Abstract
Corynebacterium glutamicum can survive by using ferulic acid as the sole carbon source. In this study, we assessed the response of C. glutamicum to ferulic acid stress by means of a global transcriptional response analysis. The transcriptional data showed that several genes involved in degradation of ferulic acid were affected. Moreover, several genes related to the stress response; protein protection or degradation and DNA repair; replication, transcription and translation; and the cell envelope were differentially expressed. Deletion of the katA or sigE gene in C. glutamicum resulted in a decrease in cell viability under ferulic acid stress. These insights will facilitate further engineering of model industrial strains, with enhanced tolerance to ferulic acid to enable easy production of biofuels from lignocellulose.
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References
Abdelkafi S, Sayadi S, Ben Ali Gam Z, Casalot L, Labat M (2006) Bioconversion of ferulic acid to vanillic acid by Halomonas elongata isolated from table-olive fermentation. FEMS Microbiol Lett 262:115–120
Almeida JRM, Modig T, Petersson A, Hähn-Hägerdal B, Lidén G, Gorwa-Grauslund MF (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol 82:340–349
Bayan N, Houssin C, Chami M, Leblon G (2003) Mycomembrane and S-layer: two important structures of Corynebacterium glutamicum cell envelope with promising biotechnology applications. J Biotechnol 104:55–67
Bellier A, Mazodier P (2004) ClgR, a novel regulator of clp and lon expression in Streptomyces. J Bacteriol 186:3238–3248
Beuth B, Pennell S, Arnvig KB, Martin SR, Taylor IA (2005) Structure of a Mycobacterium tuberculosis NusA-RNA complex. EMBO J 24:3576–3587
Bonnina E, Brunel M, Gouy Y, Lesage-Meessen L, Asther M, Thibault J (2001) Aspergillus niger I-1472 and Pycnoporus cinnabarinus MUCL39533, selected for the biotransformation of ferulic acid to vanillin, are also able to produce cell wall polysaccharide-degrading enzymes and feruloyl esterases. Enzyme Microb Technol 28:70–80
Chen X, Kohl TA, Rückert C, Rodionov DA, Li LH, Ding JY, Kalinowski J, Liu SJ (2012) Phenylacetic acid catabolism and its transcriptional regulation in Corynebacterium glutamicum. Appl Environ Microbiol 78:5796–5804
Civolani C, Barghini P, Roncetti AR, Ruzzi M, Schiesser A (2000) Bioconversion of ferulic acid into vanillic acid by means of a vanillate-negative mutant of Pseudomonas fluorescens strain BF13. Appl Environ Microbiol 66:2311–2317
Davis EO, Dullaghan EM, Rand L (2002) Definition of the mycobacterial SOS box and use to identify LexA-regulated genes in Mycobacterium tuberculosis. J Bacteriol 184:3287–3295
Ding W, Si MR, Zhang WP, Zhang YL, Chen C, Zhang L, Lu ZQ, Chen SL, Shen XH (2015) Functional and biochemical characterization of a vanillin dehydrogenase in Corynebacterium glutamicum. Sci Rep 5:8044
Du L, Ma L, Qi F, Zheng X, Jiang C, Li A, Wan X, Liu SJ, Li S (2016) Characterization of a unique pathway for 4-Cresol catabolism initiated by phosphorylation in Corynebacterium glutamicum. J Biol Chem 291:6583–6594
Engels S, Schweitzer JE, Ludwig C, Bott M, Schaffer S (2004) clpC and clpP1P2 gene expression in Corynebacterium glutamicum is controlled by a regulatory network involving the transcriptional regulators ClgR and HspR as well as the ECF sigma factor σH. Mol Microbiol 52:285–302
Engels S, Ludwig C, Schweitzer JE, Mack C, Bott M, Schaffer S (2005) The transcriptional activator ClgR controls transcription of genes involved in proteolysis and DNA repair in Corynebacterium glutamicum. Mol Microbiol 57:576–591
Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24:469–486
Helmann JD (2002) The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47–110
Hlavácek O, Váchová L (2002) ATP-dependent proteinases in bacteria. Folia Microbiol (Praha) 47:203–212
Huang Y, Zhao KX, Shen XH, Jiang CY, Liu SJ (2008) Genetic and biochemical characterization of a 4-hydroxybenzoate hydroxylase from Corynebacterium glutamicum. Appl Microbiol Biotechnol 78:75–83
Jiang XM, Fitzgerald M, Grant CM, Hogg PJ (1999) Redox control of exofacial protein thiols/disulfides by protein disulfide isomerase. J Biol Chem 274:2416–2423
Jönsson LJ, Alriksson B, Nilvebrant NO (2013) Bioconversion of lignocellulose: inhibitors and detoxification. Biotechnol Biofuels 6:16
Kallscheuer N, Vogt M, Kappelmann J, Krumbach K, Noack S, Bott M, Marienhagen J (2016) Identification of the phd gene cluster responsible for phenylpropanoid utilization in Corynebacterium glutamicum. Appl Microbiol Biotechnol 100:1871–1881
Kot B, Wicha J, Piechota M, Wolska K, Gruzewska A (2015) Antibiofilm activity of trans-cinnamaldehyde, p-coumaric, and ferulic acids on uropathogenic Escherichia coli. Turk J Med Sci 45:919–924
Larisch C, Nakunst D, Hüser AT, Tauch A, Kalinowski J (2007) The alternative sigma factor SigB of Corynebacterium glutamicum modulates global gene expression during transition from exponential growth to stationary phase. BMC Genom 8:4
