Gene expression changes throughout the life cycle allow a bacterial plant pathogen to persist in diverse environmental habitats
Bacterial pathogens exhibit a remarkable ability to persist and thrive in diverse ecological niches. Understanding the mechanisms enabling their transition between habitats is crucial to control dissemination and potential disease outbreaks. Here, we use Ralstonia solanacearum, the causing agent of...
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creator | de Pedro-Jové, Roger Corral, Jordi Rocafort, Mercedes Puigvert, Marina Azam, Fàtima Latif Vandecaveye, Agustina Macho, Alberto P Balsalobre, Carlos Coll, Núria S Orellano, Elena Valls, Marc |
description | Bacterial pathogens exhibit a remarkable ability to persist and thrive in diverse ecological niches. Understanding the mechanisms enabling their transition between habitats is crucial to control dissemination and potential disease outbreaks. Here, we use Ralstonia solanacearum, the causing agent of the bacterial wilt disease, as a model to investigate pathogen adaptation to water and soil, two environments that act as bacterial reservoirs, and compare this information with gene expression in planta. Gene expression in water resembled that observed during late xylem colonization, with an intriguing induction of the type 3 secretion system (T3SS). Alkaline pH and nutrient scarcity-conditions also encountered during late infection stages-were identified as the triggers for this T3SS induction. In the soil environment, R. solanacearum upregulated stress-responses and genes for the use of alternate carbon sources, such as phenylacetate catabolism and the glyoxylate cycle, and downregulated virulence-associated genes. We proved through gain- and loss-of-function experiments that genes associated with the oxidative stress response, such as the regulator OxyR and the catalase KatG, are key for bacterial survival in soil, as their deletion cause a decrease in culturability associated with a premature induction of the viable but non culturable state (VBNC). This work identifies essential factors necessary for R. solanacearum to complete its life cycle and is the first comprehensive gene expression analysis in all environments occupied by a bacterial plant pathogen, providing valuable insights into its biology and adaptation to unexplored habitats. |
doi_str_mv | 10.1371/journal.ppat.1011888 |
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Understanding the mechanisms enabling their transition between habitats is crucial to control dissemination and potential disease outbreaks. Here, we use Ralstonia solanacearum, the causing agent of the bacterial wilt disease, as a model to investigate pathogen adaptation to water and soil, two environments that act as bacterial reservoirs, and compare this information with gene expression in planta. Gene expression in water resembled that observed during late xylem colonization, with an intriguing induction of the type 3 secretion system (T3SS). Alkaline pH and nutrient scarcity-conditions also encountered during late infection stages-were identified as the triggers for this T3SS induction. In the soil environment, R. solanacearum upregulated stress-responses and genes for the use of alternate carbon sources, such as phenylacetate catabolism and the glyoxylate cycle, and downregulated virulence-associated genes. We proved through gain- and loss-of-function experiments that genes associated with the oxidative stress response, such as the regulator OxyR and the catalase KatG, are key for bacterial survival in soil, as their deletion cause a decrease in culturability associated with a premature induction of the viable but non culturable state (VBNC). This work identifies essential factors necessary for R. solanacearum to complete its life cycle and is the first comprehensive gene expression analysis in all environments occupied by a bacterial plant pathogen, providing valuable insights into its biology and adaptation to unexplored habitats.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1011888</identifier><identifier>PMID: 38113281</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptation ; Analysis ; Animals ; Bacteria ; Bacterial infections ; Biology and Life Sciences ; Carbon sources ; Catabolism ; Catalase ; Disease control ; Ecological niches ; Ecology and Environmental Sciences ; Environmental conditions ; Enzymes ; Epidemics ; Gene Expression ; Genes ; Genetic research ; Glyoxylate cycle ; Habitats ; Life Cycle Stages ; Life cycles ; Medical research ; Medicine and Health Sciences ; Medicine, Experimental ; Metabolism ; Motility ; Niche (Ecology) ; Oxidative stress ; Pathogens ; Plant Diseases - genetics ; Plant Diseases - microbiology ; Plant-pathogen relationships ; Prevention ; Principal components analysis ; Protection