2‐Methylcitrate cycle: a well‐regulated controller of Bacillus sporulation
Summary Bacillus thuringiensis is the most widely used eco‐friendly biopesticide, containing two primary determinants of biocontrol, endospore and insecticidal crystal proteins (ICPs). The 2‐methylcitrate cycle is a widespread carbon metabolic pathway playing a crucial role in channelling propionyl‐...
Gespeichert in:
| Veröffentlicht in: | Environmental microbiology 2020-03, Vol.22 (3), p.1125-1140 |
|---|---|
| Hauptverfasser: | , , , , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 1140 |
|---|---|
| container_issue | 3 |
| container_start_page | 1125 |
| container_title | Environmental microbiology |
| container_volume | 22 |
| creator | Zheng, Cao Yu, Zhaoqing Du, Cuiying Gong, Yujing Yin, Wen Li, Xinfeng Li, Zhou Römling, Ute Chou, Shan‐Ho He, Jin |
| description | Summary
Bacillus thuringiensis is the most widely used eco‐friendly biopesticide, containing two primary determinants of biocontrol, endospore and insecticidal crystal proteins (ICPs). The 2‐methylcitrate cycle is a widespread carbon metabolic pathway playing a crucial role in channelling propionyl‐CoA, but with poorly understood metabolic regulatory mechanisms. Here, we dissect the transcriptional regulation of the 2‐methylcitrate cycle operon prpCDB and report its unprecedented role in controlling the sporulation process of B. thuringiensis. We found that the transcriptional activity of the prp operon encoding the three critical enzymes PrpC, PrpD, and PrpB in the 2‐methylcitrate cycle was negatively regulated by the two global transcription factors CcpA and AbrB, while positively regulated by the LysR family regulator CcpC, which jointly account for the fact that the 2‐methylcitrate cycle is specifically and highly active in the stationary phase of growth. We also found that the prpD mutant accumulated 2‐methylcitrate, the intermediate metabolite of the 2‐methylcitrate cycle, which delayed and inhibited sporulation at the early stage. Thus, our results not only revealed sophisticated transcriptional regulatory mechanisms for the metabolic 2‐methylcitrate cycle but also identified 2‐methylcitrate as a novel regulator of sporulation in B. thuringiensis. |
| doi_str_mv | 10.1111/1462-2920.14901 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_swepu</sourceid><recordid>TN_cdi_swepub_primary_oai_swepub_ki_se_474753</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2329738295</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4091-d75a1797af4924fd43f2e28f2756276e2799df75d02e8daa50efa8014129e8343</originalsourceid><addsrcrecordid>eNqFkcGO0zAQhi0Eot2FMzcUictesrXHThxzY6tdqNTCBc6Wm4whxa2LnajqjUfgGXkSHNLNgQu-zHjm868Z_4S8YvSWpbNgooQcFKSrUJQ9IfOp8nTKGczIVYw7Spnkkj4nM86qoirLak4-wu-fvzbYfTu7uu2C6TCrz7XDt5nJTuhc6gb82rvUaLLaH7rgncOQeZvdmbp1ro9ZPPowEK0_vCDPrHERX17iNfnycP95-SFff3q_Wr5b57WgiuWNLAyTShorFAjbCG4BobIgixJkiSCVaqwsGgpYNcYUFK2pKBMMFFZc8GuSj7rxhMd-q4-h3Ztw1t60-lL6njLUQgpZ8MTfjPwx-B89xk7v21in_cwBfR81cFCSV6CKhL75B935PhzSNokqFStB8DJRi5Gqg48xoJ1GYFQP1ujh8_VghP5rTXrx-qLbb_fYTPyjFwkoRuDUOjz_T0_fb1aj8B8qZ5ky</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2369162436</pqid></control><display><type>article</type><title>2‐Methylcitrate cycle: a well‐regulated controller of Bacillus sporulation</title><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><creator>Zheng, Cao ; Yu, Zhaoqing ; Du, Cuiying ; Gong, Yujing ; Yin, Wen ; Li, Xinfeng ; Li, Zhou ; Römling, Ute ; Chou, Shan‐Ho ; He, Jin</creator><creatorcontrib>Zheng, Cao ; Yu, Zhaoqing ; Du, Cuiying ; Gong, Yujing ; Yin, Wen ; Li, Xinfeng ; Li, Zhou ; Römling, Ute ; Chou, Shan‐Ho ; He, Jin</creatorcontrib><description>Summary
