The absence of pupylation (prokaryotic ubiquitin-like protein modification) affects morphological and physiological differentiation in Streptomyces coelicolor

Journal of Bacteriology

Volumn 197, Issue 21, 2015, Pages 3388-3399

  Boubakri, Hasna ^a,f   Seghezzi, Nicolas ^b,c,g   Duchateau, Magalie ^b,c   Gominet, Myriam ^b,c   Kofroňová, Olga ^d   Benada, Oldřich ^d,e   Mazodier, Philippe ^b,c   Pernodet, Jean Luc ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b INSTITUT PASTEUR   (France)

^c CNRS   (France)

^d INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^e J E PURKINJE UNIVERSITY   (Czech Republic)

^f UNIVERSITÉ LYON 1   (France)

^g UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROKARYOTIC UBIQUITIN LIKE PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

AGAR DIFFUSION; ARTICLE; BACTERIAL GROWTH; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; DELETION MUTANT; DRUG MANUFACTURE; IMMUNOBLOTTING; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; STREPTOMYCES COELICOLOR; UBIQUITINATION; AMINO ACID SEQUENCE; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; GENE DELETION; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE ALIGNMENT; STREPTOMYCES COELICOLOR;

EID: 84944626663     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00591-15     Document Type: Article

References (60)

