A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism

ABSTRACT Most animal-microbe mutualistic associations are characterized by nutrient exchange between the partners. When the host provides the nutrients, it can gain the capacity to shape its microbial community, control the stability of the interaction, and promote its health and fitness. Using the...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Min Pan, Julia A. Schwartzman, Anne K. Dunn, Zuhong Lu, Edward G. Ruby
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/73b638b1704d4401b43464af3c7af252
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:73b638b1704d4401b43464af3c7af252
record_format	dspace
spelling	oai:doaj.org-article:73b638b1704d4401b43464af3c7af2522021-11-15T15:41:26ZA Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism10.1128/mBio.00811-152150-7511https://doaj.org/article/73b638b1704d4401b43464af3c7af2522015-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00811-15https://doaj.org/toc/2150-7511ABSTRACT Most animal-microbe mutualistic associations are characterized by nutrient exchange between the partners. When the host provides the nutrients, it can gain the capacity to shape its microbial community, control the stability of the interaction, and promote its health and fitness. Using the bioluminescent squid-vibrio model, we demonstrate how a single host-derived glycan, chitin, regulates the metabolism of Vibrio fischeri at key points in the development and maintenance of the symbiosis. We first characterized the pathways for catabolism of chitin sugars by V. fischeri, demonstrating that the Ccr-dependent phosphoenolpyruvate-pyruvate phosphotransferase system (PTS) prioritizes transport of these sugars in V. fischeri by blocking the uptake of non-PTS carbohydrates, such as glycerol. Next, we found that PTS transport of chitin sugars into the bacterium shifted acetate homeostasis toward a net excretion of acetate and was sufficient to override an activation of the acetate switch by AinS-dependent quorum sensing. Finally, we showed that catabolism of chitin sugars decreases the rate of cell-specific oxygen consumption. Collectively, these three metabolic functions define a physiological shift that favors fermentative growth on chitin sugars and may support optimal symbiont luminescence, the functional basis of the squid-vibrio mutualism. IMPORTANCE Host-derived glycans have recently emerged as a link between symbiont nutrition and innate immune function. Unfortunately, the locations at which microbes typically access host-derived glycans are inaccessible to experimentation and imaging, and they take place in the context of diverse microbe-microbe interactions, creating a complex symbiotic ecology. Here we describe the metabolic state of a single microbial symbiont in a natural association with its coevolved host and, by doing so, infer key points at which a host-controlled tissue environment might regulate the physiological state of its symbionts. We show that the presence of a regulatory glycan is sufficient to shift symbiont carbohydrate catabolism, acetate homeostasis, and oxygen consumption.Min PanJulia A. SchwartzmanAnne K. DunnZuhong LuEdward G. RubyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 4 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Min Pan Julia A. Schwartzman Anne K. Dunn Zuhong Lu Edward G. Ruby A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism
description	ABSTRACT Most animal-microbe mutualistic associations are characterized by nutrient exchange between the partners. When the host provides the nutrients, it can gain the capacity to shape its microbial community, control the stability of the interaction, and promote its health and fitness. Using the bioluminescent squid-vibrio model, we demonstrate how a single host-derived glycan, chitin, regulates the metabolism of Vibrio fischeri at key points in the development and maintenance of the symbiosis. We first characterized the pathways for catabolism of chitin sugars by V. fischeri, demonstrating that the Ccr-dependent phosphoenolpyruvate-pyruvate phosphotransferase system (PTS) prioritizes transport of these sugars in V. fischeri by blocking the uptake of non-PTS carbohydrates, such as glycerol. Next, we found that PTS transport of chitin sugars into the bacterium shifted acetate homeostasis toward a net excretion of acetate and was sufficient to override an activation of the acetate switch by AinS-dependent quorum sensing. Finally, we showed that catabolism of chitin sugars decreases the rate of cell-specific oxygen consumption. Collectively, these three metabolic functions define a physiological shift that favors fermentative growth on chitin sugars and may support optimal symbiont luminescence, the functional basis of the squid-vibrio mutualism. IMPORTANCE Host-derived glycans have recently emerged as a link between symbiont nutrition and innate immune function. Unfortunately, the locations at which microbes typically access host-derived glycans are inaccessible to experimentation and imaging, and they take place in the context of diverse microbe-microbe interactions, creating a complex symbiotic ecology. Here we describe the metabolic state of a single microbial symbiont in a natural association with its coevolved host and, by doing so, infer key points at which a host-controlled tissue environment might regulate the physiological state of its symbionts. We show that the presence of a regulatory glycan is sufficient to shift symbiont carbohydrate catabolism, acetate homeostasis, and oxygen consumption.
format	article
author	Min Pan Julia A. Schwartzman Anne K. Dunn Zuhong Lu Edward G. Ruby
author_facet	Min Pan Julia A. Schwartzman Anne K. Dunn Zuhong Lu Edward G. Ruby
author_sort	Min Pan
title	A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism
title_short	A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism
title_full	A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism
title_fullStr	A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism
title_full_unstemmed	A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism
title_sort	single host-derived glycan impacts key regulatory nodes of symbiont metabolism in a coevolved mutualism
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/73b638b1704d4401b43464af3c7af252
work_keys_str_mv	AT minpan asinglehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT juliaaschwartzman asinglehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT annekdunn asinglehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT zuhonglu asinglehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT edwardgruby asinglehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT minpan singlehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT juliaaschwartzman singlehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT annekdunn singlehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT zuhonglu singlehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism AT edwardgruby singlehostderivedglycanimpactskeyregulatorynodesofsymbiontmetabolisminacoevolvedmutualism
_version_	1718427711130566656

A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism

Ejemplares similares