Role of the twin arginine protein transport pathway in the assembly of the Streptomyces coelicolor cytochrome bc1 complex

Journal of Bacteriology

Volumn 196, Issue 1, 2014, Pages 50-59

  Hopkins, Adam ^a   Buchanan, Grant ^a   Palmer, Tracy ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; IRON SULFUR PROTEIN; UBIQUINOL CYTOCHROME C REDUCTASE;

ABSORPTION SPECTROSCOPY; AFFINITY CHROMATOGRAPHY; ARTICLE; BACTERIAL MEMBRANE; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN TRANSPORT; STREPTOMYCES COELICOLOR;

CELL MEMBRANE; ELECTRON TRANSPORT COMPLEX III; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; STREPTOMYCES COELICOLOR;

EID: 84890282871     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00776-13     Document Type: Article

References (57)

1. Shi L, Sohaskey CD, Kana BD, Dawes S, North RJ, Mizrahi V, Gennaro ML. 2005. Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc. Natl. Acad. Sci. U. S. A. 102:15629-15634. http://dx.doi.org/10.1073/pnas.0507850102.
2. van Keulen G, Alderson J, White J, Sawers RG. 2007. The obligate aerobic actinomycete Streptomyces coelicolor A3(2) survives extended periods of anaerobic stress. Environ. Microbiol. 9:3143-3149. http://dx.doi.org/10.1111/j.1462-2920.2007.01433.x.
3. Watanabe S, Zimmermann M, Goodwin MB, Sauer U, Barry CE, III, BoshoffHI. 2011. Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis. PLoS Pathog. 7:e1002287. http://dx.doi.org/10.1371/journal.ppat.1002287.
4. D'Mello R, Hill S, Poole RK. 1996. The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen- binding haems: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142:755-763. http://dx.doi.org/10.1099/00221287-142-4-755.
5. Matsoso LG, Kana BD, Crellin PK, Lea-Smith DJ, Pelosi A, Powell D, Dawes SS, Rubin H, Coppel RL, Mizrahi V. 2005. Function of the cytochrome bc1-aa3 branch of the respiratory network in mycobacteria and network adaptation occurring in response to its disruption. J. Bacteriol. 187:6300-6308. http://dx.doi.org/10.1128/JB.187.18.6300-6308.2005.
6. Baker SC, Ferguson SJ, Ludwig B, Page MD, Richter OM, van Spanning RJ. 1998. Molecular genetics of the genus Paracoccus: metabolically versatile bacteria with bioenergetic flexibility. Microbiol. Mol. Biol. Rev. 62: 1046-1078.
7. Lenaz G, Genova ML. 2012. Supramolecular organisation of the mitochondrial respiratory chain: a new challenge for the mechanism and control of oxidative phosphorylation. Adv. Exp. Med. Biol. 748:107-144. http://dx.doi.org/10.1007/978-1-4614-3573-0_5.
8. Xia D, Yu CA, Kim H, Xia JZ, Kachurin AM, Zhang L, Yu L, Deisenhofer J. 1997. Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science 277:60-66. http://dx.doi.org/10.1126/science.277.5322.60.
9. Niebisch A, Bott M. 2003. Purification of a cytochrome bc1-aa3 supercomplex with quinol oxidase activity from Corynebacterium glutamicum. Identification of a fourth subunit of cytochrome aa3 oxidase and mutational analysis of diheme cytochrome c1. J. Biol. Chem. 278:4339-4346. http://dx.doi.org/10.1074/jbc. M210499200.
10. Sone N, Nagata K, Kojima H, Tajima J, Kodera Y, Kanamaru T, Noguchi S, Sakamoto J. 2001. A novel hydrophobic diheme c-type cytochrome. Purification from Corynebacterium glutamicum and analysis of the QcrCBA operon encoding three subunit proteins of a putative cytochrome reductase complex. Biochim. Biophys. Acta 1503:279-290. http://dx.doi.org/10.1016/S0005-2728(00)00205-X.
11. Kurisu G, Zhang H, Smith JL, Cramer WA. 2003. Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009-1014. http://dx.doi.org/10.1126/science.1090165.
12. Keller R, de Keyzer J, Driessen AJ, Palmer T. 2012. Co-operation between different targeting pathways during integration of a membrane protein. J. Cell Biol. 199:303-315. http://dx.doi.org/10.1083/jcb.201204149.
13. Driessen AJ, Nouwen N. 2008. Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 77:643-667. http://dx.doi.org/10.1146/annurev.biochem.77.061606.160747.
14. Park E, Rapoport TA. 2012. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu. Rev. Biophys. 41:21-40. http://dx.doi.org/10.1146/annurev-biophys-050511-102312.
15. Schulz H, Hennecke H, Thony-Meyer L. 1998. Prototype of a heme chaperone essential for cytochrome c maturation. Science 281:1197-1200. http://dx.doi.org/10.1126/science.281.5380.1197.
