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Phylogenomic Analyses Uncover Origin and Spread of the Wolbachia Pandemic

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Phylogenomic Analyses Uncover Origin and Spread of the Wolbachia Pandemic ARTICLE Received 7 Apr 2014 | Accepted 1 Sep 2014 | Published 6 Oct 2014 DOI: 10.1038/ncomms6117 Phylogenomic analyses uncover origin and spread of the Wolbachia pandemic Michael Gerth1, Marie-Theres Gansauge2, Anne Weigert1 & Christoph Bleidorn1,3 Of all obligate intracellular bacteria, Wolbachia is probably the most common. In general, Wolbachia are either widespread, opportunistic reproductive parasites of arthropods or essential mutualists in a single group of filarial nematodes, including many species of medical significance. To date, a robust phylogenetic backbone of Wolbachia is lacking and consequently, many Wolbachia-related phenomena cannot be discussed in a broader evolu- tionary context. Here we present the first comprehensive phylogenomic analysis of Wolbachia supergroup relationships based on new whole-genome-shotgun data. Our results suggest that Wolbachia has switched between its two major host groups at least twice. The ability of some arthropod-infecting Wolbachia to universally infect and to adapt to a broad range of hosts quickly is restricted to a single monophyletic lineage (containing supergroups A and B). Thus, the currently observable pandemic has likely a single evolutionary origin and is unique within the radiation of Wolbachia strains. 1 Molecular Evolution and Systematics of Animals, Institute of Biology, University of Leipzig, Talstrasse 33, 04103 Leipzig, Germany. 2 Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany. 3 German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5d, 04103 Leipzig, Germany. Correspondence and requests for materials should be addressed to M.G. (email: [email protected]). NATURE COMMUNICATIONS | 5:5117 | DOI: 10.1038/ncomms6117 | www.nature.com/naturecommunications 1 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6117 ike all members of the order Rickettsiales (Alphaproteobac- robust and well-supported phylogenetic hypothesis for the teria), Wolbachia are obligate intracellular symbionts. Main evolution of Wolbachia strains. Our findings indicate that the Levolutionary Wolbachia lineages are termed ‘supergroups’1 ubiquitous Wolbachia supergroups A and B belong to a single, and differ markedly in their host distribution and biology. monophyletic lineage and consequently, the ability to adapt to a Supergroup A and B Wolbachia strains are found in many groups large range of taxonomically and physiologically diverse hosts has of terrestrial arthropods, making it one of the most common a single origin in that lineage. Furthermore, the Wolbachia strains endosymbionts worldwide. An estimated 40% of all species are that are obligate mutualists of nematodes are a paraphyletic infected2. In many arthropod hosts, Wolbachia enhance their assemblage, suggesting that host switches from arthopods to spread by inducing reproductive alterations such as cytoplasmic nematodes (or back) occurred at least twice in the evolutionary incompatibility (CI), parthenogenesis, male-killing and history of Wolbachia. feminization3. Although Wolbachia is generally transmitted vertically (from mother to offspring), regular horizontal Results transmissions between arthropod hosts as well as recurrent Reconstructing Wolbachia’s evolutionary history. To recon- gains and losses are evident from a lack of co-cladogenesis of struct Wolbachia supergroup relationships via a phylogenomic Wolbachia with its hosts4,5. pipeline, we utilized available genomic sequences of Wolbachia In stark contrast, Wolbachia of supergroups C and D are found supergroups A, B, C and D as well as supergroup F Wolbachia exclusively in some filarial nematodes and their long-lasting sequences originating from a Strepsiptera genome project intimate association has led to various mutual dependencies6. (Table 1). In addition, we performed WGS sequencing of four Other distinct Wolbachia strain groups are known only from a arthropod hosts carrying distinct Wolbachia strains so far not small number of hosts: supergroup E is found in springtails represented by genomic data (Table 1). BLAST searches in the (Hexapoda, Collembola), supergroup H in termites (Hexapoda, corresponding assemblies allowed us to identify most of the 90 Isoptera) and further, so far unclassified strains were detected in loci to be employed for phylogenetic analyses from wOc (87/90), Ctenocephalides felis (Hexapoda, Siphonaptera), Dipetalonema wFol (82/90) and wCte (78/90). For wZoo and wMen, only 19 gracile (Nematoda, Filarioidea), Bryobia sp. (Arachnida, Acari) and 38 loci were recovered, respectively. Preliminary