The virulome of Streptomyces scabiei in response to cello-oligosaccharide elicitors
The development of spots or lesions symptomatic of common scab on root and tuber crops is caused by few pathogenic with 87-22 as the model species. Thaxtomin phytotoxins are the primary virulence determinants, mainly acting by impairing cellulose synthesis, and their production in is in turn boosted...
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creator | Deflandre, Benoit Stulanovic, Nudzejma Planckaert, Sören Anderssen, Sinaeda Bonometti, Beatrice Karim, Latifa Coppieters, Wouter Devreese, Bart Rigali, Sébastien |
description | The development of spots or lesions symptomatic of common scab on root and tuber crops is caused by few pathogenic
with
87-22 as the model species. Thaxtomin phytotoxins are the primary virulence determinants, mainly acting by impairing cellulose synthesis, and their production in
is in turn boosted by cello-oligosaccharides released from host plants. In this work we aimed to determine which molecules and which biosynthetic gene clusters (BGCs) of the specialized metabolism of
87-22 show a production and/or a transcriptional response to cello-oligosaccharides. Comparative metabolomic analyses revealed that molecules of the virulome of
induced by cellobiose and cellotriose include (i) thaxtomin and concanamycin phytotoxins, (ii) desferrioxamines, scabichelin and turgichelin siderophores in order to acquire iron essential for housekeeping functions, (iii) ectoine for protection against osmotic shock once inside the host, and (iv) bottromycin and concanamycin antimicrobials possibly to prevent other microorganisms from colonizing the same niche. Importantly, both cello-oligosaccharides reduced the production of the spore germination inhibitors germicidins thereby giving the 'green light' to escape dormancy and trigger the onset of the pathogenic lifestyle. For most metabolites - either with induced or reduced production - cellotriose was revealed to be a slightly stronger elicitor compared to cellobiose, supporting an earlier hypothesis which suggested the trisaccharide was the real trigger for virulence released from the plant cell wall through the action of thaxtomins. Interestingly, except for thaxtomins, none of these BGCs' expression seems to be under direct control of the cellulose utilization repressor CebR suggesting the existence of a yet unknown mechanism for switching on the virulome. Finally, a transcriptomic analysis revealed nine additional cryptic BGCs that have their expression awakened by cello-oligosaccharides, suggesting that other and yet to be discovered metabolites could be part of the virulome of
. |
doi_str_mv | 10.1099/mgen.0.000760 |
format | Article |
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with
87-22 as the model species. Thaxtomin phytotoxins are the primary virulence determinants, mainly acting by impairing cellulose synthesis, and their production in
is in turn boosted by cello-oligosaccharides released from host plants. In this work we aimed to determine which molecules and which biosynthetic gene clusters (BGCs) of the specialized metabolism of
87-22 show a production and/or a transcriptional response to cello-oligosaccharides. Comparative metabolomic analyses revealed that molecules of the virulome of
induced by cellobiose and cellotriose include (i) thaxtomin and concanamycin phytotoxins, (ii) desferrioxamines, scabichelin and turgichelin siderophores in order to acquire iron essential for housekeeping functions, (iii) ectoine for protection against osmotic shock once inside the host, and (iv) bottromycin and concanamycin antimicrobials possibly to prevent other microorganisms from colonizing the same niche. Importantly, both cello-oligosaccharides reduced the production of the spore germination inhibitors germicidins thereby giving the 'green light' to escape dormancy and trigger the onset of the pathogenic lifestyle. For most metabolites - either with induced or reduced production - cellotriose was revealed to be a slightly stronger elicitor compared to cellobiose, supporting an earlier hypothesis which suggested the trisaccharide was the real trigger for virulence released from the plant cell wall through the action of thaxtomins. Interestingly, except for thaxtomins, none of these BGCs' expression seems to be under direct control of the cellulose utilization repressor CebR suggesting the existence of a yet unknown mechanism for switching on the virulome. Finally, a transcriptomic analysis revealed nine additional cryptic BGCs that have their expression awakened by cello-oligosaccharides, suggesting that other and yet to be discovered metabolites could be part of the virulome of
