Redox-responsive repressor rex modulates alcohol production and oxidative stress tolerance in Clostridium acetobutylicum

Journal of Bacteriology

Volumn 196, Issue 22, 2014, Pages 3949-3963

  Zhang, Lei ^a   Nie, Xiaoqun ^a   Ravcheev, Dmitry A ^b,c   Rodionov, Dmitry A ^b,c   Sheng, Jia ^a   Gu, Yang ^a   Yang, Sheng ^a   Jiang, Weihong ^a   Yang, Chen ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b BURNHAM INSTITUTE   (United States)

^c INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; HYDROGEN; HYDROGEN PEROXIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NITRATE; PARAQUAT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REX PROTEIN; SULFITE; ALCOHOL DERIVATIVE; BACTERIAL PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ALCOHOL PRODUCTION; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BINDING ASSAY; BINDING SITE; BIOSYNTHESIS; CITRIC ACID CYCLE; CLOSTRIDIUM ACETOBUTYLICUM; CONTROLLED STUDY; FERMENTATION; GENE EXPRESSION; GENETIC VARIABILITY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PURIFICATION; REGULATORY MECHANISM; REGULON; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

CLOSTRIDIA; CLOSTRIDIUM; CLOSTRIDIUM ACETOBUTYLICUM;

ALCOHOLS; BACTERIAL PROTEINS; CLOSTRIDIUM ACETOBUTYLICUM; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HYDROGEN PEROXIDE; MUTATION; NAD; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN BINDING; REGULON; TRANSCRIPTION FACTORS;

EID: 84917730110     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02037-14     Document Type: Article

References (49)

