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Comparative Genomics of Bdelloid Rotifers

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Comparative Genomics of Bdelloid Rotifers bioRxiv preprint doi: https://doi.org/10.1101/226720; this version posted December 4, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. 1 Comparative genomics of bdelloid rotifers: 2 evaluating the effects of asexuality and 3 desiccation tolerance on genome evolution 4 Authors 5 Reuben W. Nowell1,*, Pedro Almeida1,¶, Christopher G. Wilson1, Thomas P. Smith1, Diego 6 Fontaneto2, Alastair Crisp3,¶, Gos Micklem4, Alan Tunnacliffe3, Chiara Boschetti3,5,*,† and Timothy G. 7 Barraclough1,*,† 8 Author affiliations 9 1 Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, 10 Ascot, Berkshire, SL5 7PY, UK 2 National Research Council of Italy, Institute of Ecosystem Study, 11 Largo Tonolli 50, 28922 Verbania Pallanza, Italy 3 Department of Chemical Engineering and 12 Biotechnology, University of Cambridge, West Cambridge Site, Philippa Fawcett Drive, Cambridge, 13 CB3 0AS, UK 4 Department of Genetics, Cambridge Systems Biology Centre, Downing Site, 14 University of Cambridge, Cambridge CB2 3EH, UK 5 School of Biological and Marine Sciences, 15 Plymouth University, Portland Square Building, Drake Circus, Plymouth, PL4 8AA, UK 16 * Corresponding authors 17 Email: [email protected]; [email protected]; [email protected] 18 † Contributions 19 These authors contributed equally to this work. 20 ¶ Current addresses 21 Department of Genetics, Evolution and Environment, University College London, Darwin Building, 22 Gower Street, London WC1E 6BT, UK (PA); MRC Laboratory of Molecular Biology, Francis Crick 23 Avenue, Cambridge Biomedical Campus, Cambridge, CB2 0QH, UK (AC). 1 bioRxiv preprint doi: https://doi.org/10.1101/226720; this version posted December 4, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. 24 Abstract 25 Bdelloid rotifers are microscopic invertebrates that have existed for millions of years apparently 26 without sex or meiosis. They inhabit a variety of temporary and permanent freshwater habitats 27 globally, and many species are remarkably tolerant of desiccation. Bdelloids offer an opportunity to 28 better understand the evolution of sex and recombination, but previous work has emphasized 29 desiccation as the cause of several unusual genomic features in this group. Here, we evaluate the 30 relative effects of asexuality and desiccation tolerance on genome evolution by comparing whole 31 genome sequences for three bdelloid species: Adineta ricciae (desiccation tolerant), Rotaria macrura 32 and Rotaria magnacalcarata (both desiccation intolerant) to the only published bdelloid genome to 33 date, that of Adineta vaga (also desiccation tolerant). We find that tetraploidy is conserved among all 34 four bdelloid species, but homologous divergence in obligately aquatic Rotaria genomes is low, well 35 within the range observed between alleles in obligately sexual, diploid animals. In addition, we find 36 that homologous regions in A. ricciae are largely collinear and do not form palindromic repeats as 37 observed in the published A. vaga assembly. These findings are contrary to current understanding of 38 the role of desiccation in shaping the bdelloid genome, and indicate that various features interpreted 39 as genomic evidence for long-term ameiotic evolution are not general to all bdelloid species, even 40 within the same genus. Finally, we substantiate previous findings of high levels of horizontally 41 transferred non-metazoan genes encoded in both desiccating and non-desiccating bdelloid species, 42 and show that this is a unique feature of bdelloids among related animal phyla. Comparisons within 43 bdelloids and to other desiccation-tolerant animals, however, again call into question the purported 44 role of desiccation in horizontal transfer. 2 bioRxiv preprint doi: https://doi.org/10.1101/226720; this version posted December 4, 2017. 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-ND 4.0 International license. 