Horizontal transfers of feminizing versus non-feminizing Wolbachia strains: From harmless passengers to pathogens

Environmental Microbiology

Volumn 15, Issue 11, 2013, Pages 2922-2936

  Le Clec'h, Winka ^a,b   Raimond, Maryline ^a   Guillot, Sylvain ^a   Bouchon, Didier ^a   Sicard, Mathieu ^a  

^a UNIVERSITÉ DE POITIERS   (France)

^b SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARMADILLIDIUM VULGARE; ISOPODA; PORCELLIO; PORCELLIO DILATATUS DILATATUS; WOLBACHIA; WOLBACHIA PIPIENTIS;

ANIMAL; CLASSIFICATION; GENETICS; ISOPODA; MICROBIOLOGY; PATHOGENICITY; PHENOTYPE; SYMBIOSIS; VIRULENCE; WOLBACHIA;

ANIMALS; ISOPODA; PHENOTYPE; SYMBIOSIS; VIRULENCE; WOLBACHIA;

EID: 84886420100     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12172     Document Type: Article

References (42)

1. Bandi, C., Anderson, T.J., Genchi, C., and Blaxter, M.L. (1998) Phylogeny of Wolbachia in filarial nematodes. Proc Biol Sci 265: 2407-2413.
2. Bouchon, D., Rigaud, T., and Juchault, P. (1998) Infection in isopod crustaceans: molecular identification and host feminization. Proc Biol Sci 265: 1081-1090.
3. Bouchon, D., Cordaux, R., and Grève, P. (2008) Feminizing Wolbachia and the evolution of sex determination in isopods. In Insect Symbiosis. Bourtzis, K., and Miller, T. (eds). Boca Raton, FL, USA: CRC press, pp. 273-294.
4. Braquart-Varnier, C., Lachat, M., Herbinière, J., Johnson, M., Caubet, Y., Bouchon, D., etal. (2008) Wolbachia mediate variation of host immunocompetence. PLoS ONE 3: e3286.
5. Clancy, D.J., and Hoffmann, A.A. (1997) Behavior of Wolbachia endosymbionts from Drosophila simulans in Drosophila serrata, a novel host. Am Nat 149: 975-988.
6. Cordaux, R., Michel-Salzat, A., and Bouchon, D. (2001) Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission. J Evol Biol 14: 237-243.
7. Cordaux, R., Michel Salzat, A., Frelon Raimond, M., Rigaud, T., and Bouchon, D. (2004) Evidence for a new feminizing Wolbachia strain in the isopod Armadillidium vulgare: evolutionary implications. Heredity 93: 78-84.
8. Cordaux, R., Pichon, S., Hatira, H.B.A., Doublet, V., Grève, P., Marcadé, I., etal. (2012) Widespread Wolbachia infection in terrestrial isopods and other crustaceans. Zookeys 176: 123-131.
9. Engelstädter, J., and Hurst, G.D.D. (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40: 127-149.
10. Grenier, S., Pintureau, B., Heddi, A., Lassabliére, F., Coenraad, J., Louis, C., etal. (1998) Successful horizontal transfer of Wolbachia symbionts between trichogramma wasps. Proc Biol Sci 265: 1441-1445.
11. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
12. Heath, B.D., Butcher, D.J., Whitfield, W.G.F., and Hubbard, S.F. (1999) Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9: 313-316.
13. Huigens, M.E., de Almeida, R.P., Boons, P.A.H., Luck, R.F., and Stouthamer, R. (2004) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc Biol Sci 271: 509-515.
14. Jeyaprakash, A., and Hoy, M.A. (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 9: 393-405.
15. Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X., etal. (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86: 6196-6200.
16. Kraaijeveld, K., Franco, P., De Knijff, P., Stouthamer, R., and Van Alphen, J.J.M. (2011) Clonal genetic variation in a Wolbachia-infected asexual wasp: horizontal transmission or historical sex? Mol Ecol 20: 3644-3652.
17. Lachat, M. (2009) Impact de deux souches de Wolbachia sur les traits d'histoire de vie de leurs hôtes Armadillidium vulgare. PhD Thesis. Université de Poitiers.
18. Le Clec'h, W., Braquart-Varnier, C., Raimond, M., Ferdy, J.B., Bouchon, D., and Sicard, M. (2012) High virulence of Wolbachia after host switching: when autophagy hurts. PLoS Pathog 8: e1002844.
19. Legrand, J.J., Martin, G., and Artault, J.C. (1978) Corrélation entre la présence d'un symbionte bactérien dans les ovocytes de Porcellio dilatatus petiti et la stérilité du croisement P.d. petiti mâle x P. d. dilatatus femelle. Arch Inst Pasteur Tunis 55: 507-514.
