The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>

ABSTRACT In Ralstonia solanacearum, a devastating phytopathogen whose metabolism is poorly understood, we observed that the Entner-Doudoroff (ED) pathway and nonoxidative pentose phosphate pathway (non-OxPPP) bypass glycolysis and OxPPP under glucose oxidation. Evidence derived from 13C stable isoto...

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Autores principales:	Poonam Jyoti, Manu Shree, Chandrakant Joshi, Tulika Prakash, Suvendra Kumar Ray, Siddhartha Sankar Satapathy, Shyam Kumar Masakapalli
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Ralstonia solanacearum ED pathway 13C tracers central metabolism mass isotopomers GC-MS Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b0dc11a343e244509cf76d987878763c
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spelling	oai:doaj.org-article:b0dc11a343e244509cf76d987878763c2021-12-02T19:46:19ZThe Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>10.1128/mSystems.00091-202379-5077https://doaj.org/article/b0dc11a343e244509cf76d987878763c2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00091-20https://doaj.org/toc/2379-5077ABSTRACT In Ralstonia solanacearum, a devastating phytopathogen whose metabolism is poorly understood, we observed that the Entner-Doudoroff (ED) pathway and nonoxidative pentose phosphate pathway (non-OxPPP) bypass glycolysis and OxPPP under glucose oxidation. Evidence derived from 13C stable isotope feeding and genome annotation-based comparative metabolic network analysis supported the observations. Comparative metabolic network analysis derived from the currently available 53 annotated R. solanacearum strains, including a recently reported strain (F1C1), representing the four phylotypes, confirmed the lack of key genes coding for phosphofructokinase (pfk-1) and phosphogluconate dehydrogenase (gnd) enzymes that are relevant for glycolysis and OxPPP, respectively. R. solanacearum F1C1 cells fed with [13C]glucose (99% [1-13C]glucose or 99% [1,2-13C]glucose or 40% [13C6]glucose) followed by gas chromatography-mass spectrometry (GC-MS)-based labeling analysis of fragments from amino acids, glycerol, and ribose provided clear evidence that rather than glycolysis and the OxPPP, the ED pathway and non-OxPPP are the main routes sustaining metabolism in R. solanacearum. The 13C incorporation in the mass ions of alanine (m/z 260 and m/z 232), valine (m/z 288 and m/z 260), glycine (m/z 218), serine (m/z 390 and m/z 362), histidine (m/z 440 and m/z 412), tyrosine (m/z 466 and m/z 438), phenylalanine (m/z 336 and m/z 308), glycerol (m/z 377), and ribose (m/z 160) mapped the pathways supporting the observations. The outcomes help better define the central carbon metabolic network of R. solanacearum that can be integrated with 13C metabolic flux analysis as well as flux balance analysis studies for defining the metabolic phenotypes. IMPORTANCE Understanding the metabolic versatility of Ralstonia solanacearum is important, as it regulates the trade-off between virulence and metabolism (1, 2) in a wide range of plant hosts. Due to a lack of clear evidence until this work, several published research papers reported on the potential roles of glycolysis and the oxidative pentose phosphate pathway (OxPPP) in R. solanacearum (3, 4). This work provided evidence from 13C stable isotope feeding and genome annotation-based comparative metabolic network analysis that the Entner-Doudoroff pathway and non-OxPPP bypass glycolysis and OxPPP during the oxidation of glucose, a component of the host xylem pool that serves as a potential carbon source (5). The outcomes help better define the central carbon metabolic network of R. solanacearum that can be integrated with 13C metabolic flux analysis as well as flux balance analysis studies for defining the metabolic phenotypes. The study highlights the need to critically examine phytopathogens whose metabolism is poorly understood.Poonam JyotiManu ShreeChandrakant JoshiTulika PrakashSuvendra Kumar RaySiddhartha Sankar SatapathyShyam Kumar MasakapalliAmerican Society for MicrobiologyarticleRalstonia solanacearumED pathway13C tracerscentral metabolismmass isotopomersGC-MSMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Ralstonia solanacearum ED pathway 13C tracers central metabolism mass isotopomers GC-MS Microbiology QR1-502
