title: Host-Pathogen Coevolution: The Selective Advantage of Bacillus thuringiensis Virulence and Its Cry Toxin Genes.
abstract: Reciprocal coevolution between host and pathogen is widely seen as a major driver of evolution and biological innovation. Yet, to date, the underlying genetic mechanisms and associated trait functions that are unique to rapid coevolutionary change are generally unknown. We here combined experimental evolution of the bacterial biocontrol agent Bacillus thuringiensis and its nematode host Caenorhabditis elegans with large-scale phenotyping, whole genome analysis, and functional genetics to demonstrate the selective benefit of pathogen virulence and the underlying toxin genes during the adaptation process. We show that: (i) high virulence was specifically favoured during pathogen-host coevolution rather than pathogen one-sided adaptation to a nonchanging host or to an environment without host; (ii) the pathogen genotype BT-679 with known nematocidal toxin genes and high virulence specifically swept to fixation in all of the independent replicate populations under coevolution but only some under one-sided adaptation; (iii) high virulence in the BT-679-dominated populations correlated with elevated copy numbers of the plasmid containing the nematocidal toxin genes; (iv) loss of virulence in a toxin-plasmid lacking BT-679 isolate was reconstituted by genetic reintroduction or external addition of the toxins. We conclude that sustained coevolution is distinct from unidirectional selection in shaping the pathogen's genome and life history characteristics. To our knowledge, this study is the first to characterize the pathogen genes involved in coevolutionary adaptation in an animal host-pathogen interaction system.
authors.affiliation: Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts-University of Kiel, Kiel, Germany; Department of Animal Evolutionary Ecology, Institute of Evolution and Ecology, University of Tuebingen, Tuebingen, Germany.
authors.forename: Leila
authors.initials: L
authors.lastname: Masri
authors.affiliation: Institute for Evolution and Biodiversity, University of Muenster, Muenster, Germany.
authors.forename: Antoine
authors.initials: A
authors.lastname: Branca
authors.affiliation: Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts-University of Kiel, Kiel, Germany.
authors.forename: Anna E
authors.initials: AE
authors.lastname: Sheppard
authors.affiliation: Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts-University of Kiel, Kiel, Germany.
authors.forename: Andrei
authors.initials: A
authors.lastname: Papkou
authors.affiliation: Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts-University of Kiel, Kiel, Germany; Department of Animal Evolutionary Ecology, Institute of Evolution and Ecology, University of Tuebingen, Tuebingen, Germany.
authors.forename: David
authors.initials: D
authors.lastname: Laehnemann
authors.affiliation: Department of Animal Evolutionary Ecology, Institute of Evolution and Ecology, University of Tuebingen, Tuebingen, Germany.
authors.forename: Patrick S
authors.initials: PS
authors.lastname: Guenther
authors.affiliation: Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts-University of Kiel, Kiel, Germany.
authors.forename: Swantje
authors.initials: S
authors.lastname: Prahl
authors.affiliation: Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts-University of Kiel, Kiel, Germany.
authors.forename: Manja
authors.initials: M
authors.lastname: Saebelfeld
authors.affiliation: Goettingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August-University of Goettingen, Goettingen, Germany.
authors.forename: Jacqueline
authors.initials: J
authors.lastname: Hollensteiner
authors.affiliation: Goettingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August-University of Goettingen, Goettingen, Germany.
authors.forename: Heiko
authors.initials: H
authors.lastname: Liesegang
authors.affiliation: Goettingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August-University of Goettingen, Goettingen, Germany.
authors.forename: Elzbieta
authors.initials: E
authors.lastname: Brzuszkiewicz
authors.affiliation: Goettingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August-University of Goettingen, Goettingen, Germany.
authors.forename: Rolf
authors.initials: R
authors.lastname: Daniel
authors.affiliation: Department of Animal Evolutionary Ecology, Institute of Evolution and Ecology, University of Tuebingen, Tuebingen, Germany.
authors.forename: Nicolaas K
authors.initials: NK
authors.lastname: Michiels
authors.affiliation: Department of Behavioural Biology, University of Osnabrueck, Osnabrueck, Germany.
authors.forename: Rebecca D
authors.initials: RD
authors.lastname: Schulte
authors.affiliation: Institute for Evolution and Biodiversity, University of Muenster, Muenster, Germany.
authors.forename: Joachim
authors.initials: J
authors.lastname: Kurtz
authors.affiliation: Institute for Clinical Molecular Biology, Christian-Albrechts-University, Kiel, Germany.
authors.forename: Philip
authors.initials: P
authors.lastname: Rosenstiel
authors.affiliation: Institute for Evolution and Biodiversity, University of Muenster, Muenster, Germany.
authors.forename: Arndt
authors.initials: A
authors.lastname: Telschow
authors.affiliation: Institute for Evolution and Biodiversity, University of Muenster, Muenster, Germany.
authors.forename: Erich
authors.initials: E
authors.lastname: Bornberg-Bauer
authors.affiliation: Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts-University of Kiel, Kiel, Germany; Department of Animal Evolutionary Ecology, Institute of Evolution and Ecology, University of Tuebingen, Tuebingen, Germany.
authors.forename: Hinrich
authors.initials: H
authors.lastname: Schulenburg
mesh_terms: D000818:Animals; D001413:Bacillus thuringiensis / Q000235:genetics* / Q000472:pathogenicity; D001426:Bacterial Proteins / Q000235:genetics*; D005075:Biological Evolution; D017173:Caenorhabditis elegans / Q000382:microbiology; D016680:Genome, Bacterial; D023281:Genomics; D005838:Genotype; D054884:Host-Pathogen Interactions / Q000235:genetics*; D019476:Insect Proteins; D010641:Phenotype; D011956:Receptors, Cell Surface / Q000235:genetics*; D012641:Selection, Genetic; D014774:Virulence
chemical_list: D001426:Bacterial Proteins; C095416:Cry toxin receptors; D019476:Insect Proteins; D011956:Receptors, Cell Surface