Lee S, Lee JH, Mitchell RJ (2015) Analysis of Clostridium beijerinckii NCIMB 8052’s transcriptional response to ferulic acid and its application to enhance the strain tolerance. Biotechnol Biofuels 8:68
Li K, Jiang T, Yu B, Wang L, Gao C, Ma C, Xu P, Ma Y (2013) Escherichia coli transcription termination factor NusA: heat-induced oligomerization and chaperone activity. Sci Rep 3:2347
Li T, Chen X, Chaudhry MT, Zhang B, Jiang CY, Liu SJ (2014) Genetic characterization of 4-cresol catabolism in Corynebacterium glutamicum. J Biotechnol 192(Pt B):355–365
Liu YB, Long MX, Yin YJ, Si MR, Zhang L, Lu ZQ, Wang Y, Shen XH (2013) Physiological roles of mycothiol in detoxification and tolerance to multiple poisonous chemicals in Corynebacterium glutamicum. Arch Microbiol 195:419–429
Liu Y, Chen C, Chaudhry MT, Si M, Zhang L, Wang Y, Shen X (2014) Enhancing Corynebacterium glutamicum robustness by over-expressing a gene, mshA, for mycothiol glycosyltransferase. Biotechnol Lett 36:1453–1459
Merkens H, Beckers G, Wirtz A, Burkovski A (2005) Vanillate metabolism in Corynebacterium glutamicum. Curr Microbiol 51:59–65
Mills TY, Sandoval NR, Gill RT (2009) Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotechnol Biofuels 2:26
Pacheco LG, Castro TL, Carvalho RD, Moraes PM, Dorella FA, Carvalho NB, Slade SE, Scrivens JH, Feelisch M, Meyer R, Miyoshi A, Oliveira SC, Dowson CG, Azevedo V (2012) A role for sigma factor σE in Corynebacterium pseudotuberculosis resistance to nitric oxide/peroxide stress. Front Microbiol 3:126
Parawira W, Tekere M (2011) Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review. Crit Rev Biotechnol 31:20–31
Park SD, Youn JW, Kim YJ, Lee SM, Kim Y, Lee HS (2008) Corynebacterium glutamicum σE is involved in responses to cell surface stresses and its activity is controlled by the anti-σ factor CseE. Microbiology 154:915–923
Plaggenborg R, Overhage J, Loos A, Archer JA, Lessard P, Sinskey AJ, Steinbüchel A, Priefert H (2006) Potential of Rhodococcus strains for biotechnological vanillin production from ferulic acid and eugenol. Appl Microbiol Biotechnol 72:745–755
Schirmer EC, Glover JR, Singer MA, Lindquist S (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21:289–296
Schurig-Briccio LA, Farías RN, Rodríguez-Montelongo L, Rintoul MR, Rapisarda VA (2009) Protection against oxidative stress in Escherichia coli stationary phase. Arch Biochem Biophys 483:106–110
Shen X, Jiang C, Huang Y, Liu Z, Liu S (2005) Functional identification of novel genes involved in the glutathione-independent gentisate pathway in Corynebacterium glutamicum. Appl Environ Microbiol 71:3442–3452
Shen X, Zhou N, Liu S (2012) Degradation and assimilation of aromatic compounds by Corynebacterium glutamicum: another potential for applications for this bacterium? Appl Microbiol Biotechnol 95:77–89
Si MR, Long MX, Chaudhry MT, Xu Y, Zhang P, Zhang L, Shen X (2014) Functional characterization of Corynebacterium glutamicum mycothiol S-conjugate amidase. PLoS ONE 9:e115075
Si M, Xu Y, Wang T, Long M, Ding W, Chen C, Guan X, Liu Y, Wang Y, Shen X, Liu SJ (2015) Functional characterization of a mycothiol peroxidase in Corynebacterium glutamicum that uses both mycoredoxin and thioredoxin reducing systems in the response to oxidative stress. Biochem J 469:45–57
Stepanova E, Lee J, Ozerova M, Semenova E, Datsenko K, Wanner BL, Severinov K, Borukhov S (2007) Analysis of promoter targets for Escherichia coli transcription elongation factor GreA in vivo and in vitro. J Bacteriol 189:8772–8785
Tsujiyama S, Ueno M (2008) Formation of 4-vinyl guaiacol as an intermediate in bioconversion of ferulic acid by Schizophyllum commune. Biosci Biotechnol Biochem 72:212–215
Wang T, Si M, Song Y, Zhu W, Gao F, Wang Y, Zhang L, Zhang W, Wei G, Luo ZQ, Shen X (2015) Type VI secretion system transports Zn2+ to combat multiple stresses and host immunity. PLoS Pathog 11:e1005020
Winkler J, Kao KC (2011) Transcriptional analysis of Lactobacillus brevis to N-butanol and ferulic acid stress responses. PLoS ONE 6:e21438
Acknowledgments
This work was supported by the National Natural Science Foundation of China (Nos. 31270078, 31370150 and 31500087), Key Science and Technology R&D Program of Shaanxi Province, China (2014K02-12-01) and the Natural Science Foundation of Shandong Province, China (ZR2015CM012).
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Communicated by Jorge Membrillo-Hernández.
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Chen, C., Pan, J., Yang, X. et al. Global transcriptomic analysis of the response of Corynebacterium glutamicum to ferulic acid. Arch Microbiol 199, 325–334 (2017). https://doi.org/10.1007/s00203-016-1306-5
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DOI: https://doi.org/10.1007/s00203-016-1306-5