20. Lindstrom, M.J., and Bates, D.M. (1988) Newton-Raphson and EM algorithms for linear mixed-effects models for repeated-measures data. J Am Stat Assoc 83: 1014-1022.
21. McMeniman, C.J., Lane, A.M., Fong, A.W.C., Voronin, D.A., Iturbe-Ormaetxe, I., Yamada, R., etal. (2008) Host adaptation of a Wolbachia strain after long-term serial passage in mosquito cell lines. Appl Environ Microbiol 74: 6963-6969.
22. McMeniman, C.J., Lane, R.V., Cass, B.N., Fong, A.W.C., Sidhu, M., Wang, Y.F., and O'Neill, S.L. (2009) Stable infection of a life-shortening Wolbachia infection in the mosquito Aedes aegypti. Science 323: 141-144.
23. Michel-Salzat, A., Cordaux, R., and Bouchon, D. (2001) Wolbachia diversity in the Porcellionides pruinosus complex of species (crustacea: oniscidea): evidence for host-dependent patterns of infection. Heredity 87: 428-434.
24. Moreira, L.A., Saig, E., Turley, P.A., Ribeiro, J.C., O'Neill, S.L., and McGraw, E.A. (2009) Human probing behavior of Aedes aegypti when infected with a life-shortening strain of Wolbachia. PLoS Negl Trop Dis 3: e568.
25. Moret, Y., Juchault, P., and Rigaud, T. (2001) Endosymbiont responsible for cytoplasmic incompatibility in a terrestrial crustacean: effects in natural and foreign hosts. Heredity 86: 325-332.
26. Raychoudhury, R., Baldo, L., Oliveira, D.C., and Werren, J.H. (2009) Mode of acquisition of Wolbachia: horizontal tranfer, hybrid introgression and codivergence in the Nasonia species complex. Evolution 63: 165-183.
27. Riegler, M., Charlat, S., Stauffer, C., and Merçot, H. (2004) Wolbachia transfer from Rhagoletis cerasi to Drosophila simulans: investigating the outcomes of host-symbiont coevolution. Appl Environ Microbiol 70: 273-279.
28. Rigaud, T., and Juchault, P. (1995) Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. J Evol Biol 8: 249-255.
29. Rigaud, T., Moreau, J., and Juchault, P. (1999) Wolbachia infection in the terrestrial isopod Oniscus asellus: sex ratio distortion and effect on fecundity. Heredity 83: 469-475.
30. Rigaud, T., Pennings, P.S., and Juchault, P. (2001) Wolbachia bacteria effects after experimental interspecific transfers in terrestrial isopods. J Invertebr Pathol 77: 251-257.
31. Ruang-areerate, T., and Kittayapong, P. (2006) Wolbachia transinfection in Aedes aegypti: a potential gene driver of dengue vector. Proc Natl Acad Sci USA 103: 12534-12539.
32. Schneider, D.S., and Ayres, J.S. (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 8: 889-895.
33. Suh, E., Mercer, D.R., Fu, Y., and Dobson, S.L. (2009) Pathogenicity of life-shortening Wolbachia in Aedes albopictus after transfert from Drosophila melanogaster. Appl Environ Microbiol 75: 7783-7788.
34. Tamura, K., and Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512-526.
35. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
36. Vavre, F., Fleury, F., Lepetit, D., Fouillet, P., and Boulétreau, M. (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16: 1711-1723.
37. Watanabe, M., Tagami, Y., Miura, K., Kageyama, D., and Stouthamer, R. (2012) Distribution patterns of Wolbachia endosymbionts in the closely related flower bugs of the genus Orius: implications for coevolution and horizontal transfer. Microb Ecol 64: 537-545.
38. Werren, J.H., Zhang, W., and Guo, L.R. (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci 261: 55-63.
39. Werren, J.H., Baldo, L., and Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741-751.
40. Xi, Z., Khoo, C.C.H., and Dobson, S.L. (2005) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310: 326-328.
41. Xi, Z., Khoo, C.C.H., and Dobson, S.L. (2006) Interspecific transfer of Wolbachia into the mosquito disease vector Aedes albopictus. Proc Biol Sci 273: 1317-1322.
42. Zabalou, S., Riegler, M., Theodorakopoulou, M., Stauffer, C., Savakis, C., and Bourtzis, K. (2004) Wolbachia-induced cytoplasmic incompatibility as mean for insect pest population control. Proc Natl Acad Sci USA 101: 15042-15045.