An acidic microenvironment produced by the V-type ATPase of Euprymna scolopes promotes specificity during Vibrio fischeri recruitment.

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Autori principali: Hargadon, Alexis C, Viliunas, Joani W, Koehler, Sabrina, Thies, Angus B, Chen, Grischa Y, Ladinsky, Mark S, Kuwabara, Jill, Avila-Magana, Viridiana, Ruby, Edward G, Tresguerres, Martin, McFall-Ngai, Margaret J
Natura: Artículo científico
Lingua:en
Pubblicazione: Communications biology 2024
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author Hargadon, Alexis C
Viliunas, Joani W
Koehler, Sabrina
Thies, Angus B
Chen, Grischa Y
Ladinsky, Mark S
Kuwabara, Jill
Avila-Magana, Viridiana
Ruby, Edward G
Tresguerres, Martin
McFall-Ngai, Margaret J
author_facet Hargadon, Alexis C
Viliunas, Joani W
Koehler, Sabrina
Thies, Angus B
Chen, Grischa Y
Ladinsky, Mark S
Kuwabara, Jill
Avila-Magana, Viridiana
Ruby, Edward G
Tresguerres, Martin
McFall-Ngai, Margaret J
Hargadon, Alexis C
Viliunas, Joani W
Koehler, Sabrina
Thies, Angus B
Chen, Grischa Y
Ladinsky, Mark S
Kuwabara, Jill
Avila-Magana, Viridiana
Ruby, Edward G
Tresguerres, Martin
McFall-Ngai, Margaret J
collection PubMed - marine biology
contents An acidic microenvironment produced by the V-type ATPase of Euprymna scolopes promotes specificity during Vibrio fischeri recruitment. Hargadon, Alexis C Viliunas, Joani W Koehler, Sabrina Thies, Angus B Chen, Grischa Y Ladinsky, Mark S Kuwabara, Jill Avila-Magana, Viridiana Ruby, Edward G Tresguerres, Martin McFall-Ngai, Margaret J Aliivibrio fischeri Animals Decapodiformes Symbiosis Hydrogen-Ion Concentration Vacuolar Proton-Translocating ATPases Animals often acquire their microbial symbionts from the environment, but the mechanisms underlying how specificity of the association is achieved are poorly understood. We demonstrate that the conserved proton pump, V-type ATPase (VHA), plays a key role in the establishment of the model light-organ symbiosis between the squid Euprymna scolopes and its bacterial partner, Vibrio fischeri. Recruitment of V. fischeri from the surrounding seawater is mediated by juvenile-specific ciliated fields on the organ's surface. These epithelia produce acidic mucus containing antimicrobials with low-pH optima, creating a chemical environment fostering specific recruitment of V. fischeri. We provide evidence that this critical acidic landscape is created by activity of VHA. VHA inhibition abolished epithelial-cell acidity, resulting in increased mucus pH and inefficient symbiont colonization. Thus, VHA provides a mechanistic link between host modulation of microenvironmental acidity, immune function, and selection of microbial symbionts, a strategy for specificity that may govern other symbioses.
format Artículo científico
id pubmed_39695176
institution PubMed
language en
publishDate 2024
publisher Communications biology
record_format pubmed
spellingShingle An acidic microenvironment produced by the V-type ATPase of Euprymna scolopes promotes specificity during Vibrio fischeri recruitment.
Hargadon, Alexis C
Viliunas, Joani W
Koehler, Sabrina
Thies, Angus B
Chen, Grischa Y
Ladinsky, Mark S
Kuwabara, Jill
Avila-Magana, Viridiana
Ruby, Edward G
Tresguerres, Martin
McFall-Ngai, Margaret J
Aliivibrio fischeri
Animals
Decapodiformes
Symbiosis
Hydrogen-Ion Concentration
Vacuolar Proton-Translocating ATPases
An acidic microenvironment produced by the V-type ATPase of Euprymna scolopes promotes specificity during Vibrio fischeri recruitment. Hargadon, Alexis C Viliunas, Joani W Koehler, Sabrina Thies, Angus B Chen, Grischa Y Ladinsky, Mark S Kuwabara, Jill Avila-Magana, Viridiana Ruby, Edward G Tresguerres, Martin McFall-Ngai, Margaret J Aliivibrio fischeri Animals Decapodiformes Symbiosis Hydrogen-Ion Concentration Vacuolar Proton-Translocating ATPases Animals often acquire their microbial symbionts from the environment, but the mechanisms underlying how specificity of the association is achieved are poorly understood. We demonstrate that the conserved proton pump, V-type ATPase (VHA), plays a key role in the establishment of the model light-organ symbiosis between the squid Euprymna scolopes and its bacterial partner, Vibrio fischeri. Recruitment of V. fischeri from the surrounding seawater is mediated by juvenile-specific ciliated fields on the organ's surface. These epithelia produce acidic mucus containing antimicrobials with low-pH optima, creating a chemical environment fostering specific recruitment of V. fischeri. We provide evidence that this critical acidic landscape is created by activity of VHA. VHA inhibition abolished epithelial-cell acidity, resulting in increased mucus pH and inefficient symbiont colonization. Thus, VHA provides a mechanistic link between host modulation of microenvironmental acidity, immune function, and selection of microbial symbionts, a strategy for specificity that may govern other symbioses.
title An acidic microenvironment produced by the V-type ATPase of Euprymna scolopes promotes specificity during Vibrio fischeri recruitment.
topic Aliivibrio fischeri
Animals
Decapodiformes
Symbiosis
Hydrogen-Ion Concentration
Vacuolar Proton-Translocating ATPases
url https://pubmed.ncbi.nlm.nih.gov/39695176/