Two Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>

ABSTRACT Myxococcus xanthus produces several extracellular signals that guide fruiting body morphogenesis and spore differentiation. Mutants defective in producing a signal may be rescued by codevelopment with wild-type cells or cell fractions containing the signal. In this paper, we identify two mo...

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Autores principales:	Swapna Bhat, Tilman Ahrendt, Christina Dauth, Helge B. Bode, Lawrence J. Shimkets
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bffe0e747ecd4931acc92797d2cd8bb3
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spelling	oai:doaj.org-article:bffe0e747ecd4931acc92797d2cd8bb32021-11-15T15:45:11ZTwo Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>10.1128/mBio.00939-132150-7511https://doaj.org/article/bffe0e747ecd4931acc92797d2cd8bb32014-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00939-13https://doaj.org/toc/2150-7511ABSTRACT Myxococcus xanthus produces several extracellular signals that guide fruiting body morphogenesis and spore differentiation. Mutants defective in producing a signal may be rescued by codevelopment with wild-type cells or cell fractions containing the signal. In this paper, we identify two molecules that rescue development of the E signal-deficient mutant LS1191 at physiological concentrations, iso15:0 branched-chain fatty acid (FA) and 1-iso15:0-alkyl-2,3-di-iso15:0-acyl glycerol (TG1), a development-specific monoalkyl-diacylglycerol. The physiological concentrations of the bioactive lipids were determined by mass spectrometry from developing wild-type cells using chemically synthesized standards. Synthetic TG1 restored fruiting body morphogenesis and sporulation and activated the expression of the developmentally regulated gene with locus tag MXAN_2146 at physiological concentrations, unlike its nearly identical tri-iso15:0 triacylglycerol (TAG) counterpart, which has an ester linkage instead of an ether linkage. iso15:0 FA restored development at physiological concentrations, unlike palmitic acid, a straight-chain fatty acid. The addition of either lipid stimulates cell shortening, with an 87% decline in membrane surface area, concomitantly with the production of lipid bodies at each cell pole and in the center of the cell. We suggest that cells produce triacylglycerol from membrane phospholipids. Bioactive lipids may be released by programmed cell death (PCD), which claims up to 80% of developing cells, since cells undergoing PCD produce lipid bodies before lysing. IMPORTANCE Like mammalian adipose tissue, many of the M. xanthus lipid body lipids are triacylglycerols (TAGs), containing ester-linked fatty acids. In both systems, ester-linked fatty acids are retrieved from TAGs with lipases and consumed by the fatty acid degradation cycle. Both mammals and M. xanthus also produce lipids containing ether-linked fatty alcohols with alkyl or vinyl linkages, such as plasmalogens. Alkyl and vinyl linkages are not hydrolyzed by lipases, and no clear role has emerged for lipids bearing them. For example, plasmalogen deficiency in mice has detrimental consequences to spermatocyte development, myelination, axonal survival, eye development, and long-term survival, though the precise reasons remain elusive. Lipids containing alkyl- and vinyl-linked fatty alcohols are development-specific products in M. xanthus. Here, we show that one of them rescues the development of E signal-producing mutants at physiological concentrations.Swapna BhatTilman AhrendtChristina DauthHelge B. BodeLawrence J. ShimketsAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 1 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Swapna Bhat Tilman Ahrendt Christina Dauth Helge B. Bode Lawrence J. Shimkets Two Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>
description	ABSTRACT Myxococcus xanthus produces several extracellular signals that guide fruiting body morphogenesis and spore differentiation. Mutants defective in producing a signal may be rescued by codevelopment with wild-type cells or cell fractions containing the signal. In this paper, we identify two molecules that rescue development of the E signal-deficient mutant LS1191 at physiological concentrations, iso15:0 branched-chain fatty acid (FA) and 1-iso15:0-alkyl-2,3-di-iso15:0-acyl glycerol (TG1), a development-specific monoalkyl-diacylglycerol. The physiological concentrations of the bioactive lipids were determined by mass spectrometry from developing wild-type cells using chemically synthesized standards. Synthetic TG1 restored fruiting body morphogenesis and sporulation and activated the expression of the developmentally regulated gene with locus tag MXAN_2146 at physiological concentrations, unlike its nearly identical tri-iso15:0 triacylglycerol (TAG) counterpart, which has an ester linkage instead of an ether linkage. iso15:0 FA restored development at physiological concentrations, unlike palmitic acid, a straight-chain fatty acid. The addition of either lipid stimulates cell shortening, with an 87% decline in membrane surface area, concomitantly with the production of lipid bodies at each cell pole and in the center of the cell. We suggest that cells produce triacylglycerol from membrane phospholipids. Bioactive lipids may be released by programmed cell death (PCD), which claims up to 80% of developing cells, since cells undergoing PCD produce lipid bodies before lysing. IMPORTANCE Like mammalian adipose tissue, many of the M. xanthus lipid body lipids are triacylglycerols (TAGs), containing ester-linked fatty acids. In both systems, ester-linked fatty acids are retrieved from TAGs with lipases and consumed by the fatty acid degradation cycle. Both mammals and M. xanthus also produce lipids containing ether-linked fatty alcohols with alkyl or vinyl linkages, such as plasmalogens. Alkyl and vinyl linkages are not hydrolyzed by lipases, and no clear role has emerged for lipids bearing them. For example, plasmalogen deficiency in mice has detrimental consequences to spermatocyte development, myelination, axonal survival, eye development, and long-term survival, though the precise reasons remain elusive. Lipids containing alkyl- and vinyl-linked fatty alcohols are development-specific products in M. xanthus. Here, we show that one of them rescues the development of E signal-producing mutants at physiological concentrations.
format	article
author	Swapna Bhat Tilman Ahrendt Christina Dauth Helge B. Bode Lawrence J. Shimkets
author_facet	Swapna Bhat Tilman Ahrendt Christina Dauth Helge B. Bode Lawrence J. Shimkets
author_sort	Swapna Bhat
title	Two Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>
title_short	Two Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>
title_full	Two Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>
title_fullStr	Two Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>
title_full_unstemmed	Two Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>
title_sort	two lipid signals guide fruiting body development of <named-content content-type="genus-species">myxococcus xanthus</named-content>
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/bffe0e747ecd4931acc92797d2cd8bb3
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Two Lipid Signals Guide Fruiting Body Development of <named-content content-type="genus-species">Myxococcus xanthus</named-content>

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