Bacillus thuringiensis is the most widely used eco‐friendly biopesticide, containing two primary determinants of biocontrol, endospore and insecticidal crystal proteins (ICPs). The 2‐methylcitrate cycle is a widespread carbon metabolic pathway playing a crucial role in channelling propionyl‐CoA, but with poorly understood metabolic regulatory mechanisms. Here, we dissect the transcriptional regulation of the 2‐methylcitrate cycle operon prpCDB and report its unprecedented role in controlling the sporulation process of B. thuringiensis. We found that the transcriptional activity of the prp operon encoding the three critical enzymes PrpC, PrpD, and PrpB in the 2‐methylcitrate cycle was negatively regulated by the two global transcription factors CcpA and AbrB, while positively regulated by the LysR family regulator CcpC, which jointly account for the fact that the 2‐methylcitrate cycle is specifically and highly active in the stationary phase of growth. We also found that the prpD mutant accumulated 2‐methylcitrate, the intermediate metabolite of the 2‐methylcitrate cycle, which delayed and inhibited sporulation at the early stage. Thus, our results not only revealed sophisticated transcriptional regulatory mechanisms for the metabolic 2‐methylcitrate cycle but also identified 2‐methylcitrate as a novel regulator of sporulation in B. thuringiensis.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.14901</identifier><identifier>PMID: 31858668</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Acyl Coenzyme A - metabolism ; Bacillus thuringiensis - enzymology ; Bacillus thuringiensis - genetics ; Bacillus thuringiensis - growth & development ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biological control ; Biopesticides ; Channeling ; Citrates - metabolism ; Crystal proteins ; Gene Expression Regulation, Bacterial - genetics ; Gene regulation ; Hydro-Lyases - genetics ; Insecticides ; Metabolic Networks and Pathways - genetics ; Metabolic pathways ; Metabolism ; Metabolites ; Mutants ; Operon - genetics ; Pesticides ; Regulatory mechanisms (biology) ; Spores, Bacterial - genetics ; Spores, Bacterial - growth & development ; Sporulation ; Stationary phase ; Transcription ; Transcription factors ; Transcription Factors - genetics</subject><ispartof>Environmental microbiology, 2020-03, Vol.22 (3), p.1125-1140</ispartof><rights>2019 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2020 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4091-d75a1797af4924fd43f2e28f2756276e2799df75d02e8daa50efa8014129e8343</citedby><cites>FETCH-LOGICAL-c4091-d75a1797af4924fd43f2e28f2756276e2799df75d02e8daa50efa8014129e8343</cites><orcidid>0000-0002-1456-8284</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%2F1462-2920.14901$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.14901$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,777,781,882,1412,27905,27906,45555,45556</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31858668$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:142589366$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Zheng, Cao</creatorcontrib><creatorcontrib>Yu, Zhaoqing</creatorcontrib><creatorcontrib>Du, Cuiying</creatorcontrib><creatorcontrib>Gong, Yujing</creatorcontrib><creatorcontrib>Yin, Wen</creatorcontrib><creatorcontrib>Li, Xinfeng</creatorcontrib><creatorcontrib>Li, Zhou</creatorcontrib><creatorcontrib>Römling, Ute</creatorcontrib><creatorcontrib>Chou, Shan‐Ho</creatorcontrib><creatorcontrib>He, Jin</creatorcontrib><title>2‐Methylcitrate cycle: a well‐regulated controller of Bacillus sporulation</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Bacillus thuringiensis is the most widely used eco‐friendly biopesticide, containing two primary determinants of biocontrol, endospore and insecticidal crystal proteins (ICPs). The 2‐methylcitrate cycle is a widespread carbon metabolic pathway playing a crucial role in channelling propionyl‐CoA, but with poorly understood metabolic regulatory mechanisms. Here, we dissect the transcriptional regulation of the 2‐methylcitrate cycle operon prpCDB and report its unprecedented role in controlling the sporulation process of B. thuringiensis. We found that the transcriptional activity of the prp operon encoding the three critical enzymes PrpC, PrpD, and PrpB in the 2‐methylcitrate cycle was negatively regulated by the two global transcription factors CcpA and AbrB, while positively regulated by the LysR family regulator CcpC, which jointly account for the fact that the 2‐methylcitrate cycle is specifically and highly active in the stationary phase of growth. We also found that the prpD mutant accumulated 2‐methylcitrate, the intermediate metabolite of the 2‐methylcitrate cycle, which delayed and inhibited sporulation at the early stage. Thus, our results not only revealed sophisticated transcriptional regulatory mechanisms for the metabolic 2‐methylcitrate cycle but also identified 2‐methylcitrate as a novel regulator of sporulation in B. thuringiensis.