Functional analysis of Salmonella Typhi adaptation to survival in water
Summary Contaminated water is a major risk factor associated with the transmission of Salmonella enterica serovar Typhi (S. Typhi), the aetiological agent of human typhoid. However, little is known about how this pathogen adapts to living in the aqueous environment. We used transcriptome analysis (R...
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| Veröffentlicht in: | Environmental microbiology 2018-11, Vol.20 (11), p.4079-4090 |
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| creator | Kingsley, Robert A. Langridge, Gemma Smith, Sarah E. Makendi, Carine Fookes, Maria Wileman, Tom M. El Ghany, Moataz Abd Keith Turner, A. Dyson, Zoe A. Sridhar, Sushmita Pickard, Derek Kay, Sally Feasey, Nicholas Wong, Vanessa Barquist, Lars Dougan, Gordon |
| description | Summary
Contaminated water is a major risk factor associated with the transmission of Salmonella enterica serovar Typhi (S. Typhi), the aetiological agent of human typhoid. However, little is known about how this pathogen adapts to living in the aqueous environment. We used transcriptome analysis (RNA‐seq) and transposon mutagenesis (TraDIS) to characterize these adaptive changes and identify multiple genes that contribute to survival. Over half of the genes in the S. Typhi genome altered expression level within the first 24 h following transfer from broth culture to water, although relatively few did so in the first 30 min. Genes linked to central metabolism, stress associated with arrested proton motive force and respiratory chain factors changed expression levels. Additionally, motility and chemotaxis genes increased expression, consistent with a scavenging lifestyle. The viaB‐associated gene tviC encoding a glcNAc epimerase that is required for Vi polysaccharide biosynthesis was, along with several other genes, shown to contribute to survival in water. Thus, we define regulatory adaptation operating in S. Typhi that facilitates survival in water. |
| doi_str_mv | 10.1111/1462-2920.14458 |
| format | Article |
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Contaminated water is a major risk factor associated with the transmission of Salmonella enterica serovar Typhi (S. Typhi), the aetiological agent of human typhoid. However, little is known about how this pathogen adapts to living in the aqueous environment. We used transcriptome analysis (RNA‐seq) and transposon mutagenesis (TraDIS) to characterize these adaptive changes and identify multiple genes that contribute to survival. Over half of the genes in the S. Typhi genome altered expression level within the first 24 h following transfer from broth culture to water, although relatively few did so in the first 30 min. Genes linked to central metabolism, stress associated with arrested proton motive force and respiratory chain factors changed expression levels. Additionally, motility and chemotaxis genes increased expression, consistent with a scavenging lifestyle. The viaB‐associated gene tviC encoding a glcNAc epimerase that is required for Vi polysaccharide biosynthesis was, along with several other genes, shown to contribute to survival in water. Thus, we define regulatory adaptation operating in S. Typhi that facilitates survival in water.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.14458</identifier><identifier>PMID: 30450829</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Adaptation ; Aqueous environments ; Biosynthesis ; Chemotaxis ; culture media ; Electron transport ; electron transport chain ; enzymes ; Epimerase ; Functional analysis ; Gene expression ; Genes ; Genomes ; humans ; lifestyle ; Metabolism ; Mutagenesis ; Nucleic acids ; Pathogens ; Polysaccharides ; proton-motive force ; Protonmotive force ; Ribonucleic acid ; Risk analysis ; Risk factors ; RNA ; Salmonella ; Salmonella Typhi ; Scavenging ; sequence analysis ; Survival ; transcriptomics ; Transposon mutagenesis ; transposons ; Typhoid ; typhoid fever ; Vaccines ; Water ; Water pollution</subject><ispartof>Environmental microbiology, 2018-11, Vol.20 (11), p.4079-4090</ispartof><rights>2018 The Authors. published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2018 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2018 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5008-4f5e733b36168f86cc85ecc7a4372c94e5448a907fc0797dc9d194ab5efba3fb3</citedby><cites>FETCH-LOGICAL-c5008-4f5e733b36168f86cc85ecc7a4372c94e5448a907fc0797dc9d194ab5efba3fb3</cites><orcidid>0000-0002-0194-6485</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.14458$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.14458$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30450829$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kingsley, Robert A.