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ARS Home » Pacific West Area » Corvallis, Oregon » Horticultural Crops Research Unit » Research » Publications at this Location » Publication #317949
Title: Living on the edge: Emergence of spontaneous gac mutations in Pseudomonas protegens during swarming motility

Author
item SONG, CHUNXU - Wageningen University
item KIDARSA, TERESA - Former ARS Employee
item VAN DE MORTEL, JUDITH - Wageningen University
item Loper, Joyce
item RAAIJMAKERS, JOS - Wageningen University

Submitted to: Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/2/2016
Publication Date: 3/4/2016
Citation: Song, C., Kidarsa, T., Van De Mortel, J.E., Loper, J.E., Raaijmakers, J.M. 2016. Living on the edge: Emergence of spontaneous gac mutations in Pseudomonas protegens during swarming motility. Environmental Microbiology. 18(10):3453-3465. doi: 10.1111/1462-2920.13288.

Interpretive Summary: Biological control provides a promising strategy for managing plant diseases, but has not yet been utilized widely in agriculture due, in part, to unexplained variation in its success in managing disease. Our research focuses on Pseudomonas fluorescens, which is a group of bacteria that occurs naturally on plant surfaces such as leaves and roots and includes many strains with biological control activity including Pseudomonas protegens Pf-5. In this study, we evaluated the evolution of P. protegens Pf-5 in expanding colonies of the bacterium. We show that mutations in two genes of a two-component regulatory system (gacA and gacA) accumulate at the periphery of these colonies. To explore the reason for this accumulation, we evaluated the transcriptomes of Pf-5 and a gacA mutant at different sites in the expanding colony. We found that the gacA mutant overexpresses genes required for resource acquisition and motility, which may explain the predominance of these mutants at the periphery of expanding colonies. This research provides information about the factors that influence the fitness and evolution of a biological control bacterium.

Technical Abstract: Swarming motility is a flagella-driven multicellular behavior that allows bacteria to colonize new niches and escape competition. Here, we investigated the spatial distribution and evolution of ‘social cheaters’ in swarming colonies of Pseudomonas protegens Pf-5. Lipopeptide surfactants in the orfamide family are produced by Pf-5 and essential for swarming motility. Two orfamide-deficient mutants, with deletions in the biosynthesis gene ofaA or in the regulatory gene gacA, cannot swarm on their own but ‘hitch-hiked’ with wildtype Pf-5. Both mutants typify social cheaters with respect to swarming motility but exhibit distinctly different spatial distributions in co-swarming colonies, with the ofaA mutant moving behind the wildtype and the gacA mutant predominating on the edge. Experimental evolution assays showed that repeated rounds of swarming by wildtype Pf-5 drives parallel evolution toward accumulation of gacS/gacA spontaneous mutants on the swarming edge. The emergence of these cheaters is context dependent as they were not detected under non-swarming conditions. Results further showed that swarming colonies collapsed with increasing frequencies of gacA mutants. Subsequent whole-genome transcriptome analyses revealed that genes associated with resource acquisition, motility, chemotaxis and efflux were significantly upregulated in gacA mutants. Moreover, gacA mutant cells were longer and more flagellated than wildtype and ofaA mutant cells, which may explain their predominance on the edge of co-swarming colonies. We postulate that adaptive convergent evolution through point mutations is a common feature of range-expanding microbial populations and that the putative fitness benefits of these mutations during dispersal of bacteria into new territories are frequency-dependent.