1. Finley D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78:477-513. http://dx.doi.org/10.1146/annurev.biochem.78.081507.101607.
2. Weissman AM. 2001. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2:169-178. http://dx.doi.org/10.1038/35056563.
3. Baker TA, Sauer RT. 2006. ATP-dependent proteases of bacteria: recognition logic and operating principles. Trends Biochem Sci 31:647-653. http://dx.doi.org/10.1016/j.tibs.2006.10.006.
4. Striebel F, Imkamp F, Sutter M, Steiner M, Mamedov A, Weber-Ban E.2009. Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat Struct Mol Biol 16:647-651. http://dx.doi.org/10.1038/nsmb.1597.
5. Tamura T, Nagy I, Lupas A, Lottspeich F, Cejka Z, Schoofs G, Tanaka K, De Mot R, Baumeister W. 1995. The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr Biol 5:766-774. http://dx.doi.org/10.1016/S0960-9822(95)00153-9.
6. Nagy I, Tamura T, Vanderleyden J, Baumeister W, De Mot R. 1998. The 20S proteasome of Streptomyces coelicolor. J Bacteriol 180:5448-5453.
7. Pouch MN, Cournoyer B, Baumeister W. 2000. Characterization of the 20S proteasome from the actinomycete Frankia. Mol Microbiol 35:368-377. http://dx.doi.org/10.1046/j.1365-2958.2000.01703.x.
8. Knipfer N, Shrader TE. 1997. Inactivation of the 20S proteasome in Mycobacterium smegmatis. Mol Microbiol 25:375-383. http://dx.doi.org/10.1046/j.1365-2958.1997.4721837.x.
9. Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF. 2003. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302:1963-1966. http://dx.doi.org/10.1126/science.1091176.
10. Gandotra S, Schnappinger D, Monteleone M, Hillen W, Ehrt S. 2007. In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat Med 13:1515-1520. http://dx.doi.org/10.1038/nm1683.
11. Hong B, Wang L, Lammertyn E, Geukens N, Van Mellaert L, Li Y, Anne J. 2005. Inactivation of the 20S proteasome in Streptomyces lividans and its influence on the production of heterologous proteins. Microbiology 151: 3137-3145. http://dx.doi.org/10.1099/mic.0.28034-0.
12. De Mot R, Schoofs G, Nagy I. 2007. Proteome analysis of Streptomyces coelicolor mutants affected in the proteasome system reveals changes in stress-responsive proteins. Arch Microbiol 188:257-271. http://dx.doi.org/10.1007/s00203-007-0243-8.
13. Mao XM, Ren NN, Sun N, Wang F, Zhou RC, Tang Y, Li YQ. 2014. Proteasome involvement in a complex cascade mediating SigT degradation during differentiation of Streptomyces coelicolor. FEBS Lett 588:608-613. http://dx.doi.org/10.1016/j.febslet.2013.12.029.
14. Burns KE, Liu WT, BoshoffHI, Dorrestein PC, Barry CE, III. 2009. Proteasomal protein degradation in mycobacteria is dependent upon a prokaryotic ubiquitin-like protein. J Biol Chem 284:3069-3075. http://dx.doi.org/10.1074/jbc. M808032200.
15. Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH. 2008. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322:1104-1107. http://dx.doi.org/10.1126/science.1163885.
16. Burns KE, Darwin KH. 2010. Pupylation versus ubiquitylation: tagging for proteasome-dependent degradation. Cell Microbiol 12:424-431. http://dx.doi.org/10.1111/j.1462-5822.2010.01447.x.
17. Bremm A, Komander D. 2010. A further case of Dop-ing in bacterialpupylation. EMBO Rep 11:722-723. http://dx.doi.org/10.1038/embor.2010.149.
18. Cerda-Maira FA, Pearce MJ, Fuortes M, Bishai WR, Hubbard SR, Darwin KH. 2010. Molecular analysis of the prokaryotic ubiquitin-like protein (Pup) conjugation pathway in Mycobacterium tuberculosis. Mol Microbiol 77:1123-1135. http://dx.doi.org/10.1111/j.1365-2958.2010.07276.x.
19. Iyer LM, Burroughs AM, Aravind L. 2008. Unraveling the biochemistry and provenance of pupylation: a prokaryotic analog of ubiquitination. Biol Direct 3:45. http://dx.doi.org/10.1186/1745-6150-3-45.
20. Wang T, Darwin KH, Li H. 2010. Binding-induced folding of prokaryotic ubiquitin-like protein on the Mycobacterium proteasomal ATPase targets substrates for degradation. Nat Struct Mol Biol 17:1352-1357. http://dx.doi.org/10.1038/nsmb.1918.
21. Chen X, Solomon WC, Kang Y, Cerda-Maira F, Darwin KH, Walters KJ. 2009. Prokaryotic ubiquitin-like protein pup is intrinsically disordered. J Mol Biol 392:208-217. http://dx.doi.org/10.1016/j.jmb.2009.07.018.
22. Liao S, Shang Q, Zhang X, Zhang J, Xu C, Tu X. 2009. Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein. Biochem J 422:207-215. http://dx.doi.org/10.1042/BJ20090738.