</description><subject>Acyl Coenzyme A - metabolism</subject><subject>Bacillus thuringiensis - enzymology</subject><subject>Bacillus thuringiensis - genetics</subject><subject>Bacillus thuringiensis - growth & development</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biological control</subject><subject>Biopesticides</subject><subject>Channeling</subject><subject>Citrates - metabolism</subject><subject>Crystal proteins</subject><subject>Gene Expression Regulation, Bacterial - genetics</subject><subject>Gene regulation</subject><subject>Hydro-Lyases - genetics</subject><subject>Insecticides</subject><subject>Metabolic Networks and Pathways - genetics</subject><subject>Metabolic pathways</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Mutants</subject><subject>Operon - genetics</subject><subject>Pesticides</subject><subject>Regulatory mechanisms (biology)</subject><subject>Spores, Bacterial - genetics</subject><subject>Spores, Bacterial - growth & development</subject><subject>Sporulation</subject><subject>Stationary phase</subject><subject>Transcription</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkcGO0zAQhi0Eot2FMzcUictesrXHThxzY6tdqNTCBc6Wm4whxa2LnajqjUfgGXkSHNLNgQu-zHjm868Z_4S8YvSWpbNgooQcFKSrUJQ9IfOp8nTKGczIVYw7Spnkkj4nM86qoirLak4-wu-fvzbYfTu7uu2C6TCrz7XDt5nJTuhc6gb82rvUaLLaH7rgncOQeZvdmbp1ro9ZPPowEK0_vCDPrHERX17iNfnycP95-SFff3q_Wr5b57WgiuWNLAyTShorFAjbCG4BobIgixJkiSCVaqwsGgpYNcYUFK2pKBMMFFZc8GuSj7rxhMd-q4-h3Ztw1t60-lL6njLUQgpZ8MTfjPwx-B89xk7v21in_cwBfR81cFCSV6CKhL75B935PhzSNokqFStB8DJRi5Gqg48xoJ1GYFQP1ujh8_VghP5rTXrx-qLbb_fYTPyjFwkoRuDUOjz_T0_fb1aj8B8qZ5ky</recordid><startdate>202003</startdate><enddate>202003</enddate><creator>Zheng, Cao</creator><creator>Yu, Zhaoqing</creator><creator>Du, Cuiying</creator><creator>Gong, Yujing</creator><creator>Yin, Wen</creator><creator>Li, Xinfeng</creator><creator>Li, Zhou</creator><creator>Römling, Ute</creator><creator>Chou, Shan‐Ho</creator><creator>He, Jin</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</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>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>ADTPV</scope><scope>AOWAS</scope><orcidid>https://orcid.org/0000-0002-1456-8284</orcidid></search><sort><creationdate>202003</creationdate><title>2‐Methylcitrate cycle: a well‐regulated controller of Bacillus sporulation</title><author>Zheng, Cao ; Yu, Zhaoqing ; Du, Cuiying ; Gong, Yujing ; Yin, Wen ; Li, Xinfeng ; Li, Zhou ; Römling, Ute ; Chou, Shan‐Ho ; He, Jin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4091-d75a1797af4924fd43f2e28f2756276e2799df75d02e8daa50efa8014129e8343</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Acyl Coenzyme A - metabolism</topic><topic>Bacillus thuringiensis - enzymology</topic><topic>Bacillus thuringiensis - genetics</topic><topic>Bacillus thuringiensis - growth & development</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biological control</topic><topic>Biopesticides</topic><topic>Channeling</topic><topic>Citrates - metabolism</topic><topic>Crystal proteins</topic><topic>Gene Expression Regulation, Bacterial - genetics</topic><topic>Gene regulation</topic><topic>Hydro-Lyases - genetics</topic><topic>Insecticides</topic><topic>Metabolic Networks and Pathways - genetics</topic><topic>Metabolic pathways</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Mutants</topic><topic>Operon - genetics</topic><topic>Pesticides</topic><topic>Regulatory mechanisms (biology)</topic><topic>Spores, Bacterial - genetics</topic><topic>Spores, Bacterial - growth & development</topic><topic>Sporulation</topic><topic>Stationary phase</topic><topic>Transcription</topic><topic>Transcription factors</topic><topic>Transcription Factors - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zheng, Cao</creatorcontrib><creatorcontrib>Yu, Zhaoqing</creatorcontrib><creatorcontrib>Du, Cuiying</creatorcontrib><creatorcontrib>Gong, Yujing</creatorcontrib><creatorcontrib>Yin, Wen</creatorcontrib><creatorcontrib>Li, Xinfeng</creatorcontrib><creatorcontrib>Li, Zhou</creatorcontrib><creatorcontrib>Römling, Ute</creatorcontrib><creatorcontrib>Chou, Shan‐Ho</creatorcontrib><creatorcontrib>He, Jin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</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>SwePub</collection><collection>SwePub