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Mutational Pressure Drives Differential Genome Conservation in Two Bacterial Endosymbionts of Sap Feeding Insects

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Mutational Pressure Drives Differential Genome Conservation in Two Bacterial Endosymbionts of Sap Feeding Insects bioRxiv preprint doi: https://doi.org/10.1101/2020.07.29.225037; this version posted July 29, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. 1 Mutational pressure drives differential genome conservation in two bacterial 2 endosymbionts of sap feeding insects 3 4 Gus Wanekaa,*, Yumary M. Vasquezb, Gordon M. Bennettb, Daniel B. Sloana - 5 6 aDepartment of Biology, Colorado State University, Fort Collins, CO 80523; and bDepartment of 7 Life and Environmental Sciences, University of California, Merced, CA 95343 8 *Author for Correspondence: Gus Waneka, Biology Department, Colorado State University, Fort 9 Collins, USA, [email protected] bioRxiv preprint doi: https://doi.org/10.1101/2020.07.29.225037; this version posted July 29, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. 10 ABSTRACT 11 Compared to free-living bacteria, endosymbionts of sap-feeding insects have tiny and 12 rapidly evolving genomes. Increased genetic drift, high mutation rates, and relaxed selection 13 associated with host control of key cellular functions all likely contribute to genome decay. 14 Phylogenetic comparisons have revealed massive variation in endosymbiont evolutionary rate, 15 but such methods make it difficult to partition the effects of mutation vs. selection. For example, 16 the ancestor of auchenorrhynchan insects contained two obligate endosymbionts, Sulcia and a 17 betaproteobacterium (BetaSymb; called Nasuia in leafhoppers) that exhibit divergent rates of 18 sequence evolution and different propensities for loss and replacement in the ensuing ~300 Ma. 19 Here, we use the auchenorrhynchan leafhopper Macrosteles sp. nr. severini, which retains both 20 of the ancestral endosymbionts, to test the hypothesis that differences in evolutionary rate are 21 driven by differential mutagenesis. We used a high-fidelity technique known as duplex 22 sequencing to measure and compare low-frequency variants in each endosymbiont. Our direct 23 detection of de novo mutations reveals that the rapidly evolving endosymbiont (Nasuia) has a 24 much higher frequency of single-nucleotide variants than the more stable endosymbiont (Sulcia) 25 and a mutation spectrum that is even more AT-biased than implied by the 83.1% AT content of 26 its genome. We show that indels are common in both endosymbionts but differ substantially in 27 length and distribution around repetitive regions. Our results suggest that differences in long- 28 term rates of sequence evolution in Sulcia vs. BetaSymb, and perhaps the contrasting degrees of 29 stability of their relationships with the host, are driven by differences in mutagenesis. 30 31 KEYWORDS 32 mutation spectra, insertion, deletion, variant, genome decay, extinction 33 34 SIGNIFICANCE STATEMENT 35 Two ancient endosymbionts in the same host lineage display stark differences in genome 36 conservation over phylogenetic scales. We show the rapidly evolving endosymbiont has a higher 37 frequency of mutations, as measured with duplex sequencing. Therefore, differential 38 mutagenesis likely drives evolutionary rate variation in these endosymbionts. 39 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.29.225037; this version posted July 29, 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-ND 4.0 International license. 40 INTRODUCTION 41 Sap feeding insects in the order Hemiptera feed exclusively on nutrient deficient plant- 42 saps (phloem and xylem) and rely on bacterial endosymbionts to provide lacking essential amino 43 acids and vitamins (Buchner 1965; Sandström and Moran 1999). Such endosymbionts are 44 housed intracellularly in specialized organs called bacteriomes and are subject to strict vertical 45 transmission from mother to offspring. This repeated transmission bottlenecking and 46 confinement within a host lineage results in genetic drift and endosymbiont genome decay 47 (Moran 1996; Mira and Moran 2002; McCutcheon and Moran 2012; Bennett and Moran 2015; 48 McCutcheon et al. 2019). 