45 Introduction 46 The bdelloid rotifers are a class of microscopic invertebrates found in freshwater habitats 47 worldwide. Two life-history characteristics make these soft-bodied filter-feeders extraordinary 48 among animals. First, bdelloids famously lack males [1] or cytological evidence of meiosis [2,3], and 49 are only known to reproduce via mitotic parthenogenesis. They are therefore one of the best- 50 substantiated examples of a eukaryotic taxon that seems to have evolved without sex or meiosis for 51 tens of millions of years [1,2,4,5]. Famously labelled as “an evolutionary scandal” [6], bdelloids have 52 diversified into over 500 species [7,8] in apparent defiance of the usual fate of asexual lineages [9– 53 11]. Their persistence has implications for theories of the evolution of sex and recombination, a 54 fundamental puzzle in biology [12–15]. A second key feature is that most bdelloid species are 55 remarkably resilient to desiccation, and can survive the loss of almost all cellular water at any stage 56 in their life cycle, including as adults [16,17]. On desiccation, animals contract their body into a flat, 57 ellipsoid “tun” shape and enter a dormant state called anhydrobiosis, during which all metabolic 58 activities associated with life are suspended [5,16,18]. Individuals can remain in this condition for 59 long periods, usually days or weeks but occasionally several years [19,20]. The return of water 60 restores metabolism and reproduction, with little evidence of negative fitness consequences for 61 survivors [21]. Species that live in limnoterrestrial habitats such as puddles, leaf litter and moss are 62 subject to cycles of drying, and the ability to survive desiccation has been proposed to play a key 63 role in bdelloid evolution [5,22]. 64 Initial marker-based analyses of bdelloid genomes recovered highly divergent gene copies that were 65 interpreted as non-recombining descendants of ancient former alleles [4]. Along with the low copy- 66 number of vertically inherited transposable elements (TEs) [23], this result was considered positive 67 genomic evidence of long-term asexual evolution. However, subsequent investigations of larger 68 genomic regions revealed evidence of tetraploidy, probably arising from an ancient hybridization or 69 genome duplication event affecting diploid ancestors prior to the diversification of the bdelloid 70 families [5,24,25]. Thus, genes generally comprise up to four copies, arranged as two pairs with 71 greater divergence between pairs (“ohnologs”, also known as homeologs in other polyploid systems) 72 than within (“homologs”) [5,24,25]. Another extraordinary feature of bdelloid genomes was 73 discovered concurrently: a remarkably high proportion of bdelloid genes show a high degree of 74 similarity to non-metazoan orthologs, mostly from bacteria, but also fungi and plants, suggesting a 75 rate of horizontal gene transfer (HGT) into the bdelloid genome at least an order of magnitude 76 greater than that observed in other eukaryotes [26]. Later work confirmed that many genes 77 originating by horizontal gene transfer from non-metazoans are expressed and functional [27]. 3 bioRxiv preprint doi: https://doi.org/10.1101/226720; this version posted December 4, 2017. 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-ND 4.0 International license. 78 The first whole genome sequence for a bdelloid [28] substantiated many of these findings. The 79 degenerate tetraploid genome of Adineta vaga comprises homologous regions with low divergence 80 (median 1.4% for coding sequences) and high collinearity (i.e., conserved gene order), and 81 ohnologous regions with higher divergence (median 24.9%) but lower collinearity. The genome 82 encodes remarkably few TEs (~3% of the genome) but a high proportion (~8%) of HGT candidates, 83 many of which (~20%) were found as quartets and were therefore presumably acquired prior to 84 tetraploidization [28]. A number of unusual structural features were also reported, including a large 85 number of breaks in collinearity between homologous regions, and the linkage of homologs on the 86 same assembly scaffold, often arranged as genomic palindromes [28]. This assembly cannot therefore 87 be decomposed into haploid sets, a finding that was interpreted as further evidence of long-term 88 ameiotic evolution in A. vaga [28]. 89 To what extent are the genomic characteristics of bdelloid rotifers explained by their unusual 90 biology and ecology? An important starting point was the discovery that bdelloids can survive doses 91 of ionizing radiation that would be lethal to nearly any other animal, owing to their ability to repair 92 the resulting DNA double-strand breaks (DSBs) and recover from extensive genome fragmentation 93 [29,30]. Later experiments in A. vaga showed that genome fragmentation also occurs during 94 desiccation, and led to the view that bdelloid genomes may
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