Evolutionary patchwork of an insecticidal toxin shared between plant-associated pseudomonads and the insect pathogens Photorhabdus and Xenorhabdus.
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.
Pathology, Institute of Integrative Biology, ETH Zurich, Universitätstrasse 2, CH-8092, Zurich, Switzerland. beat.ruffner@usys.ethz.ch.
Beat
B
Ruffner
Department of Fundamental Microbiology, University of Lausanne, Biophore Building, CH-1015, Lausanne, Switzerland. maria.pechy-tarr@unil.ch.
Maria
M
Péchy-Tarr
Laboratory of Phytopathology, Department of Crop Protection, Ghent University, Ghent, Belgium. monica.hofte@ugent.be.
Monica
M
Höfte
Institute of Medical Microbiology, University of Zurich, Zurich, Switzerland. bloemberg@imm.uzh.ch.
Guido
G
Bloemberg
Natural Resources Sciences, University of Applied Sciences ZHAW, Wädenswil, Switzerland.
Jürg
J
Grunder
Department of Fundamental Microbiology, University of Lausanne, Biophore Building, CH-1015, Lausanne, Switzerland. christoph.keel@unil.ch.
Christoph
C
Keel
Pathology, Institute of Integrative Biology, ETH Zurich, Universitätstrasse 2, CH-8092, Zurich, Switzerland. monika.maurhofer@usys.ethz.ch.
Monika
M
Maurhofer
D000818:Animals; D001427:Bacterial Toxins / Q000235:genetics*; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D007313:Insecta / Q000382:microbiology; D007306:Insecticides / Q000494:pharmacology; D005810:Multigene Family; D020637:Photorhabdus / Q000235:genetics / Q000378:metabolism*; D010802:Phylogeny; D010944:Plants / Q000382:microbiology; D011551:Pseudomonas fluorescens / Q000235:genetics / Q000378:metabolism*; D020593:Xenorhabdus / Q000235:genetics / Q000378:metabolism*
D001427:Bacterial Toxins; D007306:Insecticides