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Spo0A links de novo fatty acid synthesis to sporulation and biofilm development in Bacillus subtilis
Summary During sporulation in Bacillus subtilis, the committed‐cell undergoes substantial membrane rearrangements to generate two cells of different sizes and fates: the mother cell and the forespore. Here, we demonstrate that the master transcription factor Spo0A reactivates lipid synthesis during...
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Published in: | Molecular microbiology 2013-01, Vol.87 (2), p.348-367 |
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creator | Pedrido, María E. Oña, Paula Ramirez, Walter Leñini, Cecilia Goñi, Anibal Grau, Roberto |
description | Summary
During sporulation in Bacillus subtilis, the committed‐cell undergoes substantial membrane rearrangements to generate two cells of different sizes and fates: the mother cell and the forespore. Here, we demonstrate that the master transcription factor Spo0A reactivates lipid synthesis during development. Maximal Spo0A‐dependent lipid synthesis occurs during the key stages of asymmetric division and forespore engulfment. Spo0A reactivates the accDA operon that encodes the carboxylase component of the acetyl‐CoA carboxylase enzyme, which catalyses the first and rate‐limiting step in de novo lipid biosynthesis, malonyl‐CoA formation. The disruption of the Spo0A‐binding box in the promoter region of accDA impairs its transcriptional reactivation and blocks lipid synthesis. The Spo0A‐insensitive accDA0A cells were proficient in planktonic growth but defective in sporulation (σE activation) and biofilm development (cell cluster formation and water repellency). Exogenous fatty acid supplementation to accDA0A cells overcomes their inability to synthesize lipids during development and restores sporulation and biofilm proficiencies. The transient exclusion of the lipid synthesis regulon from the forespore and the known compartmentalization of Spo0A and ACP in the mother cell suggest that de novo lipid synthesis is confined to the mother cell. The significance of the Spo0A‐controlled de novo lipid synthesis during B. subtilis development is discussed. |
doi_str_mv | 10.1111/mmi.12102 |
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During sporulation in Bacillus subtilis, the committed‐cell undergoes substantial membrane rearrangements to generate two cells of different sizes and fates: the mother cell and the forespore. Here, we demonstrate that the master transcription factor Spo0A reactivates lipid synthesis during development. Maximal Spo0A‐dependent lipid synthesis occurs during the key stages of asymmetric division and forespore engulfment. Spo0A reactivates the accDA operon that encodes the carboxylase component of the acetyl‐CoA carboxylase enzyme, which catalyses the first and rate‐limiting step in de novo lipid biosynthesis, malonyl‐CoA formation. The disruption of the Spo0A‐binding box in the promoter region of accDA impairs its transcriptional reactivation and blocks lipid synthesis. The Spo0A‐insensitive accDA0A cells were proficient in planktonic growth but defective in sporulation (σE activation) and biofilm development (cell cluster formation and water repellency). Exogenous fatty acid supplementation to accDA0A cells overcomes their inability to synthesize lipids during development and restores sporulation and biofilm proficiencies. The transient exclusion of the lipid synthesis regulon from the forespore and the known compartmentalization of Spo0A and ACP in the mother cell suggest that de novo lipid synthesis is confined to the mother cell. The significance of the Spo0A‐controlled de novo lipid synthesis during B. subtilis development is discussed.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.12102</identifier><identifier>PMID: 23170957</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Bacillus subtilis ; Bacillus subtilis - growth & development ; Bacillus subtilis - metabolism ; Bacterial Proteins - metabolism ; Biofilms ; Biofilms - growth & development ; Biosynthesis ; Cells ; Fatty acids ; Fatty Acids - biosynthesis ; Gene Expression Regulation, Bacterial ; Lipids ; Plankton ; Probiotics ; Spores, Bacterial - growth & development ; Spores, Bacterial - metabolism ; Transcription Factors - metabolism</subject><ispartof>Molecular microbiology, 2013-01, Vol.87 (2), p.348-367</ispartof><rights>2012 Blackwell Publishing Ltd</rights><rights>2012 Blackwell Publishing Ltd.</rights><rights>Copyright Blackwell Publishing Ltd. Jan 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23170957$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pedrido, María E.</creatorcontrib><creatorcontrib>Oña, Paula</creatorcontrib><creatorcontrib>Ramirez, Walter</creatorcontrib><creatorcontrib>Leñini, Cecilia</creatorcontrib><creatorcontrib>Goñi, Anibal</creatorcontrib><creatorcontrib>Grau, Roberto</creatorcontrib><title>Spo0A links de novo fatty acid synthesis to sporulation and biofilm development in Bacillus subtilis</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
During sporulation in Bacillus subtilis, the committed‐cell undergoes substantial membrane rearrangements to generate two cells of different sizes and fates: the mother cell and the forespore. Here, we demonstrate that the master transcription factor Spo0A reactivates lipid synthesis during development. Maximal Spo0A‐dependent lipid synthesis occurs during the key stages of asymmetric division and forespore engulfment. Spo0A reactivates the accDA operon that encodes the carboxylase component of the acetyl‐CoA carboxylase enzyme, which catalyses the first and rate‐limiting step in de novo lipid biosynthesis, malonyl‐CoA formation. The disruption of the Spo0A‐binding box in the promoter region of accDA impairs its transcriptional reactivation and blocks lipid synthesis. The Spo0A‐insensitive accDA0A cells were proficient in planktonic growth but defective in sporulation (σE activation) and biofilm development (cell cluster formation and water repellency). Exogenous fatty acid supplementation to accDA0A cells overcomes their inability to synthesize lipids during development and restores sporulation and biofilm proficiencies. The transient exclusion of the lipid synthesis regulon from the forespore and the known compartmentalization of Spo0A and ACP in the mother cell suggest that de novo lipid synthesis is confined to the mother cell. The significance of the Spo0A‐controlled de novo lipid synthesis during B. subtilis development is discussed.