Type VI secretion system contributes to Enterohemorrhagic Escherichia coli virulence by secreting catalase against host reactive oxygen species (ROS)
Enterohemorrhagic Escherichia coli (EHEC) is one major type of contagious and foodborne pathogens. The type VI secretion system (T6SS) has been shown to be involved in the bacterial pathogenicity and bacteria-bacteria competition. Here, we show that EHEC could secrete a novel effector KatN, a Mn-con...
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creator | Wan, Baoshan Zhang, Qiufen Ni, Jinjing Li, Shuxian Wen, Donghua Li, Jun Xiao, Haihan He, Ping Ou, Hong-Yu Tao, Jing Teng, Qihui Lu, Jie Wu, Wenjuan Yao, Yu-Feng |
description | Enterohemorrhagic Escherichia coli (EHEC) is one major type of contagious and foodborne pathogens. The type VI secretion system (T6SS) has been shown to be involved in the bacterial pathogenicity and bacteria-bacteria competition. Here, we show that EHEC could secrete a novel effector KatN, a Mn-containing catalase, in a T6SS-dependent manner. Expression of katN is promoted by RpoS and OxyR and repressed by H-NS, and katN contributes to bacterial growth under oxidative stress in vitro. KatN could be secreted into host cell cytosol after EHEC is phagocytized by macrophage, which leads to decreased level of intracellular reactive oxygen species (ROS) and facilitates the intramacrophage survival of EHEC. Finally, animal model results show that the deletion mutant of T6SS was attenuated in virulence compared with the wild type strain, while the deletion mutant of katN had comparable virulence to the wild type strain. Taken together, our findings suggest that EHEC could sense oxidative stress in phagosome and decrease the host cell ROS by secreting catalase KatN to facilitate its survival in the host cells. |
doi_str_mv | 10.1371/journal.ppat.1006246 |
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The type VI secretion system (T6SS) has been shown to be involved in the bacterial pathogenicity and bacteria-bacteria competition. Here, we show that EHEC could secrete a novel effector KatN, a Mn-containing catalase, in a T6SS-dependent manner. Expression of katN is promoted by RpoS and OxyR and repressed by H-NS, and katN contributes to bacterial growth under oxidative stress in vitro. KatN could be secreted into host cell cytosol after EHEC is phagocytized by macrophage, which leads to decreased level of intracellular reactive oxygen species (ROS) and facilitates the intramacrophage survival of EHEC. Finally, animal model results show that the deletion mutant of T6SS was attenuated in virulence compared with the wild type strain, while the deletion mutant of katN had comparable virulence to the wild type strain. Taken together, our findings suggest that EHEC could sense oxidative stress in phagosome and decrease the host cell ROS by secreting catalase KatN to facilitate its survival in the host cells.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1006246</identifier><identifier>PMID: 28288207</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acetylation ; Adhesion ; Alkyl hydroperoxide reductase ; Animal models ; Animals ; Antiinfectives and antibacterials ; Attenuation ; Bacteria ; BASIC (programming language) ; Biochemistry ; Biology and Life Sciences ; Biotechnology ; Blotting, Western ; Catalase ; Catalase - secretion ; Cell survival ; Clonal deletion ; Colitis ; Colonization ; Competition ; Cullin ; Cytoplasm ; Cytosol ; Data acquisition ; Data collection ; Deletion mutant ; Deoxyribonucleic acid ; Diarrhea ; Digestive tract ; Disease Models, Animal ; Dissection ; DNA ; Drug dosages ; E coli ; Engineering ; Enterohemorrhagic Escherichia coli - metabolism ; Enterohemorrhagic Escherichia coli - pathogenicity ; Escherichia coli ; Escherichia coli Infections - metabolism ; Escherichia coli Infections - microbiology ; Escherichia coli Proteins - secretion ; Fermentation ; Flow Cytometry ; Fluorescent Antibody Technique ; Foodborne pathogens ; Gastrointestinal tract ; Gene expression ; Grants ; Hemorrhage ; Hospitals ; Host-Pathogen Interactions - physiology ; Hydrogen peroxide ; Immunoglobulins ; Immunology ; Inactivation ; Infections ; Infectious diseases ; Institutions ; Intestine ; Laboratories ; Life sciences ; Macromolecules ; Macrophages ; Medicine ; Medicine and Health Sciences ; Metabolism ; Mice ; Mice, Inbred BALB C ; Microbiology ; Microorganisms ; Modulation ; Oxidative stress ; Oxygen ; Pathogenesis ; Pathogenicity ; Pathogens ; Peroxidase ; Polyamines ; R&D ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Real-Time Polymerase Chain Reaction ; Research & development ; Research and Analysis Methods ; Rodents ; Salmonella ; Survival ; Type VI Secretion Systems - metabolism ; Type VI Secretion Systems - secretion ; Virulence (Microbiology) ; Virulence - physiology</subject><ispartof>PLoS pathogens, 2017-03, Vol.13 (3), p.e1006246-e1006246</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. 