Literature DB >> 28835539

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

Janna C Nawroth1,2,3, Hanliang Guo4, Eric Koch3, Elizabeth A C Heath-Heckman5, John C Hermanson6, Edward G Ruby3, John O Dabiri2,7, Eva Kanso8, Margaret McFall-Ngai9.   

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.

Entities:  

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

Mesh:

Year:  2017        PMID: 28835539      PMCID: PMC5594677          DOI: 10.1073/pnas.1706926114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  42 in total

1.  Chaotic mixer for microchannels.

Authors:  Abraham D Stroock; Stephan K W Dertinger; Armand Ajdari; Igor Mezic; Howard A Stone; George M Whitesides
Journal:  Science       Date:  2002-01-25       Impact factor: 47.728

Review 2.  Mucus clearance as a primary innate defense mechanism for mammalian airways.

Authors:  Michael R Knowles; Richard C Boucher
Journal:  J Clin Invest       Date:  2002-03       Impact factor: 14.808

3.  Ciliostasis is a key early event during colonization of canine tracheal tissue by Bordetella bronchiseptica.

Authors:  Tracy L Anderton; Duncan J Maskell; Andrew Preston
Journal:  Microbiology       Date:  2004-09       Impact factor: 2.777

4.  Respiratory and brain ependymal ciliary function.

Authors:  C O'Callaghan; K Sikand; A Rutman
Journal:  Pediatr Res       Date:  1999-12       Impact factor: 3.756

Review 5.  Overview of structure and function of mammalian cilia.

Authors:  Peter Satir; Søren Tvorup Christensen
Journal:  Annu Rev Physiol       Date:  2007       Impact factor: 19.318

6.  Filter feeders and plankton increase particle encounter rates through flow regime control.

Authors:  Stuart Humphries
Journal:  Proc Natl Acad Sci U S A       Date:  2009-04-28       Impact factor: 11.205

7.  A millisecond micromixer via single-bubble-based acoustic streaming.

Authors:  Daniel Ahmed; Xiaole Mao; Jinjie Shi; Bala Krishna Juluri; Tony Jun Huang
Journal:  Lab Chip       Date:  2009-06-23       Impact factor: 6.799

8.  Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment.

Authors:  S V Nyholm; E V Stabb; E G Ruby; M J McFall-Ngai
Journal:  Proc Natl Acad Sci U S A       Date:  2000-08-29       Impact factor: 11.205

9.  Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ.

Authors:  Spencer V Nyholm; Bart Deplancke; H Rex Gaskins; Michael A Apicella; Margaret J McFall-Ngai
Journal:  Appl Environ Microbiol       Date:  2002-10       Impact factor: 4.792

10.  Motile cilia of human airway epithelia are chemosensory.

Authors:  Alok S Shah; Yehuda Ben-Shahar; Thomas O Moninger; Joel N Kline; Michael J Welsh
Journal:  Science       Date:  2009-07-23       Impact factor: 47.728

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  34 in total

Review 1.  Links between metamorphosis and symbiosis in holometabolous insects.

Authors:  Tobin J Hammer; Nancy A Moran
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-08-26       Impact factor: 6.237

2.  Vibrio2017: the seventh international conference on the biology of Vibrios.

Authors:  Karl E Klose; Karla J F Satchell
Journal:  J Bacteriol       Date:  2018-06-04       Impact factor: 3.490

3.  Vibrio fischeri: Laboratory Cultivation, Storage, and Common Phenotypic Assays.

Authors:  David G Christensen; Karen L Visick
Journal:  Curr Protoc Microbiol       Date:  2020-06

4.  The model squid-vibrio symbiosis provides a window into the impact of strain- and species-level differences during the initial stages of symbiont engagement.

Authors:  Sabrina Koehler; Roxane Gaedeke; Cecilia Thompson; Clotilde Bongrand; Karen L Visick; Edward Ruby; Margaret McFall-Ngai
Journal:  Environ Microbiol       Date:  2018-08-22       Impact factor: 5.491

Review 5.  Housing microbial symbionts: evolutionary origins and diversification of symbiotic organs in animals.

Authors:  Angela E Douglas
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-08-10       Impact factor: 6.237

6.  Profile of Margaret J. McFall-Ngai.

Authors:  Jennifer Viegas
Journal:  Proc Natl Acad Sci U S A       Date:  2017-08-22       Impact factor: 11.205

7.  On the unity and diversity of cilia.

Authors:  Kirsty Y Wan; Gáspár Jékely
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-12-30       Impact factor: 6.237

8.  Diversity of cilia-based mechanosensory systems and their functions in marine animal behaviour.

Authors:  Luis Alberto Bezares-Calderón; Jürgen Berger; Gáspár Jékely
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-12-30       Impact factor: 6.237

Review 9.  The impact of Vibrio fischeri strain variation on host colonization.

Authors:  Clotilde Bongrand; Edward G Ruby
Journal:  Curr Opin Microbiol       Date:  2019-10-06       Impact factor: 7.934

10.  Acoustic Actuation of in situ Fabricated Artificial Cilia.

Authors:  Sinem Orbay; Adem Ozcelik; Hunter Bachman; Tony Jun Huang
Journal:  J Micromech Microeng       Date:  2018-01-09       Impact factor: 1.881

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