Recent studies have demonstrated that beneficial and pathogenic microbial associations often use the same host and bacterial surface molecules and bioactive compounds to mediate their interactions at epithelial cell surfaces. These findings beg the question: how does the host promote health by simultaneously discouraging pathogens and encouraging beneficial microbial partners? The symbiosis between the epithelial tissues of the squid Euprymna scolopes and its Gram- negative bacterial partner Vibrio fischeri is being exploited as an experimental system by which to address this critical question. In this association, derivatives of lipopolysaccharide and peptidoglycan of the bacterial partner interact with epithelial cells to direct host development during the establishment of the symbiosis. The proposed research seeks to define the molecular underpinnings of this communication. The principal aims are: 1. To characterize when and where host pattern-recognition receptors for bacterial products are expressed during the onset of the symbiosis - Sensitive techniques to localize specific mRNAs and proteins in animal tissues will be used to ask: How does the expression of host receptors mediate or restrict the interaction of the partners to promote a beneficial association? 2. To determine the influence on symbiosis of defects in V. fischeri's capacity to produce bioactive ligands - Using bacterial genetic techniques developed for V. fischeri, under- and overproducing mutants will be created to ask: How does a normal level of bacterial ligand synthesis promote beneficial interactions? 3. To identify host responses to bacterial ligands using host genomic analyses - Microarray studies of genes of the host tissues expressed in early development will address: What gene-expression patterns of the host underlie the interactions with a beneficial partner? Relevance: Host-receptor/bacterial-ligand interactions have been conserved throughout animal evolution. The binary squid-vibrio symbiosis offers a relatively simple model in which to identify and define the basic, shared mechanisms by which essential bacteria colonize human and other animal epithelia. It provides a powerful complement to the similar, yet more complex, germ-free vertebrate models of beneficial associations.

National Institute of Health (NIH)
National Institute of Allergy and Infectious Diseases (NIAID)
Research Project (R01)
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Host Interactions with Bacterial Pathogens Study Section (HIBP)
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Hall, Robert H
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University of Wisconsin Madison
Schools of Medicine
United States
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Kremer, Natacha; Koch, Eric J; El Filali, Adil et al. (2018) Persistent Interactions with Bacterial Symbionts Direct Mature-Host Cell Morphology and Gene Expression in the Squid-Vibrio Symbiosis. mSystems 3:
Koehler, Sabrina; Gaedeke, Roxane; Thompson, Cecilia et al. (2018) The model squid-vibrio symbiosis provides a window into the impact of strain- and species-level differences during the initial stages of symbiont engagement. Environ Microbiol :
Peyer, Suzanne M; Kremer, Natacha; McFall-Ngai, Margaret J (2018) Involvement of a host Cathepsin L in symbiont-induced cell death. Microbiologyopen 7:e00632
Bongrand, Clotilde; Ruby, Edward G (2018) Achieving a multi-strain symbiosis: strain behavior and infection dynamics. ISME J :
Peyer, Suzanne M; Heath-Heckman, Elizabeth A C; McFall-Ngai, Margaret J (2017) Characterization of the cell polarity gene crumbs during the early development and maintenance of the squid-vibrio light organ symbiosis. Dev Genes Evol 227:375-387
Nawroth, Janna C; Guo, Hanliang; Koch, Eric et al. (2017) Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome. Proc Natl Acad Sci U S A 114:9510-9516
Chen, Fangmin; Krasity, Benjamin C; Peyer, Suzanne M et al. (2017) Bactericidal Permeability-Increasing Proteins Shape Host-Microbe Interactions. MBio 8:
Pan, Shu; Nikolakakis, Kiel; Adamczyk, Paul A et al. (2017) Model-enabled gene search (MEGS) allows fast and direct discovery of enzymatic and transport gene functions in the marine bacterium Vibrio fischeri. J Biol Chem 292:10250-10261
Aschtgen, Marie-Stephanie; Wetzel, Keith; Goldman, William et al. (2016) Vibrio fischeri-derived outer membrane vesicles trigger host development. Cell Microbiol 18:488-99
Aschtgen, Marie-Stephanie; Lynch, Jonathan B; Koch, Eric et al. (2016) Rotation of Vibrio fischeri Flagella Produces Outer Membrane Vesicles That Induce Host Development. J Bacteriol 198:2156-65

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