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ARS Home » Pacific West Area » Corvallis, Oregon » Horticultural Crops Research » Research » Publications at this Location » Publication #347345

Research Project: Integrated Disease Management of Exotic and Emerging Plant Diseases of Horticultural Crops

Location: Horticultural Crops Research

Title: Secondary metabolism and interspecific competition affect accumulation of spontaneous mutants in the GacS-GacA regulatory system in Pseudomonas protegens

Author
item Yan, Qing - Oregon State University
item Lopes, Lucas Dantas - Universidade De Sao Paulo
item Shaffer, Brenda
item Kidarsa, Teresa - Former ARS Employee
item Vining, Oliver - Oregon State University
item Philmus, Benjamin - Oregon State University
item Song, Chunxu - Netherlands Institute Of Ecology
item Stockwell, Virginia
item Raaijmakers, Jos - Netherlands Institute Of Ecology
item Mcphail, Kerry - Oregon State University
item Andreote, Fernando Dini - Universidade De Sao Paulo
item Chang, Jeff - Oregon State University
item Loper, Joyce - Oregon State University

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/21/2017
Publication Date: 1/16/2018
Citation: Yan, Q., Lopes, L., Shaffer, B.T., Kidarsa, T.A., Vining, O., Philmus, B., Song, C., Stockwell, V.O., Raaijmakers, J., McPhail, K.L., Andreote, F., Chang, J.H., Loper, J.E. 2018. Secondary metabolism and interspecific competition affect accumulation of spontaneous mutants in the GacS-GacA regulatory system in Pseudomonas protegens. mBio. 9(1):e01845-17. https://doi.org/10.1128/mBio.01845-17.

Interpretive Summary: Many microorganisms produce antibiotics, which contribute to ecological fitness in natural environments where microbes consistently compete for resources with other organisms. However, biosynthesis of antibiotics is costly due to metabolic burdens posed to producing microorganism. Our results provide an example of the fitness trade-off associated with antibiotic production. Under non-competitive 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 inform on the evolution of antibiotic biosynthesis, and provide a framework for their discovery and regulation.

Technical 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 GacS/GacA global regulatory system. Intriguingly, spontaneous gacS/gacA mutants are commonly observed in laboratory cultures. Here we investigated the role of secondary metabolism in the accumulation of gacS/gacA mutants in P. protegens strain Pf-5. Our results showed that secondary metabolism, specifically biosynthesis of the antimicrobial compound pyoluteorin, contributes significantly to accumulation of gacS/gacA mutants. Pyoluteorin biosynthesis, which poses a metabolic burden to the producer cells, but not pyoluteorin itself, leads to the accumulation of the spontaneous mutants. Interspecific competition also influenced the accumulation of the gacS/gacA mutants: a reduced proportion of gacS/gacA mutants accumulated when P. protegens Pf-5 was co-cultured with Bacillus subtilis than in pure cultures of 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 gacS/gacA spontaneous mutants.