Host–pathogen coevolution: The selective advantage of Bacillus thuringiensis virulence and its cry toxin genes

Autor: Jacqueline Hollensteiner, Patrick S. Guenther, Manja Saebelfeld, Arndt Telschow, Joachim Kurtz, Leila Masri, Hinrich Schulenburg, Rebecca D. Schulte, Andrei Papkou, Heiko Liesegang, Elzbieta Brzuszkiewicz, Anna E. Sheppard, Erich Bornberg-Bauer, Philip Rosenstiel, Antoine Branca, David Laehnemann, Swantje Prahl, Rolf Daniel, N. K. Michiels
Rok vydání: 2015
Předmět:
0106 biological sciences
Genotype
QH301-705.5
Bacillus thuringiensis
Virulence
Receptors
Cell Surface
Biology
010603 evolutionary biology
01 natural sciences
Genome
General Biochemistry
Genetics and Molecular Biology
03 medical and health sciences
Plasmid
Bacterial evolution
Bacterial pathogens
Coevolution
Evolutionary adaptation
Genome evolution
Host-pathogen interactions
Toxins
Bacterial Proteins
Animals
Biology (General)
Selection
Genetic
Caenorhabditis elegans
Gene
Pathogen
030304 developmental biology
Genetics
0303 health sciences
Experimental evolution
General Immunology and Microbiology
General Neuroscience
Genomics
Biological Evolution
Phenotype
Host-Pathogen Interactions
Insect Proteins
570 Life sciences
biology
Adaptation
General Agricultural and Biological Sciences
Genome
Bacterial
Research Article
Zdroj: PLoS Biology
PLoS Biology, Vol 13, Iss 6, p e1002169 (2015)
Popis: 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.
A combination of experimental evolution with large-scale phenotyping, genomics and functional genetics reveals the specific role of virulence and toxin genes during the evolutionary adaptation of a pathogen to an animal host.
Author Summary Evolution can be extremely fast and dramatic, especially when infectious disease agents such as bacterial pathogens engage in a continuous arms race with their host organism. Rounds of novel pathogen attack strategies and associated host counterdefenses conspire to drive host–pathogen coevolution and biological innovation. To better understand the underlying genetic mechanisms and the exact trait characteristics under selection, we conducted experimental evolution using a simple host–pathogen model system (nematode versus bacterium) under controlled laboratory conditions. We analysed the associated adaptive changes in real time using large-scale phenotyping, population whole genome sequencing, and genetic analysis of the identified candidate genes. We show that coevolution (rather than one-sided adaptation) particularly favors and maintains pathogen virulence, and that two specific toxin genes significantly influence this virulence during coevolution.
Databáze: OpenAIRE
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