Dataset Information

Ralstonia solanacearum uses inorganic nitrogen metabolism for virulence, ATP production, and detoxification in the oxygen-limited host xylem environment.

ABSTRACT:

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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 (?narG), denitrification (?aniA, ?norB, and ?nosZ), or NO detoxification (?hmpX). The ?narG, ?aniA, and ?norB 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.

SUBMITTER: Dalsing BL

PROVIDER: S-EPMC4453514 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Publications

Ralstonia solanacearum uses inorganic nitrogen metabolism for virulence, ATP production, and detoxification in the oxygen-limited host xylem environment.

Dalsing Beth L BL Truchon Alicia N AN Gonzalez-Orta Enid T ET Milling Annett S AS Allen Caitilyn C

mBio 20150317 2

<h4>Unlabelled</h4>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. so ...[more]

PMID: 25784703

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Project description:Following a request from the European Commission, the EFSA Panel on Plant Health performed a pest categorisation of the Ralstonia solanacearum species complex (RSSC), a distinguishable cosmopolitan group of bacterial plant pathogens (including R. solanacearum, Ralstonia pseudosolanacearum and two subspecies of Ralstonia syzygii) of the family Burkholderiaceae. The RSSC causes bacterial wilt in solanaceous crops, such as potato, tomato and pepper, but can also cause wilts in other important food crops such as fruit banana, plantain banana and cassava. The pest survives in the soil, and a number of weed species can also be infected by the pest, often asymptomatically. The RSSC is regulated in Council Directive 2000/29/EC (Annex IAII) (indicated by its former name R. solanacearum, as delimited by Yabuuchi et al.) as a harmful organism whose introduction into the EU is banned. In addition, Council Directive 1998/57/EC (amended by Commission Directive 2006/63/CE) concerns the measures to be taken within EU Member States (MS) against the RSSC to (a) detect it and determine its distribution, (b) prevent its occurrence and spread, and (c) control it with the aim of eradication. The pest is present in several EU MS, but in all cases with a restricted distribution and under official control. New phylotypes of the RSSC could enter the EU primarily via host plants for planting (including seed tubers). The pest could establish in the EU, as climatic conditions are favourable, hosts are common and the pathogen has high adaptability. Spread is mainly via plants for planting. Substantial crop losses in the EU would occur in the presence of RSSC epidemics. The RSSC is regarded as one of the world's most important phytopathogenic bacteria due to its broad geographical distribution, large host range, aggressiveness, genetic diversity and long persistence in soil and water. The list of hosts and commodities for which the pest is regulated is incomplete due to the high diversity of hosts and the lack of knowledge of the complete host range. Moreover, the comparative epidemiology of the different pathogen species has not yet been studied. The criteria assessed by the Panel for consideration of the RSSC as potential quarantine pest are met, while, for regulated non-quarantine pests, the criterion on the widespread presence in the EU is not met.

Dataset Information

Ralstonia solanacearum uses inorganic nitrogen metabolism for virulence, ATP production, and detoxification in the oxygen-limited host xylem environment.

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Importance

Publications

Ralstonia solanacearum uses inorganic nitrogen metabolism for virulence, ATP production, and detoxification in the oxygen-limited host xylem environment.

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