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Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome

Nawroth, Janna C. and Guo, Hanliang and Koch, Eric and Heath-Heckman, Elizabeth A. C. and Hermanson, John C. and Ruby, Edward G. and Dabiri, John O. and Kanso, Eva and McFall-Ngai, Margaret (2017) Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome. Proceedings of the National Academy of Sciences of the United States of America, 114 (36). pp. 9510-9516. ISSN 0027-8424. PMCID PMC5594677. http://resolver.caltech.edu/CaltechAUTHORS:20170901-104738795

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Abstract

We show that mucociliary membranes of animal epithelia can create fluid-mechanical microenvironments for the active recruitment of the specific microbiome of the host. In terrestrial vertebrates, these tissues are typically colonized by complex consortia and are inaccessible to observation. Such tissues can be directly examined in aquatic animals, providing valuable opportunities for the analysis of mucociliary activity in relation to bacteria recruitment. Using the squid–vibrio model system, we provide a characterization of the initial engagement of microbial symbionts along ciliated tissues. Specifically, we developed an empirical and theoretical framework to conduct a census of ciliated cell types, create structural maps, and resolve the spatiotemporal flow dynamics. Our multiscale analyses revealed two distinct, highly organized populations of cilia on the host tissues. An array of long cilia (∼25 μm) with metachronal beat creates a flow that focuses bacteria-sized particles, at the exclusion of larger particles, into sheltered zones; there, a field of randomly beating short cilia (∼10 μm) mixes the local fluid environment, which contains host biochemical signals known to prime symbionts for colonization. This cilia-mediated process represents a previously unrecognized mechanism for symbiont recruitment. Each mucociliary surface that recruits a microbiome such as the case described here is likely to have system-specific features. However, all mucociliary surfaces are subject to the same physical and biological constraints that are imposed by the fluid environment and the evolutionary conserved structure of cilia. As such, our study promises to provide insight into universal mechanisms that drive the recruitment of symbiotic partners.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1706926114DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5594677/PubMed CentralArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1706926114/-/DCSupplementalPublisherSupporting Information
ORCID:
AuthorORCID
Dabiri, John O.0000-0002-6722-9008
Additional Information:© 2017 National Academy of Sciences. Contributed by Margaret McFall-Ngai, July 21, 2017 (sent for review April 26, 2017; reviewed by Christophe Eloy and M. A. R. Koehl). Published online before print August 23, 2017. This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2014. We thank B. Boettner, S. Fraser, and M. Kinzel for helpful discussion of the manuscript. Funding was provided by National Institutes of Health grants from The National Institute of Allergy and Infectious Diseases (AI050661) (to M.M.-N.) and Office of Research Infrastructure Programs (RR012294/OD011024) (to E.G.R.), by the Gordon & Betty Moore Foundation (3396) (to E.G.R.), and by a National Science Foundation Integrated NSF Support Promoting Interdisciplinary Research and Education Grant (NSF-MCB1608744) (to M.M.-N., E.G.R., and E. Kanso). Author contributions: J.C.N., H.G., E.G.R., J.O.D., E. Kanso, and M.M.-N. designed research; J.C.N., H.G., and E. Kanso performed research; J.C.N., H.G., E. Kanso, and M.M.-N. contributed new reagents/analytic tools; J.C.N., E. Koch, E.A.C.H.-H., and J.C.H. conducted biological imaging; J.C.N., H.G., E.G.R., J.O.D., E. Kanso, and M.M.-N. analyzed data; and J.C.N., H.G., E.G.R., E. Kanso, and M.M.-N. wrote the paper. Reviewers: C.E., Institut de Recherche sur les Phénomènes Hors Equilibre; and M.A.R.K., University of California, Berkeley. Conflict of interest statement: Coauthor E.A.C.H.-H. and reviewer M.A.R.K. are both affiliated with the University of California, Berkeley, but in different departments. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1706926114/-/DCSupplemental.
Group:GALCIT
Funders:
Funding AgencyGrant Number
NIHAI050661
NIHRR012294
NIHOD011024
Gordon and Betty Moore Foundation3396
NSFMCB-1608744
Subject Keywords:cilia; microfluidics; host–bacterial symbiosis; biological fluid mechanics, biofiltration
PubMed Central ID:PMC5594677
Record Number:CaltechAUTHORS:20170901-104738795
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20170901-104738795
Official Citation:Janna C. Nawroth, Hanliang Guo, Eric Koch, Elizabeth A. C. Heath-Heckman, John C. Hermanson, Edward G. Ruby, John O. Dabiri, Eva Kanso, and Margaret McFall-Ngai Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome PNAS 2017 114 (36) 9510-9516; published ahead of print August 23, 2017, doi:10.1073/pnas.1706926114
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:81068
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:01 Sep 2017 18:08
Last Modified:22 Apr 2019 23:53

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