Expanding the regulatory network governed by the extracytoplasmic function sigma factor σH in Corynebacterium glutamicum

Journal of Bacteriology

Volumn 197, Issue 3, 2015, Pages 483-496

  Toyoda, Koichi ^a   Teramoto, Haruhiko ^a   Yukawa, Hideaki ^a   Inui, Masayuki ^a,b  

^a RESEARCH INSTITUTE OF INNOVATIVE TECHNOLOGY FOR THE EARTH   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DIHYDROXY ACID DEHYDRATASE; EXTRACYTOPLASMIC FUNCTION SIGMA FACTOR; FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE; HYDROLYASE; PROTEINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RIBOFLAVIN; SIGMA FACTOR; UNCLASSIFIED DRUG; ZINC; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CARBON SOURCE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; DELETION MUTANT; DNA MICROARRAY; ENVIRONMENTAL STRESS; FEEDBACK SYSTEM; GENE; GENE CLUSTER; GENE EXPRESSION; HEAT; HEAT SHOCK RESPONSE; HEAT STRESS; MICROARRAY ANALYSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; PROMOTER REGION; REGULON; START CODON; UPREGULATION; GENE DELETION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; MULTIGENE FAMILY;

CORYNEBACTERIUM GLUTAMICUM;

CHROMATIN IMMUNOPRECIPITATION; CORYNEBACTERIUM GLUTAMICUM; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; METABOLIC NETWORKS AND PATHWAYS; MICROARRAY ANALYSIS; MULTIGENE FAMILY; OPERON; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SIGMA FACTOR;

EID: 84920771771     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02248-14     Document Type: Article

References (77)