</description><subject>Bacillus subtilis</subject><subject>Bacillus subtilis - growth & development</subject><subject>Bacillus subtilis - metabolism</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biofilms</subject><subject>Biofilms - growth & development</subject><subject>Biosynthesis</subject><subject>Cells</subject><subject>Fatty acids</subject><subject>Fatty Acids - biosynthesis</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Lipids</subject><subject>Plankton</subject><subject>Probiotics</subject><subject>Spores, Bacterial - growth & development</subject><subject>Spores, Bacterial - metabolism</subject><subject>Transcription Factors - metabolism</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqFkUtLxTAQhYMoen0s_AMScOOm3iTTNOlSL75AcaGCu5I2KUbTpDatcv-98fpYuHE2M3C-MzBzENqn5JimmnedPaaMEraGZhQKnrGSy3U0IyUnGUj2uIW2Y3wmhAIpYBNtMaAiiWKG9F0fyAl21r9ErA324S3gVo3jEqvGahyXfnwy0UY8Bhz7MExOjTZ4rLzGtQ2tdV3yvRkX-s74EVuPT5PTuSniONWjdTbuoo1WuWj2vvsOejg_u19cZte3F1eLk-ush1ywDHRDC2Aiz1XdKEVzw2jbQCFzTTmUHDjIQuRKaiiMkqWphWy5ZMLopgbVwA46-trbD-F1MnGsOhsb45zyJkyxosBAEpZL8T_KBHDChMwTevgHfQ7T4NMhiSpKTjkpWKIOvqmp7oyu-sF2alhWP69OwPwLeLfOLH91SqrPDKuUYbXKsLq5uVoN8AEmeo1N</recordid><startdate>201301</startdate><enddate>201301</enddate><creator>Pedrido, María E.</creator><creator>Oña, Paula</creator><creator>Ramirez, Walter</creator><creator>Leñini, Cecilia</creator><creator>Goñi, Anibal</creator><creator>Grau, Roberto</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope></search><sort><creationdate>201301</creationdate><title>Spo0A links de novo fatty acid synthesis to sporulation and biofilm development in Bacillus subtilis</title><author>Pedrido, María E. ; Oña, Paula ; Ramirez, Walter ; Leñini, Cecilia ; Goñi, Anibal ; Grau, Roberto</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p3472-3dc1632744abcaa14e21fc3684d153953538674a8d36ea89eb78f5827edcb3ac3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Bacillus subtilis</topic><topic>Bacillus subtilis - growth & development</topic><topic>Bacillus subtilis - metabolism</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biofilms</topic><topic>Biofilms - growth & development</topic><topic>Biosynthesis</topic><topic>Cells</topic><topic>Fatty acids</topic><topic>Fatty Acids - biosynthesis</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Lipids</topic><topic>Plankton</topic><topic>Probiotics</topic><topic>Spores, Bacterial - growth & development</topic><topic>Spores, Bacterial - metabolism</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pedrido, María E.</creatorcontrib><creatorcontrib>Oña, Paula</creatorcontrib><creatorcontrib>Ramirez, Walter</creatorcontrib><creatorcontrib>Leñini, Cecilia</creatorcontrib><creatorcontrib>Goñi, Anibal</creatorcontrib><creatorcontrib>Grau, Roberto</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pedrido, María E.</au><au>Oña, Paula</au><au>Ramirez, Walter</au><au>Leñini, Cecilia</au><au>Goñi, Anibal</au><au>Grau, Roberto</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Spo0A links de novo fatty acid synthesis to sporulation and biofilm development in Bacillus subtilis</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2013-01</date><risdate>2013</risdate><volume>87</volume><issue>2</issue><spage>348</spage><epage>367</epage><pages>348-367</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
During sporulation in Bacillus subtilis, the committed‐cell undergoes substantial membrane rearrangements to generate two cells of different sizes and fates: the mother cell and the forespore. Here, we demonstrate that the master transcription factor Spo0A reactivates lipid synthesis during development. Maximal Spo0A‐dependent lipid synthesis occurs during the key stages of asymmetric division and forespore engulfment. Spo0A reactivates the accDA operon that encodes the carboxylase component of the acetyl‐CoA carboxylase enzyme, which catalyses the first and rate‐limiting step in de novo lipid biosynthesis, malonyl‐CoA formation. The disruption of the Spo0A‐binding box in the promoter region of accDA impairs its transcriptional reactivation and blocks lipid synthesis. The Spo0A‐insensitive accDA0A cells were proficient in planktonic growth but defective in sporulation (σE activation) and biofilm development (cell cluster formation and water repellency). Exogenous fatty acid supplementation to accDA0A cells overcomes their inability to synthesize lipids during development and restores sporulation and biofilm proficiencies. The transient exclusion of the lipid synthesis regulon from the forespore and the known compartmentalization of Spo0A and ACP in the mother cell suggest that de novo lipid synthesis is confined to the mother cell. The significance of the Spo0A‐controlled de novo lipid synthesis during B. subtilis development is discussed.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>23170957</pmid><doi>10.1111/mmi.12102</doi><tpages>20</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Bacillus subtilis Bacillus subtilis - growth & development Bacillus subtilis - metabolism Bacterial Proteins - metabolism Biofilms Biofilms - growth & development Biosynthesis Cells Fatty acids Fatty Acids - biosynthesis Gene Expression Regulation, Bacterial Lipids Plankton Probiotics Spores, Bacterial - growth & development Spores, Bacterial - metabolism Transcription Factors - metabolism |
title | Spo0A links de novo fatty acid synthesis to sporulation and biofilm development in Bacillus subtilis |
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