Physiological roles of sigma factor SigD in Corynebacterium glutamicum
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
PubMed
28701150
PubMed Central
PMC5508688
DOI
10.1186/s12866-017-1067-6
PII: 10.1186/s12866-017-1067-6
Knihovny.cz E-zdroje
- Klíčová slova
- Corynebacterium glutamicum, Mycomembrane, SigD, Sigma factor, Trehalose dicorynomycolate,
- MeSH
- bakteriální proteiny genetika metabolismus MeSH
- Corynebacterium glutamicum genetika růst a vývoj metabolismus MeSH
- kyseliny mykolové metabolismus MeSH
- regulace genové exprese u bakterií MeSH
- sigma faktor genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- bakteriální proteiny MeSH
- corynomycolic acid MeSH Prohlížeč
- kyseliny mykolové MeSH
- sigma faktor MeSH
BACKGROUND: Sigma factors are one of the components of RNA polymerase holoenzymes, and an essential factor of transcription initiation in bacteria. Corynebacterium glutamicum possesses seven genes coding for sigma factors, most of which have been studied to some detail; however, the role of SigD in transcriptional regulation in C. glutamicum has been mostly unknown. RESULTS: In this work, pleiotropic effects of sigD overexpression at the level of phenotype, transcripts, proteins and metabolites were investigated. Overexpression of sigD decreased the growth rate of C. glutamicum cultures, and induced several physiological effects such as reduced culture foaming, turbid supernatant and cell aggregation. Upon overexpression of sigD, the level of Cmt1 (corynomycolyl transferase) in the supernatant was notably enhanced, and carbohydrate-containing compounds were excreted to the supernatant. The real-time PCR analysis revealed that sigD overexpression increased the expression of genes related to corynomycolic acid synthesis (fadD2, pks), genes encoding corynomycolyl transferases (cop1, cmt1, cmt2, cmt3), L, D-transpeptidase (lppS), a subunit of the major cell wall channel (porH), and the envelope lipid regulation factor (elrF). Furthermore, overexpression of sigD resulted in trehalose dicorynomycolate accumulation in the cell envelope. CONCLUSIONS: This study demonstrated that SigD regulates the synthesis of corynomycolate and related compounds, and expanded the knowledge of regulatory functions of sigma factors in C. glutamicum.
Center for Biotechnology Bielefeld University Bielefeld Germany
Genetics of Prokaryotes Faculty of Biology Bielefeld University Bielefeld Germany
Institute of Microbiology Academy of Sciences of the Czech Republic Prague Czech Republic
Proteome and Metabolome Research Faculty of Biology Bielefeld University Bielefeld Germany
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Feklístov A, Sharon BD, Darst SA, Gross CA. Bacterial sigma factors: a historical, structural, and genomic perspective. Annu Rev Microbiol. 2014;68:357–376. doi: 10.1146/annurev-micro-092412-155737. PubMed DOI
Rodrigue S, Provvedi R, Jacques P-E, Gaudreau L, Manganelli R. The sigma factors of Mycobacterium tuberculosis. FEMS Microbiol Rev. 2006;30:926–941. doi: 10.1111/j.1574-6976.2006.00040.x. PubMed DOI
Staroń A, Sofia HJ, Dietrich S, Ulrich LE, Liesegang H, Mascher T. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) σ factor protein family. Mol Microbiol. 2009;74:557–581. doi: 10.1111/j.1365-2958.2009.06870.x. PubMed DOI
Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A, Pigeonneau N. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science. 2012;335:1103–1106. doi: 10.1126/science.1206848. PubMed DOI
Cho B-K, Kim D, Knight EM, Zengler K, Palsson BO. Genome-scale reconstruction of the sigma factor network in Escherichia coli: topology and functional states. BMC Biol. 2014;12:4. doi: 10.1186/1741-7007-12-4. PubMed DOI PMC
Österberg S, Peso-Santos T de., and Shingler V. Regulation of alternative sigma factor use. Annu Rev Microbiol 2011;65:37–55. PubMed
Kinoshita S, Udaka S, Shimono M. Studies on the amino acid fermentation. J Gen Appl Microbiol. 1957;3:193–205. doi: 10.2323/jgam.3.193. PubMed DOI
Eggeling L, Bott M. Handbook of Corynebacterium glutamicum. FL, USA: CRC Press; 2005.
Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A. The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J Biotechnol. 2003;104:5–25. doi: 10.1016/S0168-1656(03)00154-8. PubMed DOI
Ikeda M, Nakagawa S. The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl Microbiol Biotechnol. 2003;62:99–109. doi: 10.1007/s00253-003-1328-1. PubMed DOI
Pátek M, Nešvera J. Sigma factors and promoters in Corynebacterium glutamicum. J Biotechnol. 2011;154:101–113. doi: 10.1016/j.jbiotec.2011.01.017. PubMed DOI
Barksdale L. Corynebacterium diphtheriae and its relatives. Bacteriol Rev. 1970;34:378–422. PubMed PMC
Lanéelle M-A, Tropis M, Daffé M. Current knowledge on mycolic acids in Corynebacterium glutamicum and their relevance for biotechnological processes. Appl Microbiol Biotechnol. 2013;97:9923–9930. doi: 10.1007/s00253-013-5265-3. PubMed DOI
Peters-Wendisch PG, Schiel B, Wendisch VF, Katsoulidis E, Möckel B, Sahm H. Pyruvate carboxylase is a major bottleneck for glutamate and lysine production by Corynebacterium glutamicum. J Mol Microbiol Biotechnol. 2001;3:295–300. PubMed
Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G, Pühler A. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene. 1994;145:69–73. doi: 10.1016/0378-1119(94)90324-7. PubMed DOI
Sambrook J. Molecular cloning: A laboratory manual. third. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2001.
Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6:343–345. doi: 10.1038/nmeth.1318. PubMed DOI
Nováková J, Izsáková A, Grivalský T, Ottmann C, Farkašovský M. Improved method for high-efficiency electrotransformation of Escherichia coli with the large BAC plasmids. Folia Microbiol (Praha) 2014;59:53–61. doi: 10.1007/s12223-013-0267-1. PubMed DOI
van der Rest ME, Lange C, Molenaar D. A heat shock following electroporation induces highly efficient transformation of Corynebacterium glutamicum with xenogeneic plasmid DNA. Appl Microbiol Biotechnol. 1999;52:541–545. doi: 10.1007/s002530051557. PubMed DOI
Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc. 2006;1:2856–2860. doi: 10.1038/nprot.2006.468. PubMed DOI
Musa YR, Bäsell K, Schatschneider S, Vorhölter F-J, Becher D, Niehaus K. Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach. J Biotechnol. 2013;167:111–122. doi: 10.1016/j.jbiotec.2013.06.009. PubMed DOI
Dallies N, François J, Paquet V. A new method for quantitative determination of polysaccharides in the yeast cell wall. Application to the cell wall defective mutants of Saccharomyces cerevisiae. Yeast. 1998;14:1297–1306. doi: 10.1002/(SICI)1097-0061(1998100)14:14<1297::AID-YEA310>3.0.CO;2-L. PubMed DOI
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28:350–356. doi: 10.1021/ac60111a017. DOI
Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S-I, Lee YC. Carbohydrate analysis by a phenol–sulfuric acid method in microplate format. Anal Biochem. 2005;339:69–72. doi: 10.1016/j.ab.2004.12.001. PubMed DOI
Hüser AT, Becker A, Brune I, Dondrup M, Kalinowski J, Plassmeier J. Development of a Corynebacterium glutamicum DNA microarray and validation by genome-wide expression profiling during growth with propionate as carbon source. J Biotechnol. 2003;106:269–286. doi: 10.1016/j.jbiotec.2003.08.006. PubMed DOI
Busche T, Winkler A, Wedderhoff I, Rückert C, Kalinowski J, Ortiz de Orué Lucana D. Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes. PLoS One. 2016;11 doi: 10.1371/journal.pone.0159873. PubMed DOI PMC
Blom J, Jakobi T, Doppmeier D, Jaenicke S, Kalinowski J, Stoye J, et al. Exact and complete short-read alignment to microbial genomes using Graphics Processing Unit programming. Bioinforma Oxf Engl. 2011;27:1351–1358. doi: 10.1093/bioinformatics/btr151. PubMed DOI
Pfeifer-Sancar K, Mentz A, Rückert C, Kalinowski J. Comprehensive analysis of the Corynebacterium glutamicum transcriptome using an improved RNAseq technique. BMC Genomics. 2013;14:888. doi: 10.1186/1471-2164-14-888. PubMed DOI PMC