1. Kumagai H. 2000. Microbial production of amino acids in Japan. Adv Biochem Eng Biotechnol 69:71-85. http://dx.doi.org/10.1007/3-540-44964-7_3.
2. Hermann T. 2003. Industrial production of amino acids by coryneform bacteria. J Biotechnol 104:155-172. http://dx.doi.org/10.1016/S0168-1656(03)00149-4.
3. Inui M, Kawaguchi H, Murakami S, Vertès AA, Yukawa H. 2004. Metabolic engineering of Corynebacterium glutamicum for fuel ethanol production under oxygen-deprivation conditions. J Mol Microbiol Biotechnol 8:243-254. http://dx.doi.org/10.1159/000086705.
4. Wendisch VF, Bott M, Eikmanns BJ. 2006. Metabolic engineering of Escherichia coli and Corynebacterium glutamicum for biotechnological production of organic acids and amino acids. Curr Opin Microbiol 9:268-274. http://dx.doi.org/10.1016/j.mib.2006.03.001.
5. Smith KM, Cho KM, Liao JC. 2010. Engineering Corynebacterium glutamicum for isobutanol production. Appl Microbiol Biotechnol 87:1045-1055. http://dx.doi.org/10.1007/s00253-010-2522-6.
6. Yamamoto S, Suda M, Niimi S, Inui M, Yukawa H. 2013. Strain optimization for efficient isobutanol production using Corynebacterium glutamicum under oxygen deprivation. Biotechnol Bioeng 110:2938-2948. http://dx.doi.org/10.1002/bit.24961.
7. Schneider J, Wendisch VF. 2010. Putrescine production by engineered Corynebacterium glutamicum. Appl Microbiol Biotechnol 88:859-868. http://dx.doi.org/10.1007/s00253-010-2778-x.
8. Mimitsuka T, Sawai H, Hatsu M, Yamada K. 2007. Metabolic engineering of Corynebacterium glutamicum for cadaverine fermentation. Biosci Biotechnol Biochem 71:2130-2135. http://dx.doi.org/10.1271/bbb.60699.
9. Okino S, Suda M, Fujikura K, Inui M, Yukawa H. 2008. Production of D-lactic acid by Corynebacterium glutamicum under oxygen deprivation. Appl Microbiol Biotechnol 78:449-454. http://dx.doi.org/10.1007/s00253-007-1336-7.
10. Lonetto MA, Brown KL, Rudd KE, Buttner MJ. 1994. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci USA 91:7573-7577. http://dx.doi.org/10.1073/pnas.91.16.7573.
11. Helmann JD. 2002. The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47-110. http://dx.doi.org/10.1016/S0065-2911(02)46002-X.
12. H. Mol Microbiol 52:285-302. http://dx.doi.org/10.1111/j.1365-2958.2003.03979.x.
13. Kim TH, Kim HJ, Park JS, Kim Y, Kim P, Lee HS. 2005. Functional analysis of sigH expression in Corynebacterium glutamicum. Biochem Biophys Res Commun 331:1542-1547. http://dx.doi.org/10.1016/j.bbrc.2005.04.073.
14. Ehira S, Teramoto H, Inui M, Yukawa H. 2009. Regulation of Corynebacterium glutamicum heat shock response by the extracytoplasmicfunction sigma factor SigH and transcriptional regulators HspR and HrcA. J Bacteriol 191:2964-2972. http://dx.doi.org/10.1128/JB.00112-09.
15. Kaushal D, Schroeder BG, Tyagi S, Yoshimatsu T, Scott C, Ko C, Carpenter L, Mehrotra J, Manabe YC, Fleischmann RD, Bishai WR. 2002. Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH. Proc Natl Acad Sci USA 99:8330-8335. http://dx.doi.org/10.1073/pnas.102055799.
16. Raman S, Song T, Puyang X, Bardarov S, Jacobs WR, Jr, Husson RN. 2001. The alternative sigma factor SigH regulates major components of oxidative and heat stress responses in Mycobacterium tuberculosis. J Bacteriol 183: 6119-6125. http://dx.doi.org/10.1128/JB.183.20.6119-6125.2001.
17. Manganelli R, Dubnau E, Tyagi S, Kramer FR, Smith I. 1999. Differential expression of 10 sigma factor genes in Mycobacterium tuberculosis. Mol Microbiol 31:715-724. http://dx.doi.org/10.1046/j.1365-2958.1999.01212.x.
18. Paget MS, Bae JB, Hahn MY, Li W, Kleanthous C, Roe JH, Buttner MJ. 2001. Mutational analysis of RsrA, a zinc-binding anti-sigma factor with a thiol-disulphide redox switch. Mol Microbiol 39:1036-1047. http://dx.doi.org/10.1046/j.1365-2958.2001.02298.x.
19. Paget MS, Kang JG, Roe JH, Buttner MJ. 1998. sigmaR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J 17:5776-5782. http://dx.doi.org/10.1093/emboj/17.19.5776.
20. Park JH, Roe JH. 2008. Mycothiol regulates and is regulated by a thiolspecific antisigma factor RsrA and sigma(R) in Streptomyces coelicolor. Mol Microbiol 68:861-870. http://dx.doi.org/10.1111/j.1365-2958.2008.06191.x.
