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An Updated Phylogeny of the Alphaproteobacteria Reveals That the Parasitic Rickettsiales and Holosporales Have Independent Origi

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An Updated Phylogeny of the Alphaproteobacteria Reveals That the Parasitic Rickettsiales and Holosporales Have Independent Origi bioRxiv preprint doi: https://doi.org/10.1101/462648; this version posted November 5, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 1 TITLE 2 An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales 3 and Holosporales have independent origins 4 AUTHORS 5 Sergio A. Muñoz-Gómez1,2, Sebastian Hess1,2, Gertraud Burger3, B. Franz Lang3, 6 Edward Susko2,4, Claudio H. Slamovits1,2*, and Andrew J. Roger1,2* 7 AUTHOR AFFILIATIONS 8 1 Department of Biochemistry and Molecular Biology; Dalhousie University; Halifax, 9 Nova Scotia, B3H 4R2; Canada. 10 2 Centre for Comparative Genomics and Evolutionary Bioinformatics; Dalhousie 11 University; Halifax, Nova Scotia, B3H 4R2; Canada. 12 3 Department of Biochemistry, Robert-Cedergren Center in Bioinformatics and 13 Genomics, Université de Montréal, Montreal, Quebec, Canada. 14 4 Department of Mathematics and Statistics; Dalhousie University; Halifax, Nova Scotia, 15 B3H 4R2; Canada. 16 17 *Correspondence to: Department of Biochemistry and Molecular Biology; Dalhousie 18 University; Halifax, Nova Scotia, B3H 4R2; Canada; 1 902 494 7894, 19 [email protected] 20 *Correspondence to: Department of Biochemistry and Molecular Biology; Dalhousie 21 University; Halifax, Nova Scotia, B3H 4R2; Canada; 1 902 494 2881, [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/462648; this version posted November 5, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 22 ABSTRACT 23 The Alphaproteobacteria is an extraordinarily diverse and ancient group of bacteria. 24 Previous attempts to infer its deep phylogeny have been plagued with methodological 25 artefacts. To overcome this, we analyzed a dataset of 200 single-copy and conserved 26 genes and employed diverse strategies to reduce compositional artefacts. Such 27 strategies include using novel dataset-specific profile mixture models and recoding 28 schemes, and removing sites, genes and taxa that are compositionally biased. We 29 show that the Rickettsiales and Holosporales (both groups of intracellular parasites of 30 eukaryotes) are not sisters to each other, but instead, the Holosporales has a derived 31 position within the Rhodospirillales. Furthermore, we find that the Rhodospirillales might 32 be paraphyletic and that the Geminicoccaceae could be sister to all ancestrally free- 33 living alphaproteobacteria. Our robust phylogeny will serve as a framework for future 34 studies that aim to place mitochondria, and novel environmental diversity, within the 35 Alphaproteobacteria. 36 KEYWORDS: Holosporaceae, Holosporales, mitochondria, origin, Finniella inopinata, 37 Stachyamoba, Peranema, photosynthesis, Rhodospirillales, Azospirillaceae, 38 Rhodovibriaceae. 2 bioRxiv preprint doi: https://doi.org/10.1101/462648; this version posted November 5, 2018. 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. 39 INTRODUCTION 40 The Alphaproteobacteria is an extraordinarily diverse and disparate group of bacteria 41 and well-known to most biologists for also encompassing the mitochondrial lineage 42 (Williams, Sobral, and Dickerman 2007; Roger, Muñoz-Gómez, and Kamikawa 2017). 43 The Alphaproteobacteria has massively diversified since its origin, giving rise to, for 44 example, some of the most abundant (e.g., Pelagibacter ubique) and metabolically 45 versatile (e.g., Rhodobacter sphaeroides) cells on Earth (Giovannoni 2017; Madigan, 46 Jung, and Madigan 2009). The basic structure of the tree of the Alphaproteobacteria 47 has largely been revealed through the analyses of 16S rRNA genes and several 48 conserved proteins (Garrity 2005; Lee et al. 2005; Rosenberg et al. 2014; Fitzpatrick, 49 Creevey, and McInerney 2006; Williams, Sobral, and Dickerman 2007; Brindefalk et al. 50 2011; Georgiades et al. 2011; Thrash et al. 2011; Luo 2015). Today, eight major orders 51 are well recognized, namely the Caulobacterales, Rhizobiales, Rhodobacterales, 52 Pelagibacterales, Sphingomonadales, Rhodospirillales, Holosporales and Rickettsiales 53 (the latter two formerly grouped into the Rickettsiales sensu lato), and their 54 interrelationships have also recently become better understood (Viklund, Ettema, and 55 Andersson 2012; Viklund et al. 2013; Rodríguez-Ezpeleta and Embley 2012; Wang and 56 Wu 2014, 2015). These eight orders were grouped into two subclasses by Ferla et al. 57 (2013): the subclass Rickettsiidae comprising the order Rickettsiales and 58 Pelagibacterales, and the subclass Caulobacteridae comprising all other orders. 