Skip to main content

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home
  • Log in
  • My Cart

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
Research Article

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, and Jason L. Rasgon
  1. Departments of aEntomology,
  2. bImmunology and Infectious Diseases, and
  3. dBiology, Center for Infectious Disease Dynamics, and the Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA 16802;
  4. cDepartment of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005; and
  5. eThe Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom

See allHide authors and affiliations

PNAS August 26, 2014 111 (34) 12498-12503; first published August 11, 2014; https://doi.org/10.1073/pnas.1408888111
Grant L. Hughes
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Brittany L. Dodson
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rebecca M. Johnson
bImmunology and Infectious Diseases, and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Courtney C. Murdock
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hitoshi Tsujimoto
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yasutsugu Suzuki
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Alyssa A. Patt
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Long Cui
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Carlos W. Nossa
cDepartment of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005; and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rhiannon M. Barry
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Joyce M. Sakamoto
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Emily A. Hornett
dBiology, Center for Infectious Disease Dynamics, and the Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA 16802;
eThe Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jason L. Rasgon
Departments of aEntomology,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: jlr54@psu.edu
  1. Edited by Carolina Barillas-Mury, National Institutes of Health, Bethesda, MD, and approved July 10, 2014 (received for review May 13, 2014)

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

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.

View Full Text
PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Anopheles microbiota impede Wolbachia transmission
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
Proceedings of the National Academy of Sciences Aug 2014, 111 (34) 12498-12503; DOI: 10.1073/pnas.1408888111

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
Anopheles microbiota impede Wolbachia transmission
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
Proceedings of the National Academy of Sciences Aug 2014, 111 (34) 12498-12503; DOI: 10.1073/pnas.1408888111
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley

Article Classifications

  • Biological Sciences
  • Microbiology
Proceedings of the National Academy of Sciences: 111 (34)
Table of Contents

Submit

Sign up for Article Alerts

Jump to section

  • Article
    • Abstract
    • Results
    • Discussion
    • Materials and Methods
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Water from a faucet fills a glass.
News Feature: How “forever chemicals” might impair the immune system
Researchers are exploring whether these ubiquitous fluorinated molecules might worsen infections or hamper vaccine effectiveness.
Image credit: Shutterstock/Dmitry Naumov.
Reflection of clouds in the still waters of Mono Lake in California.
Inner Workings: Making headway with the mysteries of life’s origins
Recent experiments and simulations are starting to answer some fundamental questions about how life came to be.
Image credit: Shutterstock/Radoslaw Lecyk.
Cave in coastal Kenya with tree growing in the middle.
Journal Club: Small, sharp blades mark shift from Middle to Later Stone Age in coastal Kenya
Archaeologists have long tried to define the transition between the two time periods.
Image credit: Ceri Shipton.
Illustration of groups of people chatting
Exploring the length of human conversations
Adam Mastroianni and Daniel Gilbert explore why conversations almost never end when people want them to.
Listen
Past PodcastsSubscribe
Panda bear hanging in a tree
How horse manure helps giant pandas tolerate cold
A study finds that giant pandas roll in horse manure to increase their cold tolerance.
Image credit: Fuwen Wei.

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Special Feature Articles – Most Recent
  • List of Issues

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Subscribers
  • Librarians
  • Press
  • Cozzarelli Prize
  • Site Map
  • PNAS Updates
  • FAQs
  • Accessibility Statement
  • Rights & Permissions
  • About
  • Contact

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490