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: virulence by secreting catalase against host reactive oxygen species (ROS). PLoS Pathog 13(3): e1006246. https://doi.org/10.1371/journal.ppat.1006246</rights><rights>2017 Wan et al 2017 Wan et al</rights><rights>2017 Public Library of Science. 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: virulence by secreting catalase against host reactive oxygen species (ROS). PLoS Pathog 13(3): e1006246. https://doi.org/10.1371/journal.ppat.1006246</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c661t-a0c343af598ead77718ae0126f6061ae65c5133f929838d4faf2e6ef9132ad313</citedby><cites>FETCH-LOGICAL-c661t-a0c343af598ead77718ae0126f6061ae65c5133f929838d4faf2e6ef9132ad313</cites><orcidid>0000-0003-1783-4696 ; 0000-0002-3290-5889 ; 0000-0003-0849-3797</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/PMC5363993/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5363993/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28288207$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wan, Baoshan</creatorcontrib><creatorcontrib>Zhang, Qiufen</creatorcontrib><creatorcontrib>Ni, Jinjing</creatorcontrib><creatorcontrib>Li, Shuxian</creatorcontrib><creatorcontrib>Wen, Donghua</creatorcontrib><creatorcontrib>Li, Jun</creatorcontrib><creatorcontrib>Xiao, Haihan</creatorcontrib><creatorcontrib>He, Ping</creatorcontrib><creatorcontrib>Ou, Hong-Yu</creatorcontrib><creatorcontrib>Tao, Jing</creatorcontrib><creatorcontrib>Teng, Qihui</creatorcontrib><creatorcontrib>Lu, Jie</creatorcontrib><creatorcontrib>Wu, Wenjuan</creatorcontrib><creatorcontrib>Yao, Yu-Feng</creatorcontrib><title>Type VI secretion system contributes to Enterohemorrhagic Escherichia coli virulence by secreting catalase against host reactive oxygen species (ROS)</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Enterohemorrhagic Escherichia coli (EHEC) is one major type of contagious and foodborne pathogens. The type VI secretion system (T6SS) has been shown to be involved in the bacterial pathogenicity and bacteria-bacteria competition. Here, we show that EHEC could secrete a novel effector KatN, a Mn-containing catalase, in a T6SS-dependent manner. Expression of katN is promoted by RpoS and OxyR and repressed by H-NS, and katN contributes to bacterial growth under oxidative stress in vitro. KatN could be secreted into host cell cytosol after EHEC is phagocytized by macrophage, which leads to decreased level of intracellular reactive oxygen species (ROS) and facilitates the intramacrophage survival of EHEC. Finally, animal model results show that the deletion mutant of T6SS was attenuated in virulence compared with the wild type strain, while the deletion mutant of katN had comparable virulence to the wild type strain. Taken together, our findings suggest that EHEC could sense oxidative stress in phagosome and decrease the host cell ROS by secreting catalase KatN to facilitate its survival in the host cells.</description><subject>Acetylation</subject><subject>Adhesion</subject><subject>Alkyl hydroperoxide reductase</subject><subject>Animal models</subject><subject>Animals</subject><subject>Antiinfectives and antibacterials</subject><subject>Attenuation</subject><subject>Bacteria</subject><subject>BASIC (programming language)</subject><subject>Biochemistry</subject><subject>Biology and Life Sciences</subject><subject>Biotechnology</subject><subject>Blotting, Western</subject><subject>Catalase</subject><subject>Catalase - secretion</subject><subject>Cell survival</subject><subject>Clonal deletion</subject><subject>Colitis</subject><subject>Colonization</subject><subject>Competition</subject><subject>Cullin</subject><subject>Cytoplasm</subject><subject>Cytosol</subject><subject>Data acquisition</subject><subject>Data collection</subject><subject>Deletion mutant</subject><subject>Deoxyribonucleic