter piscinae S26. We constructed a markerless in-frame deletion mutant deficient in TDA biosynthesis, S26ΔtdaB. Molecular networking demonstrated that other chemical sulfur-containing features, likely related to TDA, were also altered in the secondary metabolome. We found several changes in the physiology of the TDA-deficient mutant, ΔtdaB, compared to the wild type. Growth of the two strains was similar; however, ΔtdaB cells were shorter and more motile. Transcriptome and proteome profiling revealed an increase in gene expression and protein abundance related to a type IV secretion system, and to a prophage, and a gene transfer agent in ΔtdaB. All these systems may contribute to horizontal gene transfer (HGT), which may facilitate adaptation to novel niches. We speculate that once a TDA-producing population has been established in a new niche, the accumulation of TDA acts as a signal of successful colonization, prompting a switch to a sessile lifestyle. This would lead to a decrease in motility and the rate of HGT, while filamentous cells could form the base of a biofilm. In addition, the antibiotic properties of TDA may inhibit invading competing microorganisms. This points to a role of TDA in coordinating colonization and adaptation.
Keywords: biofilm, motility, Phaeobacter, secondary metabolites, tropodithietic acid, prophage, gene transfer agent, horizontal gene transfer, niche colonization
College: Faculty of Science and Engineering
Funders: Funding for this study was received from the Danish National Research Foundation (DNRF137) for the Center for Microbial Secondary Metabolites, from the Independent Research Fund Denmark (project 7017-00003B) and from the Novo Nordisk Foundation to research infrastructure grant NNF19OC0055625 for the infrastructure “Imaging microbial language in biocontrol (IMLiB)”. Janie Kim was supported by a Fulbright U.S. Student Grant to Denmark. Seyedsayamdost kindly provided the DSM17395 tdaB::gmR strain.
Issue: 1