Evolutionary patchwork of an insecticidal toxin shared between plant-associated pseudomonads and the insect pathogens Photorhabdus and Xenorhabdus

• DOI: 10.1186/s12864-015-1763-2
• Publication Date: 2015-08-14T23:22:15Z
• Authors: Beat Ruffner; Maria Péchy-Tarr; Monica Höfte; Guido Bloemberg; Jürg Grunder; Christoph Keel; Monika Maurhofer
• Keywords: Insecticides; Insecta; Gene Transfer, Horizontal; Bacterial Toxins; CATERPILLARS-FLOPPY MCF; Pseudomonas fluorescens; Insecticidal activity; HORIZONTAL GENE-TRANSFER; Xenorhabdus; Evolution, Molecular; 2_4-DIACETYLPHLOROGLUCINOL BIOSYNTHESIS; 03 medical and health sciences; Pseudomonas; Genetics; COMPLETE GENOME SEQUENCE; Animals; MAXIMUM-LIKELIHOOD; Photorhabdus and Xenorhabdus; Phylogeny; 0303 health sciences; Biology and Life Sciences; BLACK ROOT-ROT; Plants; BIOCONTROL FLUORESCENT PSEUDOMONADS; Toxin evolution; Multigene Family; PHENOTYPIC VARIATION; SP-NOV.; Pseudomonas; Photorhabdus and Xenorhabdus; Insecticidal activity; Toxin evolution; Photorhabdus; BIOLOGICAL-CONTROL; Biotechnology; Research Article

BMC Genomics, 16<br/>ISSN:1471-2164<br/>Background Root-colonizing fluorescent pseudomonads are known for their excellent abilities to protect plants against soil-borne fungal pathogens. Some of these bacteria produce an insecticidal toxin (Fit) suggesting that they may exploit insect hosts as a secondary niche. However, the ecological relevance of insect toxicity and the mechanisms driving the evolution of toxin production remain puzzling. Results Screening a large collection of plant-associated pseudomonads for insecticidal activity and presence of the Fit toxin revealed that Fit is highly indicative of insecticidal activity and predicts that Pseudomonas protegens and P. chlororaphis are exclusive Fit producers. A comparative evolutionary analysis of Fit toxin-producing Pseudomonas including the insect-pathogenic bacteria Photorhabdus and Xenorhadus, which produce the Fit related Mcf toxin, showed that fit genes are part of a dynamic genomic region with substantial presence/absence polymorphism and local variation in GC base composition. The patchy distribution and phylogenetic incongruence of fit genes indicate that the Fit cluster evolved via horizontal transfer, followed by functional integration of vertically transmitted genes, generating a unique Pseudomonas-specific insect toxin cluster. Conclusions Our findings suggest that multiple independent evolutionary events led to formation of at least three versions of the Mcf/Fit toxin highlighting the dynamic nature of insect toxin evolution.<br/>