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Fatty acids from membrane lipids become incorporated into lipid bodies during Myxococcus xanthus differentiation.

Bhat S, Boynton TO, Pham D, Shimkets LJ - PLoS ONE (2014)

Bottom Line: Third, peripheral rods, developing cells that do not produce lipid bodies, fail to shorten.The lipid body regulon involves many developmental genes that are not specifically involved in fatty acid synthesis or degradation.MazF RNA interferase and its target, enhancer-binding protein Nla6, appear to negatively regulate cell shortening and TAG accumulation whereas most cell-cell signals activate these processes.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology, University of Georgia, Athens, Georgia, United States of America.

ABSTRACT
Myxococcus xanthus responds to amino acid limitation by producing fruiting bodies containing dormant spores. During development, cells produce triacylglycerides in lipid bodies that become consumed during spore maturation. As the cells are starved to induce development, the production of triglycerides represents a counterintuitive metabolic switch. In this paper, lipid bodies were quantified in wild-type strain DK1622 and 33 developmental mutants at the cellular level by measuring the cross sectional area of the cell stained with the lipophilic dye Nile red. We provide five lines of evidence that triacylglycerides are derived from membrane phospholipids as cells shorten in length and then differentiate into myxospores. First, in wild type cells, lipid bodies appear early in development and their size increases concurrent with an 87% decline in membrane surface area. Second, developmental mutants blocked at different stages of shortening and differentiation accumulated lipid bodies proportionate with their cell length with a Pearson's correlation coefficient of 0.76. Third, peripheral rods, developing cells that do not produce lipid bodies, fail to shorten. Fourth, genes for fatty acid synthesis are down-regulated while genes for fatty acid degradation are up regulated. Finally, direct movement of fatty acids from membrane lipids in growing cells to lipid bodies in developing cells was observed by pulse labeling cells with palmitate. Recycling of lipids released by Programmed Cell Death appears not to be necessary for lipid body production as a fadL mutant was defective in fatty acid uptake but proficient in lipid body production. The lipid body regulon involves many developmental genes that are not specifically involved in fatty acid synthesis or degradation. MazF RNA interferase and its target, enhancer-binding protein Nla6, appear to negatively regulate cell shortening and TAG accumulation whereas most cell-cell signals activate these processes.

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M. xanthus fatty acid metabolic pathways were analyzed at the transcriptional level using available microarray data from developing cells [13].The pathway information and gene annotations were obtained from the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database. Genes that are down-regulated (≥1.5 fold), up-regulated (≥1.5 fold) or unchanged during development are shown in green, red, and black, respectively. Blue denotes genes that were not on the microarray. A dashed arrow between two compound names implies that the two names represent the same compound in different stages of polymerization or depolymerization.
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pone-0099622-g002: M. xanthus fatty acid metabolic pathways were analyzed at the transcriptional level using available microarray data from developing cells [13].The pathway information and gene annotations were obtained from the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database. Genes that are down-regulated (≥1.5 fold), up-regulated (≥1.5 fold) or unchanged during development are shown in green, red, and black, respectively. Blue denotes genes that were not on the microarray. A dashed arrow between two compound names implies that the two names represent the same compound in different stages of polymerization or depolymerization.

Mentions: To determine whether the internal carbon reservoir for lipid body production involves existing fatty acids or instead utilizes de novo fatty acid synthesis, we examined the expression of fatty acid biosynthetic genes during development. If TAGs are derived from membrane phospholipids, one might expect a decline in transcription of fatty acid biosynthesis genes. Gene expression was quantified using published microarray data from developing wild type cells (Accession number GSE9477) [13]. The M. xanthus fatty acid pathways assigned by the Kyoto Encyclopedia of Genes and Genomes (KEGG) Pathways database are shown in figure 2[14], [15]. Proteins proposed to mediate each reaction are shown next to the arrows as both MXAN numbers and, where known, 4-letter protein names.


