Journal article
Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae
Department of Biotechnology and Biomedicine, Technical University of Denmark1
National Centre for Nano Fabrication and Characterization, Technical University of Denmark2
Department of Health Technology, Technical University of Denmark3
Nanocharacterization, National Centre for Nano Fabrication and Characterization, Technical University of Denmark4
Biotherapeutic Engineering and Drug Targeting, Department of Health Technology, Technical University of Denmark5
Materials at the Interface of Biology, Nanocharacterization, National Centre for Nano Fabrication and Characterization, Technical University of Denmark6
Colloids & Biological Interfaces, Biotherapeutic Engineering and Drug Targeting, Department of Health Technology, Technical University of Denmark7
Section for Microbial and Chemical Ecology, Department of Biotechnology and Biomedicine, Technical University of Denmark8
Bacterial Ecophysiology and Biotechnology, Section for Microbial and Chemical Ecology, Department of Biotechnology and Biomedicine, Technical University of Denmark9
DTU Microbes Initiative, Centers, Technical University of Denmark10
Natural Product Discovery, Section for Microbial and Chemical Ecology, Department of Biotechnology and Biomedicine, Technical University of Denmark11
Technical University of Denmark12
Section for Protein Science and Biotherapeutics, Department of Biotechnology and Biomedicine, Technical University of Denmark13
Cell Diversity Lab, Section for Protein Science and Biotherapeutics, Department of Biotechnology and Biomedicine, Technical University of Denmark14
DTU Proteomics Core, Section for Protein Science and Biotherapeutics, Department of Biotechnology and Biomedicine, Technical University of Denmark15
...and 5 moreDespite the broad clinical usage of microbial secondary metabolites with antibiotic activity, little is known about their role in natural microbiomes. Here, we studied the effect of production of the antibiotic tropodithietic acid (TDA) on the producing strain, Phaeobacter piscinae S26, a member of the Roseobacter group.
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. IMPORTANCE Despite the broad clinical usage of microbial secondary metabolites with antibiotic activity, little is known about their role in natural microbiomes.
Here, we studied the effect of production of the antibiotic tropodithietic acid (TDA) on the producing strain, Phaeobacter piscinae S26, a member of the Roseobacter group. We show that TDA affects several phenotypes of the producing strain, including motility, cell morphology, metal metabolism, and three horizontal gene transfer systems: a prophage, a type IV secretion system, and a gene transfer agent.
Together, this indicates that TDA participates in coordinating the colonization process of the producer. TDA is thus an example of a multifunctional secondary metabolite that can mediate complex interactions in microbial communities. This work broadens our understanding of the ecological role that secondary metabolites have in microbial community dynamics.
Language: | English |
---|---|
Publisher: | American Society for Microbiology |
Year: | 2023 |
Pages: | e0051722 |
ISSN: | 15359786 , 15359778 and 23795042 |
Types: | Journal article |
DOI: | 10.1128/msphere.00517-22 |
ORCIDs: | Jarmusch, Scott A. , Sonnenschein, Eva C. , Strube, Mikael Lenz , Kempen, Paul J. , Schoof, Erwin M. , Zhang, Sheng-Da , Gram, Lone , 0000-0001-6591-0767 and 0000-0001-5600-7613 |