acid</subject><subject>Diarrhea</subject><subject>Digestive tract</subject><subject>Disease Models, Animal</subject><subject>Dissection</subject><subject>DNA</subject><subject>Drug dosages</subject><subject>E coli</subject><subject>Engineering</subject><subject>Enterohemorrhagic Escherichia coli - metabolism</subject><subject>Enterohemorrhagic Escherichia coli - pathogenicity</subject><subject>Escherichia coli</subject><subject>Escherichia coli Infections - metabolism</subject><subject>Escherichia coli Infections - microbiology</subject><subject>Escherichia coli Proteins - secretion</subject><subject>Fermentation</subject><subject>Flow Cytometry</subject><subject>Fluorescent Antibody Technique</subject><subject>Foodborne pathogens</subject><subject>Gastrointestinal tract</subject><subject>Gene expression</subject><subject>Grants</subject><subject>Hemorrhage</subject><subject>Hospitals</subject><subject>Host-Pathogen Interactions - physiology</subject><subject>Hydrogen peroxide</subject><subject>Immunoglobulins</subject><subject>Immunology</subject><subject>Inactivation</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Institutions</subject><subject>Intestine</subject><subject>Laboratories</subject><subject>Life sciences</subject><subject>Macromolecules</subject><subject>Macrophages</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbiology</subject><subject>Microorganisms</subject><subject>Modulation</subject><subject>Oxidative stress</subject><subject>Oxygen</subject><subject>Pathogenesis</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Peroxidase</subject><subject>Polyamines</subject><subject>R&D</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>Research & development</subject><subject>Research and Analysis Methods</subject><subject>Rodents</subject><subject>Salmonella</subject><subject>Survival</subject><subject>Type VI Secretion Systems - metabolism</subject><subject>Type VI Secretion Systems - secretion</subject><subject>Virulence (Microbiology)</subject><subject>Virulence - physiology</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk9Fq2zAUhs3YWLtubzA2wW7ai2SSZUvyzaCUbguUFdput-JEPnJUHCuT5NI8yN53SpuWZvRmGGQjfef_fX50iuI9o1PGJft87ccwQD9drSBNGaWirMSLYp_VNZ9ILquXT773ijcxXlNaMc7E62KvVKVSJZX7xZ-r9QrJrxmJaAIm5wcS1zHhkhg_pODmY8JIkienQ8LgF7j0ISygc4acRrPA4MzCQYZ7R25cGHscDJL5-kFv6IiBBD1EJNCBG2IiC5-XgGCSu0Hib9cdZtcVGpetDi_OL4_eFq8s9BHfbd8Hxc-vp1cn3ydn599mJ8dnEyMESxOghlccbN0ohFZKyRQgZaWwggoGKGpTM85tUzaKq7ayYEsUaBvGS2g54wfFx3vdVe-j3iYaNWsoZaJUosnE7J5oPVzrVXBLCGvtwem7DR86DSE506OuFbD2zoo31bySjWyorVBaqqypcaP1Zes2zpfYGswBQ78junsyuIXu_I2uueBNw7PA4VYg-N8jxqSXLhrsexjQj_m_lZR1WascykHx6R_0-e62VAe5ATdYn33NRlQfVw1XTNSyzNT0GSo_LS5dviZoXd7fKTjaKdhcJbxNHYwx6tnlxX-wP3bZ6p41wccY0D5mx6jeDMVDk3ozFHo7FLnsw9PcH4sepoD_BS-qCeo</recordid><startdate>20170301</startdate><enddate>20170301</enddate><creator>Wan, Baoshan</creator><creator>Zhang, Qiufen</creator><creator>Ni, Jinjing</creator><creator>Li, Shuxian</creator><creator>Wen, Donghua</creator><creator>Li, Jun</creator><creator>Xiao, Haihan</creator><creator>He, Ping</creator><creator>Ou, Hong-Yu</creator><creator>Tao, Jing</creator><creator>Teng, Qihui</creator><creator>Lu, Jie</creator><creator>Wu, Wenjuan</creator><creator>Yao, Yu-Feng</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-1783-4696</orcidid><orcidid>https://orcid.org/0000-0002-3290-5889</orcidid><orcidid>https://orcid.org/0000-0003-0849-3797</orcidid></search><sort><creationdate>20170301</creationdate><title>Type VI secretion system contributes to Enterohemorrhagic Escherichia coli virulence by secreting catalase against host reactive oxygen species (ROS)</title><author>Wan, Baoshan ; Zhang, Qiufen ; Ni, Jinjing ; Li, Shuxian ; Wen, Donghua ; Li, Jun ; Xiao, Haihan ; He, Ping ; Ou, Hong-Yu ; Tao, Jing ; Teng, Qihui ; Lu, Jie ; Wu, Wenjuan ; Yao, Yu-Feng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c661t-a0c343af598ead77718ae0126f6061ae65c5133f929838d4faf2e6ef9132ad313</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Acetylation</topic><topic>Adhesion</topic><topic>Alkyl hydroperoxide reductase</topic><topic>Animal models</topic><topic>Animals</topic><topic>Antiinfectives and antibacterials</topic><topic>Attenuation</topic><topic>Bacteria</topic><topic>BASIC (programming language)</topic><topic>Biochemistry</topic><topic>Biology and Life Sciences</topic><topic>Biotechnology</topic><topic>Blotting, Western</topic><topic>Catalase</topic><topic>Catalase - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Open Access: DOAJ - Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wan, Baoshan</au><au>Zhang, Qiufen</au><au>Ni, Jinjing</au><au>Li, Shuxian</au><au>Wen, Donghua</au><au>Li, Jun</au><au>Xiao, Haihan</au><au>He, Ping</au><au>Ou, Hong-Yu</au><au>Tao, Jing</au><au>Teng, Qihui</au><au>Lu, Jie</au><au>Wu, Wenjuan</au><au>Yao, Yu-Feng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Type VI secretion system contributes to Enterohemorrhagic Escherichia coli virulence by secreting catalase against host reactive oxygen species (ROS)</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2017-03-01</date><risdate>2017</risdate><volume>13</volume><issue>3</issue><spage>e1006246</spage><epage>e1006246</epage><pages>e1006246-e1006246</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Enterohemorrhagic Escherichia coli (EHEC) is one major type of contagious and foodborne pathogens. The type VI secretion system (T6SS) has been shown to be involved in the bacterial pathogenicity and bacteria-bacteria competition. Here, we show that EHEC could secrete a novel effector KatN, a Mn-containing catalase, in a T6SS-dependent manner. Expression of katN is promoted by RpoS and OxyR and repressed by H-NS, and katN contributes to bacterial growth under oxidative stress in vitro. KatN could be secreted into host cell cytosol after EHEC is phagocytized by macrophage, which leads to decreased level of intracellular reactive oxygen species (ROS) and facilitates the intramacrophage survival of EHEC. Finally, animal model results show that the deletion mutant of T6SS was attenuated in virulence compared with the wild type strain, while the deletion mutant of katN had comparable virulence to the wild type strain. Taken together, our findings suggest that EHEC could sense oxidative stress in phagosome and decrease the host cell ROS by secreting catalase KatN to facilitate its survival in the host cells.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28288207</pmid><doi>10.1371/journal.ppat.1006246</doi><orcidid>https://orcid.org/0000-0003-1783-4696</orcidid><orcidid>https://orcid.org/0000-0002-3290-5889</orcidid><orcidid>https://orcid.org/0000-0003-0849-3797</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1553-7374 |
ispartof | PLoS pathogens, 2017-03, Vol.13 (3), p.e1006246-e1006246 |
issn | 1553-7374 1553-7366 1553-7374 |
language | eng |
recordid | cdi_plos_journals_1900162869 |
source | Open Access: DOAJ - Directory of Open Access Journals; Open Access: PubMed Central; PLoS; MEDLINE; Free E-Journal (出版社公開部分のみ); PubMed Central Open Access |
subjects | Acetylation Adhesion Alkyl hydroperoxide reductase Animal models Animals Antiinfectives and antibacterials Attenuation Bacteria BASIC (programming language) Biochemistry Biology and Life Sciences Biotechnology Blotting, Western Catalase Catalase - secretion Cell survival Clonal deletion Colitis Colonization Competition Cullin Cytoplasm Cytosol Data acquisition Data collection Deletion mutant Deoxyribonucleic acid Diarrhea Digestive tract Disease Models, Animal Dissection DNA Drug dosages E coli Engineering Enterohemorrhagic Escherichia coli - metabolism Enterohemorrhagic Escherichia coli - pathogenicity Escherichia coli Escherichia coli Infections - metabolism Escherichia coli Infections - microbiology Escherichia coli Proteins - secretion Fermentation Flow Cytometry Fluorescent Antibody Technique Foodborne pathogens Gastrointestinal tract Gene expression Grants Hemorrhage Hospitals Host-Pathogen Interactions - physiology Hydrogen peroxide Immunoglobulins Immunology Inactivation Infections Infectious diseases Institutions Intestine Laboratories Life sciences Macromolecules Macrophages Medicine Medicine and Health Sciences Metabolism Mice Mice, Inbred BALB C Microbiology Microorganisms Modulation Oxidative stress Oxygen Pathogenesis Pathogenicity Pathogens Peroxidase Polyamines R&D Reactive oxygen species Reactive Oxygen Species - metabolism Real-Time Polymerase Chain Reaction Research & development Research and Analysis Methods Rodents Salmonella Survival Type VI Secretion Systems - metabolism Type VI Secretion Systems - secretion Virulence (Microbiology) Virulence - physiology |
title | Type VI secretion system contributes to Enterohemorrhagic Escherichia coli virulence by secreting catalase against host reactive oxygen species (ROS) |
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