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Proc Natl Acad Sci U S A. 2017 Sep 5;114(36):9510-9516. doi: 10.1073/pnas.1706926114. Epub 2017 Aug 23.

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

Author information

1
Research & Development, Emulate Inc., Boston, MA 02210.
2
Graduate Aeronautical Laboratories and Bioengineering, California Institute of Technology, Pasadena, CA 91125.
3
Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822.
4
Department of Aerospace and Mechanical Engineering, University of Southern California, Los Angeles, CA 90089-1191.
5
The Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720.
6
US Department of Agriculture Forest Products Laboratory, Madison, WI 53726.
7
Department of Civil and Environmental Engineering, Stanford University, Stanford, CA 94305.
8
Department of Aerospace and Mechanical Engineering, University of Southern California, Los Angeles, CA 90089-1191; kanso@usc.edu mcfallng@hawaii.edu.
9
Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822; kanso@usc.edu mcfallng@hawaii.edu.

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 ([Formula: see text]25 [Formula: see text]m) 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 ([Formula: see text]10 [Formula: see text]m) 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.

KEYWORDS:

biological fluid mechanics, biofiltration; cilia; host–bacterial symbiosis; microfluidics

Comment in

PMID:
28835539
PMCID:
PMC5594677
DOI:
10.1073/pnas.1706926114
[Indexed for MEDLINE]
Free PMC Article

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