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

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

doi:10.1128/msphere.00517-22

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

Laura Louise Lindqvist

, Scott A. Jarmusch

, Eva C. Sonnenschein

, Mikael Lenz Strube

, Janie Kim

, Maike Wennekers Nielsen, Paul J. Kempen

, Erwin M. Schoof

, Sheng-Da Zhang

, Lone Gram

mSphere, Volume: 8, Issue: 1

Swansea University Author: Eva C. Sonnenschein

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DOI (Published version): 10.1128/msphere.00517-22

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
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URI:	https://cronfa.swan.ac.uk/Record/cronfa62315
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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. 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spelling	v2 62315 2023-01-13 Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae f6a4027578a15ea3e6453a54b849c686 0000-0001-6959-5100 Eva C. Sonnenschein Eva C. Sonnenschein true false 2023-01-13 SBI 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. Journal Article mSphere 8 1 American Society for Microbiology 2379-5042 biofilm, motility, Phaeobacter, secondary metabolites, tropodithietic acid, prophage, gene transfer agent, horizontal gene transfer, niche colonization 9 1 2023 2023-01-09 10.1128/msphere.00517-22 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University Another institution paid the OA fee 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. 2023-06-12T17:13:19.3769014 2023-01-13T08:52:25.8076680 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Laura Louise Lindqvist 0000-0001-6591-0767 1 Scott A. Jarmusch 0000-0002-1021-1608 2 Eva C. Sonnenschein 0000-0001-6959-5100 3 Mikael Lenz Strube 0000-0003-0905-5705 4 Janie Kim 0000-0001-5600-7613 5 Maike Wennekers Nielsen 6 Paul J. Kempen 0000-0003-2179-2257 7 Erwin M. Schoof 0000-0002-3117-7832 8 Sheng-Da Zhang 0000-0002-2220-3904 9 Lone Gram 0000-0002-1076-5723 10 62315__26416__98d4731730154d27a5ddcec8f6e30fa4.pdf 62315_VoR.pdf 2023-01-27T10:14:14.5515088 Output 2322047 application/pdf Version of Record true © 2023 Lindqvist et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. true eng https://creativecommons.org/licenses/by/4.0/
title	Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae
spellingShingle	Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae Eva C. Sonnenschein
title_short	Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae
title_full	Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae
title_fullStr	Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae
title_full_unstemmed	Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae
title_sort	Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae
author_id_str_mv	f6a4027578a15ea3e6453a54b849c686
author_id_fullname_str_mv	f6a4027578a15ea3e6453a54b849c686_***_Eva C. Sonnenschein
author	Eva C. Sonnenschein
author2	Laura Louise Lindqvist Scott A. Jarmusch Eva C. Sonnenschein Mikael Lenz Strube Janie Kim Maike Wennekers Nielsen Paul J. Kempen Erwin M. Schoof Sheng-Da Zhang Lone Gram
format	Journal article
container_title	mSphere
container_volume	8
container_issue	1
publishDate	2023
institution	Swansea University
issn	2379-5042
doi_str_mv	10.1128/msphere.00517-22
publisher	American Society for Microbiology
college_str	Faculty of Science and Engineering
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hierarchy_top_id	facultyofscienceandengineering
hierarchy_top_title	Faculty of Science and Engineering
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department_str	School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str	1
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description	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.
published_date	2023-01-09T17:13:17Z
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Tropodithietic Acid, a Multifunctional Antimicrobial, Facilitates Adaption and Colonization of the Producer, Phaeobacter piscinae

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