1. Tracy BP, Jones SW, Fast AG, Indurthi DC, Papoutsakis ET. 2012. Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr. Opin. Biotechnol. 23:364-381. http://dx.doi.org/10.1016/j.copbio.2011.10.008.
2. Lütke-Eversloh T, Bahl H. 2011. Metabolic engineering of Clostridium acetobutylicum: recent advances to improve butanol production. Curr. Opin. Biotechnol. 22:634-647. http://dx.doi.org/10.1016/j.copbio.2011.01.011.
3. Dürre P. 2007. Biobutanol: an attractive biofuel. J. Biotechnol. 2:1525-1534. http://dx.doi.org/10.1002/biot.200700168.
4. Nölling J, Breton G, Omelchenko MV, Makarova KS, Zeng QD, Gibson R, Lee HM, Dubois J, Qiu DY, Hitti J, Wolf YI, Tatusov RL, Sabathe F, Doucette-Stamm L, Soucaille P, Daly MJ, Bennett GN, Koonin EV, Smith DR. 2001. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 183: 4823-4838. http://dx.doi.org/10.1128/JB.183.16.4823-4838.2001.
5. Girbal L, Soucaille P. 1998. Regulation of solvent production in Clostridium acetobutylicum. Trends Biotechnol. 16:11-16. http://dx.doi.org/10.1016/S0167-7799(97)01141-4.
6. Hönicke D, Janssen H, Grimmler C, Ehrenreich A, Lütke-Eversloh T. 2012. Global transcriptional changes of Clostridium acetobutylicum cultures with increased butanol:acetone ratios. N. Biotechnol. 29:485-493. http://dx.doi.org/10.1016/j.nbt.2012.01.001.
7. Hillmann F, Riebe O, Fischer R-J, Mot A, Caranto JD, Kurtz DM, Jr, Bahl H. 2009. Reductive dioxygen scavenging by flavo-diiron proteins of Clostridium acetobutylicum. FEBS Lett. 583:241-245. http://dx.doi.org/10.1016/j.febslet.2008.12.004.
8. 2 detoxification in Clostridium acetobutylicum. Microbiology 155:16-24. http://dx.doi.org/10.1099/mic.0.022756-0.
9. 2-responsive NADH:rubredoxin oxidoreductase-flavoprotein A2-desulfoferrodoxin operon enzymes, rubperoxin, and rubredoxin, in Clostridium acetobutylicum. Appl. Environ. Microbiol. 75:1021-1029. http://dx.doi.org/10.1128/AEM.01425-08.
10. Wietzke M, Bahl H. 2012. The redox-sensing protein Rex, a transcriptional regulator of solventogenesis in Clostridium acetobutylicum. Appl. Microbiol. Biotechnol. 96:749-761. http://dx.doi.org/10.1007/s00253-012-4112-2.
11. Brekasis D, Paget MSB. 2003. A novel sensor of NADH/NAD+ redox poise in Streptomyces coelicolor A3(2). EMBO J. 22:4856-4865. http://dx.doi.org/10.1093/emboj/cdg453.
12. Gyan S, Shiohira Y, Sato I, Takeuchi M, Sato T. 2006. Regulatory loop between redox sensing of the NADH/NAD+ ratio by Rex (YdiH) and oxidation of NADH by NADH dehydrogenase Ndh in Bacillus subtilis. J. Bacteriol. 188:7062-7071. http://dx.doi.org/10.1128/JB.00601-06.
13. Pagels M, Fuchs S, Pané-Farré J, Kohler C, Menschner L, Hecker M, McNamarra PJ, Bauer MC, von Wachenfeldt C, Liebeke M, Lalk M, Sander G, von Eiff C, Proctor RA, Engelmann S. 2010. Redox sensing by a Rex-family repressor is involved in the regulation of anaerobic gene expression in Staphylococcus aureus. Mol. Microbiol. 76:1142-1161. http://dx.doi.org/10.1111/j.1365-2958.2010.07105.x.
14. 2 accumulation by Enterococcus faecalis. J. Bacteriol. 195:1815-1824. http://dx.doi.org/10.1128/JB.02135-12.
15. Bitoun JP, Liao S, Yao X, Xie GG, Wen ZT. 2012. The redox-sensing regulator Rex modulates central carbon metabolism, stress tolerance response and biofilm formation by Streptococcus mutans. PLoS One 7:e44766. http://dx.doi.org/10.1371/journal.pone.0044766.
16. Wang E, Bauer MC, Rogstam A, Linse S, Logan DT, von Wachenfeldt C. 2008. Structure and functional properties of the Bacillus subtilis transcriptional repressor Rex. Mol. Microbiol. 69:466-478. http://dx.doi.org/10.1111/j.1365-2958.2008.06295.x.
17. + redox sensing by a Rex family repressor. Mol. Cell 38:563-575. http://dx.doi.org/10.1016/j.molcel.2010.05.006.
18. Wang E, Ikonen TP, Knaapila M, Svergun D, Logan DT, von Wachenfeld C. 2011. Small-angle X-ray scattering study of a Rex family repressor: conformational response to NADH and NAD(+) binding in solution. J. Mol. Biol. 408:670-683. http://dx.doi.org/10.1016/j.jmb.2011.02.050.
19. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389.
20. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404.
21. Rodionov DA. 2007. Comparative genomic reconstruction of transcriptional regulatory networks in bacteria. Chem. Rev. 107:3467-3497. http://dx.doi.org/10.1021/cr068309+.
22. Novichkov PS, Rodionov DA, Stavrovskaya ED, Novichkova ES, Kazakov AE, Gelfand MS, Arkin AP, Mironov AA, Dubchak I. 2010. Reg Predict: an integrated system for regulon inference in prokaryotes by comparative genomics approach. Nucleic Acids Res. 38:W299-W307. http://dx.doi.org/10.1093/nar/gkq531.
23. Mironov AA, Vinokurova NP, Gelfand MS. 2000. Software for analysis of bacterial genomes. Mol. Biol. 34:222-231. http://dx.doi.org/10.1007/BF02759643.
24. Ravcheev DA, Li X, Latif H, Zengler K, Leyn SA, Korostelev YD, Kazakov AE, Novichkov PS, Osterman AL, Rodionov DA. 2012. Transcriptional regulation of central carbon and energy metabolism in bacteria by redox-responsive repressor Rex. J. Bacteriol. 194:1145-1157. http://dx.doi.org/10.1128/JB.06412-11.
25. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch GD, Rodionov DA, Ruckert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y, Zagnitko O, Vonstein V. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33:5691-5702. http://dx.doi.org/10.1093/nar/gki866.
26. Wiesenborn DP, Rudolph FB, Papoutsakis ET. 1988. Thiolase from Clostridium acetobutylicum ATCC 824 and its role in the synthesis of acids and solvents. Appl. Environ. Microbiol. 54:2717-2722.