.</description><identifier>ISSN: 2057-5858</identifier><identifier>EISSN: 2057-5858</identifier><identifier>DOI: 10.1099/mgen.0.000760</identifier><identifier>PMID: 35040428</identifier><language>eng</language><publisher>England: Microbiology Society</publisher><subject>Biosynthetic Pathways - drug effects ; Cellobiose - pharmacology ; Cellulose - pharmacology ; Gene Expression Profiling ; Gene Expression Regulation, Bacterial - drug effects ; Life sciences ; Macrolides - metabolism ; Metabolomics ; Microbiologie ; Microbiology ; Multigene Family - drug effects ; Piperazines - metabolism ; Plant Tubers - growth & development ; Plant Tubers - microbiology ; RNA-Seq ; Sciences du vivant ; Streptomyces - drug effects ; Streptomyces - growth & development ; Streptomyces - metabolism ; Streptomyces - pathogenicity ; Trioses - pharmacology ; Virulence Factors - metabolism</subject><ispartof>Microbial genomics, 2022-01, Vol.8 (1)</ispartof><rights>2022 The Authors 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c431t-ab0eeac7f2e13f873289a124c25ec45667a55e93d500ff26f6d410d8c86ec30e3</citedby><cites>FETCH-LOGICAL-c431t-ab0eeac7f2e13f873289a124c25ec45667a55e93d500ff26f6d410d8c86ec30e3</cites><orcidid>0000-0003-4022-7325 ; 0000-0002-4337-9028 ; 0000-0003-0965-357X ; 0000-0001-6426-541X ; 0000-0002-9764-2581 ; 0000-0001-8109-7825 ; 0000-0003-3243-4973</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/PMC8914351/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8914351/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35040428$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Deflandre, Benoit</creatorcontrib><creatorcontrib>Stulanovic, Nudzejma</creatorcontrib><creatorcontrib>Planckaert, Sören</creatorcontrib><creatorcontrib>Anderssen, Sinaeda</creatorcontrib><creatorcontrib>Bonometti, Beatrice</creatorcontrib><creatorcontrib>Karim, Latifa</creatorcontrib><creatorcontrib>Coppieters, Wouter</creatorcontrib><creatorcontrib>Devreese, Bart</creatorcontrib><creatorcontrib>Rigali, Sébastien</creatorcontrib><title>The virulome of Streptomyces scabiei in response to cello-oligosaccharide elicitors</title><title>Microbial genomics</title><addtitle>Microb Genom</addtitle><description>The development of spots or lesions symptomatic of common scab on root and tuber crops is caused by few pathogenic
with
87-22 as the model species. Thaxtomin phytotoxins are the primary virulence determinants, mainly acting by impairing cellulose synthesis, and their production in
is in turn boosted by cello-oligosaccharides released from host plants. In this work we aimed to determine which molecules and which biosynthetic gene clusters (BGCs) of the specialized metabolism of
87-22 show a production and/or a transcriptional response to cello-oligosaccharides. Comparative metabolomic analyses revealed that molecules of the virulome of
induced by cellobiose and cellotriose include (i) thaxtomin and concanamycin phytotoxins, (ii) desferrioxamines, scabichelin and turgichelin siderophores in order to acquire iron essential for housekeeping functions, (iii) ectoine for protection against osmotic shock once inside the host, and (iv) bottromycin and concanamycin antimicrobials possibly to prevent other microorganisms from colonizing the same niche. Importantly, both cello-oligosaccharides reduced the production of the spore germination inhibitors germicidins thereby giving the 'green light' to escape dormancy and trigger the onset of the pathogenic lifestyle. For most metabolites - either with induced or reduced production - cellotriose was revealed to be a slightly stronger elicitor compared to cellobiose, supporting an earlier hypothesis which suggested the trisaccharide was the real trigger for virulence released from the plant cell wall through the action of thaxtomins. Interestingly, except for thaxtomins, none of these BGCs' expression seems to be under direct control of the cellulose utilization repressor CebR suggesting the existence of a yet unknown mechanism for switching on the virulome. Finally, a transcriptomic analysis revealed nine additional cryptic BGCs that have their expression awakened by cello-oligosaccharides, suggesting that other and yet to be discovered metabolites could be part of the virulome of
