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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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Evolution of Wolbachia Mutualism and Reproductive Parasitism: Insight from Two Novel Strains That Co-Infect Cat Fleas bioRxiv preprint doi: https://doi.org/10.1101/2020.06.01.128066; this version posted June 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 1 Evolution of Wolbachia Mutualism and Reproductive Parasitism: 2 Insight from Two Novel Strains that Co-infect Cat Fleas 3 4 Timothy P. Driscoll a, Victoria I. Verhoeve b, Cassia Brockway a, Darin L. Shrewsberry a, 5 Mariah L. Plumer b, Spiridon E. Sevdalis b, John F. Beckmann c, Laura M. Krueger 6 Prelesnik d, Kevin R. Macaluso e, Abdu F. Azad b, Joseph J. Gillespie b,# 7 8 a Department of Biology, West Virginia University, Morgantown, West Virginia. 9 b Department of Microbiology and Immunology, University of Maryland School of 10 Medicine, Baltimore, Maryland. 11 c Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama. 12 d Orange County Mosquito and Vector Control District, Garden Grove, California. 13 e Department of Microbiology and Immunology, University of South Alabama, Mobile, 14 Alabama. 15 16 Running Head: Mechanisms of Evolution in Wolbachia-host associations 17 18 # Address correspondence to: Joe Gillespie, [email protected] 19 Timothy P. Driscoll and Victoria I. Verhoeve contributed equally to this work. Author 20 order is alphabetical. bioRxiv preprint doi: https://doi.org/10.1101/2020.06.01.128066; this version posted June 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Mechanisms of Evolution in Wolbachia-host associations 2 21 Abstract 22 Wolbachiae are obligate intracellular bacteria that infect arthropods and certain 23 nematodes. Usually maternally inherited, they may provision nutrients to (mutualism) or 24 alter sexual biology of (reproductive parasitism) their invertebrate hosts. We report the 25 assembly of closed genomes for two novel wolbachiae, wCfeT and wCfeJ, found co- 26 infecting cat fleas (Ctenocephalides felis) of the Elward Laboratory colony (Soquel, CA). 27 wCfeT is basal to nearly all described Wolbachia supergroups, while wCfeJ is related to 28 supergroups C, D and F. Both genomes contain laterally transferred genes that inform 29 on the evolution of Wolbachia host associations. wCfeT carries the Biotin synthesis 30 Operon of Obligate intracellular Microbes (BOOM); our analyses reveal five 31 independent acquisitions of BOOM across the Wolbachia tree, indicating parallel 32 evolution towards mutualism. Alternately, wCfeJ harbors a toxin-antidote operon 33 analogous to the wPip cinAB operon recently characterized as an inducer of 34 cytoplasmic incompatibility (CI) in flies. wCfeJ cinB and immediate-5’ end genes are 35 syntenic to large modular toxins encoded in CI-like operons of certain Wolbachia strains 36 and Rickettsia species, signifying that CI toxins streamline by fission of larger toxins. 37 Remarkably, the C. felis genome itself contains two CI-like antidote genes, divergent 38 from wCfeJ cinA, revealing episodic reproductive parasitism in cat fleas and evidencing 39 mobility of CI loci independent of WO-phage. Additional screening revealed 40 predominant co-infection (wCfeT/wCfeJ) amongst C. felis colonies, though occasionally 41 wCfeJ singly infects fleas in wild populations. Collectively, genomes of wCfeT, wCfeJ, 42 and their cat flea host supply instances of lateral gene transfers that could drive 43 transitions between parasitism and mutualism. bioRxiv preprint doi: https://doi.org/10.1101/2020.06.01.128066; this version posted June 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Mechanisms of Evolution in Wolbachia-host associations 3 44 Importance 45 Many arthropod and certain nematode species are infected with wolbachiae which are 46 intracellular bacteria well known for reproductive parasitism (RP). Like other RP 47 strategies, Wolbachia-induced cytoplasmic incompatibility, CI, increases prevalence and 48 frequency in host populations. Mutualism is another strategy employed by wolbachiae 49 to maintain host infection, with some strains synthesizing and supplementing certain B 50 vitamins (particularly biotin) to invertebrate hosts. Curiously, we discovered two novel 51 Wolbachia strains that co-infect cat fleas (Ctenocephalides felis): wCfeT carries biotin 52 synthesis genes, while wCfeJ carries a CI-inducing toxin-antidote operon. Our analyses 53 of these genes highlight their mobility across the Wolbachia phylogeny and source to 54 other intracellular bacteria. Remarkably, the C. felis genome also carries two CI-like 55 antidote genes divergent from the wCfeJ antidote gene, indicating episodic RP in cat 56 fleas. Collectively, wCfeT and wCfeJ inform on the rampant dissemination of diverse 57 factors that mediate Wolbachia strategies for persisting in invertebrate host populations. 