<named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment

ABSTRACT Genomic data predict that, in addition to oxygen, the bacterial plant pathogen Ralstonia solanacearum can use nitrate (NO3−), nitrite (NO2−), nitric oxide (NO), and nitrous oxide (N2O) as terminal electron acceptors (TEAs). Genes encoding inorganic nitrogen reduction were highly expressed d...

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Autores principales:	Beth L. Dalsing, Alicia N. Truchon, Enid T. Gonzalez-Orta, Annett S. Milling, Caitilyn Allen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/046f6ea7a8bc4873919baa4c024a2b31
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spelling	oai:doaj.org-article:046f6ea7a8bc4873919baa4c024a2b312021-11-15T15:41:34Z<named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment10.1128/mBio.02471-142150-7511https://doaj.org/article/046f6ea7a8bc4873919baa4c024a2b312015-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02471-14https://doaj.org/toc/2150-7511ABSTRACT Genomic data predict that, in addition to oxygen, the bacterial plant pathogen Ralstonia solanacearum can use nitrate (NO3−), nitrite (NO2−), nitric oxide (NO), and nitrous oxide (N2O) as terminal electron acceptors (TEAs). Genes encoding inorganic nitrogen reduction were highly expressed during tomato bacterial wilt disease, when the pathogen grows in xylem vessels. Direct measurements found that tomato xylem fluid was low in oxygen, especially in plants infected by R. solanacearum. Xylem fluid contained ~25 mM NO3−, corresponding to R. solanacearum's optimal NO3− concentration for anaerobic growth in vitro. We tested the hypothesis that R. solanacearum uses inorganic nitrogen species to respire and grow during pathogenesis by making deletion mutants that each lacked a step in nitrate respiration (ΔnarG), denitrification (ΔaniA, ΔnorB, and ΔnosZ), or NO detoxification (ΔhmpX). The ΔnarG, ΔaniA, and ΔnorB mutants grew poorly on NO3− compared to the wild type, and they had reduced adenylate energy charge levels under anaerobiosis. While NarG-dependent NO3− respiration directly enhanced growth, AniA-dependent NO2− reduction did not. NO2− and NO inhibited growth in culture, and their removal depended on denitrification and NO detoxification. Thus, NO3− acts as a TEA, but the resulting NO2− and NO likely do not. None of the mutants grew as well as the wild type in planta, and strains lacking AniA (NO2− reductase) or HmpX (NO detoxification) had reduced virulence on tomato. Thus, R. solanacearum exploits host NO3− to respire, grow, and cause disease. Degradation of NO2− and NO is also important for successful infection and depends on denitrification and NO detoxification systems. IMPORTANCE The plant-pathogenic bacterium Ralstonia solanacearum causes bacterial wilt, one of the world's most destructive crop diseases. This pathogen's explosive growth in plant vascular xylem is poorly understood. We used biochemical and genetic approaches to show that R. solanacearum rapidly depletes oxygen in host xylem but can then respire using host nitrate as a terminal electron acceptor. The microbe uses its denitrification pathway to detoxify the reactive nitrogen species nitrite (a product of nitrate respiration) and nitric oxide (a plant defense signal). Detoxification may play synergistic roles in bacterial wilt virulence by converting the host's chemical weapon into an energy source. Mutant bacterial strains lacking elements of the denitrification pathway could not grow as well as the wild type in tomato plants, and some mutants were also reduced in virulence. Our results show how a pathogen's metabolic activity can alter the host environment in ways that increase pathogen success.Beth L. DalsingAlicia N. TruchonEnid T. Gonzalez-OrtaAnnett S. MillingCaitilyn AllenAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 2 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Beth L. Dalsing Alicia N. Truchon Enid T. Gonzalez-Orta Annett S. Milling Caitilyn Allen <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment
description	ABSTRACT Genomic data predict that, in addition to oxygen, the bacterial plant pathogen Ralstonia solanacearum can use nitrate (NO3−), nitrite (NO2−), nitric oxide (NO), and nitrous oxide (N2O) as terminal electron acceptors (TEAs). Genes encoding inorganic nitrogen reduction were highly expressed during tomato bacterial wilt disease, when the pathogen grows in xylem vessels. Direct measurements found that tomato xylem fluid was low in oxygen, especially in plants infected by R. solanacearum. Xylem fluid contained ~25 mM NO3−, corresponding to R. solanacearum's optimal NO3− concentration for anaerobic growth in vitro. We tested the hypothesis that R. solanacearum uses inorganic nitrogen species to respire and grow during pathogenesis by making deletion mutants that each lacked a step in nitrate respiration (ΔnarG), denitrification (ΔaniA, ΔnorB, and ΔnosZ), or NO detoxification (ΔhmpX). The ΔnarG, ΔaniA, and ΔnorB mutants grew poorly on NO3− compared to the wild type, and they had reduced adenylate energy charge levels under anaerobiosis. While NarG-dependent NO3− respiration directly enhanced growth, AniA-dependent NO2− reduction did not. NO2− and NO inhibited growth in culture, and their removal depended on denitrification and NO detoxification. Thus, NO3− acts as a TEA, but the resulting NO2− and NO likely do not. None of the mutants grew as well as the wild type in planta, and strains lacking AniA (NO2− reductase) or HmpX (NO detoxification) had reduced virulence on tomato. Thus, R. solanacearum exploits host NO3− to respire, grow, and cause disease. Degradation of NO2− and NO is also important for successful infection and depends on denitrification and NO detoxification systems. IMPORTANCE The plant-pathogenic bacterium Ralstonia solanacearum causes bacterial wilt, one of the world's most destructive crop diseases. This pathogen's explosive growth in plant vascular xylem is poorly understood. We used biochemical and genetic approaches to show that R. solanacearum rapidly depletes oxygen in host xylem but can then respire using host nitrate as a terminal electron acceptor. The microbe uses its denitrification pathway to detoxify the reactive nitrogen species nitrite (a product of nitrate respiration) and nitric oxide (a plant defense signal). Detoxification may play synergistic roles in bacterial wilt virulence by converting the host's chemical weapon into an energy source. Mutant bacterial strains lacking elements of the denitrification pathway could not grow as well as the wild type in tomato plants, and some mutants were also reduced in virulence. Our results show how a pathogen's metabolic activity can alter the host environment in ways that increase pathogen success.
format	article
author	Beth L. Dalsing Alicia N. Truchon Enid T. Gonzalez-Orta Annett S. Milling Caitilyn Allen
author_facet	Beth L. Dalsing Alicia N. Truchon Enid T. Gonzalez-Orta Annett S. Milling Caitilyn Allen
author_sort	Beth L. Dalsing
title	<named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment
title_short	<named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment
title_full	<named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment
title_fullStr	<named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment
title_full_unstemmed	<named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment
title_sort	<named-content content-type="genus-species">ralstonia solanacearum</named-content> uses inorganic nitrogen metabolism for virulence, atp production, and detoxification in the oxygen-limited host xylem environment
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/046f6ea7a8bc4873919baa4c024a2b31
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<named-content content-type="genus-species">Ralstonia solanacearum</named-content> Uses Inorganic Nitrogen Metabolism for Virulence, ATP Production, and Detoxification in the Oxygen-Limited Host Xylem Environment

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