The Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>

ABSTRACT Previous work from our laboratory showed that the Gram-negative aquatic pathogen Vibrio cholerae can take up a much wider repertoire of fatty acids than other Gram-negative organisms. The current work elaborated on the ability of V. cholerae to exploit an even more diverse pool of lipid nut...

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Autores principales:	Aaron C. Pride, Carmen M. Herrera, Ziqiang Guan, David K. Giles, M. Stephen Trent
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/80c2c7c66617404692aa151371ab7db2
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spelling	oai:doaj.org-article:80c2c7c66617404692aa151371ab7db22021-11-15T15:40:06ZThe Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>10.1128/mBio.00305-132150-7511https://doaj.org/article/80c2c7c66617404692aa151371ab7db22013-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00305-13https://doaj.org/toc/2150-7511ABSTRACT Previous work from our laboratory showed that the Gram-negative aquatic pathogen Vibrio cholerae can take up a much wider repertoire of fatty acids than other Gram-negative organisms. The current work elaborated on the ability of V. cholerae to exploit an even more diverse pool of lipid nutrients from its environment. We have demonstrated that the bacterium can use lysophosphatidylcholine as a metabolite for growth. Using a combination of thin-layer chromatography and mass spectrometry, we also showed that lysophosphatidylcholine-derived fatty acid moieties can be used for remodeling the V. cholerae membrane architecture. Furthermore, we have identified a lysophospholipase, VolA (Vibrio outer membrane lysophospholipase A), required for these activities. The enzyme is well conserved in Vibrio species, is coexpressed with the outer membrane fatty acid transporter FadL, is one of very few surface-exposed lipoprotein enzymes to be identified in Gram-negative bacteria and the first instance of a surface lipoprotein phospholipase. We propose a model whereby the bacterium efficiently couples the liberation of fatty acid from lysophosphatidylcholine to its subsequent metabolic uptake. An expanded ability to scavenge diverse environmental lipids at the bacterial surface increases overall bacterial fitness and promotes homeoviscous adaptation through membrane remodeling. IMPORTANCE Our understanding of how bacteria utilize environmental lipid sources has been limited to lipids such as fatty acids and cholesterol. This narrow scope may be attributed to both the intricate nature of lipid uptake mechanisms and the diversity of lipid substrates encountered within an ecological niche. By examining the ability of the pathogen Vibrio cholerae to utilize exogenous lipids, we uncovered a surface-exposed lipoprotein (VolA) that is required for processing the prevalent host lipid lysophosphatidylcholine. VolA functions as a lipase liberating a fatty acid from exogenous lysophospholipids. The freed fatty acid is then transported into the cell, serving as a carbon source, or shunted into phospholipid synthesis for membrane assembly. A limited number of surface-exposed lipoproteins have been found in Gram-negative organisms, and few have enzymatic function. This work highlights the ability of bacteria to exploit exogenous lipids for both maintenance of the membrane and carbon source acquisition.Aaron C. PrideCarmen M. HerreraZiqiang GuanDavid K. GilesM. Stephen TrentAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 3 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Aaron C. Pride Carmen M. Herrera Ziqiang Guan David K. Giles M. Stephen Trent The Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>
description	ABSTRACT Previous work from our laboratory showed that the Gram-negative aquatic pathogen Vibrio cholerae can take up a much wider repertoire of fatty acids than other Gram-negative organisms. The current work elaborated on the ability of V. cholerae to exploit an even more diverse pool of lipid nutrients from its environment. We have demonstrated that the bacterium can use lysophosphatidylcholine as a metabolite for growth. Using a combination of thin-layer chromatography and mass spectrometry, we also showed that lysophosphatidylcholine-derived fatty acid moieties can be used for remodeling the V. cholerae membrane architecture. Furthermore, we have identified a lysophospholipase, VolA (Vibrio outer membrane lysophospholipase A), required for these activities. The enzyme is well conserved in Vibrio species, is coexpressed with the outer membrane fatty acid transporter FadL, is one of very few surface-exposed lipoprotein enzymes to be identified in Gram-negative bacteria and the first instance of a surface lipoprotein phospholipase. We propose a model whereby the bacterium efficiently couples the liberation of fatty acid from lysophosphatidylcholine to its subsequent metabolic uptake. An expanded ability to scavenge diverse environmental lipids at the bacterial surface increases overall bacterial fitness and promotes homeoviscous adaptation through membrane remodeling. IMPORTANCE Our understanding of how bacteria utilize environmental lipid sources has been limited to lipids such as fatty acids and cholesterol. This narrow scope may be attributed to both the intricate nature of lipid uptake mechanisms and the diversity of lipid substrates encountered within an ecological niche. By examining the ability of the pathogen Vibrio cholerae to utilize exogenous lipids, we uncovered a surface-exposed lipoprotein (VolA) that is required for processing the prevalent host lipid lysophosphatidylcholine. VolA functions as a lipase liberating a fatty acid from exogenous lysophospholipids. The freed fatty acid is then transported into the cell, serving as a carbon source, or shunted into phospholipid synthesis for membrane assembly. A limited number of surface-exposed lipoproteins have been found in Gram-negative organisms, and few have enzymatic function. This work highlights the ability of bacteria to exploit exogenous lipids for both maintenance of the membrane and carbon source acquisition.
format	article
author	Aaron C. Pride Carmen M. Herrera Ziqiang Guan David K. Giles M. Stephen Trent
author_facet	Aaron C. Pride Carmen M. Herrera Ziqiang Guan David K. Giles M. Stephen Trent
author_sort	Aaron C. Pride
title	The Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_short	The Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_full	The Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_fullStr	The Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_full_unstemmed	The Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_sort	outer surface lipoprotein vola mediates utilization of exogenous lipids by <named-content content-type="genus-species">vibrio cholerae</named-content>
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/80c2c7c66617404692aa151371ab7db2
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The Outer Surface Lipoprotein VolA Mediates Utilization of Exogenous Lipids by <named-content content-type="genus-species">Vibrio cholerae</named-content>

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