.</description><subject>Biosynthetic Pathways - drug effects</subject><subject>Cellobiose - pharmacology</subject><subject>Cellulose - pharmacology</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Bacterial - drug effects</subject><subject>Life sciences</subject><subject>Macrolides - metabolism</subject><subject>Metabolomics</subject><subject>Microbiologie</subject><subject>Microbiology</subject><subject>Multigene Family - drug effects</subject><subject>Piperazines - metabolism</subject><subject>Plant Tubers - growth & development</subject><subject>Plant Tubers - microbiology</subject><subject>RNA-Seq</subject><subject>Sciences du vivant</subject><subject>Streptomyces - drug effects</subject><subject>Streptomyces - growth & development</subject><subject>Streptomyces - metabolism</subject><subject>Streptomyces - pathogenicity</subject><subject>Trioses - pharmacology</subject><subject>Virulence Factors - metabolism</subject><issn>2057-5858</issn><issn>2057-5858</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkc9L5TAQx4O4qLge9yo5eulzkjRpehFE1BWEPeieQ5pO-yJp80zaB_739vlccU8zMJ_5zo8vIb8YrBjU9eXQ47iCFQBUCg7ICQdZFVJLffgtPyZnOb8sDJNa1ZU8IsdCQgkl1yfk6XmNdOvTHOKANHb0aUq4meLw5jDT7Gzj0VM_0oR5E8eMdIrUYQixiMH3MVvn1jb5FikG7_wUU_5JfnQ2ZDz7jKfk793t883v4vHP_cPN9WPhSsGmwjaAaF3VcWSi05XguraMl45LdKVUqrJSYi1aCdB1XHWqLRm02mmFTgCKU3K1193MzYCtw3FKNphN8oNNbyZab_6vjH5t-rg1umalkGwREHuB4LFHE1PjzZZ_NH7kc-iNdaZBw7nShqvlfXrpuvgcm-LrjHkyg8-7l9gR45wXjDNgWgu5oMUedSnmnLD7Wo6B2Tlodg4aMHsHF_78-0Vf9D-_xDuPmJkR</recordid><startdate>20220101</startdate><enddate>20220101</enddate><creator>Deflandre, Benoit</creator><creator>Stulanovic, Nudzejma</creator><creator>Planckaert, Sören</creator><creator>Anderssen, Sinaeda</creator><creator>Bonometti, Beatrice</creator><creator>Karim, Latifa</creator><creator>Coppieters, Wouter</creator><creator>Devreese, Bart</creator><creator>Rigali, Sébastien</creator><general>Microbiology Society</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>7X8</scope><scope>Q33</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4022-7325</orcidid><orcidid>https://orcid.org/0000-0002-4337-9028</orcidid><orcidid>https://orcid.org/0000-0003-0965-357X</orcidid><orcidid>https://orcid.org/0000-0001-6426-541X</orcidid><orcidid>https://orcid.org/0000-0002-9764-2581</orcidid><orcidid>https://orcid.org/0000-0001-8109-7825</orcidid><orcidid>https://orcid.org/0000-0003-3243-4973</orcidid></search><sort><creationdate>20220101</creationdate><title>The virulome of Streptomyces scabiei in response to cello-oligosaccharide elicitors</title><author>Deflandre, Benoit ; Stulanovic, Nudzejma ; Planckaert, Sören ; Anderssen, Sinaeda ; Bonometti, Beatrice ; Karim, Latifa ; Coppieters, Wouter ; Devreese, Bart ; Rigali, Sébastien</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c431t-ab0eeac7f2e13f873289a124c25ec45667a55e93d500ff26f6d410d8c86ec30e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Biosynthetic Pathways - drug effects</topic><topic>Cellobiose - pharmacology</topic><topic>Cellulose - pharmacology</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Bacterial - drug effects</topic><topic>Life sciences</topic><topic>Macrolides - metabolism</topic><topic>Metabolomics</topic><topic>Microbiologie</topic><topic>Microbiology</topic><topic>Multigene Family - drug effects</topic><topic>Piperazines - metabolism</topic><topic>Plant Tubers - growth & development</topic><topic>Plant Tubers - microbiology</topic><topic>RNA-Seq</topic><topic>Sciences du vivant</topic><topic>Streptomyces - drug effects</topic><topic>Streptomyces - growth & development</topic><topic>Streptomyces - metabolism</topic><topic>Streptomyces - pathogenicity</topic><topic>Trioses - pharmacology</topic><topic>Virulence Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Deflandre, Benoit</creatorcontrib><creatorcontrib>Stulanovic, Nudzejma</creatorcontrib><creatorcontrib>Planckaert, Sören</creatorcontrib><creatorcontrib>Anderssen, Sinaeda</creatorcontrib><creatorcontrib>Bonometti, Beatrice</creatorcontrib><creatorcontrib>Karim, Latifa</creatorcontrib><creatorcontrib>Coppieters, Wouter</creatorcontrib><creatorcontrib>Devreese, Bart</creatorcontrib><creatorcontrib>Rigali, Sébastien</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Université