supergroup and Cordylochernes scorpioides (Arachnida, Pseudoscorpiones)7–12. assignment with multilocus sequence typing (MLST) loci that The nature of the symbiosis in all of these cases is only superficially were extracted from the assemblies showed that wOc and wMen understood. Interestingly, supergroup F Wolbachia may infect clustered within arthropod and nematode supergroup F strains, both arthropods and nematodes, and strains of this super- and that wFol represents a distinct lineage of the Wolbachia group may act as a mutualist and can induce CI13–15. Although found in many higher ranked arthropod taxa (for example, insect orders), supergroup F Wolbachia are generally Table 1 | Origin of sequence data used in this study. rare11. Given the diverging lifestyles of Wolbachia supergroups, the question arises whether Wolbachia from arthropods and Short Wolbachia host Source/NCBI Supergroup name accession nematodes represent distinct, monophyletic evolutionary lineages of strain and, if so, which phylogenetic position can be attributed to wMel Drosophila PRJNA57851 A supergroup F that is not constrained to a single host group. An melanogaster intriguing hypothesis suggests that this group is a basal branching 16 wUni Muscidifurax PRJNA213628 A lineage that might represent Wolbachia’s ancestral lifestyle . uniraptor While phylogenetic analyses of Wolbachia strains based on a wRi Drosophila simulans PRJNA13364 A single or a few genes usually enable correct supergroup wSuz Drosophila suzukii PRJEB596 A assignments, relationships between supergroups remain poorly wVitB Nasonia vitripennis PRJNA74529 B resolved and consequently, partially conflicting phylogenetic wAlbB Aedes albopictus CAGB01000001-165 B hypotheses were proposed11,17–20. Furthermore, these data sets wPip Culex PRJNA55557 B are especially prone to artefacts caused by recombination between quinquefasciatus Wolbachia strains21. Owing to the fact that hitherto, whole- wPipPel Culex PRJNA61645 B quinquefasciatus genome data from supergroups other than A, B, C and D are wBm Brugia malayi PRJNA58107 D lacking, phylogenomic analyses (albeit providing well-resolved wLs Litomosoides http:// D trees) were restricted to a limited sampling of Wolbachia sigmodontis litomosoides.nematod.es 16,22 strains . In addition, a large evolutionary distance to its wDim Dirofilaria immitis http:// C closest relatives has hampered an unequivocal rooting of the dirofilaria.nematod.es Wolbachia tree23. However, a well-resolved rooted tree is needed wOo Onchocerca ochengi PRJEA171829 C to interpret the direction of major lifestyle transitions in wMen Mengenilla PRJNA72521 F Wolbachia’s evolutionary history. moldrzyki In the present study, we aim to address the major challenges in wOc Osmia caerulescens this study F wFol Folsomia candida this study E reconstructing Wolbachia’s evolutionary history by enhancing wZoo Zootermopsis this study H taxon and gene sampling. To this end, we created new whole- nevadensis genome-shotgun (WGS) data of so far unsampled supergroup E wCte Ctenocephalides this study B from the springtail Folsomia candida, supergroup H from the felis termite Zootermopsis nevadensis and supergroup F from the solitary bee Osmia caerulescens. A data set of 90 carefully selected Short name Outgroup strains Source single-copy orthologues from these data and from already Ace Anaplasma centrale str. Israel PRJNA42155 published Wolbachia genomes (supergroups A, B, C and D) Ama Anaplasma marginale str. Florida PRJNA58577 were used for phylogenomic analyses. We integrated various Ech Ehrlichia chaffeensis str. Arkansas PRJNA57933 phylogenetic approaches as well as measures to identify and Eru Ehrlichia ruminantium str. Gardel PRJNA58245 subsequently reduce systematic biases. We consequently present a 2 NATURE COMMUNICATIONS | 5:5117 | DOI: 10.1038/ncomms6117 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6117 ARTICLE wUni ol F 88 w 100 wMel E A wSuz 100 wRi D H w w 98 wPip Ls wBm Z 100 oo 95 wPipPel 93 wVitB B 100 ip wAlbB 99 wPipPelP wOo w B 100 99 wVitB C wAlbB 87 wCte 100 100 87 100 wCt 100 e wDim 100 wOc 100 99 F 100 wMen 100 100 84 wDim wOc 100 100 i wMel wMen w C R U 100 w wOo F ni –0.01 wSuz wLs A 100 D 100 wBm Figure 1 | Unrooted phylogram showing relationships between wZoo H investigated Wolbachia strains. The phylogram was inferred with RAxML wFol E from a nucleotide supermatrix including 69,677 base positions. Eru Numbers on clades correspond to bootstrap values in percent from 1,000 100 P replicates. Supergroup affiliations are given in coloured letters. Leaf labels Ech correspond to Wolbachia strain names. Scale bar corresponds to inferred 100 Ama 0.1 Ace evolutionary changes. Analysis of the same matrix with MrBayes resulted in OUTGROU
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