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Downloaded Uniprot Sequence Alignments from the Pfam Database (Finn Et Al., 2016) for The bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.165548; this version posted June 24, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 3 Rapid molecular evolution of S piroplasma symbionts of 4 Drosophila 5 0ichael Gerth 1*, Humberto 0artinez-Montoya 2, 3aulino Ramirez3 , Florent 0asson 4 , -oanne 6 S. Griffin 1, Rodolfo Aramayo 5, Stefanos Siozios 1, Bruno /emaitre4 , 0ariana 0ateos 6 7 Gregory D.D. Hurst 1 8 1 ,nstitute of ,nfection, 9eterinary and Ecological Sciences, 8niversity of /iverpool, /iverpool, 8. 9 2 /aEoratory of Genetics and Comparative Genomics, 8nidad Acadpmica 0ultidisciplinaria Reynosa : Aztlin, 8niversidad Autynoma de Tamaulipas, Reynosa, 0exico ; 3 Department of Cell Systems and Anatomy, 8niversity of Texas Health San Antonio, San Antonio, 32 Texas, 8SA 33 4 GloEal Health ,nstitute, School of /ife Sciences, ecole PolytechniTue Fpdprale de 34 /ausanne, /ausanne, Switzerland 35 5 Department of Biology, Texas A 0 8niversity, College Station, Texas, 8SA 36 6 Department of Ecology and Conservation Biology, Texas A 0 8niversity, College Station, Texas, 37 8SA 38 *Author for correspondence. 39 Current address: Department of Biological and 0edical Sciences, 2xford BrooNes 8niversity, 2xford, 3: 8. mgerth#ErooNes.ac.uN bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.165548; this version posted June 24, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 3; AEstract 42 Spiroplasma are a group of 0ollicutes whose members include plant pathogens, insect 43 pathogens, and endosymbionts of animals. In arthropods, Spiroplasma are found across a 44 broad host range, but typically with lower incidence than other bacteria with similar ecology, 45 such as :olbachia or RicNettsia. Spiroplasma symbionts of Drosophila are best known as 46 male-killers and protective symbionts, and both phenotypes are mediated by 47 Spiroplasma-encoded toxins. Spiroplasma phenotypes have been repeatedly observed to be 48 spontaneously lost in Drosophila cultures, and several studies have documented a high 49 genomic turnover in Spiroplasma symbionts and plant pathogens. These observations suggest 4: that Spiroplasma evolves quickly. Here, we systematically assess evolutionary rates and 4; patterns of Spiroplasma poulsonii , a natural symbiont of Drosophila . :e analysed genomic 52 evolution of sHy within flies, and s0el within in vitro culture over several years. :e 53 observed that S. poulsonii substitution rates are among the highest reported for any bacteria, 54 and markedly increased compared with other symbionts. The absence of mismatch repair loci 55 mutS and mut/ is conserved across Spiroplasma and likely contributes to elevated substitution 56 rates. Further, the closely related strains s0el and sHy (>99.5% sequence identity in shared 57 loci) show extensive structural genomic differences, which may be explained by a higher 58 degree of host adaptation in s Hy, a protective symbiont of Drosophila hydei . Finally, 59 comparison across diverse Spiroplasma lineages confirms previous reports of dynamic 5: evolution of toxins, and identifies loci similar to the male-killing toxin Spaid in several 5; Spiroplasma lineages and other endosymbionts. 2verall, our results highlight the peculiar 62 nature of Spiroplasma genome evolution, which may explain unusual features of its 63 evolutionary ecology. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.165548; this version posted June 24, 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 4.0 International license. 64 ,ntroduction 65 0any bacterial lineages have evolved to become associates of animal hosts (McFall-Ngai et 66 al., 2013) . In arthropods, such associations are the rule, and maternally inherited, 67 endosymbiotic bacteria are especially common and diverse (Duron et al., 2008; :einert et al., 68 2015) . 3rominent examples include obligate nutritional symbionts of blood and sap feeders 69 (Douglas, 2009) , reproductive manipulators (Drew et al., 2019) , and protective symbionts 6: (Oliver et al., 2014) . Collectively, inherited symbionts of arthropods are highly diverse with 6; respect to potential benefits and costs induced, and their degree of adaptation to hosts. For 72 example, even within a single lineage of inherited symbionts - :olbachia - there are 73 nutritional mutualists (Hosokawa et al., 2010), protective symbionts (Teixeira et al., 2008) , 74 and reproductive manipulators (Dyson et al., 2002) . Importantly, these symbiont-conferred 75 traits may be modulated by environmental factors (Corbin et al., 2017) and host genetic 76 background (Hornett et al., 2008) . 