New Insights into the Evolution of Wolbachia Infections in Filarial Nematodes Inferred from a Large Range of Screened Species

Abstract

Background Wolbachia are intriguing symbiotic endobacteria with a peculiar host range that includes arthropods and a single nematode family, the Onchocercidae encompassing agents of filariases. This raises the question of the origin of infection in filariae. Wolbachia infect the female germline and the hypodermis. Some evidences lead to the theory that Wolbachia act as mutualist and coevolved with filariae from one infection event: their removal sterilizes female filariae; all the specimens of a positive species are infected; Wolbachia are vertically inherited; a few species lost the symbiont. However, most data on Wolbachia and filaria relationships derive from studies on few species of Onchocercinae and Dirofilariinae, from mammals.Methodology/Principal FindingsWe investigated the Wolbachia distribution testing 35 filarial species, including 28 species and 7 genera and/or subgenera newly screened, using PCR, immunohistochemical staining, whole mount fluorescent analysis, and cocladogenesis analysis. (i) Among the newly screened Onchocercinae from mammals eight species harbour Wolbachia but for some of them, bacteria are absent in the hypodermis, or in variable density. (ii) Wolbachia are not detected in the pathological model Monanema martini and in 8, upon 9, species of Cercopithifilaria. (iii) Supergroup F Wolbachia is identified in two newly screened Mansonella species and in Cercopithifilaria japonica. (iv) Type F Wolbachia infect the intestinal cells and somatic female genital tract. (v) Among Oswaldofilariinae, Waltonellinae and Splendidofilariinae, from saurian, anuran and bird respectively, Wolbachia are not detected.Conclusions/SignificanceThe absence of Wolbachia in 63% of onchocercids, notably in the ancestral Oswaldofilariinae estimated 140 mya old, the diverse tissues or specimens distribution, and a recent lateral transfer in supergroup F Wolbachia, modify the current view on the role and evolution of the endosymbiont and their hosts. Further genomic analyses on some of the newly sampled species are welcomed to decipher the open questions.

Revisiting the phylogeny ofWolbachiain Collembola

“…As w Myos is the most divergent strain in supergroup E (Figure 3), its position in trees may be affected by long‐branch attraction, and its variation is probably related to the special habitat of its host (a sandy beach on an island). Generally, discordant phylogenies of hosts and Wolbachia are explained by horizontal transmission of Wolbachia (Ferri et al., 2011; Werren et al., 1995), and it might be the case in collembolan Wolbachia (Timmermans et al., 2004). However, in this study, no intragenic recombination of MLST and wsp genes was detected within supergroup E, as well as between supergroup E and other supergroups, so we have not found solid evidence to support the hypothesis on horizontal transmission of Wolbachia between different collembolan species.…”

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

“…Finally, the obligate dependency of some onchocercids on Wolbachia may not be a mutualism at all, but rather an extreme form of reproductive parasitism that has successfully hijacked normal cellular development in the embryo . These hypotheses must contend with two recent and interrelated developments in the field: the demonstration of secondary loss of Wolbachia in several members of the Onchocercidae (McNulty et al 2010), and the revelation that Wolbachia is currently present in <40% of this taxon (Ferri et al 2011). …”

“…This could explain the existence of filarial species that lack symbionts in the hypodermal cords (Ferri et al 2011), which may be at an early stage of contact with Wolbachia, and of hosts that were once infected with Wolbachia but have become aposymbiotic (such as Onchocerca flexuosa) (McNulty et al 2010), which could reflect the evolution of countermeasures to regain control of the apoptotic cascade. In addition, if Wolbachia in filarial nematodes is fundamentally a parasitic infection that has secondarily acquired mutualistic traits, the hypothesis that lateral gene transfers of symbiont DNA into the host genome could constitute the capture of useful functions is unlikely to be correct (Fenn and Blaxter 2007).…”

“…However, it also has a much more restricted prevalence in two families of nematode worms: about 20 species of animal-parasitic Onchocercidae (superfamily Filarioidea; the filariae) (Ferri et al 2011) and at least two species of plant-parasitic Pratylenchidae (Haegeman et al 2009). The most salient characteristic of Wolbachia is its astonishing ability to induce a wide diversity of phenotypes in arthropod hosts, from reproductive manipulations, such as cytoplasmic incompatibility and male-killing, to mutualistic roles, including pathogen protection and enhanced fecundity.…”

Evolutionary origin of insect– Wolbachia nutritional mutualism

“…Some F Wolbachia strains are obligatorily associated with Mansonella spp. and other filarial nematodes (29)(30)(31). However, they were placed in distinct lineages from the arthropod-associated F Wolbachia strains including wCle, although statistical supports for the groupings were not necessarily significant (Fig.…”