16. Thony-Meyer L, Kunzler P. 1997. Translocation to the periplasm and signal sequence cleavage of preapocytochrome c depend on sec and lep, but not on the ccm gene products. Eur. J. Biochem. 246:794-799. http://dx.doi.org/10.1111/j.1432-1033.1997.t01-1-00794.x.
17. Aldridge C, Spence E, Kirkilionis MA, Frigerio L, Robinson C. 2008. Tat-dependent targeting of Rieske iron-sulphur proteins to both the plasma and thylakoid membranes in the cyanobacterium Synechocystis PCC6803. Mol. Microbiol. 70:140-150. http://dx.doi.org/10.1111/j.1365-2958.2008.06401.x.
18. Bachmann J, Bauer B, Zwicker K, Ludwig B, Anderka O. 2006. The Rieske protein from Paracoccus denitrificans is inserted into the cytoplasmic membrane by the twin-arginine translocase. FEBS J. 273:4817-4830. http://dx.doi.org/10.1111/j.1742-4658.2006.05480.x.
19. De Buck E, Vranckx L, Meyen E, Maes L, Vandersmissen L, Anne J, Lammertyn E. 2007. The twin-arginine translocation pathway is necessary for correct membrane insertion of the Rieske Fe/S protein in Legionella pneumophila. FEBS Lett. 581:259-264. http://dx.doi.org/10.1016/j.febslet.2006.12.022.
20. Meloni S, Rey L, Sidler S, Imperial J, Ruiz-Argueso T, Palacios JM. 2003. The twin-arginine translocation (Tat) system is essential for Rhizobium- legume symbiosis. Mol. Microbiol. 48:1195-1207. http://dx.doi.org/10.1046/j.1365-2958.2003.03510.x.
21. Molik S, Karnauchov I, Weidlich C, Herrmann RG, Klosgen RB. 2001. The Rieske Fe/S protein of the cytochrome b6f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J. Biol. Chem. 276:42761-42766. http://dx.doi.org/10.1074/jbc.M106690200.
22. Frobel J, Rose P, Muller M. 2012. Twin-arginine-dependent translocation of folded proteins. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367:1029-1046. http://dx.doi.org/10.1098/rstb.2011.0202.
23. Palmer T, Berks BC. 2012. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10:483-496. http://dx.doi.org/10.1038/nrmicro2814.
24. Berks BC. 1996. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22:393-404. http://dx.doi.org/10.1046/j.1365-2958.1996.00114.x.
25. Stanley NR, Palmer T, Berks BC. 2000. The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275:11591-11596. http://dx.doi.org/10.1074/jbc.275.16.11591.
26. Kol S, Majczak W, Heerlien R, van der Berg JP, Nouwen N, Driessen AJ. 2009. Subunit a of the F(1)F(0) ATP synthase requires YidC and SecYEG for membrane insertion. J. Mol. Biol. 390:893-901. http://dx.doi.org/10.1016/j.jmb.2009.05.074.
27. Stanley NR, Sargent F, Buchanan G, Shi J, Stewart V, Palmer T, Berks BC. 2002. Behaviour of topological marker proteins targeted to the Tat protein transport pathway. Mol. Microbiol. 43:1005-1021. http://dx.doi.org/10.1046/j.1365-2958.2002.02797.x.
28. Tullman-Ercek D, DeLisa MP, Kawarasaki Y, Iranpour P, Ribnicky B, Palmer T, Georgiou G. 2007. Export pathway selectivity of Escherichia coli twin arginine translocation signal peptides. J. Biol. Chem. 282:8309-8316. http://dx.doi.org/10.1074/jbc. M610507200.
29. Zhu L, Wasey A, White SH, Dalbey RE. 2013. Charge composition features of model single-span membrane proteins that determine selection of YidC and SecYEG translocase pathways in Escherichia coli. J. Biol. Chem. 288:7704-7716. http://dx.doi.org/10.1074/jbc. M112.429431.
30. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580. http://dx.doi.org/10.1016/S0022-2836(83)80284-8.
32. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, United Kingdom.
33. Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O'Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147. http://dx.doi.org/10.1038/417141a.
34. Fyans JK, Bignell D, Loria R, Toth I, Palmer T. 2013. The ESX/type VII secretion system modulates development, but not virulence, of the plant pathogen Streptomyces scabies. Mol. Plant Pathol. 14:119-130. http://dx.doi.org/10.1111/j.1364-3703.2012.00835.x.
35. Gust B, Challis GL, Fowler K, Kieser T, Chater KF. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. U. S. A. 100:1541-1546. http://dx.doi.org/10.1073/pnas.0337542100.
36. Zheng L, Baumann U, Reymond JL. 2004. An efficient one-step sitedirected and site-saturation mutagenesis protocol. Nucleic Acids Res. 32: e115. http://dx.doi.org/10.1093/nar/gnh110.
