Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli
Abstract Although protein acetylation is widely observed, it has been associated with few specific regulatory functions making it poorly understood. To interrogate its functionality, we analyzed the acetylome in Escherichia coli knockout mutants of cobB, the only known sirtuin‐like deacetylase, and...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Springer Nature
2014-11-01
|
| Series: | Molecular Systems Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.15252/msb.20145227 |
| _version_ | 1827014814501699584 |
|---|---|
| author | Sara Castaño‐Cerezo Vicente Bernal Harm Post Tobias Fuhrer Salvatore Cappadona Nerea C Sánchez‐Díaz Uwe Sauer Albert JR Heck AF Maarten Altelaar Manuel Cánovas |
| author_facet | Sara Castaño‐Cerezo Vicente Bernal Harm Post Tobias Fuhrer Salvatore Cappadona Nerea C Sánchez‐Díaz Uwe Sauer Albert JR Heck AF Maarten Altelaar Manuel Cánovas |
| author_sort | Sara Castaño‐Cerezo |
| collection | DOAJ |
| description | Abstract Although protein acetylation is widely observed, it has been associated with few specific regulatory functions making it poorly understood. To interrogate its functionality, we analyzed the acetylome in Escherichia coli knockout mutants of cobB, the only known sirtuin‐like deacetylase, and patZ, the best‐known protein acetyltransferase. For four growth conditions, more than 2,000 unique acetylated peptides, belonging to 809 proteins, were identified and differentially quantified. Nearly 65% of these proteins are related to metabolism. The global activity of CobB contributes to the deacetylation of a large number of substrates and has a major impact on physiology. Apart from the regulation of acetyl‐CoA synthetase, we found that CobB‐controlled acetylation of isocitrate lyase contributes to the fine‐tuning of the glyoxylate shunt. Acetylation of the transcription factor RcsB prevents DNA binding, activating flagella biosynthesis and motility, and increases acid stress susceptibility. Surprisingly, deletion of patZ increased acetylation in acetate cultures, which suggests that it regulates the levels of acetylating agents. The results presented offer new insights into functional roles of protein acetylation in metabolic fitness and global cell regulation. |
| first_indexed | 2024-03-07T16:31:14Z |
| format | Article |
| id | doaj.art-176e2742f27b43909f37379e99f8da6d |
| institution | Directory Open Access Journal |
| issn | 1744-4292 |
| language | English |
| last_indexed | 2025-02-18T14:14:00Z |
| publishDate | 2014-11-01 |
| publisher | Springer Nature |
| record_format | Article |
| series | Molecular Systems Biology |
| spelling | doaj.art-176e2742f27b43909f37379e99f8da6d2024-10-28T09:20:37ZengSpringer NatureMolecular Systems Biology1744-42922014-11-01101111510.15252/msb.20145227Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coliSara Castaño‐Cerezo0Vicente Bernal1Harm Post2Tobias Fuhrer3Salvatore Cappadona4Nerea C Sánchez‐Díaz5Uwe Sauer6Albert JR Heck7AF Maarten Altelaar8Manuel Cánovas9Departamento de Bioquímica y Biología Molecular B e Inmunología, Facultad de Química, Universidad de Murcia, Campus de Excelencia Mare NostrumDepartamento de Bioquímica y Biología Molecular B e Inmunología, Facultad de Química, Universidad de Murcia, Campus de Excelencia Mare NostrumBiomolecular Mass Spectrometry and Proteomics Group, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht UniversityInstitute of Molecular Systems Biology, ETH ZurichBiomolecular Mass Spectrometry and Proteomics Group, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht UniversityDepartamento de Bioquímica y Biología Molecular B e Inmunología, Facultad de Química, Universidad de Murcia, Campus de Excelencia Mare NostrumInstitute of Molecular Systems Biology, ETH ZurichBiomolecular Mass Spectrometry and Proteomics Group, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht UniversityBiomolecular Mass Spectrometry and Proteomics Group, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht UniversityDepartamento de Bioquímica y Biología Molecular B e Inmunología, Facultad de Química, Universidad de Murcia, Campus de Excelencia Mare NostrumAbstract Although protein acetylation is widely observed, it has been associated with few specific regulatory functions making it poorly understood. To interrogate its functionality, we analyzed the acetylome in Escherichia coli knockout mutants of cobB, the only known sirtuin‐like deacetylase, and patZ, the best‐known protein acetyltransferase. For four growth conditions, more than 2,000 unique acetylated peptides, belonging to 809 proteins, were identified and differentially quantified. Nearly 65% of these proteins are related to metabolism. The global activity of CobB contributes to the deacetylation of a large number of substrates and has a major impact on physiology. Apart from the regulation of acetyl‐CoA synthetase, we found that CobB‐controlled acetylation of isocitrate lyase contributes to the fine‐tuning of the glyoxylate shunt. Acetylation of the transcription factor RcsB prevents DNA binding, activating flagella biosynthesis and motility, and increases acid stress susceptibility. Surprisingly, deletion of patZ increased acetylation in acetate cultures, which suggests that it regulates the levels of acetylating agents. The results presented offer new insights into functional roles of protein acetylation in metabolic fitness and global cell regulation.https://doi.org/10.15252/msb.20145227flagella biosynthesisisocitrate lyasemetabolic regulationsirtuin |
| spellingShingle | Sara Castaño‐Cerezo Vicente Bernal Harm Post Tobias Fuhrer Salvatore Cappadona Nerea C Sánchez‐Díaz Uwe Sauer Albert JR Heck AF Maarten Altelaar Manuel Cánovas Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli Molecular Systems Biology flagella biosynthesis isocitrate lyase metabolic regulation sirtuin |
| title | Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli |
| title_full | Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli |
| title_fullStr | Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli |
| title_full_unstemmed | Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli |
| title_short | Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli |
| title_sort | protein acetylation affects acetate metabolism motility and acid stress response in escherichia coli |
| topic | flagella biosynthesis isocitrate lyase metabolic regulation sirtuin |
| url | https://doi.org/10.15252/msb.20145227 |
| work_keys_str_mv | AT saracastanocerezo proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT vicentebernal proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT harmpost proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT tobiasfuhrer proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT salvatorecappadona proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT nereacsanchezdiaz proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT uwesauer proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT albertjrheck proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT afmaartenaltelaar proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli AT manuelcanovas proteinacetylationaffectsacetatemetabolismmotilityandacidstressresponseinescherichiacoli |