23. Sutter M, Striebel F, Damberger FF, Allain FH, Weber-Ban E. 2009. A distinct structural region of the prokaryotic ubiquitin-like protein (Pup) is recognized by the N-terminal domain of the proteasomal ATPase Mpa. FEBS Lett 583:3151-3157. http://dx.doi.org/10.1016/j.febslet.2009.09.020.
24. Burns KE, Cerda-Maira FA, Wang T, Li H, Bishai WR, Darwin KH.2010. "Depupylation" of prokaryotic ubiquitin-like protein from mycobacterial proteasome substrates. Mol Cell 39:821-827. http://dx.doi.org/10.1016/j.molcel.2010.07.019.
25. Imkamp F, Striebel F, Sutter M, Ozcelik D, Zimmermann N, Sander P, Weber-Ban E. 2010. Dop functions as a depupylase in the prokaryotic ubiquitin-like modification pathway. EMBO Rep 11:791-797. http://dx.doi.org/10.1038/embor.2010.119.
26. Festa RA, McAllister F, Pearce MJ, Mintseris J, Burns KE, Gygi SP, Darwin KH. 2010. Prokaryotic ubiquitin-like protein (Pup) proteome of Mycobacterium tuberculosis. PLoS One 5:e8589. http://dx.doi.org/10.1371/journal.pone.0008589.
27. Poulsen C, Akhter Y, Jeon AH, Schmitt-Ulms G, Meyer HE, Stefanski A, Stuhler K, Wilmanns M, Song YH. 2010. Proteome-wide identification of mycobacterial pupylation targets. Mol Syst Biol 6:386. http://dx.doi.org/10.1038/msb.2010.39.
28. Watrous J, Burns K, Liu WT, Patel A, Hook V, Bafna V, Barry CE, III, Bark S, Dorrestein PC. 2010. Expansion of the mycobacterial "PUPylome." Mol Biosyst 6:376-385. http://dx.doi.org/10.1039/b916104j.
29. Yun HY, Tamura N, Tamura T. 2012. Rhodococcus prokaryotic ubiquitinlike protein (Pup) is degraded by deaminase of Pup (Dop). Biosci Biotechnol Biochem 76:1959-1966. http://dx.doi.org/10.1271/bbb.120458.
30. Kuberl A, Franzel B, Eggeling L, Polen T, Wolters DA, Bott M. 2014. Pupylated proteins in Corynebacterium glutamicum revealed by MudPIT analysis. Proteomics 14:1531-1542. http://dx.doi.org/10.1002/pmic.201300531.
31. Cerda-Maira FA, McAllister F, Bode NJ, Burns KE, Gygi SP, Darwin KH. 2011. Reconstitution of the Mycobacterium tuberculosis pupylation pathway in Escherichia coli. EMBO Rep 12:863-870. http://dx.doi.org/10.1038/embor.2011.109.
32. Barandun J, Delley CL, Weber-Ban E. 2012. The pupylation pathway and its role in mycobacteria. BMC Biol 10:95. http://dx.doi.org/10.1186/1741-7007-10-95.
33. Chater K. 2011. Differentiation in Streptomyces: the properties and programming of diverse cell types, p 43-86. In Dyson P (ed), Streptomyces: molecular biology and biotechnology. Caister Academic Press, Norfolk, United Kingdom.
34. McCormick JR, Flardh K. 2012. Signals and regulators that govern Streptomyces development. FEMS Microbiol Rev 36:206-231. http://dx.doi.org/10.1111/j.1574-6976.2011.00317.x.
35. de Crecy-Lagard V, Servant-Moisson P, Viala J, Grandvalet C, Mazodier P. 1999. Alteration of the synthesis of the Clp ATP-dependent protease affects morphological and physiological differentiation in Streptomyces. Mol Microbiol 32:505-517. http://dx.doi.org/10.1046/j.1365-2958.1999.01364.x.
36. Lee CJ, Won HS, Kim JM, Lee BJ, Kang SO. 2007. Molecular domain organization of BldD, an essential transcriptional regulator for developmental process of Streptomyces coelicolor A3(2). Proteins 68:344-352. http://dx.doi.org/10.1002/prot.21338.
37. Kieser T, Bibb MJ, Chater K, Hopwood DA. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, United Kingdom.
38. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Raynal A, Karray F, Tuphile K, Darbon-Rongere E, Pernodet JL. 2006. Excisable cassettes: new tools for functional analysis of Streptomyces genomes. Appl Environ Microbiol 72:4839-4844. http://dx.doi.org/10.1128/AEM.00167-06.
40. Xu D, Seghezzi N, Esnault C, Virolle MJ. 2010. Repression of antibiotic production and sporulation in Streptomyces coelicolor by overexpression of a TetR family transcriptional regulator. Appl Environ Microbiol 76: 7741-7753. http://dx.doi.org/10.1128/AEM.00819-10.
41. Lautru S, Oves-Costales D, Pernodet JL, Challis GL. 2007. MbtH-like protein-mediated cross-talk between non-ribosomal peptide antibiotic and siderophore biosynthetic pathways in Streptomyces coelicolor M145. Microbiology 153:1405-1412. http://dx.doi.org/10.1099/mic.0.2006/003145-0.
42. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M, Yefanov A, Lee H, Zhang N, Robertson CL, Serova N, Davis S, Soboleva A. 2013. NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res 41:D991-D995. http://dx.doi.org/10.1093/nar/gks1193.
