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

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    Author
    Driscoll, T.P.
    Verhoeve, V.I.
    Brockway, C.
    Shrewsberry, D.L.
    Plumer, M.
    Sevdalis, S.E.
    Beckmann, J.F.
    Krueger, L.M.
    Macaluso, K.R.
    Azad, A.F.
    Gillespie, J.J.
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    Date
    2020-12-17
    Journal
    PeerJ
    Publisher
    PeerJ Inc.
    Type
    Article
    
    Metadata
    Show full item record
    See at
    https://doi.org/10.7717/peerj.10646
    Abstract
    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. Copyright 2020 PeerJ Inc.. All rights reserved.
    Sponsors
    This work was supported with funds from the National Institutes of Health National Institute of Allergy and Infectious Diseases grants (R21AI26108 and R21AI146773.
    Keyword
    Biotin operon
    Cat flea
    Ctenocephalides felis
    Cytoplasmic incompatibility
    Lateral gene transfer
    Mutualism
    Reproductive parasitism
    Wolbachia
    Identifier to cite or link to this item
    http://hdl.handle.net/10713/14531
    ae974a485f413a2113503eed53cd6c53
    10.7717/peerj.10646
    Scopus Count
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