Hilker R, Stadermann KB, Schwengers O, Anisiforov E, Jaenicke S, Weisshaar B, et al. ReadXplorer 2-detailed read mapping analysis and visualization from one single source. Bioinforma Oxf Engl. 2016;32:3702–3708. doi: 10.1093/bioinformatics/btw541. PubMed DOI PMC
Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:106. doi: 10.1186/gb-2010-11-10-r106. PubMed DOI PMC
Busche T, Silar R, Pičmanová M, Pátek M, Kalinowski J. Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum. BMC Genomics. 2012;13:445. doi: 10.1186/1471-2164-13-445. PubMed DOI PMC
Brand S, Niehaus K, Pühler A, Kalinowski J. Identification and functional analysis of six mycolyltransferase genes of Corynebacterium glutamicum ATCC 13032: the genes cop1, cmt1, and cmt2 can replace each other in the synthesis of trehalose dicorynomycolate, a component of the mycolic acid layer of the cell envelope. Arch Microbiol. 2003;180:33–44. doi: 10.1007/s00203-003-0556-1. PubMed DOI
Puech V, Bayan N, Salim K, Leblon G, Daffé M. Characterization of the in vivo acceptors of the mycoloyl residues transferred by the corynebacterial PS1 and the related mycobacterial antigens 85. Mol Microbiol. 2000;35:1026–1041. doi: 10.1046/j.1365-2958.2000.01738.x. PubMed DOI
Puech V, Chami M, Lemassu A, Lanéelle M-A, Schiffler B, Gounon P. Structure of the cell envelope of corynebacteria: importance of the non-covalently bound lipids in the formation of the cell wall permeability barrier and fracture plane. Microbiology. 2001;147:1365–1382. doi: 10.1099/00221287-147-5-1365. PubMed DOI
Nielsen SS. Food Analysis Laboratory Manual. Springer US: NY, USA; 2010.
Ikeda M, Baba M, Tsukumoto N, Komatsu T, Mitsuhashi S, Takeno S. Elucidation of genes relevant to the microaerobic growth of Corynebacterium glutamicum. Biosci Biotechnol Biochem. 2009;73:2806–2808. doi: 10.1271/bbb.90741. PubMed DOI
Taniguchi H, Wendisch VF. Exploring the role of sigma factor gene expression on production by Corynebacterium glutamicum: sigma factor H and FMN as example. Front Microbiol. 2015;6:740. doi: 10.3389/fmicb.2015.00740. PubMed DOI PMC
Taniguchi H, Henke NA, Heider SAE, Wendisch VF. Overexpression of the primary sigma factor gene sigA improved carotenoid production by Corynebacterium glutamicum: Application to production of β-carotene and the non-native linear C50 carotenoid bisanhydrobacterioruberin. Metab Eng Commun. 2017;4:1–11. doi: 10.1016/j.meteno.2017.01.001. PubMed DOI PMC
Gande R, Dover LG, Krumbach K, Besra GS, Sahm H, Oikawa T. The two carboxylases of Corynebacterium glutamicum essential for fatty acid and mycolic acid synthesis. J Bacteriol. 2007;189:5257–5264. doi: 10.1128/JB.00254-07. PubMed DOI PMC
Portevin D, de Sousa-D’Auria C, Montrozier H, Houssin C, Stella A, Lanéelle M-A. The acyl-AMP ligase FadD32 and AccD4-containing acyl-CoA carboxylase are required for the synthesis of mycolic acids and essential for mycobacterial growth: identification of the carboxylation product and determination of the acyl-CoA carboxylase components. J Biol Chem. 2005;280:8862–8874. doi: 10.1074/jbc.M408578200. PubMed DOI
Gavalda S, Bardou F, Laval F, Bon C, Malaga W, Chalut C. The polyketide synthase Pks13 catalyzes a novel mechanism of lipid transfer in mycobacteria. Chem Biol. 2014;21:1660–1669. doi: 10.1016/j.chembiol.2014.10.011. PubMed DOI
Portevin D, De Sousa-D’Auria C, Houssin C, Grimaldi C, Chami M, Daffé M, et al. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci U S A. 2004;101:314–319. doi: 10.1073/pnas.0305439101. PubMed DOI PMC
Lea-Smith DJ, Pyke JS, Tull D, McConville MJ, Coppel RL, Crellin PK. The reductase that catalyzes mycolic motif synthesis is required for efficient attachment of mycolic acids to arabinogalactan. J Biol Chem. 2007;282:11000–11008. doi: 10.1074/jbc.M608686200. PubMed DOI
