Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes

Grant L. Hughes, Brittany L. Dodson, Rebecca M. Johnson, Courtney C. Murdock, Hitoshi Tsujimoto, Yasutsugu Suzuki, Alyssa A. Patt, Long Cui, Carlos W. Nossa, Rhiannon M. Barry, Joyce M. Sakamoto, Emily A. Hornett, Jason L. Rasgon

Research output: Contribution to journalArticle

83 Citations (Scopus)

Abstract

Over evolutionary time, Wolbachia has been repeatedly transferred between host species contributing to the widespread distribution of the symbiont in arthropods. For novel infections to be maintained, Wolbachia must infect the female germ line after being acquired by horizontal transfer. Although mechanistic examples of horizontal transfer exist, there is a poor understanding of factors that lead to successful vertical maintenance of the acquired infection. Using Anopheles mosquitoes (which are naturally uninfected by Wolbachia) we demonstrate that the native mosquito microbiota is a major barrier to vertical transmission of a horizontally acquired Wolbachia infection. After injection into adult Anopheles gambiae, some strains of Wolbachia invade the germ line, but are poorly transmitted to the next generation. In Anopheles stephensi, Wolbachia infection elicited massive blood meal-induced mortality, preventing development of progeny. Manipulation of the mosquito microbiota by antibiotic treatment resulted in perfect maternal transmission at significantly elevated titers of the wAlbB Wolbachia strain in A. gambiae, and alleviated blood meal-induced mortality in A. stephensi enabling production of Wolbachia-infected offspring. Microbiome analysis using high-throughput sequencing identified that the bacterium Asaia was significantly reduced by antibiotic treatment in both mosquito species. Supplementation of an antibiotic-resistant mutant of Asaia to antibiotic-treated mosquitoes completely inhibited Wolbachia transmission and partly contributed to blood meal-induced mortality. These data suggest that the components of the native mosquito microbiota can impede Wolbachia transmission in Anopheles. Incompatibility between the microbiota and Wolbachia may in part explain why some hosts are uninfected by this endosymbiont in nature.

Original languageEnglish (US)
Pages (from-to)12498-12503
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number34
DOIs
StatePublished - Aug 26 2014
Externally publishedYes

Fingerprint

Wolbachia
Anopheles
Microbiota
Culicidae
Anti-Bacterial Agents
Anopheles gambiae
Meals
Infection
Germ Cells
Mortality
Arthropods

Keywords

  • Competitive exclusion
  • Dysbiosis
  • Holobiome
  • Malaria
  • Microbe-microbe interactions

ASJC Scopus subject areas

  • General
  • Medicine(all)

Cite this

Hughes, G. L., Dodson, B. L., Johnson, R. M., Murdock, C. C., Tsujimoto, H., Suzuki, Y., ... Rasgon, J. L. (2014). Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes. Proceedings of the National Academy of Sciences of the United States of America, 111(34), 12498-12503. https://doi.org/10.1073/pnas.1408888111

Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes. / Hughes, Grant L.; Dodson, Brittany L.; Johnson, Rebecca M.; Murdock, Courtney C.; Tsujimoto, Hitoshi; Suzuki, Yasutsugu; Patt, Alyssa A.; Cui, Long; Nossa, Carlos W.; Barry, Rhiannon M.; Sakamoto, Joyce M.; Hornett, Emily A.; Rasgon, Jason L.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 34, 26.08.2014, p. 12498-12503.

Research output: Contribution to journalArticle

Hughes, GL, Dodson, BL, Johnson, RM, Murdock, CC, Tsujimoto, H, Suzuki, Y, Patt, AA, Cui, L, Nossa, CW, Barry, RM, Sakamoto, JM, Hornett, EA & Rasgon, JL 2014, 'Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 34, pp. 12498-12503. https://doi.org/10.1073/pnas.1408888111
Hughes, Grant L. ; Dodson, Brittany L. ; Johnson, Rebecca M. ; Murdock, Courtney C. ; Tsujimoto, Hitoshi ; Suzuki, Yasutsugu ; Patt, Alyssa A. ; Cui, Long ; Nossa, Carlos W. ; Barry, Rhiannon M. ; Sakamoto, Joyce M. ; Hornett, Emily A. ; Rasgon, Jason L. / Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes. In: Proceedings of the National Academy of Sciences of the United States of America. 2014 ; Vol. 111, No. 34. pp. 12498-12503.
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