Fatty acids from membrane lipids become incorporated into lipid bodies during Myxococcus xanthus differentiation.

Bhat S, Boynton TO, Pham D, Shimkets LJ - PLoS ONE (2014)

M. xanthus fatty acid metabolic pathways were analyzed at the transcriptional level using available microarray data from developing cells [13].The pathway information and gene annotations were obtained from the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database. Genes that are down-regulated (≥1.5 fold), up-regulated (≥1.5 fold) or unchanged during development are shown in green, red, and black, respectively. Blue denotes genes that were not on the microarray. A dashed arrow between two compound names implies that the two names represent the same compound in different stages of polymerization or depolymerization.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4048283&req=5

pone-0099622-g002: M. xanthus fatty acid metabolic pathways were analyzed at the transcriptional level using available microarray data from developing cells [13].The pathway information and gene annotations were obtained from the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database. Genes that are down-regulated (≥1.5 fold), up-regulated (≥1.5 fold) or unchanged during development are shown in green, red, and black, respectively. Blue denotes genes that were not on the microarray. A dashed arrow between two compound names implies that the two names represent the same compound in different stages of polymerization or depolymerization.
Mentions: To determine whether the internal carbon reservoir for lipid body production involves existing fatty acids or instead utilizes de novo fatty acid synthesis, we examined the expression of fatty acid biosynthetic genes during development. If TAGs are derived from membrane phospholipids, one might expect a decline in transcription of fatty acid biosynthesis genes. Gene expression was quantified using published microarray data from developing wild type cells (Accession number GSE9477) [13]. The M. xanthus fatty acid pathways assigned by the Kyoto Encyclopedia of Genes and Genomes (KEGG) Pathways database are shown in figure 2[14], [15]. Proteins proposed to mediate each reaction are shown next to the arrows as both MXAN numbers and, where known, 4-letter protein names.

Bottom Line: Third, peripheral rods, developing cells that do not produce lipid bodies, fail to shorten.The lipid body regulon involves many developmental genes that are not specifically involved in fatty acid synthesis or degradation.MazF RNA interferase and its target, enhancer-binding protein Nla6, appear to negatively regulate cell shortening and TAG accumulation whereas most cell-cell signals activate these processes.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology, University of Georgia, Athens, Georgia, United States of America.

ABSTRACT
Myxococcus xanthus responds to amino acid limitation by producing fruiting bodies containing dormant spores. During development, cells produce triacylglycerides in lipid bodies that become consumed during spore maturation. As the cells are starved to induce development, the production of triglycerides represents a counterintuitive metabolic switch. In this paper, lipid bodies were quantified in wild-type strain DK1622 and 33 developmental mutants at the cellular level by measuring the cross sectional area of the cell stained with the lipophilic dye Nile red. We provide five lines of evidence that triacylglycerides are derived from membrane phospholipids as cells shorten in length and then differentiate into myxospores. First, in wild type cells, lipid bodies appear early in development and their size increases concurrent with an 87% decline in membrane surface area. Second, developmental mutants blocked at different stages of shortening and differentiation accumulated lipid bodies proportionate with their cell length with a Pearson's correlation coefficient of 0.76. Third, peripheral rods, developing cells that do not produce lipid bodies, fail to shorten. Fourth, genes for fatty acid synthesis are down-regulated while genes for fatty acid degradation are up regulated. Finally, direct movement of fatty acids from membrane lipids in growing cells to lipid bodies in developing cells was observed by pulse labeling cells with palmitate. Recycling of lipids released by Programmed Cell Death appears not to be necessary for lipid body production as a fadL mutant was defective in fatty acid uptake but proficient in lipid body production. The lipid body regulon involves many developmental genes that are not specifically involved in fatty acid synthesis or degradation. MazF RNA interferase and its target, enhancer-binding protein Nla6, appear to negatively regulate cell shortening and TAG accumulation whereas most cell-cell signals activate these processes.

Show MeSH
Related in: MedlinePlus