The bacteria<i>Wolbachia</i>in filariae, a biological Russian dolls’ system: new trends in antifilarial treatments

Martin, Coralie; Gavotte, Laurent

doi:10.1051/parasite/2010172079

Cited by 23 publications

(13 citation statements)

References 16 publications

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“…The bacteria of this genus are considered to be the most widely spread symbionts in the animal world, perhaps infecting half of insect species [3][4][5]. Wolbachia are maternally inherited and can induce variable phenotypes in their hosts through mutualism or parasitism [6][7][8][9]. Wolbachia are genetically diverse, as are the interactions with their hosts [10,11].…”

Section: Introductionmentioning

confidence: 99%

Pseudoscorpion Wolbachia symbionts: diversity and evidence for a new supergroup S

et al. 2020

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Background: Wolbachia are the most widely spread endosymbiotic bacteria, present in a wide variety of insects and two families of nematodes. As of now, however, relatively little genomic data has been available. The Wolbachia symbiont can be parasitic, as described for many arthropod systems, an obligate mutualist, as in filarial nematodes or a combination of both in some organisms. They are currently classified into 16 monophyletic lineage groups ("supergroups"). Although the nature of these symbioses remains largely unknown, expanded Wolbachia genomic data will contribute to understanding their diverse symbiotic mechanisms and evolution. Results: This report focuses on Wolbachia infections in three pseudoscorpion species infected by two distinct groups of Wolbachia strains, based upon multi-locus phylogenies. Geogarypus minor harbours wGmin and Chthonius ischnocheles harbours wCisc, both closely related to supergroup H, while Atemnus politus harbours wApol, a member of a novel supergroup S along with Wolbachia from the pseudoscorpion Cordylochernes scorpioides (wCsco). Wolbachia supergroup S is most closely related to Wolbachia supergroups C and F. Using target enrichment by hybridization with Wolbachia-specific biotinylated probes to capture large fragments of Wolbachia DNA, we produced two draft genomes of wApol. Annotation of wApol highlights presence of a biotin operon, which is incomplete in many sequenced Wolbachia genomes. Conclusions: The present study highlights at least two symbiont acquisition events among pseudoscorpion species. Phylogenomic analysis indicates that the Wolbachia from Atemnus politus (wApol), forms a separate supergroup ("S") with the Wolbachia from Cordylochernes scorpioides (wCsco). Interestingly, the biotin operon, present in wApol, appears to have been horizontally transferred multiple times along Wolbachia evolutionary history.

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Section: Introductionmentioning

confidence: 99%

Pseudoscorpion Wolbachia symbionts: diversity and evidence for a new supergroup S

et al. 2020

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“…First, composite dynamics of acquisition and loss of bacteria strains in arthropods has made the picture very complex at a co-evolutionary scale ( Baldo et al, 2008 ; Gerth, Rothe & Bleidorn, 2013 ; O’Neill et al, 1992 ; Vavre et al, 1999 ). Second, co-speciation of filariae and Wolbachia has been hypothesized ( Bandi et al, 1998 ), even if several cases of secondary losses and two cases of horizontal transmission between species have been detected, suggesting this scenario is too simplistic ( Ferri et al, 2011 ; Lefoulon et al, 2012 ; Martin & Gavotte, 2010 ). Moreover, to date, the notion of coevolution between Wolbachia and filariae was based on a poorly resolved evolutionary history of the Onchocercidae and limited sampling (just 10 examined species) ( Bandi et al, 1998 ).…”

Section: Introductionmentioning

confidence: 99%

Breakdown of coevolution between symbiotic bacteriaWolbachiaand their filarial hosts

Lefoulon

Bain

Makepeace

et al. 2016

PeerJ

100

134

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Wolbachia is an alpha-proteobacterial symbiont widely distributed in arthropods. Since the identification of Wolbachia in certain animal-parasitic nematodes (the Onchocercidae or filariae), the relationship between arthropod and nematode Wolbachia has attracted great interest. The obligate symbiosis in filariae, which renders infected species susceptible to antibiotic chemotherapy, was held to be distinct from the Wolbachia-arthropod relationship, typified by reproductive parasitism. While co-evolutionary signatures in Wolbachia-arthropod symbioses are generally weak, reflecting horizontal transmission events, strict co-evolution between filariae and Wolbachia has been reported previously. However, the absence of close outgroups for phylogenetic studies prevented the determination of which host group originally acquired Wolbachia. Here, we present the largest co-phylogenetic analysis of Wolbachia in filariae performed to date including: (i) a screening and an updated phylogeny of Wolbachia; (ii) a co-phylogenetic analysis; and (iii) a hypothesis on the acquisition of Wolbachia infection. First, our results show a general overestimation of Wolbachia occurrence and support the hypothesis of an ancestral absence of infection in the nematode phylum. The accuracy of supergroup J is also underlined. Second, although a global pattern of coevolution remains, the signal is derived predominantly from filarial clades associated with Wolbachia in supergroups C and J. In other filarial clades, harbouring Wolbachia supergroups D and F, horizontal acquisitions and secondary losses are common. Finally, our results suggest that supergroup C is the basal Wolbachia clade within the Ecdysozoa. This hypothesis on the origin of Wolbachia would change drastically our understanding of Wolbachia evolution.

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“…Some nematode species can host Wolbachia bacterial endosymbionts [2], [3]. A common feature of many filarial species is their ability to colonize lymphatic vessels: either they become resident and mature into adults (lymphatic filarioids e.g.…”

Section: Introductionmentioning

confidence: 99%

The Chemokine CXCL12 Is Essential for the Clearance of the Filaria Litomosoides sigmodontis in Resistant Mice

et al. 2012

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Litomosoides sigmodontis is a cause of filarial infection in rodents. Once infective larvae overcome the skin barrier, they enter the lymphatic system and then settle in the pleural cavity, causing soft tissue infection. The outcome of infection depends on the parasite's modulatory ability and also on the immune response of the infected host, which is influenced by its genetic background. The goal of this study was to determine whether host factors such as the chemokine axis CXCL12/CXCR4, which notably participates in the control of immune surveillance, can influence the outcome of the infection. We therefore set up comparative analyses of subcutaneous infection by L. sigmodontis in two inbred mouse strains with different outcomes: one susceptible strain (BALB/c) and one resistant strain (C57BL/6). We showed that rapid parasite clearance was associated with a L. sigmodontis -specific CXCL12-dependent cell response in C57BL/6 mice. CXCL12 was produced mainly by pleural mesothelial cells during infection. Conversely, the delayed parasite clearance in BALB/c mice was neither associated with an increase in CXCL12 levels nor with cell influx into the pleural cavity. Remarkably, interfering with the CXCL12/CXCR4 axis in both strains of mice delayed filarial development, as evidenced by the postponement of the fourth molting process. Furthermore, the in vitro growth of stage 4 filariae was favored by the addition of low amounts of CXCL12. The CXCL12/CXCR4 axis thus appears to have a dual effect on the L. sigmodontis life cycle: by acting as a host-cell restriction factor for infection, and as a growth factor for worms.

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The bacteriaWolbachiain filariae, a biological Russian dolls’ system: new trends in antifilarial treatments

Cited by 23 publications

References 16 publications

Pseudoscorpion Wolbachia symbionts: diversity and evidence for a new supergroup S

Pseudoscorpion Wolbachia symbionts: diversity and evidence for a new supergroup S

Breakdown of coevolution between symbiotic bacteriaWolbachiaand their filarial hosts

The Chemokine CXCL12 Is Essential for the Clearance of the Filaria Litomosoides sigmodontis in Resistant Mice

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