Novel mechanism of metabolic co-regulation coordinates the biosynthesis of secondary metabolites in Pseudomonas protegens

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Abstract

Metabolic co-regulation between biosynthetic pathways for secondary metabolites is common in microbes and can play an important role in microbial interactions. Here, we describe a novel mechanism of metabolic co-regulation in which an intermediate in one pathway is converted into signals that activate a second pathway. Our study focused on the co-regulation of 2,4-diacetylphloroglucinol (DAPG) and pyoluteorin, two antimicrobial metabolites produced by the soil bacterium Pseudomonas protegens. We show that an intermediate in DAPG biosynthesis, phloroglucinol, is transformed by a halogenase encoded in the pyoluteorin gene cluster into mono- and di-chlorinated phloroglucinols. The chlorinated phloroglucinols function as intra- and inter-cellular signals that induce the expression of pyoluteorin biosynthetic genes, pyoluteorin production, and pyoluteorin-mediated inhibition of the plant-pathogenic bacterium Erwinia amylovora. This metabolic co-regulation provides a strategy for P. protegens to optimize the deployment of secondary metabolites with distinct roles in cooperative and competitive microbial interactions.

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Qing Yan

Department of Botany and Plant Pathology, Oregon State University, Corvallis, United States

Competing interests
The authors declare that no competing interests exist.
Benjamin Philmus

Department of Pharmaceutical Sciences, Oregon State University, Corvallis, United States

Competing interests
The authors declare that no competing interests exist.
Jeff H Chang

Department of Botany and Plant Pathology, Oregon State University, Corvallis, United States

Competing interests
The authors declare that no competing interests exist.
Joyce E Loper

Department of Botany and Plant Pathology, Oregon State University, Corvallis, United States

For correspondence
joyce.loper@oregonstate.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3501-5969

Funding

National Institute of Food and Agriculture (NRI 2011-67019-30192)

Jeff H Chang
Joyce E Loper

Oregon State University (Research startup funds)

Benjamin Philmus

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.