spellingShingle	Ralstonia solanacearum ED pathway 13C tracers central metabolism mass isotopomers GC-MS Microbiology QR1-502 Poonam Jyoti Manu Shree Chandrakant Joshi Tulika Prakash Suvendra Kumar Ray Siddhartha Sankar Satapathy Shyam Kumar Masakapalli The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>
description	ABSTRACT In Ralstonia solanacearum, a devastating phytopathogen whose metabolism is poorly understood, we observed that the Entner-Doudoroff (ED) pathway and nonoxidative pentose phosphate pathway (non-OxPPP) bypass glycolysis and OxPPP under glucose oxidation. Evidence derived from 13C stable isotope feeding and genome annotation-based comparative metabolic network analysis supported the observations. Comparative metabolic network analysis derived from the currently available 53 annotated R. solanacearum strains, including a recently reported strain (F1C1), representing the four phylotypes, confirmed the lack of key genes coding for phosphofructokinase (pfk-1) and phosphogluconate dehydrogenase (gnd) enzymes that are relevant for glycolysis and OxPPP, respectively. R. solanacearum F1C1 cells fed with [13C]glucose (99% [1-13C]glucose or 99% [1,2-13C]glucose or 40% [13C6]glucose) followed by gas chromatography-mass spectrometry (GC-MS)-based labeling analysis of fragments from amino acids, glycerol, and ribose provided clear evidence that rather than glycolysis and the OxPPP, the ED pathway and non-OxPPP are the main routes sustaining metabolism in R. solanacearum. The 13C incorporation in the mass ions of alanine (m/z 260 and m/z 232), valine (m/z 288 and m/z 260), glycine (m/z 218), serine (m/z 390 and m/z 362), histidine (m/z 440 and m/z 412), tyrosine (m/z 466 and m/z 438), phenylalanine (m/z 336 and m/z 308), glycerol (m/z 377), and ribose (m/z 160) mapped the pathways supporting the observations. The outcomes help better define the central carbon metabolic network of R. solanacearum that can be integrated with 13C metabolic flux analysis as well as flux balance analysis studies for defining the metabolic phenotypes. IMPORTANCE Understanding the metabolic versatility of Ralstonia solanacearum is important, as it regulates the trade-off between virulence and metabolism (1, 2) in a wide range of plant hosts. Due to a lack of clear evidence until this work, several published research papers reported on the potential roles of glycolysis and the oxidative pentose phosphate pathway (OxPPP) in R. solanacearum (3, 4). This work provided evidence from 13C stable isotope feeding and genome annotation-based comparative metabolic network analysis that the Entner-Doudoroff pathway and non-OxPPP bypass glycolysis and OxPPP during the oxidation of glucose, a component of the host xylem pool that serves as a potential carbon source (5). The outcomes help better define the central carbon metabolic network of R. solanacearum that can be integrated with 13C metabolic flux analysis as well as flux balance analysis studies for defining the metabolic phenotypes. The study highlights the need to critically examine phytopathogens whose metabolism is poorly understood.
format	article
author	Poonam Jyoti Manu Shree Chandrakant Joshi Tulika Prakash Suvendra Kumar Ray Siddhartha Sankar Satapathy Shyam Kumar Masakapalli
author_facet	Poonam Jyoti Manu Shree Chandrakant Joshi Tulika Prakash Suvendra Kumar Ray Siddhartha Sankar Satapathy Shyam Kumar Masakapalli
author_sort	Poonam Jyoti
title	The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>
title_short	The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>
title_full	The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>
title_fullStr	The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>
title_full_unstemmed	The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>
title_sort	entner-doudoroff and nonoxidative pentose phosphate pathways bypass glycolysis and the oxidative pentose phosphate pathway in <named-content content-type="genus-species">ralstonia solanacearum</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/b0dc11a343e244509cf76d987878763c
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The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in <named-content content-type="genus-species">Ralstonia solanacearum</named-content>

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