21. Kallifidas D, Thomas D, Doughty P, Paget MS. 2010. The sR regulon of Streptomyces coelicolor A3(2) reveals a key role in protein quality control during disulphide stress. Microbiology 156:1661-1672. http://dx.doi.org/10.1099/mic.0.037804-0.
22. Song T, Dove SL, Lee KH, Husson RN. 2003. RshA, an anti-sigma factor that regulates the activity of the mycobacterial stress response sigma factor SigH. Mol Microbiol 50:949-959. http://dx.doi.org/10.1046/j.1365-2958.2003.03739.x.
23. Kang JG, Paget MS, Seok YJ, Hahn MY, Bae JB, Hahn JS, Kleanthous C, Buttner MJ, Roe JH. 1999. RsrA, an anti-sigma factor regulated by redox change. EMBO J 18:4292-4298. http://dx.doi.org/10.1093/emboj/18.15.4292.
24. Antelmann H, Helmann JD. 2011. Thiol-based redox switches and gene regulation. Antioxid Redox Signal 14:1049-1063. http://dx.doi.org/10.1089/ars.2010.3400.
25. Busche T, Šilar R, Pičmanová M, Pátek M, Kalinowski J. 2012. 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 13:445. http://dx.doi.org/10.1186/1471-2164-13-445.
26. 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. http://dx.doi.org/10.1111/j.1365-2958.2005.04710.x.
27. Nakunst D, Larisch C, Hüser AT, Tauch A, Pühler A, Kalinowski J. 2007. The extracytoplasmic function-type sigma factor SigM of Corynebacterium glutamicum ATCC 13032 is involved in transcription of disulfide stress-related genes. J Bacteriol 189:4696-4707. http://dx.doi.org/10.1128/JB.00382-07.
28. Choi WW, Park SD, Lee SM, Kim HB, Kim Y, Lee HS. 2009. The whcA gene plays a negative role in oxidative stress response of Corynebacterium glutamicum. FEMS Microbiol Lett 290:32-38. http://dx.doi.org/10.1111/j.1574-6968.2008.01398.x.
29. Kim TH, Park JS, Kim HJ, Kim Y, Kim P, Lee HS. 2005. The whcE gene of Corynebacterium glutamicum is important for survival following heat and oxidative stress. Biochem Biophys Res Commun 337:757-764. http://dx.doi.org/10.1016/j.bbrc.2005.09.115.
30. Kim MS, Dufour YS, Yoo JS, Cho YB, Park JH, Nam GB, Kim HM, Lee KL, Donohue TJ, Roe JH. 2012. Conservation of thiol-oxidative stress responses regulated by SigR orthologues in actinomycetes. Mol Microbiol 85:326-344. http://dx.doi.org/10.1111/j.1365-2958.2012.08115.x.
31. Inui M, Murakami S, Okino S, Kawaguchi H, Vertès AA, Yukawa H. 2004. Metabolic analysis of Corynebacterium glutamicum during lactate and succinate productions under oxygen deprivation conditions. J Mol Microbiol Biotechnol 7:182-196. http://dx.doi.org/10.1159/000079827.
32. Toyoda K, Teramoto H, Inui M, Yukawa H. 2011. Genome-wide identification of in vivo binding sites of GlxR, a cyclic AMP receptor proteintype regulator in Corynebacterium glutamicum. J Bacteriol 193:4123-4133. http://dx.doi.org/10.1128/JB.00384-11.
33. Toyoda K, Teramoto H, Gunji W, Inui M, Yukawa H. 2013. Involvement of regulatory interactions among global regulators GlxR, SugR, and RamA in expression of ramA in Corynebacterium glutamicum. J Bacteriol 195:1718-1726. http://dx.doi.org/10.1128/JB.00016-13.
34. Toyoda K, Teramoto H, Inui M, Yukawa H. 2008. Expression of the gapA gene encoding glyceraldehyde-3-phosphate dehydrogenase of Corynebacterium glutamicum is regulated by the global regulator SugR. Appl Microbiol Biotechnol 81:291-301. http://dx.doi.org/10.1007/s00253-008-1682-0.
35. Waldminghaus T, Skarstad K. 2010. ChIP on chip: surprising results are often artifacts. BMC Genomics 11:414. http://dx.doi.org/10.1186/1471-2164-11-414.
36. Homann OR, Johnson AD. 2010. MochiView: versatile software for genome browsing andDNAmotif analysis. BMC Biol 8:49. http://dx.doi.org/10.1186/1741-7007-8-49.
37. Bailey TL, Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf. Intell Syst Mol Biol 2:28-36.
38. Teramoto H, Suda M, Inui M, Yukawa H. 2010. Regulation of the expression of genes involved in NAD de novo biosynthesis in Corynebacterium glutamicum. Appl Environ Microbiol 76:5488-5495. http://dx.doi.org/10.1128/AEM.00906-10.
