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Edited by Carolina Barillas-Mury, National Institutes of Health, Bethesda, MD, and approved July 10, 2014 (received for review May 13, 2014)
Significance
Factors influencing Wolbachia transfer into new species remain poorly understood. This is important as Wolbachia can influence speciation and is being developed as a novel arthropod-borne disease control approach. We show the native microbiota of Anopheles impede vertical transmission of Wolbachia. Antibiotic microbiome perturbation enables Wolbachia transmission in two Anopheles species. Mosquitoes with altered microbiomes do not exhibit blood meal-induced mortality associated with Wolbachia infection, suggesting that mosquitoes are killed by interactions between Wolbachia and other bacteria present in the mosquito. We identified Asaia as the bacterium responsible for inhibiting Wolbachia transmission, and partially responsible for blood meal-induced mortality. These results suggest that microbial interactions profoundly affect the host, and that microbiome incompatibility may influence distribution of Wolbachia in arthropods.
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.
Footnotes
↵1Present address: Department of Biology, New Mexico State University, Las Cruces, NM 88001.
↵2Present address: Gene by Gene, Ltd., Houston, TX 77008.
- ↵3To whom correspondence should be addressed. Email: jlr54{at}psu.edu.
Author contributions: G.L.H. and J.L.R. designed research; G.L.H., B.L.D., R.M.J., C.C.M., H.T., Y.S., A.A.P., L.C., C.W.N., and R.M.B. performed research; G.L.H., J.M.S., E.A.H., and J.L.R. analyzed data; and G.L.H., E.A.H., and J.L.R. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1408888111/-/DCSupplemental.
- Grant L. Hughesa,
- Brittany L. Dodsona,
- Rebecca M. Johnsonb,
- Courtney C. Murdocka,
- Hitoshi Tsujimotoa,1,
- Yasutsugu Suzukia,
- Alyssa A. Patta,
- Long Cuia,
- Carlos W. Nossac,2,
- Rhiannon M. Barrya,
- Joyce M. Sakamotoa,
- Emily A. Hornettd,e, and
- Jason L. Rasgona,3
- Departments of aEntomology,
- bImmunology and Infectious Diseases, and
- dBiology, Center for Infectious Disease Dynamics, and the Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA 16802;
- cDepartment of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005; and
- eThe Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom
Edited by Carolina Barillas-Mury, National Institutes of Health, Bethesda, MD, and approved July 10, 2014 (received for review May 13, 2014)
Significance
Factors influencing Wolbachia transfer into new species remain poorly understood. This is important as Wolbachia can influence speciation and is being developed as a novel arthropod-borne disease control approach. We show the native microbiota of Anopheles impede vertical transmission of Wolbachia. Antibiotic microbiome perturbation enables Wolbachia transmission in two Anopheles species. Mosquitoes with altered microbiomes do not exhibit blood meal-induced mortality associated with Wolbachia infection, suggesting that mosquitoes are killed by interactions between Wolbachia and other bacteria present in the mosquito. We identified Asaia as the bacterium responsible for inhibiting Wolbachia transmission, and partially responsible for blood meal-induced mortality. These results suggest that microbial interactions profoundly affect the host, and that microbiome incompatibility may influence distribution of Wolbachia in arthropods.
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.
- holobiome
- dysbiosis
- competitive exclusion
- microbe–microbe interactions
- malaria
Footnotes
↵1Present address: Department of Biology, New Mexico State University, Las Cruces, NM 88001.
↵2Present address: Gene by Gene, Ltd., Houston, TX 77008.
- ↵3To whom correspondence should be addressed. Email: jlr54{at}psu.edu.
Author contributions: G.L.H. and J.L.R. designed research; G.L.H., B.L.D., R.M.J., C.C.M., H.T., Y.S., A.A.P., L.C., C.W.N., and R.M.B. performed research; G.L.H., J.M.S., E.A.H., and J.L.R. analyzed data; and G.L.H., E.A.H., and J.L.R. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1408888111/-/DCSupplemental.
Anopheles microbiota impede Wolbachia transmission
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