</creatorcontrib><creatorcontrib>Langridge, Gemma</creatorcontrib><creatorcontrib>Smith, Sarah E.</creatorcontrib><creatorcontrib>Makendi, Carine</creatorcontrib><creatorcontrib>Fookes, Maria</creatorcontrib><creatorcontrib>Wileman, Tom M.</creatorcontrib><creatorcontrib>El Ghany, Moataz Abd</creatorcontrib><creatorcontrib>Keith Turner, A.</creatorcontrib><creatorcontrib>Dyson, Zoe A.</creatorcontrib><creatorcontrib>Sridhar, Sushmita</creatorcontrib><creatorcontrib>Pickard, Derek</creatorcontrib><creatorcontrib>Kay, Sally</creatorcontrib><creatorcontrib>Feasey, Nicholas</creatorcontrib><creatorcontrib>Wong, Vanessa</creatorcontrib><creatorcontrib>Barquist, Lars</creatorcontrib><creatorcontrib>Dougan, Gordon</creatorcontrib><title>Functional analysis of Salmonella Typhi adaptation to survival in water</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Contaminated water is a major risk factor associated with the transmission of Salmonella enterica serovar Typhi (S. Typhi), the aetiological agent of human typhoid. However, little is known about how this pathogen adapts to living in the aqueous environment. We used transcriptome analysis (RNA‐seq) and transposon mutagenesis (TraDIS) to characterize these adaptive changes and identify multiple genes that contribute to survival. Over half of the genes in the S. Typhi genome altered expression level within the first 24 h following transfer from broth culture to water, although relatively few did so in the first 30 min. Genes linked to central metabolism, stress associated with arrested proton motive force and respiratory chain factors changed expression levels. Additionally, motility and chemotaxis genes increased expression, consistent with a scavenging lifestyle. The viaB‐associated gene tviC encoding a glcNAc epimerase that is required for Vi polysaccharide biosynthesis was, along with several other genes, shown to contribute to survival in water. Thus, we define regulatory adaptation operating in S. Typhi that facilitates survival in water.</description><subject>Adaptation</subject><subject>Aqueous environments</subject><subject>Biosynthesis</subject><subject>Chemotaxis</subject><subject>culture media</subject><subject>Electron transport</subject><subject>electron transport chain</subject><subject>enzymes</subject><subject>Epimerase</subject><subject>Functional analysis</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genomes</subject><subject>humans</subject><subject>lifestyle</subject><subject>Metabolism</subject><subject>Mutagenesis</subject><subject>Nucleic acids</subject><subject>Pathogens</subject><subject>Polysaccharides</subject><subject>proton-motive force</subject><subject>Protonmotive force</subject><subject>Ribonucleic acid</subject><subject>Risk analysis</subject><subject>Risk factors</subject><subject>RNA</subject><subject>Salmonella</subject><subject>Salmonella Typhi</subject><subject>Scavenging</subject><subject>sequence analysis</subject><subject>Survival</subject><subject>transcriptomics</subject><subject>Transposon mutagenesis</subject><subject>transposons</subject><subject>Typhoid</subject><subject>typhoid fever</subject><subject>Vaccines</subject><subject>Water</subject><subject>Water pollution</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNqNkb1PAyEYh4nR2Fqd3cwlLi61fB6wmBjTqkmNgzoTjnKKuR4V7mr638vZ2qiLMvD5vE-AHwDHCJ6j1EaI5niIJU5LSpnYAf3tzu52jnAPHMT4CiHihMN90COQMiiw7IPrSVubxvlaV5lO3Sq6mPkye9DV3Ne2qnT2uFq8uEzP9KLRHZk1PottWLplqnF19q4bGw7BXqmraI824wA8TcaPVzfD6f317dXldGgYhGJIS2Y5IQXJUS5KkRsjmDWGa0o4NpJaRqnQEvLSQC75zMgZklQXzJaFJmVBBuBi7V20xdzOjK2boCu1CG6uw0p57dTPk9q9qGe_VDkWWLA8Cc42guDfWhsbNXfRdA-trW-jwkhIhiij-B8oSUKOGU3o6S_01bch_ecnRaVgUKJEjdaUCT7GYMvtvRFUXZ6qS0x16anPPFPFyffnbvmvABPA1sC7q-zqL58a392uxR8pOaoZ</recordid><startdate>201811</startdate><enddate>201811</enddate><creator>Kingsley, Robert A.</creator><creator>Langridge, Gemma</creator><creator>Smith, Sarah E.</creator><creator>Makendi, Carine</creator><creator>Fookes, Maria</creator><creator>Wileman, Tom M.</creator><creator>El Ghany, Moataz Abd</creator><creator>Keith Turner, A.</creator><creator>Dyson, Zoe A.</creator><creator>Sridhar, Sushmita</creator><creator>Pickard, Derek</creator><creator>Kay, Sally</creator><creator>Feasey, Nicholas</creator><creator>Wong, Vanessa</creator><creator>Barquist, Lars</creator><creator>Dougan, Gordon</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0194-6485</orcidid></search><sort><creationdate>201811</creationdate><title>Functional analysis of Salmonella Typhi adaptation to survival in water</title><author>Kingsley, Robert A. ; Langridge, Gemma ; Smith, Sarah E. ; Makendi, Carine ; Fookes, Maria ; Wileman, Tom M. ; El Ghany, Moataz Abd ; Keith Turner, A. ; Dyson, Zoe A. ; Sridhar, Sushmita ; Pickard, Derek ; Kay, Sally ; Feasey, Nicholas ; Wong, Vanessa ; Barquist, Lars ; Dougan, Gordon</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5008-4f5e733b36168f86cc85ecc7a4372c94e5448a907fc0797dc9d194ab5efba3fb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adaptation</topic><topic>Aqueous environments</topic><topic>Biosynthesis</topic><topic>Chemotaxis</topic><topic>culture media</topic><topic>Electron transport</topic><topic>electron transport chain</topic><topic>enzymes</topic><topic>Epimerase</topic><topic>Functional analysis</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genomes</topic><topic>humans</topic><topic>lifestyle</topic><topic>Metabolism</topic><topic>Mutagenesis</topic><topic>Nucleic acids</topic><topic>Pathogens</topic><topic>Polysaccharides</topic><topic>proton-motive force</topic><topic>Protonmotive force</topic><topic>Ribonucleic acid</topic><topic>Risk analysis</topic><topic>Risk factors</topic><topic>RNA</topic><topic>Salmonella</topic><topic>Salmonella Typhi</topic><topic>Scavenging</topic><topic>sequence analysis</topic><topic>Survival</topic><topic>transcriptomics</topic><topic>Transposon mutagenesis</topic><topic>transposons</topic><topic>Typhoid</topic><topic>typhoid fever</topic><topic>Vaccines</topic><topic>Water</topic><topic>Water pollution</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kingsley, Robert A.</creatorcontrib><creatorcontrib>Langridge, Gemma</creatorcontrib><creatorcontrib>Smith, Sarah E.</creatorcontrib><creatorcontrib>Makendi, Carine</creatorcontrib><creatorcontrib>Fookes, Maria</creatorcontrib><creatorcontrib>Wileman, Tom M.</creatorcontrib><creatorcontrib>El Ghany, Moataz Abd</creatorcontrib><creatorcontrib>Keith Turner, A.</creatorcontrib><creatorcontrib>Dyson, Zoe A.</creatorcontrib><creatorcontrib>Sridhar, Sushmita</creatorcontrib><creatorcontrib>Pickard, Derek</creatorcontrib><creatorcontrib>Kay, Sally</creatorcontrib><creatorcontrib>Feasey, Nicholas</creatorcontrib><creatorcontrib>Wong, Vanessa</creatorcontrib><creatorcontrib>Barquist, Lars</creatorcontrib><creatorcontrib>Dougan, Gordon</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kingsley, Robert A.</au><au>Langridge, Gemma</au><au>Smith, Sarah E.</au><au>Makendi, Carine</au><au>Fookes, Maria</au><au>Wileman, Tom M.</au><au>El Ghany, Moataz Abd</au><au>Keith Turner, A.</au><au>Dyson, Zoe A.</au><au>Sridhar, Sushmita</au><au>Pickard, Derek</au><au>Kay, Sally</au><au>Feasey, Nicholas</au><au>Wong, Vanessa</au><au>Barquist, Lars</au><au>Dougan, Gordon</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional analysis of Salmonella Typhi adaptation to survival in water</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2018-11</date><risdate>2018</risdate><volume>20</volume><issue>11</issue><spage>4079</spage><epage>4090</epage><pages>4079-4090</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Contaminated water is a major risk factor associated with the transmission of Salmonella enterica serovar Typhi (S. Typhi), the aetiological agent of human typhoid. However, little is known about how this pathogen adapts to living in the aqueous environment. We used transcriptome analysis (RNA‐seq) and transposon mutagenesis (TraDIS) to characterize these adaptive changes and identify multiple genes that contribute to survival. Over half of the genes in the S. Typhi genome altered expression level within the first 24 h following transfer from broth culture to water, although relatively few did so in the first 30 min. Genes linked to central metabolism, stress associated with arrested proton motive force and respiratory chain factors changed expression levels. Additionally, motility and chemotaxis genes increased expression, consistent with a scavenging lifestyle. The viaB‐associated gene tviC encoding a glcNAc epimerase that is required for Vi polysaccharide biosynthesis was, along with several other genes, shown to contribute to survival in water. Thus, we define regulatory adaptation operating in S. Typhi that facilitates survival in water.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>30450829</pmid><doi>10.1111/1462-2920.14458</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-0194-6485</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adaptation Aqueous environments Biosynthesis Chemotaxis culture media Electron transport electron transport chain enzymes Epimerase Functional analysis Gene expression Genes Genomes humans lifestyle Metabolism Mutagenesis Nucleic acids Pathogens Polysaccharides proton-motive force Protonmotive force Ribonucleic acid Risk analysis Risk factors RNA Salmonella Salmonella Typhi Scavenging sequence analysis Survival transcriptomics Transposon mutagenesis transposons Typhoid typhoid fever Vaccines Water Water pollution |
| title | Functional analysis of Salmonella Typhi adaptation to survival in water |
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