Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>

ABSTRACT Secondary metabolites are synthesized by many microorganisms and provide a fitness benefit in the presence of competitors and predators. Secondary metabolism also can be costly, as it shunts energy and intermediates from primary metabolism. In Pseudomonas spp., secondary metabolism is contr...

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Autores principales:	Qing Yan, Lucas D. Lopes, Brenda T. Shaffer, Teresa A. Kidarsa, Oliver Vining, Benjamin Philmus, Chunxu Song, Virginia O. Stockwell, Jos M. Raaijmakers, Kerry L. McPhail, Fernando D. Andreote, Jeff H. Chang, Joyce E. Loper
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	interspecific competition Pseudomonas secondary metabolism spontaneous mutations GacS-GacA Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d160e658f8c84183a5b8975b7cc9fd6a
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spelling	oai:doaj.org-article:d160e658f8c84183a5b8975b7cc9fd6a2021-11-15T15:53:25ZSecondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>10.1128/mBio.01845-172150-7511https://doaj.org/article/d160e658f8c84183a5b8975b7cc9fd6a2018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01845-17https://doaj.org/toc/2150-7511ABSTRACT Secondary metabolites are synthesized by many microorganisms and provide a fitness benefit in the presence of competitors and predators. Secondary metabolism also can be costly, as it shunts energy and intermediates from primary metabolism. In Pseudomonas spp., secondary metabolism is controlled by the GacS-GacA global regulatory system. Intriguingly, spontaneous mutations in gacS or gacA (Gac− mutants) are commonly observed in laboratory cultures. Here we investigated the role of secondary metabolism in the accumulation of Gac− mutants in Pseudomonas protegens strain Pf-5. Our results showed that secondary metabolism, specifically biosynthesis of the antimicrobial compound pyoluteorin, contributes significantly to the accumulation of Gac− mutants. Pyoluteorin biosynthesis, which poses a metabolic burden on the producer cells, but not pyoluteorin itself, leads to the accumulation of the spontaneous mutants. Interspecific competition also influenced the accumulation of the Gac− mutants: a reduced proportion of Gac− mutants accumulated when P. protegens Pf-5 was cocultured with Bacillus subtilis than in pure cultures of strain Pf-5. Overall, our study associated a fitness trade-off with secondary metabolism, with metabolic costs versus competitive benefits of production influencing the evolution of P. protegens, assessed by the accumulation of Gac− mutants. IMPORTANCE Many microorganisms produce antibiotics, which contribute to ecologic fitness in natural environments where microbes constantly compete for resources with other organisms. However, biosynthesis of antibiotics is costly due to the metabolic burdens of the antibiotic-producing microorganism. Our results provide an example of the fitness trade-off associated with antibiotic production. Under noncompetitive conditions, antibiotic biosynthesis led to accumulation of spontaneous mutants lacking a master regulator of antibiotic production. However, relatively few of these spontaneous mutants accumulated when a competitor was present. Results from this work provide information on the evolution of antibiotic biosynthesis and provide a framework for their discovery and regulation.Qing YanLucas D. LopesBrenda T. ShafferTeresa A. KidarsaOliver ViningBenjamin PhilmusChunxu SongVirginia O. StockwellJos M. RaaijmakersKerry L. McPhailFernando D. AndreoteJeff H. ChangJoyce E. LoperAmerican Society for Microbiologyarticleinterspecific competitionPseudomonassecondary metabolismspontaneous mutationsGacS-GacAMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	interspecific competition Pseudomonas secondary metabolism spontaneous mutations GacS-GacA Microbiology QR1-502
spellingShingle	interspecific competition Pseudomonas secondary metabolism spontaneous mutations GacS-GacA Microbiology QR1-502 Qing Yan Lucas D. Lopes Brenda T. Shaffer Teresa A. Kidarsa Oliver Vining Benjamin Philmus Chunxu Song Virginia O. Stockwell Jos M. Raaijmakers Kerry L. McPhail Fernando D. Andreote Jeff H. Chang Joyce E. Loper Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>
description	ABSTRACT Secondary metabolites are synthesized by many microorganisms and provide a fitness benefit in the presence of competitors and predators. Secondary metabolism also can be costly, as it shunts energy and intermediates from primary metabolism. In Pseudomonas spp., secondary metabolism is controlled by the GacS-GacA global regulatory system. Intriguingly, spontaneous mutations in gacS or gacA (Gac− mutants) are commonly observed in laboratory cultures. Here we investigated the role of secondary metabolism in the accumulation of Gac− mutants in Pseudomonas protegens strain Pf-5. Our results showed that secondary metabolism, specifically biosynthesis of the antimicrobial compound pyoluteorin, contributes significantly to the accumulation of Gac− mutants. Pyoluteorin biosynthesis, which poses a metabolic burden on the producer cells, but not pyoluteorin itself, leads to the accumulation of the spontaneous mutants. Interspecific competition also influenced the accumulation of the Gac− mutants: a reduced proportion of Gac− mutants accumulated when P. protegens Pf-5 was cocultured with Bacillus subtilis than in pure cultures of strain Pf-5. Overall, our study associated a fitness trade-off with secondary metabolism, with metabolic costs versus competitive benefits of production influencing the evolution of P. protegens, assessed by the accumulation of Gac− mutants. IMPORTANCE Many microorganisms produce antibiotics, which contribute to ecologic fitness in natural environments where microbes constantly compete for resources with other organisms. However, biosynthesis of antibiotics is costly due to the metabolic burdens of the antibiotic-producing microorganism. Our results provide an example of the fitness trade-off associated with antibiotic production. Under noncompetitive conditions, antibiotic biosynthesis led to accumulation of spontaneous mutants lacking a master regulator of antibiotic production. However, relatively few of these spontaneous mutants accumulated when a competitor was present. Results from this work provide information on the evolution of antibiotic biosynthesis and provide a framework for their discovery and regulation.
format	article
author	Qing Yan Lucas D. Lopes Brenda T. Shaffer Teresa A. Kidarsa Oliver Vining Benjamin Philmus Chunxu Song Virginia O. Stockwell Jos M. Raaijmakers Kerry L. McPhail Fernando D. Andreote Jeff H. Chang Joyce E. Loper
author_facet	Qing Yan Lucas D. Lopes Brenda T. Shaffer Teresa A. Kidarsa Oliver Vining Benjamin Philmus Chunxu Song Virginia O. Stockwell Jos M. Raaijmakers Kerry L. McPhail Fernando D. Andreote Jeff H. Chang Joyce E. Loper
author_sort	Qing Yan
title	Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>
title_short	Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>
title_full	Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>
title_fullStr	Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>
title_full_unstemmed	Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>
title_sort	secondary metabolism and interspecific competition affect accumulation of spontaneous mutants in the gacs-gaca regulatory system in <italic toggle="yes">pseudomonas protegens</italic>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/d160e658f8c84183a5b8975b7cc9fd6a
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Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in <italic toggle="yes">Pseudomonas protegens</italic>

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