Secondary metabolite production facilitates establishment of rhizobacteria by reducing both protozoan predation and the competitive effects of indigenous bacteria

Abstract

Summary 1.Rhizosphere bacteria live in close contact to plant roots feeding on root exudates and rhizodeposits. By producing toxic exoproducts rhizobacteria may inhibit plant pathogens thereby functioning as biocontrol agents and increasing plant fitness. However, the evolutionary basis why rhizobacteria protect plants is little understood. To persist toxin production needs to improve the competitiveness of the bacteria themselves. 2. We investigated the importance of secondary metabolite production for the establishment of the model soil biocontrol bacterium Pseudomonas fluorescens CHA0 in the rhizosphere of rice. We compared the performance of this toxin-producing strain and its isogenic gacS deficient mutant defective in secondary metabolite production. The bacteria were added to the rhizosphere of rice, where they had to compete with the indigenous flora for resources and to resist predation by the protist Acanthamoeba castellanii . 3. Secondary metabolite production strongly enhanced the establishment of the inoculated bacteria by improving competitive strength and predator resistance. The fitness gain due to attenuation of predation exceeded that due to competition by a factor of 2-3, confirming the importance of grazing resistance for rhizosphere bacteria. 4. Biocontrol properties of Plant Growth Promoting Bacteria such as P. fluorescens therefore gain a new dimension. Toxicity primary plays a role in the interaction with competitors and especially predators, and not in the protection of the host plant. Thus, establishment and efficiency of biocontrol bacteria may be improved by fostering predator defence via toxin production.

Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana

“…The strong and highly reproducible changes in the gacA-banding pattern further revealed a major shift in this master gene controlling antibiotics production of pseudomonads (De Souza et al, 2003). We suggest that pseudomonads quickly upregulated secondary metabolite production in response to protozoan predators, which is in accordance with Jousset et al (2006) who demonstrated that antibiotics of P. fluorescens are of particular toxicity to protozoa; and that antibiotic-producing P. fluorescens disproportionally benefit from protozoan predation when their bacterial competitors are consumed and nutrients excreted by the protozoan predators (Jousset et al, 2008).…”

“…Soil amoebae have been shown to graze preferentially on Gram-negative bacteria (Foster and Dormaar, 1991;Andersen and Winding, 2004). Not surprising, the gacA regulated antibiotic production of pseudomonads has been found to play also a significant role in bacterial defence against protozoan predators (Jousset et al, 2006(Jousset et al, , 2008.…”

Sanctions, Cooperation, and the Stability of Plant-Rhizosphere Mutualisms

“…Data showing a role for phenazine antibiotics in microbial competitiveness (Mazzola et al 1992) are consistent with our hypothesis that antibiotic production does not depend on whether plants benefit. This conclusion is emphasized by more recent results, including bacteriocin-mediated antagonism among G. diazotrophicus strains (Munoz-Rojas et al 2005) and a role for antibiotics in defense against predation by protozoa and competition with other bacteria (Jousset et al 2006(Jousset et al , 2008.…”

Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters

“…Fluorescent pseudomonads are ubiquitous rhizosphere bacteria, and many species produce toxic exoproducts that increase their resistance to microfaunal predators and improve their competitiveness against other bacteria (Jousset et al, 2008). These toxins often inhibit plant pathogens, making pseudomonads as potent biological control agents in agricultural systems (Haas and Defago, 2005).…”