Despite myriad challenges, clinicians see room for progress.
Image credit: Shutterstock/David Tadevosian.
Edited by Margaret McFall-Ngai, University of Wisconsin–Madison, Madison, WI, and accepted by the Editorial Board August 5, 2013 (received for review March 18, 2013)
Significance
Animals form functional unities with communities of microbes. Often, these bacterial communities are highly specific to host species and resemble host phylogeny. But which factors determine community membership? Which host-factors are capable of selecting suitable bacteria by inhibiting colonization by potential foreign colonizers? In this study, we show that animals express a species-specific repertoire of antimicrobial peptides, which supports and maintains a species-specific bacterial community. Loss-of-function experiments showed that antimicrobial peptide composition is a predictor for bacterial colonization.
Abstract
Animals are colonized by coevolved bacterial communities, which contribute to the host’s health. This commensal microbiota is often highly specific to its host-species, inferring strong selective pressures on the associated microbes. Several factors, including diet, mucus composition, and the immune system have been proposed as putative determinants of host-associated bacterial communities. Here we report that species-specific antimicrobial peptides account for different bacterial communities associated with closely related species of the cnidarian Hydra. Gene family extensions for potent antimicrobial peptides, the arminins, were detected in four Hydra species, with each species possessing a unique composition and expression profile of arminins. For functional analysis, we inoculated arminin-deficient and control polyps with bacterial consortia characteristic for different Hydra species and compared their selective preferences by 454 pyrosequencing of the bacterial microbiota. In contrast to control polyps, arminin-deficient polyps displayed decreased potential to select for bacterial communities resembling their native microbiota. This finding indicates that species-specific antimicrobial peptides shape species-specific bacterial associations.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: sfraune{at}zoologie.uni-kiel.de.
Author contributions: S. Franzenburg, T.C.G.B., and S. Fraune designed research; S. Franzenburg, J. Walter, and S. Fraune performed research; S.K., J. Wang, and J.F.B. contributed new reagents/analytic tools; S. Franzenburg, J. Walter, and S. Fraune analyzed data; and S. Franzenburg, T.C.G.B., and S. Fraune wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. M.M.-N. is a guest editor invited by the Editorial Board.
Data deposition: The 454 data are deposited in the Metagenomics RAST (MG-RAST) database, metagenomics.anl.gov (Project IDs: 3512, 3514, and 3526). The arminin sequences have been deposited in the GenBank database, http://www.ncbi.nlm.nih.gov/genbank/ (accession nos. KC701494–KC701520).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1304960110/-/DCSupplemental.
Role of AMPs in shaping the microbiota
Sign up for Article Alerts
Jump to section
You May Also be Interested in
Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Using CRISPR, researchers showed that a region some used to label “junk DNA” has a major role in a rare genetic disorder.
Image credit: Nathan Devery.
Mara Reed and Michael Manga explore why Yellowstone's Steamboat Geyser resumed erupting in 2018.
Some songbird parents might improve their own fitness by manipulating their offspring into leaving the nest early, at the cost of fledgling survival, a study finds.
Image credit: Gil Eckrich (photographer).