27. Baer SH, Blaschek HP, Smith TL. 1987. Effect of butanol challenge and temperature on lipid composition and membrane fluidity of butanoltolerant Clostridium acetobutylicum. Appl. Environ. Microbiol. 53:2854-2861.
28. Imlay JA, Chin SM, Linn S. 1988. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240: 640-642. http://dx.doi.org/10.1126/science.2834821.
29. Hillmann F, Fischer R-J, Saint-Prix F, Girbal L, Bahl H. 2008. PerR acts as a switch for oxygen tolerance in the strict anaerobe Clostridium acetobutylicum. Mol. Microbiol. 68:848-860. http://dx.doi.org/10.1111/j.1365-2958.2008.06192.x.
30. Shao L, Hu S, Yang Y, Gu Y, Chen J, Jiang W, Yang S. 2007. Targeted gene disruption by use of a group II intron (targetron) vector in Clostridium acetobutylicum. Cell Res. 17:963-965. http://dx.doi.org/10.1038/cr.2007.91.
31. Xiao H, Gu Y, Ning Y, Yang Y, Mitchell WJ, Jiang W, Yang S. 2011. Confirmation and elimination of xylose metabolism bottlenecks in glucose phosphoenolpyruvate-dependent phosphotransferase systemdeficient Clostridium acetobutylicum for simultaneous utilization of glucose, xylose, and arabinose. Appl. Environ. Microbiol. 77:7886-7895. http://dx.doi.org/10.1128/AEM.00644-11.
32. Mermelstein LD, Papoutsakis ET. 1993. In vivo methylation in Escherichia coli by the Bacillus subtilis phage phi 3T I methyltransferase to protect plasmids from restriction upon transformation of Clostridium acetobutylicum ATCC 824. Appl. Environ. Microbiol. 59:1077-1081.
33. Ren C, Gu Y, Hu S, Wu Y, Wang P, Yang Y, Yang C, Yang S, Jiang W. 2010. Identification and inactivation of pleiotropic regulator CcpA to eliminate glucose repression of xylose utilization in Clostridium acetobutylicum. Metab. Eng. 12:446-454. http://dx.doi.org/10.1016/j.ymben.2010.05.002.
34. Tummala SB, Welker NE, Papoutsakis ET. 1999. Development and characterization of a gene expression reporter system for Clostridium acetobutylicum ATCC 824. Appl. Environ. Microbiol. 65:3793-3799.
35. Alsaker KV, Paredes CJ, Papoutsakis ET. 2005. Design, optimization and validation of genomic DNA microarrays for examining the Clostridium acetobutylicum transcriptome. Biotechnol. Bioprocess Eng. 10:432-443. http://dx.doi.org/10.1007/BF02989826.
36. Yang C, Rodionov DA, Rodionova IA, Li X, Osterman AL. 2008. Glycerate 2-kinase of Thermotoga maritima and genomic reconstruction of related metabolic pathways. J. Bacteriol. 190:1773-1782. http://dx.doi.org/10.1128/JB.01469-07.
37. Terracciano JS, Kashket ER. 1986. Intracellular conditions required for initiation of solvent production by Clostridium acetobutylicum. Appl. Environ. Microbiol. 52:86-91.
38. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, Cai J, Hippe H, Farrow JAE. 1994. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int. J. Syst. Bacteriol. 44:812-826. http://dx.doi.org/10.1099/00207713-44-4-812.
39. Amador-Noguez D, Brasg IA, Feng X-J, Roquet N, Rabinowitz JD. 2011. Metabolome remodeling during the acidogenic-solventogenic transition in Clostridium acetobutylicum. Appl. Environ. Microbiol. 77:7984-7997. http://dx.doi.org/10.1128/AEM.05374-11.
40. Chauvatcharin S, Siripatana C, Seki T, Takagi M, Yoshida T. 1998. Metabolism analysis and on-line physiological state diagnosis of acetone-butanol fermentation. Biotechnol. Bioeng. 58:561-571. http://dx.doi.org/10.1002/(SICI)1097-0290(19980620)58:6<561::AID-BIT1>3.0.CO;2-G.
41. Fontaine L, Meynial-Salles I, Girbal L, Yang XH, Croux C, Soucaille P. 2002. Molecular characterization and transcriptional analysis of adhE2, the gene encoding the NADH-dependent aldehyde/alcohol dehydrogenase responsible for butanol production in alcohologenic cultures of Clostridium acetobutylicum ATCC 824. J. Bacteriol. 184:821-830. http://dx.doi.org/10.1128/JB.184.3.821-830.2002.
42. Ravagnani A, Jennert KCB, Steiner E, Grunberg R, Jefferies JR, Wilkinson SR, Young DI, Tidswell EC, Brown DP, Youngman P, Morris JG, Young M. 2000. Spo0A directly controls the switch from acid to solvent production in solvent-forming clostridia. Mol. Microbiol. 37:1172-1185. http://dx.doi.org/10.1046/j.1365-2958.2000.02071.x.
43. Alsaker KV, Spitzer TR, Papoutsakis ET. 2004. Transcriptional analysis of spo0A overexpression in Clostridium acetobutylicum and its effect on the cell's response to butanol stress. J. Bacteriol. 186:1959-1971. http://dx.doi.org/10.1128/JB.186.7.1959-1971.2004.
44. Lehmann D, Hönicke D, Ehrenreich A, Schmidt M, Weuster-Botz D, Bahl H, Luetke-Eversloh T. 2012. Modifying the product pattern of Clostridium acetobutylicum. Appl. Microbiol. Biotechnol. 94:743-754. http://dx.doi.org/10.1007/s00253-011-3852-8.
45. Jiang Y, Xu C, Dong F, Yang Y, Jiang W, Yang S. 2009. Disruption of the acetoacetate decarboxylase gene in solvent-producing Clostridium acetobutylicum increases the butanol ratio. Metab. Eng. 11:284-291. http://dx.doi.org/10.1016/j.ymben.2009.06.002.
46. 2-affected gene expression of Clostridium acetobutylicum. J. Bacteriol. 191:6082-6093. http://dx.doi.org/10.1128/JB.00351-09.
47. Wang Y, Li X, Mao Y, Blaschek HP. 2012. Genome-wide dynamic transcriptional profiling in Clostridium beijerinckii NCIMB 8052 using single-nucleotide resolution RNA-Seq. BMC Genomics 13:102. http://dx.doi.org/10.1186/1471-2164-13-102.
48. 2 production in the fermentative pure culture Clostridium beijerinckii. Curr. Microbiol. 56:268-273. http://dx.doi.org/10.1007/s00284-007-9073-9.
49. Bengelsdorf FR, Straub M, Dürre P. 2013. Bacterial synthesis gas (syngas) fermentation. Environ. Technol. 34:1639-1651. http://dx.doi.org/10.1080/09593330.2013.827747.