Varela C, Rittmann D, Singh A, Krumbach K, Bhatt K, Eggeling L. MmpL genes are associated with mycolic acid metabolism in mycobacteria and corynebacteria. Chem Biol. 2012;19:498–506. doi: 10.1016/j.chembiol.2012.03.006. PubMed DOI PMC
Yamaryo-Botte Y, Rainczuk AK, Lea-Smith DJ, Brammananth R, van der Peet PL, Meikle P. Acetylation of trehalose mycolates is required for efficient mmpl-mediated membrane transport in Corynebacterineae. ACS Chem Biol. 2015;10:734–746. doi: 10.1021/cb5007689. PubMed DOI
De Sousa-D’Auria C, Kacem R, Puech V, Tropis M, Leblon G, Houssin C. New insights into the biogenesis of the cell envelope of corynebacteria: identification and functional characterization of five new mycoloyltransferase genes in Corynebacterium glutamicum. FEMS Microbiol Lett. 2003;224:35–44. doi: 10.1016/S0378-1097(03)00396-3. PubMed DOI
Huc E, de Sousa-D’Auria C, de la Sierra-Gallay IL, Salmeron C, van Tilbeurgh H, Bayan N. Identification of a mycoloyl transferase selectively involved in O-acylation of polypeptides in Corynebacteriales. J Bacteriol. 2013;195:4121–4128. doi: 10.1128/JB.00285-13. PubMed DOI PMC
Burkovski A. Cell envelope of corynebacteria: structure and influence on pathogenicity. ISRN Microbiol. 2013;2013:935736. doi: 10.1155/2013/935736. PubMed DOI PMC
Barth E, Barceló MA, Kläckta C, Benz R. Reconstitution experiments and gene deletions reveal the existence of two-component major cell wall channels in the genus Corynebacterium. J Bacteriol. 2010;192:786–800. doi: 10.1128/JB.01142-09. PubMed DOI PMC
Meniche X, Labarre C, de Sousa-d’Auria C, Huc E, Laval F, Tropis M, et al. Identification of a stress-induced factor of Corynebacterineae that is involved in the regulation of the outer membrane lipid composition. J Bacteriol. 2009;191:7323–7332. doi: 10.1128/JB.01042-09. PubMed DOI PMC
Raman S, Hazra R, Dascher CC, Husson RN. Transcription regulation by the Mycobacterium tuberculosis alternative sigma factor SigD and its role in virulence. J Bacteriol. 2004;186:6605–6616. doi: 10.1128/JB.186.19.6605-6616.2004. PubMed DOI PMC
Calamita H, Ko C, Tyagi S, Yoshimatsu T, Morrison NE, Bishai WR. The Mycobacterium tuberculosis SigD sigma factor controls the expression of ribosome-associated gene products in stationary phase and is required for full virulence. Cell Microbiol. 2004;7:233–244. doi: 10.1111/j.1462-5822.2004.00454.x. PubMed DOI
Kacem R, De Sousa-D’Auria C, Tropis M, Chami M, Gounon P, Leblon G. Importance of mycoloyltransferases on the physiology of Corynebacterium glutamicum. Microbiol Read Engl. 2004;150:73–84. doi: 10.1099/mic.0.26583-0. PubMed DOI
He N, Li Y, Chen J, Lun S-Y. Identification of a novel bioflocculant from a newly isolated Corynebacterium glutamicum. Biochem Eng J. 2002;11:137–148. doi: 10.1016/S1369-703X(02)00018-9. DOI
Anton V, Rougé P, Daffé M. Identification of the sugars involved in mycobacterial cell aggregation. FEMS Microbiol Lett. 1996;144:167–170. doi: 10.1111/j.1574-6968.1996.tb08525.x. PubMed DOI
Jayawardana KW, Wijesundera SA, Yan M. Aggregation-based detection of M. smegmatis using D-arabinose-functionalized fluorescent silica nanoparticles. Chem Commun. 2015;51:15964–15966. doi: 10.1039/C5CC05772H. PubMed DOI PMC
Chami M, Andréau K, Lemassu A, Petit J-F, Houssin C, Puech V. Priming and activation of mouse macrophages by trehalose 6,6-dicorynomycolate vesicles from Corynebacterium glutamicum. FEMS Immunol Med Microbiol. 2002;32:141–147. PubMed
Gebhardt H, Meniche X, Tropis M, Krämer R, Daffé M, Morbach S. The key role of the mycolic acid content in the functionality of the cell wall permeability barrier in Corynebacterineae. Microbiology. 2007;153:1424–1434. doi: 10.1099/mic.0.2006/003541-0. PubMed DOI
RIP-seq reveals RNAs that interact with RNA polymerase and primary sigma factors in bacteria
Overlapping SigH and SigE sigma factor regulons in Corynebacterium glutamicum