The Wolbachia Endosymbionts

Abstract

The Wolbachia endosymbionts encompass a large group of intracellular bacteria of biomedical and veterinary relevance, closely related to Anaplasma, Ehrlichia, and Rickettsia. This genus of Gram-negative members of the Alphaproteobacteria does not infect vertebrates but is instead restricted to ecdysozoan species, including terrestrial arthropods and a family of parasitic filarial nematodes, the Onchocercidae. The Wolbachia profoundly impact not only the ecology and evolution but also the reproductive biology of their hosts, through a wide range of symbiotic interactions. Because they are essential to the survival and reproduction of their filarial nematode hosts, they represent an attractive target to fight filariasis. Their abilities to spread through insect populations and to affect vector competence through pathogen protection have made Wolbachia a staple for controlling vector-borne diseases. Estimated to be present in up to 66% of insect species, the Wolbachia are probably the most abundant endosymbionts on earth. Their success resides in their unique capacity to infect and manipulate the host germ line to favor their vertical transmission through the maternal lineage. Because the Wolbachia resist genetic manipulation and growth in axenic culture, our understanding of their biology is still in its infancy. Despite these limitations, the "-omics" revolution combined with the use of well-established and emerging experimental host models is accelerating our comprehension of the host phenotypes caused by Wolbachia, and the identification of Wolbachia effectors is ongoing.

FIGURE 1

Overview of Wolbachia diversity. (A) Unrooted phylogenic tree of the main Wolbachia supergroups. The triangle size represents the described diversity within each supergroup. (B) Comparison of genomic features of Wolbachia endosymbionts with other Rickettsiales pathogens. wBm and wMel, endosymbionts from B. malayi and D. melanogaster; R. conorii, Rickettsia conorii; R. prowazekii, Rickettsia prowazekii. Adapted from references and .

FIGURE 2

The four reproductive outcomes caused by Wolbachia, with an example of arthropod species described in the text. (A) Parthenogenesis, MK, and feminization cause a sex ratio distortion. (B) CI (left) and the rescue cross (right). Uninfected females cannot successfully mate with infected males (CI), while infected females have the selective advantage to mate with noninfected males or with males infected with a compatible strain.

FIGURE 3

Germ line tropism and Wolbachia transmission in insect and nematode species. (A) Schematic representation of D. melanogaster oogenesis. The germ line is in white, and the surrounding somatic follicle cells are in gray. For the sake of clarity, Wolbachia are not represented within the germarium, where they colonize the GSCs and associated niche (GSCN) (dark and light purple, respectively), as well as the somatic stem cell niche (SSCN; pink). In developing cysts, polar cells (PCs) are yellow, the microtubule (green) polarity is indicated by plus and minus signs, and the Wolbachia organisms are red foci. Nuclei of developing cysts are depicted in blue. (B) Asymmetric segregation of Wolbachia during early embryogenesis in B. malayi. The confocal image of a fertilized egg shows the Wolbachia (red foci) in the posterior compartment around the centrosome (green) during the first anaphase. The route followed by Wolbachia to reach the hypodermis in the early lineage is highlighted in black. The P lineage represents the germ line precursor lineage, left by Wolbachia after the P2 division to concentrate in the hypodermal precursor C blastomere. (C) Schematic cross section of a B. malayi female, with an emphasis on the tissues infected by Wolbachia. The confocal image shows the tropism of some Wolbachia organisms from the hypodermis to the somatic gonad in a juvenile female. Asterisks indicate the entry and proliferation of Wolbachia in the somatic ovarian distal sheath cells.