39. Takemoto N, Tanaka Y, Inui M, Yukawa H. 2014. The physiological role of riboflavin transporter and involvement of FMN-riboswitch in its gene expression in Corynebacterium glutamicum. Appl Microbiol Biotechnol 98:4159-4168. http://dx.doi.org/10.1007/s00253-014-5570-5.
40. Inui M, Suda M, Okino S, Nonaka H, Puskás LG, Vertès AA, Yukawa H. 2007. Transcriptional profiling of Corynebacterium glutamicum metabolism during organic acid production under oxygen deprivation conditions. Microbiology 153:2491-2504. http://dx.doi.org/10.1099/mic.0.2006/005587-0.
41. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Yukawa H, Omumasaba CA, Nonaka H, Kós P, Okai N, Suzuki N, Suda M, Tsuge Y, Watanabe J, Ikeda Y, Vertès AA, Inui M. 2007. Comparative analysis of the Corynebacterium glutamicum group and complete genome sequence of strain R. Microbiology 153:1042-1058. http://dx.doi.org/10.1099/mic.0.2006/003657-0.
43. Fernandes ND, Wu QL, Kong D, Puyang X, Garg S, Husson RN. 1999. A mycobacterial extracytoplasmic sigma factor involved in survival following heat shock and oxidative stress. J Bacteriol 181:4266-4274.
44. Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A, Dusch N, Eggeling L, Eikmanns BJ, Gaigalat L, Goesmann A, Hartmann M, Huthmacher K, Kramer R, Linke B, McHardy AC, Meyer F, Mockel B, Pfefferle W, Pühler A, Rey DA, Ruckert C, Rupp O, Sahm H, Wendisch VF, Wiegrabe I, Tauch A. 2003. The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J Biotechnol 104:5-25. http://dx.doi.org/10.1016/S0168-1656(03)00154-8.
45. Holátko J, Elišáková V, Prouza M, Sobotka M, Nešvera J, Pátek M. 2009. Metabolic engineering of the L-valine biosynthesis pathway in Corynebacterium glutamicum using promoter activity modulation. J Biotechnol 139:203-210. http://dx.doi.org/10.1016/j.jbiotec.2008.12.005.
46. Flint DH, Emptage MH, Finnegan MG, Fu W, Johnson MK. 1993. The role and properties of the iron-sulfur cluster in Escherichia coli dihydroxyacid dehydratase. J Biol Chem 268:14732-14742.
47. Flint DH, Tuminello JF, Emptage MH. 1993. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 268:22369-22376.
48. Ren B, Zhang N, Yang J, Ding H. 2008. Nitric oxide-induced bacteriostasis and modification of iron-sulphur proteins in Escherichia coli. Mol Microbiol 70:953-964. http://dx.doi.org/10.1111/j.1365-2958.2008.06464.x.
49. Hyduke DR, Jarboe LR, Tran LM, Chou KJ, Liao JC. 2007. Integrated network analysis identifies nitric oxide response networks and dihydroxyacid dehydratase as a crucial target in Escherichia coli. Proc Natl Acad Sci USA 104:8484-8489. http://dx.doi.org/10.1073/pnas.0610888104.
50. Brown OR, Yein F. 1978. Dihydroxyacid dehydratase: the site of hyperbaric oxygen poisoning in branch-chain amino acid biosynthesis. Biochem Biophys Res Commun 85:1219-1224. http://dx.doi.org/10.1016/0006-291X(78)90672-1.
51. Cronan JE, Zhao X, Jiang Y. 2005. Function, attachment and synthesis of lipoic acid in Escherichia coli. Adv Microb Physiol 50:103-146. http://dx.doi.org/10.1016/S0065-2911(05)50003-1.
52. Zhao X, Miller JR, Jiang Y, Marletta MA, Cronan JE. 2003. Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem Biol 10:1293-1302. http://dx.doi.org/10.1016/j.chembiol.2003.11.016.
53. Perham RN. 2000. Swinging arms and swinging domains in multifunctional enzymes: catalytic machines for multistep reactions. Annu Rev Biochem 69:961-1004. http://dx.doi.org/10.1146/annurev.biochem.69.1.961.
54. Miller JR, Busby RW, Jordan SW, Cheek J, Henshaw TF, Ashley GW, Broderick JB, Cronan JE, Jr, Marletta MA. 2000. Escherichia coli LipA is a lipoyl synthase: in vitro biosynthesis of lipoylated pyruvate dehydrogenase complex from octanoyl-acyl carrier protein. Biochemistry 39:15166-15178. http://dx.doi.org/10.1021/bi002060n.
55. Ollagnier-de Choudens S, Fontecave M. 1999. The lipoate synthase from Escherichia coli is an iron-sulfur protein. FEBS Lett 453:25-28. http://dx.doi.org/10.1016/S0014-5793(99)00694-8.
56. 32, reveals a multifaceted cellular response to heat stress. Genes Dev 20:1776-1789. http://dx.doi.org/10.1101/gad.1428206.
