Copper homeostasis-related genes in three separate transcriptional units regulated by CsoR in Corynebacterium glutamicum

Applied Microbiology and Biotechnology

Volumn 99, Issue 8, 2015, Pages 3505-3517

  Teramoto, Haruhiko ^a   Yukawa, Hideaki ^a   Inui, Masayuki ^a  

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

Author keywords

Corynebacterium; Metal homeostasis; Metal dependent gene expression; Transcriptional regulation

Indexed keywords

COPPER; CROSSTALK; ENCODING (SYMBOLS); GENE EXPRESSION; GENES; PHYSIOLOGY; TRANSITION METALS; ZINC;

CORYNEBACTERIUM; CORYNEBACTERIUM GLUTAMICUM; INDUCIBLE EXPRESSION; METAL HOMEOSTASIS; MULTI-LAYERED SYSTEMS; TRANSCRIPTIONAL REGULATION; TRANSCRIPTIONAL REPRESSORS; TRANSCRIPTIONAL UNITS;

GENE EXPRESSION REGULATION;

BACTERIAL DNA; COPPER; PROTEIN BINDING; REPRESSOR PROTEIN;

BINDING SITE; CORYNEBACTERIUM GLUTAMICUM; DRUG EFFECTS; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; OPERON; PROMOTER REGION;

BINDING SITES; COPPER; CORYNEBACTERIUM GLUTAMICUM; DNA, BACTERIAL; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; OPERON; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS;

EID: 84936874924     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6373-z     Document Type: Article

References (55)