37. Margoliash E, Walasek OF. 1967. Cytochrome c from vertebrate and invertebrate sources. Methods Enzymol. 10:339-348. http://dx.doi.org/10.1016/0076-6879(67)10064-5.
38. Zoltner M, Fyfe PK, Palmer T, Hunter WN. 2013. Characterization of Staphylococcus aureus EssB, an integral membrane component of the type VII secretion system: atomic resolution crystal structure of the cytoplasmic segment. Biochem. J. 449:469-477. http://dx.doi.org/10.1042/BJ20121209.
39. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685. http://dx.doi.org/10.1038/227680a0.
40. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76:4350-4354. http://dx.doi.org/10.1073/pnas.76.9.4350.
41. Joshi MV, Mann SG, Antelmann H, Widdick DA, Fyans JK, Chandra G, Hutchings MI, Toth I, Hecker M, Loria R, Palmer T. 2010. The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies. Mol. Microbiol. 77:252-271. http://dx.doi.org/10.1111/j.1365-2958.2010.07206.x.
42. Schaerlaekens K, Van Mellaert L, Lammertyn E, Geukens N, Anne J. 2004. The importance of the Tat-dependent protein secretion pathway in Streptomyces as revealed by phenotypic changes in tat deletion mutants and genome analysis. Microbiology 150:21-31. http://dx.doi.org/10.1099/mic.0.26684-0.
43. Widdick DA, Dilks K, Chandra G, Bottrill A, Naldrett M, Pohlschroder M, Palmer T. 2006. The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor. Proc. Natl. Acad. Sci. U. S. A. 103:17927-17932. http://dx.doi.org/10.1073/pnas.0607025103.
44. Nicholls DG, Ferguson SJ. 2002. Bioenergetics 3. Academic Press, London, United Kingdom.
45. Megehee JA, Hosler JP, Lundrigan MD. 2006. Evidence for a cytochrome bc1-aa3 interaction in the respiratory chain of Mycobacterium smegmatis. Microbiology 152:823-829. http://dx.doi.org/10.1099/mic.0.28723-0.
46. Nicholls P, Petersen LC, Miller M, Hansen FB. 1976. Ligand-induced spectral changes in cytochrome c oxidase and their possible significance. Biochim. Biophys. Acta 449:188-196. http://dx.doi.org/10.1016/0005-2728(76)90132-8.
47. Ahuja U, Kjelgaard P, Schulz BL, Thony-Meyer L, Hederstedt L. 2009. Haem-delivery proteins in cytochrome c maturation System II. Mol. Microbiol. 73:1058-1071. http://dx.doi.org/10.1111/j.1365-2958.2009.06833.x.
48. Aigle B, Wietzorrek A, Takano E, Bibb MJ. 2000. A single amino acid substitution in region 1.2 of the principal sigma factor of Streptomyces coelicolor A3(2) results in pleiotropic loss of antibiotic production. Mol. Microbiol. 37:995-1004. http://dx.doi.org/10.1046/j.1365-2958.2000.02022.x.
49. Palmer T, Hutchings MI. 2010. Protein secretion in Streptomyces, p 87-104. In Dyson PJ (ed), Streptomyces molecular biology and biotechnology. Caister Academic Press, Norfolk, United Kingdom.
50. Saint-Joanis B, Demangel C, Jackson M, Brodin P, Marsollier L, BoshoffH, Cole ST. 2006. Inactivation of Rv2525c, a substrate of the twin arginine translocation (Tat) system of Mycobacterium tuberculosis, increases beta-lactam susceptibility and virulence. J. Bacteriol. 188: 6669-6679. http://dx.doi.org/10.1128/JB.00631-06.
51. Sassetti CM, Boyd DH, Rubin EJ. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48:77-84. http://dx.doi.org/10.1046/j.1365-2958.2003.03425.x.
52. Casadaban MJ, Cohen SN. 1979. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc. Natl. Acad. Sci. U. S. A. 76:4530-4533. http://dx.doi.org/10.1073/pnas.76.9.4530.
53. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
54. MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH, MacNeil T. 1992. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111:61-68. http://dx.doi.org/10.1016/0378-1119(92)90603-M.
55. Paget MS, Chamberlin L, Atrih A, Foster SJ, Buttner MJ. 1999. Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J. Bacteriol. 181:204-211.
56. Gust B, Chandra G, Jakimowicz D, Yuqing T, Bruton CJ, Chater KF. 2004. Lambda red-mediated genetic manipulation of antibioticproducing Streptomyces. Adv. Appl. Microbiol. 54:107-128. http://dx.doi.org/10.1016/S0065-2164(04)54004-2.
57. Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, Schoner BE. 1992. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43-49. http://dx.doi.org/10.1016/0378-1119(92)90627-2.