Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree

Abstract

Phylogeny ofCurrent phylogenies of the intracellular bacteria belonging to the genus Wolbachia identify six major clades (A-F), termed 'supergroups', but the branching order of these supergroups remains unresolved. Supergroups A, B and E include most of the wolbachiae found thus far in arthropods, while supergroups C and D include most of those found in filarial nematodes. Members of supergroup F have been found in arthropods (i.e. termites), and have previously been detected in the nematode Mansonella ozzardi, a causative agent of human filariasis. To resolve the phylogenetic positions of Wolbachia from Mansonella spp., and other novel strains from the flea Ctenocephalides felis and the filarial nematode Dipetalonema gracile, the authors generated new DNA sequences of the Wolbachia genes encoding citrate synthase (gltA), heat-shock protein 60 (groEL), and the cell division protein ftsZ. Phylogenetic analysis confirmed the designation of Wolbachia from Mansonella spp. as a member of the F supergroup. In addition, it was found that divergent lineages from Dip. gracile and Cte. felis lack any clear affiliation with known supergroups, indicating further genetic diversity within the Wolbachia genus. Finally, although the data generated did not permit clear resolution of the root of the global Wolbachia tree, the results suggest that the transfer of Wolbachia spp. from arthropods to nematodes (or vice versa) probably occurred more than once. INTRODUCTIONThe genus Wolbachia encompasses obligately intracellular bacteria that are cytoplasmically transmitted in arthropods and filarial nematodes (Werren, 1997;Bandi et al., 2001;Bordenstein et al., 2003). Unlike most other obligately intracellular bacteria, the genus Wolbachia forms a monophyletic clade comprising both mutualistic and parasitic lineages that showcase the diversity of symbiotic associations. In arthropods, Wolbachia spp. are commonly known as reproductive parasites, since they distort host reproductive strategies to selfishly enhance their maternal transmission into the next generation (Werren, 1997). Wolbachia spp. have a remarkably high prevalence in some arthropod groups (Jeyaprakash & Hoy, 2000). In contrast, the Wolbachia lineages infecting filarial nematodes are beneficial 3Present address: Dipartimento di Biotecnologie e Bioscienze, Università degli Studi di Milano Bicocca, Milano, Italy.4Present address: Department of Biology, University of California, 900 University Avenue, Riverside, CA, USA.The GenBank/EMBL/DDBJ accession numbers for the nucleotide sequences reported in this paper are listed in Table 1.The phylogeny inferred from the concatenated dataset (gltA, groEL, ftsZ), rooted with two outgroup species (Anaplasma marginale and Ehrlichia ruminantium), is shown in Supplementary Fig. S1, available with the online version of this paper.Abbreviations: BI, Bayesian inference; ML, maximum-likelihood; TBR, tree bisection and reconnection.

Distribution and Evolutionary Impact of Wolbachia on Butterfly Hosts

“…Supergroup F is highly diverse and found to break renowned barrier by infecting both nematode Mansonella and arthropods like termites, butterflies, cockroaches, etc. [12][13][14][15][16].…”

The Nematoda Filarioidea: critical analysis linking molecular and traditional approaches

“…In Australia, C. johnstoni Spratt & Varughese, 1975, type host-Muridae, is found in marsupials and monotremes as well (communication by D. Spratt) and this might represent the first step of future speciations. Interestingly, Wolbachia is absent from species of the genus, except C. japonica (Uni, 1983) from bears, which harbours the form F of the endosymbiont (work in progress), a Wolbachia type shared with filariae of the genus Mansonella and with some arthropod hosts (Casiraghi et al, 2005). 32 species have been described in Litomosoides, from microchiropterans, marsupials, murids and a few other rodents.…”

“…According to the hypothesis proposed by Chabaud & Bain (1994), these would be close to the roots of Gondwanian Acanthocheilonema-like filariae from which stemmed Dipetalonema s. s. in the Neotropical region, when platyrhinian monkeys arrived after their transoceanic migration (late Eocene). D. gracile, the single species studied in this derived branch, harbours a Wolbachia related to the C supergroup, even though its real assignation is still under discussion (see below and Casiraghi et al, 2004;2005).…”

16S rRNA-, GroEL- and MucZ-based assessment of the taxonomic position of 'Rickettsiella melolonthae' and its implications for the organization of the genus Rickettsiella

“…On the other hand, a presumed unnamed Rickettsiella strain infecting the terrestrial isopod Porcellio scaber that shows 'a high degree of morphological similarity with Rickettsiella grylli ' (Drobne et al, 1999) and a putative rickettsiellal pathogen of the cockroach Blatta orientalis ('Rickettsiella blattae ', Huger, 1963; 'Rickettsiella crassificans', Radek, 2000) were transferred to the newly created candidate genus 'Rhabdochlamydia' within the order Chlamydiales after the respective 16S rRNA gene sequences had been determined (Kostanjsek et al, 2004;Corsaro et al, 2006). Irrespective of these conflicting results, monophyly has recently been claimed for the genus Rickettsiella (Cordaux et al, 2007).The highly conserved Hsp60 chaperonin GroEL is distributed ubiquitously throughout the eubacterial lineage, appears functionally involved in bacterial endosymbiosis (Fares et al, 2004) and pathogenicity (Garduño et al, 1998) and has been used in molecular phylogenetic studies of proteobacterial endosymbionts of insects (Viale et al, 1994;Casiraghi et al, 2005). The mucZ gene product from C. burnetii induces capsule synthesis (mucoidy) when expressed in Escherichia coli (Zuber et al, 1995).…”

“…The highly conserved Hsp60 chaperonin GroEL is distributed ubiquitously throughout the eubacterial lineage, appears functionally involved in bacterial endosymbiosis (Fares et al, 2004) and pathogenicity (Garduño et al, 1998) and has been used in molecular phylogenetic studies of proteobacterial endosymbionts of insects (Viale et al, 1994;Casiraghi et al, 2005). The mucZ gene product from C. burnetii induces capsule synthesis (mucoidy) when expressed in Escherichia coli (Zuber et al, 1995).…”