1. ¹Institute of Zoology, Darmstadt University of Technology, Darmstadt, Germany
2. ²Département de Microbiologie Fondamentale, Université de Lausanne, Lausanne, Switzerland

Correspondence: A Jousset, Institute of Zoology, Darmstadt University of Technology, Schnittspahnstr. 3, D-64287 Darmstadt, Germany. E-mail: alexandre.jousset@gmx.net

³These authors contributed equally to this study.

⁴Current address: Terrestrial Ecology and Rhizosphere Research, Institute of Zoology, University of Cologne, Weyertal 119, 50931 Köln, Germany

⁵Current address: JF Blumenbach Institute of Zoology and Anthropology, Georg August University of Göttingen, Berliner Street 28, 37073 Göttingen, Germany

Received 12 January 2009; Revised 13 February 2009; Accepted 17 February 2009; Published online 26 March 2009.

Abstract

Soil pseudomonads increase their competitiveness by producing toxic secondary metabolites, which inhibit competitors and repel predators. Toxin production is regulated by cell–cell signalling and efficiently protects the bacterial population. However, cell communication is unstable, and natural populations often contain signal blind mutants displaying an altered phenotype defective in exoproduct synthesis. Such mutants are weak competitors, and we hypothesized that their fitness depends on natural communities on the exoproducts of wild-type bacteria, especially defence toxins. We established mixed populations of wild-type and signal blind, non-toxic gacS-deficient mutants of Pseudomonas fluorescens CHA0 in batch and rhizosphere systems. Bacteria were grazed by representatives of the most important bacterial predators in soil, nematodes (Caenorhabditis elegans) and protozoa (Acanthamoeba castellanii). The gacS mutants showed a negative frequency-dependent fitness and could reach up to one-third of the population, suggesting that they rely on the exoproducts of the wild-type bacteria. Both predators preferentially consumed the mutant strain, but populations with a low mutant load were resistant to predation, allowing the mutant to remain competitive at low relative density. The results suggest that signal blind Pseudomonas increase their fitness by exploiting the toxins produced by wild-type bacteria, and that predation promotes the production of bacterial defence compounds by selectively eliminating non-toxic mutants. Therefore, predators not only regulate population dynamics of soil bacteria but also structure the genetic and phenotypic constitution of bacterial communities.