49 Ancient endosymbiont genomes are characterized by their extreme nucleotide 50 composition bias and small size. In fact, many of these genomes are among the smallest known, 51 lacking genes considered essential in free living bacteria (e.g., cell envelope biogenesis, gene 52 expression regulation, and DNA replication/repair; McCutcheon and Moran 2012; Moran and 53 Bennett 2014). Ancient endosymbiont genomes experience rapid sequence evolution and 54 extensive lineage-specific gene deletions, leaving only a set of ‘core’ genes necessary to sustain 55 a functioning nutritional symbiosis (Moran et al. 2009; Bennett, McCutcheon, et al. 2016). At the 56 same time, these genomes exhibit remarkable structural stability, often displaying perfectly 57 conserved synteny between lineages that diverged 10s to 100s of millions of years ago 58 (McCutcheon et al. 2009a). 59 Missing DNA replication and repair genes, and conditions of relaxed selection, allow the 60 AT mutation bias (which is common to most bacteria; Hershberg and Petrov 2010; Hildebrand et 61 al. 2010; Long, Sung, et al. 2018) to drive AT content to levels above 75% in many 62 endosymbionts (Moran et al. 2009; Moran and Bennett 2014; Wernegreen 2016). A notable 63 exception is the GC rich genome of Candidatus Hodgkinia cicadicola (hereafter Hodgkinia; 64 58.4% GC), an endosymbiont of cicadas with an extremely small genome (144 kb) (McCutcheon 65 et al. 2009b). However, population level estimates of the Hodgkinia mutation spectrum reveal an 66 AT mutation bias, indicating that GC prevalence in Hodgkinia likely results from selection on 67 nucleotide identity (Van Leuven and McCutcheon 2012). 68 In extreme cases of genome decay, ancient endosymbionts can go extinct when they are 69 outcompeted and replaced by newly colonizing bacteria or yeast (Matsuura et al. 2018; 70 McCutcheon et al. 2019). Comparisons amongst ancient endosymbionts reveal massive bioRxiv preprint doi: https://doi.org/10.1101/2020.07.29.225037; this version posted July 29, 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-ND 4.0 International license. 71 variability in genome stability and extinction rates. Insects in the suborder Auchenorrhyncha 72 maintain two bacterial endosymbionts: “Candidatus Sulcia muelleri” (hereafter Sulcia) and a 73 betaproteobacterium (hereafter BetaSymb), which are both thought to be ancestral to the group 74 (~300 Ma) (Moran et al. 2005; Dietrich 2009; Bennett and Moran 2013; Bennett and Mao 2018). 75 The partner endosymbionts provision distinct and complementary sets of the 10 essential amino 76 acids that animals are unable to synthesize and are unavailable in the host diet. Sulcia has been 77 nearly universally retained over the ~300 million year diversification of the Auchenorrhyncha 78 (~40,000 described species); in contrast, BetaSymb has been replaced in at least six major 79 lineages, highlighting its relative instability (Dietrich 2009; Bennett and Moran 2015). 80 The apparent unreliability and relatively frequent loss of the BetaSymb lineage is 81 mirrored by rapid rates of molecular evolution. Pairwise divergence estimates for the two 82 ancestral symbionts in closely related leafhopper species (family Cicadellidae) reveal that Sulcia 83 genomes are highly similar (99.68% nucleotide identity), while BetaSymb genomes are 30-fold 84 more divergent (90.47% nucleotide identity) (Bennett, Abbà, et al. 2016). The dramatic 85 differences in Sulcia and BetaSymb rates of molecular evolution have also been documented 86 across more divergent auchenorrhynchan lineages (Bennett and Moran 2013; Mao et al. 2017; 87 Bennett and Mao 2018). 88 While phylogenetic comparisons have greatly improved our understanding of the changes 89 that endosymbiotic genomes experience, they do not adequately parse the relative contributions 90 of mutagenesis, genetic drift, and natural selection. Although it is possible that selection 91 differentially constrains sequence change in Sulcia and BetaSymb (Wernegreen 2016), it has 92 been suggested that the low rate of evolution in Sulcia may correlate with decreased DNA 93 replication (Silva and Santos-Garcia 2015) or low mutational input (Bennett et al. 2014). 94 However, these hypotheses are difficult to test directly as traditional approaches for measuring 95 bacterial mutation, such as mutation accumulation lines (Kucukyildirim et al. 2016; Long, 96 Miller, et al. 2018), are not feasible for obligate endosymbionts. In one case, researchers were 97 able to use the recent demographic history of the insect host to infer endosymbiont mutation 98 rates (Moran et al. 2009), but the challenge of directly measuring mutation in endosymbionts 99 continues to inhibit efforts to disentangle mutagenesis, drift, and selection in endosymbionts. 100 A direct measurement of mutation would ideally capture all variants, before some can be 101 filtered
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