de Liège - Open Repository and Bibliography (ORBI)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Microbial genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Deflandre, Benoit</au><au>Stulanovic, Nudzejma</au><au>Planckaert, Sören</au><au>Anderssen, Sinaeda</au><au>Bonometti, Beatrice</au><au>Karim, Latifa</au><au>Coppieters, Wouter</au><au>Devreese, Bart</au><au>Rigali, Sébastien</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The virulome of Streptomyces scabiei in response to cello-oligosaccharide elicitors</atitle><jtitle>Microbial genomics</jtitle><addtitle>Microb Genom</addtitle><date>2022-01-01</date><risdate>2022</risdate><volume>8</volume><issue>1</issue><issn>2057-5858</issn><eissn>2057-5858</eissn><abstract>The development of spots or lesions symptomatic of common scab on root and tuber crops is caused by few pathogenic
with
87-22 as the model species. Thaxtomin phytotoxins are the primary virulence determinants, mainly acting by impairing cellulose synthesis, and their production in
is in turn boosted by cello-oligosaccharides released from host plants. In this work we aimed to determine which molecules and which biosynthetic gene clusters (BGCs) of the specialized metabolism of
87-22 show a production and/or a transcriptional response to cello-oligosaccharides. Comparative metabolomic analyses revealed that molecules of the virulome of
induced by cellobiose and cellotriose include (i) thaxtomin and concanamycin phytotoxins, (ii) desferrioxamines, scabichelin and turgichelin siderophores in order to acquire iron essential for housekeeping functions, (iii) ectoine for protection against osmotic shock once inside the host, and (iv) bottromycin and concanamycin antimicrobials possibly to prevent other microorganisms from colonizing the same niche. Importantly, both cello-oligosaccharides reduced the production of the spore germination inhibitors germicidins thereby giving the 'green light' to escape dormancy and trigger the onset of the pathogenic lifestyle. For most metabolites - either with induced or reduced production - cellotriose was revealed to be a slightly stronger elicitor compared to cellobiose, supporting an earlier hypothesis which suggested the trisaccharide was the real trigger for virulence released from the plant cell wall through the action of thaxtomins. Interestingly, except for thaxtomins, none of these BGCs' expression seems to be under direct control of the cellulose utilization repressor CebR suggesting the existence of a yet unknown mechanism for switching on the virulome. Finally, a transcriptomic analysis revealed nine additional cryptic BGCs that have their expression awakened by cello-oligosaccharides, suggesting that other and yet to be discovered metabolites could be part of the virulome of
.</abstract><cop>England</cop><pub>Microbiology Society</pub><pmid>35040428</pmid><doi>10.1099/mgen.0.000760</doi><orcidid>https://orcid.org/0000-0003-4022-7325</orcidid><orcidid>https://orcid.org/0000-0002-4337-9028</orcidid><orcidid>https://orcid.org/0000-0003-0965-357X</orcidid><orcidid>https://orcid.org/0000-0001-6426-541X</orcidid><orcidid>https://orcid.org/0000-0002-9764-2581</orcidid><orcidid>https://orcid.org/0000-0001-8109-7825</orcidid><orcidid>https://orcid.org/0000-0003-3243-4973</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biosynthetic Pathways - drug effects Cellobiose - pharmacology Cellulose - pharmacology Gene Expression Profiling Gene Expression Regulation, Bacterial - drug effects Life sciences Macrolides - metabolism Metabolomics Microbiologie Microbiology Multigene Family - drug effects Piperazines - metabolism Plant Tubers - growth & development Plant Tubers - microbiology RNA-Seq Sciences du vivant Streptomyces - drug effects Streptomyces - growth & development Streptomyces - metabolism Streptomyces - pathogenicity Trioses - pharmacology Virulence Factors - metabolism |
title | The virulome of Streptomyces scabiei in response to cello-oligosaccharide elicitors |
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