1. 1B-ATPases. Biometals 20:233–248. doi:10.1007/s10534-006-9055-6
2. Badarau A, Baslé A, Firbank SJ, Dennison C (2013) Crosstalk between Cu(I) and Zn(II) homeostasis via Atx1 and cognate domains. Chem Commun 49:8000–8002. doi:10.1039/c3cc42709a
3. Baker J, Sengupta M, Jayaswal RK, Morrissey JA (2011) The Staphylococcus aureus CsoR regulates both chromosomal and plasmid-encoded copper resistance mechanisms. Environ Microbiol 13:2495–2507. doi:10.1111/j.1462-2920.2011.02522.x
4. Blombach B, Riester T, Wieschalka S, Ziert C, Youn JW, Wendisch VF, Eikmanns BJ (2011) Corynebacterium glutamicum tailored for efficient isobutanol production. Appl Environ Microbiol 77:3300–3310. doi:10.1128/AEM. 02972-10
5. Brune I, Werner H, Hüser AT, Kalinowski J, Pühler A, Tauch A (2006) The DtxR protein acting as dual transcriptional regulator directs a global regulatory network involved in iron metabolism of Corynebacterium glutamicum. BMC Genomics 7:21. doi:10.1186/1471-2164-7-21
6. Cobine P, Wickramasinghe WA, Harrison MD, Weber T, Solioz M, Dameron CT (1999) The Enterococcus hirae copper chaperone CopZ delivers copper(I) to the CopY repressor. FEBS Lett 445:27–30. doi:10.1016/S0014-5793(99)00091-5
7. Corbett D, Schuler S, Glenn S, Andrew PW, Cavet JS, Roberts IS (2011) The combined actions of the copper-responsive repressor CsoR and copper-metallochaperone CopZ modulate CopA-mediated copper efflux in the intracellular pathogen Listeria monocytogenes. Mol Microbiol 81:457–472. doi:10.1111/j.1365-2958.2011.07705.x
8. Dainty SJ, Patterson CJ, Waldron KJ, Robinson NJ (2010) Interaction between cyanobacterial copper chaperone Atx1 and zinc homeostasis. J Biol Inorg Chem 15:77–85. doi:10.1007/s00775-009-0555-z
9. Dwarakanath S, Chaplin AK, Hough MA, Rigali S, Vijgenboom E, Worrall JRA (2012) Response to copper stress in Streptomyces lividans extends beyond genes under direct control of a copper-sensitive operon repressor protein (CsoR). J Biol Chem 287:17833–17847. doi:10.1074/jbc.M112.352740
10. Festa RA, Jones MB, Butler-Wu S, Sinsimer D, Gerads R, Bishai WR, Peterson SN, Darwin KH (2011) A novel copper-responsive regulon in Mycobacterium tuberculosis. Mol Microbiol 79:133–148. doi:10.1111/j.1365-2958.2010.07431.x
11. Foster AW, Patterson CJ, Pernil R, Hess CR, Robinson NJ (2012) Cytosolic Ni(II) sensor in cyanobacterium: nickel detection follows nickel affinity across four families of metal sensors. J Biol Chem 287:12142–12151. doi:10.1074/jbc.M111.338301
12. Foster AW, Pernil R, Patterson CJ, Robinson NJ (2014) Metal specificity of cyanobacterial nickel-responsive repressor InrS: cells maintain zinc and copper below the detection threshold for InrS. Mol Microbiol 92:797–812. doi:10.1111/mmi.12594
13. Gaballa A, Helmann JD (2003) Bacillus subtilis CPx-type ATPases: characterization of Cd, Zn, Co and Cu efflux systems. Biometals 16:497–505. doi:10.1023/A:1023425321617
14. Grossoehme N, Kehl-Fie TE, Ma Z, Adams KW, Cowart DM, Scott RA, Skaar EP, Giedroc DP (2011) Control of copper resistance and inorganic sulfur metabolism by paralogous regulators in Staphylococcus aureus. J Biol Chem 286:13522–13531. doi:10.1074/jbc.M111.220012
15. Hermann T (2003) Industrial production of amino acids by coryneform bacteria. J Biotechnol 104:155–172. doi:10.1016/S0168-1656(03)00149-4
16. Higgins KA, Chivers PT, Maroney MJ (2012) Role of the N-terminus in determining metal-specific responses in the E. coli Ni- and Co-responsive metalloregulator, RcnR. J Am Chem Soc 134:7081–7093. doi:10.1021/ja300834b
17. Higgins KA, Hu HQ, Chivers PT, Maroney MJ (2013) Effects of select histidine to cysteine mutations on transcriptional regulation by Escherichia coli RcnR. Biochemistry 52:84–97. doi:10.1021/bi300886q
18. Ikeda M, Takeno S (2012) Amino acid production by Corynebacterium glutamicum. In: Yukawa H, Inui M, Steinbüchel A (eds) Corynebacterium glutamicum Biology and Biotechnology Microbiology Monographs. vol 23. Springer, Heidelberg, pp 107–148
19. Inui M, Kawaguchi H, Murakami S, Vertès AA, Yukawa H (2004a) Metabolic engineering of Corynebacterium glutamicum for fuel ethanol production under oxygen-deprivation conditions. J Mol Microbiol Biotechnol 8:243–254. doi:10.1159/000086705
20. Inui M, Murakami S, Okino S, Kawaguchi H, Vertès AA, Yukawa H (2004b) Metabolic analysis of Corynebacterium glutamicum during lactate and succinate productions under oxygen deprivation conditions. J Mol Microbiol Biotechnol 7:182–196. doi:10.1159/000079827
21. 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. doi:10.1099/mic. 0.2006/005587-0
22. Iwig JS, Leitch S, Herbst RW, Maroney MJ, Chivers PT (2008) Ni(II) and Co(II) sensing by Escherichia coli RcnR. J Am Chem Soc 130:7592–7606. doi:10.1021/ja710067d
23. Jojima T, Inui M, Yukawa H (2012) Biorefinery applications of Corynebacterium glutamicum. In: Yukawa H, Inui M, Steinbüchel A (eds) Corynebacterium glutamicum Biology and Biotechnology Microbiology Monographs. vol 23. Springer, Heidelberg, pp 149–172
24. Kinoshita S, Udaka S, Shimonō M (1957) Studies on the amino acid fermentation. Part 1. Production of L-glutamic acid by various microorganisms. J Gen Appl Microbiol 3:193–205. doi:10.2323/jgam.3.193