59 The great diversity of the Alphaproteobacteria itself presents a challenge to deciphering 60 the deepest divergences within the group. Such diversity encompasses a broad 61 spectrum of genome (nucleotide) and proteome (amino acid) compositions (e.g., the 62 A+T%-rich Pelagibacterales versus the G+C%-rich Acetobacteraceae) and molecular 63 evolutionary rates (e.g., the fast-evolving Pelagibacteriales, Rickettsiales or 64 Holosporales versus many slow-evolving species in the Rhodospirillales) (Ettema and 65 Andersson 2009). This diversity may lead to pervasive artefacts when inferring the 66 phylogeny of the Alphaproteobacteria, e.g., long-branch attraction (LBA) between the 67 Rickettsiales and Pelagibacterales, especially when including mitochondria (Rodríguez- 68 Ezpeleta and Embley 2012; Viklund, Ettema, and Andersson 2012; Viklund et al. 2013). 3 bioRxiv preprint doi: https://doi.org/10.1101/462648; this version posted November 5, 2018. 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. 69 Moreover, there are still important unknowns about the deep phylogeny of the 70 Alphaproteobacteria (Williams, Sobral, and Dickerman 2007; Ferla et al. 2013), for 71 example, the divergence order among the Rhizobiales, Rhodobacterales and 72 Caulobacterales (Williams, Sobral, and Dickerman 2007), the monophyly of the 73 Pelagibacterales (Viklund et al. 2013) and the Rhodospirillales (Ferla et al. 2013), and 74 the precise placement of the Rickettsiales and its relationship to the Holosporales 75 (Wang and Wu 2015; Martijn et al. 2018). 76 Systematic errors stemming from using over-simplified evolutionary models are perhaps 77 the major confounding and limiting factor to inferring deep evolutionary relationships; 78 the number of taxa and genes (or sites) can also be important factors. Previous multi- 79 gene tree studies of the Alphaproteobacteria were compromised by at least one of 80 these problems, namely, simple or unrealistic evolutionary models (because they were 81 not available at the time; e.g., Williams, Sobral, and Dickerman 2007), poor taxon 82 sampling (because the focus was too narrow or few genomes were available; e.g., 83 Williams, Sobral, and Dickerman 2007; Georgiades et al. 2011; Martijn et al. 2015) or a 84 small number of genes (because the focus was mitochondria; e.g., Rodríguez-Ezpeleta 85 and Embley 2012; Wang and Wu 2015; Martijn et al. 2018). The most recent study on 86 the phylogeny of the Alphaproteobacteria, and mitochondria, attempted to counter 87 systematic errors (or phylogenetic artefacts) by reducing amino acid compositional 88 heterogeneity (Martijn et al. 2018). Even though some deep relationships were not 89 robustly resolved, these analyses suggested that the Pelagibacterales, Rickettsiales 90 and Holosporales, which have compositionally biased genomes, are not each other’s 91 closest relatives (Martijn et al. 2018). A resolved and robust phylogeny of the 92 Alphaproteobacteria is fundamental to addressing questions such as how streamlined 93 bacteria, intracellular parasitic bacteria, or mitochondria evolved from their 94 alphaproteobacterial ancestors. Therefore, a systematic study of the different biases 95 affecting the phylogeny of the Alphaproteobacteria, and its underlying data, is much 96 needed. 97 Here, we revised the phylogeny of the Alphaproteobacteria by using a large dataset of 98 200 conserved single-copy genes and employing carefully designed strategies aimed at 4 bioRxiv preprint doi: https://doi.org/10.1101/462648; this version posted November 5, 2018. 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. 99 alleviating phylogenetic artefacts. We found that amino acid compositional 100 heterogeneity, and more generally long-branch attraction, were major confounding 101 factors in estimating phylogenies of the Alphaproteobacteria. In order to counter these 102 biases, we used novel dataset-specific profile mixture models and recoding schemes 103 (both specifically designed to ameliorate compositional heterogeneity), and removed 104 sites, genes and taxa that were compositionally biased. We also present three draft 105 genomes for
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