Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome [Biophysics and Computational Biology]
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 (
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 (
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.
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