and preservation ; Ralstonia solanacearum - genetics ; Ralstonia solanacearum - metabolism ; Ribonucleic acid ; Risk factors ; RNA ; Soil ; Soil ecology ; Soil environment ; Soil microbiology ; Soil microorganisms ; Soil water ; Solanum lycopersicum ; Streptococcus infections ; Virulence ; Virulence (Microbiology) ; Water ; Water - metabolism ; Wilt ; Xylem</subject><ispartof>PLoS pathogens, 2023-12, Vol.19 (12), p.e1011888-e1011888</ispartof><rights>Copyright: © 2023 de Pedro-Jové et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 de Pedro-Jové et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 de Pedro-Jové et al 2023 de Pedro-Jové et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c545t-3fa3bd17f4e1fc720f1e7d3e6d28569ddb4c8be5a80ca8c5864fb7f6c8fb1f093</cites><orcidid>0000-0003-2312-0091</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10763947/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10763947/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38113281$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Mackey, David</contributor><creatorcontrib>de Pedro-Jové, Roger</creatorcontrib><creatorcontrib>Corral, Jordi</creatorcontrib><creatorcontrib>Rocafort, Mercedes</creatorcontrib><creatorcontrib>Puigvert, Marina</creatorcontrib><creatorcontrib>Azam, Fàtima Latif</creatorcontrib><creatorcontrib>Vandecaveye, Agustina</creatorcontrib><creatorcontrib>Macho, Alberto P</creatorcontrib><creatorcontrib>Balsalobre, Carlos</creatorcontrib><creatorcontrib>Coll, Núria S</creatorcontrib><creatorcontrib>Orellano, Elena</creatorcontrib><creatorcontrib>Valls, Marc</creatorcontrib><title>Gene expression changes throughout the life cycle allow a bacterial plant pathogen to persist in diverse environmental habitats</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Bacterial pathogens exhibit a remarkable ability to persist and thrive in diverse ecological niches. Understanding the mechanisms enabling their transition between habitats is crucial to control dissemination and potential disease outbreaks. Here, we use Ralstonia solanacearum, the causing agent of the bacterial wilt disease, as a model to investigate pathogen adaptation to water and soil, two environments that act as bacterial reservoirs, and compare this information with gene expression in planta. Gene expression in water resembled that observed during late xylem colonization, with an intriguing induction of the type 3 secretion system (T3SS). Alkaline pH and nutrient scarcity-conditions also encountered during late infection stages-were identified as the triggers for this T3SS induction. In the soil environment, R. solanacearum upregulated stress-responses and genes for the use of alternate carbon sources, such as phenylacetate catabolism and the glyoxylate cycle, and downregulated virulence-associated genes. We proved through gain- and loss-of-function experiments that genes associated with the oxidative stress response, such as the regulator OxyR and the catalase KatG, are key for bacterial survival in soil, as their deletion cause a decrease in culturability associated with a premature induction of the viable but non culturable state (VBNC). This work identifies essential factors necessary for R. solanacearum to complete its life cycle and is the first comprehensive gene expression analysis in all environments occupied by a bacterial plant pathogen, providing valuable insights into its biology and adaptation to unexplored habitats.</description><subject>Adaptation</subject><subject>Analysis</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacterial infections</subject><subject>Biology and Life Sciences</subject><subject>Carbon sources</subject><subject>Catabolism</subject><subject>Catalase</subject><subject>Disease control</subject><subject>Ecological niches</subject><subject>Ecology and Environmental Sciences</subject><subject>Environmental conditions</subject><subject>Enzymes</subject><subject>Epidemics</subject><subject>Gene Expression</subject><subject>Genes</subject><subject>Genetic research</subject><subject>Glyoxylate cycle</subject><subject>Habitats</subject><subject>Life Cycle Stages</subject><subject>Life cycles</subject><subject>Medical research</subject><subject>Medicine and Health Sciences</subject><subject>Medicine, Experimental</subject><subject>Metabolism</subject><subject>Motility</subject><subject>Niche (Ecology)</subject><subject>Oxidative stress</subject><subject>Pathogens</subject><subject>Plant Diseases - 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genetics</topic><topic>Plant Diseases - microbiology</topic><topic>Plant-pathogen relationships</topic><topic>Prevention</topic><topic>Principal components analysis</topic><topic>Protection and preservation</topic><topic>Ralstonia solanacearum - genetics</topic><topic>Ralstonia solanacearum - metabolism</topic><topic>Ribonucleic acid</topic><topic>Risk factors</topic><topic>RNA</topic><topic>Soil</topic><topic>Soil ecology</topic><topic>Soil environment</topic><topic>Soil microbiology</topic><topic>Soil microorganisms</topic><topic>Soil water</topic><topic>Solanum lycopersicum</topic><topic>Streptococcus infections</topic><topic>Virulence</topic><topic>Virulence (Microbiology)</topic><topic>Water</topic><topic>Water - metabolism</topic><topic>Wilt</topic><topic>Xylem</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>de Pedro-Jové, Roger</creatorcontrib><creatorcontrib>Corral, Jordi</creatorcontrib><creatorcontrib>Rocafort, Mercedes</creatorcontrib><creatorcontrib>Puigvert, Marina</creatorcontrib><creatorcontrib>Azam, Fàtima Latif</creatorcontrib><creatorcontrib>Vandecaveye, Agustina</creatorcontrib><creatorcontrib>Macho, Alberto P</creatorcontrib><creatorcontrib>Balsalobre, Carlos</creatorcontrib><creatorcontrib>Coll, Núria S</creatorcontrib><creatorcontrib>Orellano, Elena</creatorcontrib><creatorcontrib>Valls, Marc</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>de Pedro-Jové, Roger</au><au>Corral, Jordi</au><au>Rocafort, Mercedes</au><au>Puigvert, Marina</au><au>Azam, Fàtima Latif</au><au>Vandecaveye, Agustina</au><au>Macho, Alberto P</au><au>Balsalobre, Carlos</au><au>Coll, Núria S</au><au>Orellano, Elena</au><au>Valls, Marc</au><au>Mackey, David</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Gene expression changes throughout the life cycle allow a bacterial plant pathogen to persist in diverse environmental habitats</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2023-12-19</date><risdate>2023</risdate><volume>19</volume><issue>12</issue><spage>e1011888</spage><epage>e1011888</epage><pages>e1011888-e1011888</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Bacterial pathogens exhibit a remarkable ability to persist and thrive in diverse ecological niches. Understanding the mechanisms enabling their transition between habitats is crucial to control dissemination and potential disease outbreaks. Here, we use Ralstonia solanacearum, the causing agent of the bacterial wilt disease, as a model to investigate pathogen adaptation to water and soil, two environments that act as bacterial reservoirs, and compare this information with gene expression in planta. Gene expression in water resembled that observed during late xylem colonization, with an intriguing induction of the type 3 secretion system (T3SS). Alkaline pH and nutrient scarcity-conditions also encountered during late infection stages-were identified as the triggers for this T3SS induction. In the soil environment, R. solanacearum upregulated stress-responses and genes for the use of alternate carbon sources, such as phenylacetate catabolism and the glyoxylate cycle, and downregulated virulence-associated genes. We proved through gain- and loss-of-function experiments that genes associated with the oxidative stress response, such as the regulator OxyR and the catalase KatG, are key for bacterial survival in soil, as their deletion cause a decrease in culturability associated with a premature induction of the viable but non culturable state (VBNC). This work identifies essential factors necessary for R. solanacearum to complete its life cycle and is the first comprehensive gene expression analysis in all environments occupied by a bacterial plant pathogen, providing valuable insights into its biology and adaptation to unexplored habitats.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>38113281</pmid><doi>10.1371/journal.ppat.1011888</doi><tpages>e1011888</tpages><orcidid>https://orcid.org/0000-0003-2312-0091</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation Analysis Animals Bacteria Bacterial infections Biology and Life Sciences Carbon sources Catabolism Catalase Disease control Ecological niches Ecology and Environmental Sciences Environmental conditions Enzymes Epidemics Gene Expression Genes Genetic research Glyoxylate cycle Habitats Life Cycle Stages Life cycles Medical research Medicine and Health Sciences Medicine, Experimental Metabolism Motility Niche (Ecology) Oxidative stress Pathogens Plant Diseases - genetics Plant Diseases - microbiology Plant-pathogen relationships Prevention Principal components analysis Protection and preservation Ralstonia solanacearum - genetics Ralstonia solanacearum - metabolism Ribonucleic acid Risk factors RNA Soil Soil ecology Soil environment Soil microbiology Soil microorganisms Soil water Solanum lycopersicum Streptococcus infections Virulence Virulence (Microbiology) Water Water - metabolism Wilt Xylem |
title | Gene expression changes throughout the life cycle allow a bacterial plant pathogen to persist in diverse environmental habitats |
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