58 59 Key words 60 Wolbachia, Ctenocephalides felis, cat flea, reproductive parasitism, mutualism, lateral 61 gene transfer, cytoplasmic incompatibility, biotin operon 62 63 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.01.128066; this version posted June 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Mechanisms of Evolution in Wolbachia-host associations 4 64 Introduction 65 Wolbachiae (Alphaproteobacteria: Rickettsiales: Anaplasmataceae) comprise Gram- 66 negative, obligate intracellular bacteria that infect over half the world’s described insect 67 species as well as certain parasitic nematodes (1). Unlike other notable rickettsial 68 genera that contain human pathogens (e.g., Rickettsia, Orientia, Neorickettsia, 69 Anaplasma, and Ehrlichia), wolbachiae do not infect vertebrates (2). A single species, 70 Wolbachia pipientis, is formally recognized with numerous members designated as 71 strains within 15 reported supergroups (3–9). Genomic divergence indicates further 72 species names are warranted (10), though increasing diversity and community 73 consensus suggest caution regarding further Wolbachia classification at the species 74 level (11, 12). 75 Like other obligate intracellular microbes, wolbachiae are metabolic parasites that 76 complement a generally reduced metabolism with pilfering of host metabolites (13, 14)). 77 Their ability to survive and flourish is also heavily influenced by the acquisition of key 78 functions through lateral gene transfer (LGT). Several described Wolbachia strains 79 demonstrate characteristics of limited mutualism with their invertebrate partner (15, 16), 80 through the synthesis and provisioning of riboflavin (17) and biotin (18, 19). While 81 riboflavin biosynthesis genes are highly conserved in wolbachiae (20), biotin 82 biosynthesis genes are rare and likely originated via LGT with taxonomically divergent 83 intracellular bacteria (21). Still other strains of Wolbachia exert varying degrees of 84 reproductive parasitism (RP) on their insect host (22), influencing host sexual 85 reproduction via processes such as male-killing, feminization, parthenogenesis and 86 cytoplasmic incompatibility (CI) (23). Wolbachia genes underpinning CI and male bioRxiv preprint doi: https://doi.org/10.1101/2020.06.01.128066; this version posted June 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Mechanisms of Evolution in Wolbachia-host associations 5 87 killing have been characterized (24–29) and occur predominantly in the eukaryotic 88 association module (EAM) of Wolbachia prophage genomes (30). These genes 89 highlight the role of LGT in providing wolbachiae with factors facilitating mutualism or 90 RP, both of which are highly successful strategies for increasing infection frequency in 91 invertebrate host populations. 92 Compared to reproductive parasites, Wolbachia mutualists appear to form more 93 stable, long-term relationships with their hosts, as supported by Wolbachia-host 94 codivergence in certain filarial nematodes (31) and Nomada bees (32). In contrast to 95 the stability of mutualists, relationships of reproductive parasites appear more 96 ephemeral. RP can be a strong mechanism to increase infection frequency, and CI 97 inducing strains can replace populations without infections (33, 34). Despite this, CI is 98 prone to neutralization through the evolution of host suppression (23, 35, 36) and 99 purifying selection on the host doesn’t preserve CI (36). A weakened CI background 100 might be a ripe setting for invasions to begin. Whether invasion occurs at the level of 101 alternate wolbachiae, WO-phages, or CI operons themselves is an area of active 102 evolutionary research, but a clear result of this evolutionary complexity is that RP 103 inducing Wolbachia phylogenies are discordant with those of their hosts (37–39). 104 Horizontal transmissions, which can occur through direct
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