Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas

PeerJ

article

Timothy P. Driscoll¹  Victoria I. Verhoeve²  Cassia Brockway¹  Darin L. Shrewsberry¹  Mariah Plumer²  Spiridon E. Sevdalis²  John F. Beckmann³  Laura M. Krueger⁴  Kevin R. Macaluso⁵  Abdu F. Azad²  Joseph J. Gillespie² 

[1] Biology, West Virginia University;Microbiology and Immunology, University of Maryland at Baltimore;Entomology and Plant Pathology, Auburn University;Orange County Mosquito and Vector Control District;Microbiology and Immunology, University of South Alabama

关键词: Wolbachia;    Ctenocephalides felis;    Cat flea;    Reproductive parasitism;    Mutualism;    Lateral gene transfer;    Cytoplasmic incompatibility;    Biotin operon;   

DOI  :  10.7717/peerj.10646

学科分类：社会科学、人文和艺术（综合）

来源: Inra

【 摘 要 】

Wolbachiae are obligate intracellular bacteria that infect arthropods and certain nematodes. Usually maternally inherited, they may provision nutrients to (mutualism) or alter sexual biology of (reproductive parasitism) their invertebrate hosts. We report the assembly of closed genomes for two novel wolbachiae, wCfeT and wCfeJ, found co-infecting cat fleas (Ctenocephalides felis) of the Elward Laboratory colony (Soquel, CA, USA). wCfeT is basal to nearly all described Wolbachia supergroups, while wCfeJ is related to supergroups C, D and F. Both genomes contain laterally transferred genes that inform on the evolution of Wolbachia host associations. wCfeT carries the Biotin synthesis Operon of Obligate intracellular Microbes (BOOM); our analyses reveal five independent acquisitions of BOOM across the Wolbachia tree, indicating parallel evolution towards mutualism. Alternately, wCfeJ harbors a toxin-antidote operon analogous to the wPip cinAB operon recently characterized as an inducer of cytoplasmic incompatibility (CI) in flies. wCfeJ cinB and three adjacent genes are collectively similar to large modular toxins encoded in CI-like operons of certain Wolbachia strains and Rickettsia species, signifying that CI toxins streamline by fission of large modular toxins. Remarkably, the C. felis genome itself contains two CI-like antidote genes, divergent from wCfeJ cinA, revealing episodic reproductive parasitism in cat fleas and evidencing mobility of CI loci independent of WO-phage. Additional screening revealed predominant co-infection (wCfeT/wCfeJ) amongst C. felis colonies, though fleas in wild populations mostly harbor wCfeT alone. Collectively, genomes of wCfeT, wCfeJ, and their cat flea host supply instances of lateral gene transfers that could drive transitions between parasitism and mutualism.

【 授权许可】

CC BY