Agrobacterium tumefaciens Deploys a Versatile Antibacterial Strategy to Increase its Competitiveness.
Identifieur interne : 000247 ( Main/Exploration ); précédent : 000246; suivant : 000248Agrobacterium tumefaciens Deploys a Versatile Antibacterial Strategy to Increase its Competitiveness.
Auteurs : Manda Yu [Taïwan] ; Yi-Chieh Wang [Taïwan] ; Ching-Jou Huang [Taïwan] ; Lay-Sun Ma [Taïwan] ; Erh-Min Lai [Taïwan]Source :
- Journal of bacteriology [ 1098-5530 ] ; 2020.
Abstract
The Type VI secretion system (T6SS) is a widespread antibacterial weapon capable of secreting multiple effectors for inhibition of competitor cells. Most of the effectors in the system share the same purpose of target intoxication, but the rationale for maintaining various types of effectors in a species is not well studied. In this study, we showed that a peptidoglycan amidase effector in Agrobacterium tumefaciens, Tae, cleaves mDAP and D-Glu bonds in peptidoglycan, and is able to suppress the growth of Escherichia coli recipient cells. The growth suppression was only effective in the condition which E. coli cells are actively growing. In contrast, the Tde DNase effectors in the strain possessed a dominant killing effect under carbon starvation. Microscopic analysis showed that Tde triggers cell elongation and DNA degradation while Tae causes cell enlargement without DNA damage in E. coli recipient cells. In rich medium, A. tumefaciens harbouring only functional Tae was able to maintain competitiveness among E. coli and its own sibling cells. Growth suppression and the competitive advantage of A. tumefaciens was abrogated when recipient cells produce the Tae-specific immunity protein Tai. Given that Tae is highly conserved among A. tumefaciens strains, the combination of Tae and Tde effectors could allow A. tumefaciens to better compete with various competitors by increasing its survival during changing environmental conditions.IMPORTANCE The type VI secretion system (T6SS) encodes multiple effectors with diverse functions but little is known about the biological significance of harboring such a repertoire of effectors. We reported that the T6SS antibacterial activity of the plant pathogen Agrobacterium tumefaciens can be enhanced under carbon starvation or when recipient cell-wall peptidoglycan is disturbed. This led to a newly discovered role for the T6SS peptidoglycan amidase Tae effector in providing a growth advantage dependent on the growth status of the target cell. This is in contrast to the Tde DNase effectors that are dominant during carbon starvation. Our study suggests that combining Tae and other effectors could allow A. tumefaciens to increase its competitiveness among changing environmental conditions.
DOI: 10.1128/JB.00490-20
PubMed: 33168638
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Taipei, Taiwan.</nlm:affiliation><country xml:lang="fr">Taïwan</country><wicri:regionArea>Institute of Plant and Microbial Biology, Academia Sinica, Taipei</wicri:regionArea><wicri:noRegion>Taipei</wicri:noRegion></affiliation></author><author><name sortKey="Huang, Ching Jou" sort="Huang, Ching Jou" uniqKey="Huang C" first="Ching-Jou" last="Huang">Ching-Jou Huang</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan.</nlm:affiliation><country xml:lang="fr">Taïwan</country><wicri:regionArea>Institute of Plant and Microbial Biology, Academia Sinica, Taipei</wicri:regionArea><wicri:noRegion>Taipei</wicri:noRegion></affiliation></author><author><name sortKey="Ma, Lay Sun" sort="Ma, Lay Sun" uniqKey="Ma L" first="Lay-Sun" last="Ma">Lay-Sun Ma</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan.</nlm:affiliation><country xml:lang="fr">Taïwan</country><wicri:regionArea>Institute of Plant and Microbial Biology, Academia Sinica, Taipei</wicri:regionArea><wicri:noRegion>Taipei</wicri:noRegion></affiliation></author><author><name sortKey="Lai, Erh Min" sort="Lai, Erh Min" uniqKey="Lai E" first="Erh-Min" last="Lai">Erh-Min Lai</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan emlai@gate.sinica.edu.tw.</nlm:affiliation><country wicri:rule="url">Taïwan</country><wicri:regionArea>Institute of Plant and Microbial Biology, Academia Sinica, Taipei</wicri:regionArea><wicri:noRegion>Taipei</wicri:noRegion></affiliation></author></analytic><series><title level="j">Journal of bacteriology</title><idno type="eISSN">1098-5530</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The Type VI secretion system (T6SS) is a widespread antibacterial weapon capable of secreting multiple effectors for inhibition of competitor cells. Most of the effectors in the system share the same purpose of target intoxication, but the rationale for maintaining various types of effectors in a species is not well studied. In this study, we showed that a peptidoglycan amidase effector in <i>Agrobacterium tumefaciens</i>, Tae, cleaves mDAP and D-Glu bonds in peptidoglycan, and is able to suppress the growth of <i>Escherichia coli</i> recipient cells. The growth suppression was only effective in the condition which <i>E. coli</i> cells are actively growing. In contrast, the Tde DNase effectors in the strain possessed a dominant killing effect under carbon starvation. Microscopic analysis showed that Tde triggers cell elongation and DNA degradation while Tae causes cell enlargement without DNA damage in <i>E. coli</i> recipient cells. In rich medium, <i>A. tumefaciens</i> harbouring only functional Tae was able to maintain competitiveness among <i>E. coli</i> and its own sibling cells. Growth suppression and the competitive advantage of <i>A. tumefaciens</i> was abrogated when recipient cells produce the Tae-specific immunity protein Tai. Given that Tae is highly conserved among <i>A. tumefaciens</i> strains, the combination of Tae and Tde effectors could allow <i>A. tumefaciens</i> to better compete with various competitors by increasing its survival during changing environmental conditions.