Articles</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zheng, Cao</au><au>Yu, Zhaoqing</au><au>Du, Cuiying</au><au>Gong, Yujing</au><au>Yin, Wen</au><au>Li, Xinfeng</au><au>Li, Zhou</au><au>Römling, Ute</au><au>Chou, Shan‐Ho</au><au>He, Jin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>2‐Methylcitrate cycle: a well‐regulated controller of Bacillus sporulation</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2020-03</date><risdate>2020</risdate><volume>22</volume><issue>3</issue><spage>1125</spage><epage>1140</epage><pages>1125-1140</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Bacillus thuringiensis is the most widely used eco‐friendly biopesticide, containing two primary determinants of biocontrol, endospore and insecticidal crystal proteins (ICPs). The 2‐methylcitrate cycle is a widespread carbon metabolic pathway playing a crucial role in channelling propionyl‐CoA, but with poorly understood metabolic regulatory mechanisms. Here, we dissect the transcriptional regulation of the 2‐methylcitrate cycle operon prpCDB and report its unprecedented role in controlling the sporulation process of B. thuringiensis. We found that the transcriptional activity of the prp operon encoding the three critical enzymes PrpC, PrpD, and PrpB in the 2‐methylcitrate cycle was negatively regulated by the two global transcription factors CcpA and AbrB, while positively regulated by the LysR family regulator CcpC, which jointly account for the fact that the 2‐methylcitrate cycle is specifically and highly active in the stationary phase of growth. We also found that the prpD mutant accumulated 2‐methylcitrate, the intermediate metabolite of the 2‐methylcitrate cycle, which delayed and inhibited sporulation at the early stage. Thus, our results not only revealed sophisticated transcriptional regulatory mechanisms for the metabolic 2‐methylcitrate cycle but also identified 2‐methylcitrate as a novel regulator of sporulation in B. thuringiensis.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>31858668</pmid><doi>10.1111/1462-2920.14901</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-1456-8284</orcidid></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1462-2912 |
| ispartof | Environmental microbiology, 2020-03, Vol.22 (3), p.1125-1140 |
| issn | 1462-2912 1462-2920 |
| language | eng |
| recordid | cdi_swepub_primary_oai_swepub_ki_se_474753 |
| source | MEDLINE; Wiley Online Library Journals Frontfile Complete |
| subjects | Acyl Coenzyme A - metabolism Bacillus thuringiensis - enzymology Bacillus thuringiensis - genetics Bacillus thuringiensis - growth & development Bacterial Proteins - genetics Bacterial Proteins - metabolism Biological control Biopesticides Channeling Citrates - metabolism Crystal proteins Gene Expression Regulation, Bacterial - genetics Gene regulation Hydro-Lyases - genetics Insecticides Metabolic Networks and Pathways - genetics Metabolic pathways Metabolism Metabolites Mutants Operon - genetics Pesticides Regulatory mechanisms (biology) Spores, Bacterial - genetics Spores, Bacterial - growth & development Sporulation Stationary phase Transcription Transcription factors Transcription Factors - genetics |
| title | 2‐Methylcitrate cycle: a well‐regulated controller of Bacillus sporulation |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-20T23%3A53%3A56IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_swepu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=2%E2%80%90Methylcitrate%20cycle:%20a%20well%E2%80%90regulated%20controller%20of%20Bacillus%20sporulation&rft.jtitle=Environmental%20microbiology&rft.au=Zheng,%20Cao&rft.date=2020-03&rft.volume=22&rft.issue=3&rft.spage=1125&rft.epage=1140&rft.pages=1125-1140&rft.issn=1462-2912&rft.eissn=1462-2920&rft_id=info:doi/10.1111/1462-2920.14901&rft_dat=%3Cproquest_swepu%3E2329738295%3C/proquest_swepu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2369162436&rft_id=info:pmid/31858668&rfr_iscdi=true |