25. Liu T, Ramesh A, Ma Z, Ward SK, Zhang L, George GN, Talaat AM, Sacchettini JC, Giedroc DP (2007) CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator. Nat Chem Biol 3:60–68. doi:10.1038/nchembio844
26. Ma Z, Cowart DM, Scott RA, Giedroc DP (2009a) Molecular insights into the metal selectivity of the Cu(I)-sensing repressor CsoR from Bacillus subtilis. Biochemistry 48:3325–3334. doi:10.1021/bi900115w
27. Ma Z, Jacobsen FE, Giedroc DP (2009b) Coordination chemistry of bacterial metal transport and sensing. Chem Rev 109:4644–4681. doi:10.1021/cr900077w
28. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
29. Nakata K, Inui M, Kos PB, Vertès AA, Yukawa H (2003) Vectors for the genetics engineering of corynebacteria. In: Saha BC (ed) Fermentation Biotechnology. American Chemical Society, Washington, pp 175–191
30. Odermatt A, Suter H, Krapf R, Solioz M (1993) Primary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae. J Biol Chem 268:12775–12779
31. Okino S, Noburyu R, Suda M, Jojima T, Inui M, Yukawa H (2008a) An efficient succinic acid production process in a metabolically engineered Corynebacterium glutamicum strain. Appl Microbiol Biotechnol 81:459–464. doi:10.1007/s00253-008-1668-y
32. Okino S, Suda M, Fujikura K, Inui M, Yukawa H (2008b) Production of D-lactic acid by Corynebacterium glutamicum under oxygen deprivation. Appl Microbiol Biotechnol 78:449–454. doi:10.1007/s00253-007-1336-7
33. Palumaa P (2013) Copper chaperones. The concept of conformational control in the metabolism of copper. FEBS Lett 587:1902–1910. doi:10.1016/j.febslet.2013.05.019
34. Pátek M, Nešvera J (2011) Sigma factors and promoters in Corynebacterium glutamicum. J Biotechnol 154:101–113. doi:10.1016/j.jbiotec.2011.01.017
35. Rademacher C, Masepohl B (2012) Copper-responsive gene regulation in bacteria. Microbiology 158:2451–2464. doi:10.1099/mic. 0.058487-0
36. Radford DS, Kihlken MA, Borrelly GPM, Harwood CR, Le Brun NE, Cavet JS (2003) CopZ from Bacillus subtilis interacts in vivo with a copper exporting CPx-type ATPase CopA. FEMS Microbiol Lett 220:105–112. doi:10.1016/S0378-1097(03)00095-8
37. Sakamoto K, Agari Y, Agari K, Kuramitsu S, Shinkai A (2010) Structural and functional characterization of the transcriptional repressor CsoR from Thermus thermophilus HB8. Microbiology 156:1993–2005. doi:10.1099/mic. 0.037382-0
38. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
39. Schelder S, Zaade D, Litsanov B, Bott M, Brocker M (2011) The two-component signal transduction system CopRS of Corynebacterium glutamicum is required for adaptation to copper-excess stress. PLoS One 6:e22143. doi:10.1371/journal.pone.0022143
40. Schröder J, Jochmann N, Rodionov DA, Tauch A (2010) The Zur regulon of Corynebacterium glutamicum ATCC 13032. BMC Genomics 11:12. doi:10.1186/1471-2164-11-12
41. Smaldone GT, Helmann JD (2007) CsoR regulates the copper efflux operon copZA in Bacillus subtilis. Microbiology 153:4123–4128. doi:10.1099/mic. 0.2007/011742-0
42. Smith KM, Cho KM, Liao JC (2010) Engineering Corynebacterium glutamicum for isobutanol production. Appl Microbiol Biotechnol 87:1045–1055. doi:10.1007/s00253-010-2522-6
43. Suzuki N, Okai N, Nonaka H, Tsuge Y, Inui M, Yukawa H (2006) High-throughput transposon mutagenesis of Corynebacterium glutamicum and construction of a single-gene disruptant mutant library. Appl Environ Microbiol 72:3750–3755. doi:10.1128/AEM. 72.5.3750-3755.2006
44. 4 dicarboxylates in Corynebacterium glutamicum. Appl Environ Microbiol 74:5290–5296. doi:10.1128/AEM. 00832-08
45. 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. doi:10.1128/AEM. 00906-10
46. 1B-type ATPase operons. Biosci Biotechnol Biochem 76:1952–1958. doi:10.1271/bbb.120437
47. Teramoto H, Inui M, Yukawa H (2012b) 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. doi:10.1111/febs.12028
48. Vertès AA, Inui M, Kobayashi M, Kurusu Y, Yukawa H (1993) Presence of mrr- and mcr-like restriction systems in coryneform bacteria. Res Microbiol 144:181–185. doi:10.1016/0923-2508(93)90043-2
49. Waldron KJ, Robinson NJ (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 7:25–35. doi:10.1038/nrmicro2057
50. Ward SK, Abomoelak B, Hoye EA, Steinberg H, Talaat AM (2010) CtpV: a putative copper exporter required for full virulence of Mycobacterium tuberculosis. Mol Microbiol 77:1096–1110. doi:10.1111/j.1365-2958.2010.07273.x
51. Wennerhold J, Bott M (2006) The DtxR regulon of Corynebacterium glutamicum. J Bacteriol 188:2907–2918. doi:10.1128/JB.188.8.2907-2918.2006
52. Wennerhold J, Krug A, Bott M (2005) The AraC-type regulator RipA represses aconitase and other iron proteins from Corynebacterium under iron limitation and is itself repressed by DtxR. J Biol Chem 280:40500–40508. doi:10.1074/jbc.M508693200
53. Wieschalka S, Blombach B, Bott M, Eikmanns BJ (2013) Bio-based production of organic acids with Corynebacterium glutamicum. Microb Biotechnol 6:87–102. doi:10.1111/1751-7915.12013
54. 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. doi:10.1002/bit.24961
55. 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. doi:10.1099/mic. 0.2006/003657-0