<b>IMPORTANCE</b> The type VI secretion system (T6SS) encodes multiple effectors with diverse functions but little is known about the biological significance of harboring such a repertoire of effectors. We reported that the T6SS antibacterial activity of the plant pathogen <i>Agrobacterium tumefaciens</i> can be enhanced under carbon starvation or when recipient cell-wall peptidoglycan is disturbed. This led to a newly discovered role for the T6SS peptidoglycan amidase Tae effector in providing a growth advantage dependent on the growth status of the target cell. This is in contrast to the Tde DNase effectors that are dominant during carbon starvation. Our study suggests that combining Tae and other effectors could allow <i>A. tumefaciens</i> to increase its competitiveness among changing environmental conditions.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33168638</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>10</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1098-5530</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Nov</Month><Day>09</Day></PubDate></JournalIssue><Title>Journal of bacteriology</Title><ISOAbbreviation>J Bacteriol</ISOAbbreviation></Journal><ArticleTitle><i>Agrobacterium tumefaciens</i> Deploys a Versatile Antibacterial Strategy to Increase its Competitiveness.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">JB.00490-20</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/JB.00490-20</ELocationID><Abstract><AbstractText>The Type VI secretion system (T6SS) is a widespread antibacterial weapon capable of secreting multiple effectors for inhibition of competitor cells. Most of the effectors in the system share the same purpose of target intoxication, but the rationale for maintaining various types of effectors in a species is not well studied. In this study, we showed that a peptidoglycan amidase effector in <i>Agrobacterium tumefaciens</i>, Tae, cleaves mDAP and D-Glu bonds in peptidoglycan, and is able to suppress the growth of <i>Escherichia coli</i> recipient cells. The growth suppression was only effective in the condition which <i>E. coli</i> cells are actively growing. In contrast, the Tde DNase effectors in the strain possessed a dominant killing effect under carbon starvation. Microscopic analysis showed that Tde triggers cell elongation and DNA degradation while Tae causes cell enlargement without DNA damage in <i>E. coli</i> recipient cells. In rich medium, <i>A. tumefaciens</i> harbouring only functional Tae was able to maintain competitiveness among <i>E. coli</i> and its own sibling cells. Growth suppression and the competitive advantage of <i>A. tumefaciens</i> was abrogated when recipient cells produce the Tae-specific immunity protein Tai. Given that Tae is highly conserved among <i>A. tumefaciens</i> strains, the combination of Tae and Tde effectors could allow <i>A. tumefaciens</i> to better compete with various competitors by increasing its survival during changing environmental conditions.<b>IMPORTANCE</b> The type VI secretion system (T6SS) encodes multiple effectors with diverse functions but little is known about the biological significance of harboring such a repertoire of effectors. We reported that the T6SS antibacterial activity of the plant pathogen <i>Agrobacterium tumefaciens</i> can be enhanced under carbon starvation or when recipient cell-wall peptidoglycan is disturbed. This led to a newly discovered role for the T6SS peptidoglycan amidase Tae effector in providing a growth advantage dependent on the growth status of the target cell. This is in contrast to the Tde DNase effectors that are dominant during carbon starvation. Our study suggests that combining Tae and other effectors could allow <i>A. tumefaciens</i> to increase its competitiveness among changing environmental conditions.</AbstractText><CopyrightInformation>Copyright © 2020 Yu et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Yu</LastName><ForeName>Manda</ForeName><Initials>M</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-5932-9597</Identifier><AffiliationInfo><Affiliation>Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yi-Chieh</ForeName><Initials>YC</Initials><AffiliationInfo><Affiliation>Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huang</LastName><ForeName>Ching-Jou</ForeName><Initials>CJ</Initials><AffiliationInfo><Affiliation>Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ma</LastName><ForeName>Lay-Sun</ForeName><Initials>LS</Initials><AffiliationInfo><Affiliation>Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lai</LastName><ForeName>Erh-Min</ForeName><Initials>EM</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-3630-8683</Identifier><AffiliationInfo><Affiliation>Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan emlai@gate.sinica.edu.tw.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>11</Month><Day>09</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Bacteriol</MedlineTA><NlmUniqueID>2985120R</NlmUniqueID><ISSNLinking>0021-9193</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>11</Month><Day>10</Day><Hour>5</Hour><Minute>38</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>11</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>11</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33168638</ArticleId><ArticleId IdType="pii">JB.00490-20</ArticleId><ArticleId IdType="doi">10.1128/JB.00490-20</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Taïwan</li></country></list><tree><country name="Taïwan"><noRegion><name sortKey="Yu, Manda" sort="Yu, Manda" uniqKey="Yu M" first="Manda" last="Yu">Manda Yu</name></noRegion><name sortKey="Huang, Ching Jou" sort="Huang, Ching Jou" uniqKey="Huang C" first="Ching-Jou" last="Huang">Ching-Jou Huang</name><name sortKey="Lai, Erh Min" sort="Lai, Erh Min" uniqKey="Lai E" first="Erh-Min" last="Lai">Erh-Min Lai</name><name sortKey="Ma, Lay Sun" sort="Ma, Lay Sun" uniqKey="Ma L" first="Lay-Sun" last="Ma">Lay-Sun Ma</name><name sortKey="Wang, Yi Chieh" sort="Wang, Yi Chieh" uniqKey="Wang Y" first="Yi-Chieh" last="Wang">Yi-Chieh Wang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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