57. Frunzke J, Engels V, Hasenbein S, Gatgens C, Bott M. 2008. Coordinated regulation of gluconate catabolism and glucose uptake in Corynebacterium glutamicum by two functionally equivalent transcriptional regulators, GntR1 and GntR2. Mol Microbiol 67:305-322. http://dx.doi.org/10.1111/j.1365-2958.2007.06020.x.
58. Novotna J, Vohradsky J, Berndt P, Gramajo H, Langen H, Li X-M, Minas W, Orsaria L, Roeder D, Thompson CJ. 2003. Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol Microbiol 48:1289-1303. http://dx.doi.org/10.1046/j.1365-2958.2003.03529.x.
59. Abbas CA, Sibirny AA. 2011. Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiol Mol Biol. Rev 75:321-360. http://dx.doi.org/10.1128/MMBR.00030-10.
60. Halliwell B, Gutteridge JMC. 1989. Free radicals in biology and medicine, 2nd ed. Oxford University Press, Oxford, United Kingdom.
61. Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS. 2002. Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res 30:3141-3151. http://dx.doi.org/10.1093/nar/gkf433.
62. Winkler WC, Cohen-Chalamish S, Breaker RR. 2002. An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci USA 99:15908-15913. http://dx.doi.org/10.1073/pnas.212628899.
63. Koh YS, Chung WH, Lee JH, Roe JH. 1999. The reversed SoxS-binding site upstream of the ribA promoter in Escherichia coli. Mol Gen Genet 261:374-380. http://dx.doi.org/10.1007/s004380050978.
64. Skliarova SA, Kreneva RA, Perumov DA, Mironov AS. 2012. The characterization of internal promoters in the Bacillus subtilis riboflavin biosynthesis operon. Genetika 48:967-974. http://dx.doi.org/10.1134/S1022795412100109. (In Russian).
65. Schröder J, Jochmann N, Rodionov DA, Tauch A. 2010. The Zur regulon of Corynebacterium glutamicum ATCC 13032. BMC Genomics 11:12. http://dx.doi.org/10.1186/1471-2164-11-12.
66. Teramoto H, Inui M, Yukawa H. 2012. Corynebacterium glutamicum Zur acts as a zinc-sensing transcriptional repressor of both zinc-inducible and zinc-repressible genes involved in zinc homeostasis. FEBS J 279:4385-4397. http://dx.doi.org/10.1111/febs.12028.
67. Gaballa A, Helmann JD. 2002. A peroxide-induced zinc uptake system plays an important role in protection against oxidative stress in Bacillus subtilis. Mol Microbiol 45:997-1005. http://dx.doi.org/10.1046/j.1365-2958.2002.03068.x.
68. Gaballa A, Helmann JD. 1998. Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180:5815-5821.
69. R in actinomycetes. Mol Microbiol 73:815-825. http://dx.doi.org/10.1111/j.1365-2958.2009.06824.x.
70. H in Mycobacterium tuberculosis global gene expression. Mol Microbiol 45:365-374. http://dx.doi.org/10.1046/j.1365-2958.2002.03005.x.
71. Jochmann N, Kurze AK, Czaja LF, Brinkrolf K, Brune I, Hüser AT, Hansmeier N, Pühler A, Borovok I, Tauch A. 2009. Genetic makeup of the Corynebacterium glutamicum LexA regulon deduced from comparative transcriptomics and in vitro DNA band shift assays. Microbiology 155:1459-1477. http://dx.doi.org/10.1099/mic.0.025841-0.
72. Halgasova N, Bukovska G, Timko J, Kormanec J. 2001. Cloning and transcriptional characterization of two sigma factor genes, sigA and sigB, from Brevibacterium flavum. Curr Microbiol 43:249-254. http://dx.doi.org/10.1007/s002840010296.
73. Taylor WE, Straus DB, Grossman AD, Burton ZF, Gross CA, Burgess RR. 1984. Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell 38:371-381. http://dx.doi.org/10.1016/0092-8674(84)90492-6.
74. Grossman AD, Erickson JW, Gross CA. 1984. The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell 38:383-390. http://dx.doi.org/10.1016/0092-8674(84)90493-8.
75. Carter HL, III, Wang LF, Doi RH, Moran CP, Jr. 1988. rpoD operon promoter used by sigma H-RNA polymerase in Bacillus subtilis. J Bacteriol 170:1617-1621.
76. Qi FX, He XS, Doi RH. 1991. Localization of a new promoter, P5, in the sigA operon of Bacillus subtilis and its regulation in some spo mutant strains. J Bacteriol 173:7050-7054.
77. Qi FX, Doi RH. 1990. Localization of a second SigH promoter in the Bacillus subtilis sigA operon and regulation of dnaE expression by the promoter. J Bacteriol 172:5631-5636.