77 Spiroplasma are small, helical bacteria that lack cell-walls. /ike other 0ollicutes 78 (Mycoplasma-like organisms), they are exclusively found in host association and are often 79 pathogenic (Razin, 2006) . Among the first discovered spiroplasmas were plant pathogens 7: (reviewed in Saglio and :hitcomb, 1979) and an inherited symbiont of Drosophila with the 7; ability to shift sex ratios towards females (Poulson and Sakaguchi, 1961). Subsequently, 82 Spiroplasma symbionts were found in a number of different Drosophila species (Haselkorn, 83 2010) , as well as many other arthropods (Gasparich, 2002) . 0ore recently, molecular 84 evidence was brought forward for Spiroplasma symbionts in non-arthropod animals 85 (Duperron et al., 2013; He et al., 2018) . In insects, two phenotypes induced by inherited 86 Spiroplasma have been studied in detail (reviewed in Anbutsu and Fukatsu, 2011; Ballinger 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.165548; this version posted June 24, 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 4.0 International license. 87 and 3erlman, 2019) . Firstly, Spiroplasma can enhance survival rates of its hosts under parasite 88 or parasitoid attack. In Drosophila neotestecea , Spiroplasma inhibits growth and reproduction 89 of the parasitic nematode Howardula , and thus reverses nematode-induced sterility (Jaenike 8: et al., 2010) . Further, Spiroplasma symbionts may greatly enhance Drosophila survival when 8; attacked by parasitoids (J. Xie et al., 2014; Xie et al., 2010) . Both protective phenotypes are 92 mediated by Spiroplasma encoded 5,3 toxins (ribosome-inactivating proteins), which target 93 the attackers‘ ribosomes (Ballinger and 3erlman, 2017; Hamilton et al., 2015, 2014) . These 94 processes may be complementary to protection through competition between Spiroplasma 95 and parasitoids for lipids in the host hemolymph (Paredes et al., 2016) . Secondly, 96 Spiroplasma kills males early in development in several species of Drosophila, planthoppers 97 (Sanada-Morimura et al., 2013) , ladybird beetles (Tinsley and 0aMerus, 2006) , lacewings 98 (Hayashi et al., 2016), and butterflies (Jiggins et al., 2000) . The male-killing phenotype is 99 also linked to a toxin: in Drosophila melanogaster , a Spiroplasma protein containing 2T8 9: (Ovarian Tumour-like deubiquitinase) and ankyrin domains was demonstrated to kill male 9; embryos, and thus termed Spiroplasma poulsonii androcidin (—Spaid“, Harumoto and :2 /emaitre, 2018). :3 Spiroplasma induced phenotypes were commonly observed to be dynamic compared with :4 other symbiont traits, with repeated observation of phenotype change over relatively short :5 time frames. For example, spontaneous loss of male killing was found in Spiroplasma :6 symbionts of Drosophila nebulosa (Yamada et al., 1982) , and Drosophila willistoni (Ebbert, :7 1991) , and spontaneous emergence of non male-killing Spiroplasma in Drosophila :8 melanogaster has occurred at least twice in a single culture (Harumoto and /emaitre, 2018; :9 0asson et al., 2020) . In addition, Spiroplasma symbionts artificially transferred from their :: native host Drosophila hydei into D. melanogaster initially caused pathogenesis, but evolved 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.165548; this version posted June 24, 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 4.0 International license. :; to become benign over Must a few host generations (Nakayama et al., 2015) . Genomic analysis ;2 has further documented dynamic Spiroplasma evolution driven by viral proliferation (Carle et ;3 al., 2010; .u et al., 2013; Ye et al., 1996) and by extensive transfer of genetic material ;4 between plasmids, and from plasmids to chromosomes (Joshi et al., 2005; 0ouches et al., ;5 1984) . 1otably, plasmids in Spiroplasma commonly encode the systems that establish their ;6 phenotypic effect on their host (Berho et al., 2006). Examples include Spaid (Harumoto and ;7 /emaitre, 2018) and 5,3 genes (Ballinger and 3erlman, 2017), and rapid plasmid evolution ;8 may therefore contribute to the high
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