43. Castro-Melchor M, Charaniya S, Karypis G, Takano E, Hu WS. 2010. Genome-wide inference of regulatory networks in Streptomyces coelicolor. BMC Genomics 11:578. http://dx.doi.org/10.1186/1471-2164-11-578.
44. Thomas L, Hodgson DA, Wentzel A, Nieselt K, Ellingsen TE, Moore J, Morrissey ER, Legaie R, Wohlleben W, Rodriguez-Garcia A, Martin JF, Burroughs NJ, Wellington EM, Smith MC. 2012. Metabolic switches and adaptations deduced from the proteomes of Streptomyces coelicolor wild type and phoP mutant grown in batch culture. Mol Cell Proteomics 11: M111.013797. http://dx.doi.org/10.1074/mcp. M111.013797.
45. Bibb MJ, White J, Ward JM, Janssen GR. 1994. The mRNA for the 23S rRNA methylase encoded by the ermE gene of Saccharopolyspora erythraea is translated in the absence of a conventional ribosomebinding site. Mol Microbiol 14:533-545. http://dx.doi.org/10.1111/j.1365-2958.1994.tb02187.x.
46. Mao XM, Sun N, Wang F, Luo S, Zhou Z, Feng WH, Huang FL, Li YQ.2013. Dual positive feedback regulation of protein degradation of an extra-cytoplasmic function sigma factor for cell differentiation in Streptomyces coelicolor. J Biol Chem 288:31217-31228. http://dx.doi.org/10.1074/jbc. M113.491498.
47. Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, Hopwood DA, van Wezel GP. 2008. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9:670-675. http://dx.doi.org/10.1038/embor.2008.83.
48. Chater KF. 1972. A morphological and genetic mapping study of white colony mutants of Streptomyces coelicolor. J Gen Microbiol 72:9-28. http://dx.doi.org/10.1099/00221287-72-1-9.
49. Fowler-Goldsworthy K, Gust B, Mouz S, Chandra G, Findlay KC, Chater KF. 2011. The actinobacteria-specific gene wblA controls major developmental transitions in Streptomyces coelicolor A3(2). Microbiology 157:1312-1328. http://dx.doi.org/10.1099/mic.0.047555-0.
50. Hopwood DA, Wildermuth H, Palmer HM. 1970. Mutants of Streptomyces coelicolor defective in sporulation. J Gen Microbiol 61:397-408. http://dx.doi.org/10.1099/00221287-61-3-397.
51. Darwin KH, Lin G, Chen Z, Li H, Nathan CF. 2005. Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue. Mol Microbiol 55:561-571.
52. Lamichhane G, Raghunand TR, Morrison NE, Woolwine SC, Tyagi S, Kandavelou K, Bishai WR. 2006. Deletion of a Mycobacterium tuberculosis proteasomal ATPase homologue gene produces a slow-growing strain that persists in host tissues. J Infect Dis 194:1233-1240. http://dx.doi.org/10.1086/508288.
53. Chen X, Qiu JD, Shi SP, Suo SB, Liang RP. 2013. Systematic analysis and prediction of pupylation sites in prokaryotic proteins. PLoS One 8:e74002. http://dx.doi.org/10.1371/journal.pone.0074002.
54. Liu Z, Ma Q, Cao J, Gao X, Ren J, Xue Y. 2011. GPS-PUP: computational prediction of pupylation sites in prokaryotic proteins. Mol Biosyst 7:2737-2740. http://dx.doi.org/10.1039/c1mb05217a.
55. Tung CW. 2013. Prediction of pupylation sites using the composition ofk-spaced amino acid pairs. J Theor Biol 336:11-17. http://dx.doi.org/10.1016/j.jtbi.2013.07.009.
56. Liu G, Chater KF, Chandra G, Niu G, Tan H. 2013. Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev 77:112-143. http://dx.doi.org/10.1128/MMBR.00054-12.
57. Bishop A, Fielding S, Dyson P, Herron P. 2004. Systematic insertional mutagenesis of a streptomycete genome: a link between osmoadaptation and antibiotic production. Genome Res 14:893-900. http://dx.doi.org/10.1101/gr.1710304.
58. Bennett JA, Yarnall J, Cadwallader AB, Kuennen R, Bidey P, Stadelmaier B, McCormick JR. 2009. Medium-dependent phenotypes of Streptomyces coelicolor with mutations in ftsI or ftsW. J Bacteriol 191:661-664. http://dx.doi.org/10.1128/JB.01048-08.
59. Springer B, Master S, Sander P, Zahrt T, McFalone M, Song J, Papavinasasundaram KG, Colston MJ, Boettger E, Deretic V. 2001. Silencing of oxidative stress response in Mycobacterium tuberculosis: expression patterns of ahpC in virulent and avirulent strains and effect of ahpC inactivation. Infect Immun 69:5967-5973. http://dx.doi.org/10.1128/IAI.69.10.5967-5973.2001.
60. Compton CL, Fernandopulle MS, Nagari RT, Sello JK. 2015. Genetic and proteomic analyses of pupylation in Streptomyces coelicolor. J Bacteriol 197:2747-2753. http://dx.doi.org/10.1128/JB.00302-15.