Quantitative proteome analysis of streptomyces coelicolor nonsporulating liquid cultures demonstrates a complex differentiation process comparable to that occurring in sporulating solid cultures

Journal of Proteome Research

Volumn 9, Issue 9, 2010, Pages 4801-4811

  Manteca, Angel ^a,b   Jung, Hye R ^a   Schwaömmle, Veit ^a   Jensen, Ole N ^a   Sanchez, Jesus ^b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSIDAD DE OVIEDO   (Spain)

Author keywords

differentiation; iTRAQ; proteome; Streptomyces coelicolor

Indexed keywords

PROTEOME;

ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; LIQUID CULTURE; MYCELIUM; NONHUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; QUANTITATIVE ANALYSIS; STREPTOMYCES COELICOLOR; UPREGULATION;

BACTERIAL PROTEINS; CELL CULTURE TECHNIQUES; CLUSTER ANALYSIS; FERMENTATION; FUZZY LOGIC; INDUSTRIAL MICROBIOLOGY; ISOTOPE LABELING; PROTEOME; PROTEOMICS; STREPTOMYCES COELICOLOR;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 77956329728     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100513p     Document Type: Article

References (51)

1. Tamaoki, T.; Nakano, H. Potent and specific inhibitors of protein kinase C of microbial origin Biotechnology 1990, 8 (8) 732-735
2. Omura, S. The expanded horizon for microbial metabolites - a review Gene 1992, 115 (1-2) 141-149
3. 3Umezawa, K. Induction of cellular differentiation and apoptosis by signal transduction inhibitors Adv. Enzyme Regul. 1997, 37, 393-401
4. Champness, W. C. Prokaryotic Development; Brun, Y. V.; Skimkets, L. J, Ed.; Actinomycete Development, Antibiotic Production and Phylogeny: Questions and Challenges; American Society for Microbiology: Washington, DC, 2000; pp 11 - 31.
5. Rueda, B.; Miguelez, E. M.; Hardisson, C.; Manzanal, M. B. Mycelial differentiation and spore formation by Streptomyces brasiliensis in liquid culture Can. J. Microbiol. 2001, 47 (11) 1042-1047
6. Stocks, S. M.; Thomas, C. R. Viability, strength, and fragmentation of Saccharopolyspora erythraea in submerged fermentation Biotechnol. Bioeng. 2001, 75 (6) 702-709
7. Pamboukian, C. R. D.; Guimaraes, L. M.; Candida, M. Applications of image analysis in the characterization of Streptomyces olindensis in submerged culture Braz. J. Microbiol. 2002, 33, 17-21
8. Manteca, A.; Alvarez, R.; Salazar, N.; Yaguöe, P.; Sanchez, J. Mycelium differentiation and antibiotic production in liquid cultures of Streptomyces coelicolor Appl. Environ. Microbiol. 2008, 74 (12) 3877-3886
9. Yaguöe, P.; Manteca, A.; Simon, A.; Diaz-Garcia, M. E.; Sanchez, J. A new method for monitoring programmed cell death and differentiation in submerged cultures of Streptomyces Appl. Environ. Microbiol. 2010, 76 (10) 3401-3404
10. Flaördh, K.; Buttner, M. J. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium Nat. Rev. Microbiol. 2009, 7 (1) 36-49
11. Manteca, A.; Fernandez, M.; Sanchez, J. A death round affecting a young compartmentalized mycelium precedes aerial mycelium dismantling in confluent solid cultures of Streptomyces antibioticus Microbiology 2005, 151 (11) 3689-3697
12. Manteca, A.; Fernandez, M.; Sanchez, J. Mycelium development in Streptomyces antibioticus ATCC11891 occurs in an orderly pattern which determines multiphase growth curves BMC Microbiol. 2005, 5, 51
13. Manteca, A.; Fernandez, M.; Sanchez, J. Cytological and biochemical evidence for an early cell dismantling event in solid cultures of Streptomyces antibioticus Res. Microbiol. 2006, 157 (2) 143-152
14. Manteca, A.; Maöder, U.; Connolly, B. A.; Sanchez, J. A proteomic analysis of Streptomyces coelicolor programmed cell death Proteomics 2006, 6 (22) 6008-6022
15. Manteca, A.; Claessen, D.; Lopez-Iglesias, C.; Sanchez, J. Aerial hyphae in solid cultures of Streptomyces lividans and Streptomyces coelicolor originate from viable segments surviving an early programmed cell death event FEMS Microbiol. Lett. 2007, 274 (1) 118-125
16. Manteca, A.; Sanchez, J. Streptomyces development in colonies and soils Appl. Environ. Microbiol. 2009, 75 (9) 2920-2924
17. Manteca, A.; Sanchez, J.; Jung, H. R.; Schwaömmle, V.; Jensen, O. N. Quantitative proteomic analysis of Streptomyces coelicolor development demonstrates that onset of secondary metabolism coincides with hyphae differentiation Mol. Cell. Proteomics 2010, 9 (7) 1423-1436
18. Claessen, D.; Woösten, H. A. B.; van Keulen, G.; Faber, O. G.; Alves, A. M.; Meijer, W. G.; Dijkhuizen, L. Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic solid Mol. Microbiol. 2002, 44 (6) 1483-1492
19. Claessen, D.; Rink, R.; de Jong, W.; Siebring, J.; e Vreugd, P.; Boersma, F. G. H.; Dijkhuizen, L.; Wosten, H. A. A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils Genes Dev. 2003, 17 (14) 1714-1726
20. Bobek, J.; Halada, P.; Angelis, J.; Vohradsky, J.; Mikulík, K. Activation and expression of proteins during synchronous germination of aerial spores of Streptomyces granaticolor Proteomics 2004, 4 (12) 3864-3880
21. Piette, A.; Derouaux, A.; Gerkens, P.; Noens, E. E.; Mazzucchelli, G.; Vion, S.; Koerten, H. K.; Titgemeyer, F.; De Pauw, E.; Leprince, P.; van Wezel, G. P.; Galleni, M.; Rigali, S. From dormant to germinating spores of Streptomyces coelicolor A3(2): new perspectives from the crp null mutant J. Proteome Res. 2005, 4 (5) 1699-1708
22. Kim, D. W.; Chater, K.; Lee, K. J.; Hesketh, A. Changes in the extracellular proteome caused by the absence of the bldA gene product, a developmentally significant tRNA, reveal a new target for the pleiotropic regulator AdpA in Streptomyces coelicolor J. Bacteriol. 2005, 187 (9) 2957-2966
23. Kim, D. W.; Chater, K. F.; Lee, K. J.; Hesketh, A. Effects of growth phase and the developmentally significant bldA-specified tRNA on the membrane-associated proteome of Streptomyces coelicolor Microbiology 2005, 151 (8) 2707-2720
24. Hesketh, A.; Bucca, G.; Laing, E.; Flett, F.; Hotchkiss, G.; Smith, C. P.; Chater, K. F. New pleiotropic effects of eliminating a rare tRNA from Streptomyces coelicolor, revealed by combined proteomic and transcriptomic analysis of liquid cultures BMC Genomics 2007, 8, 261
25. Rodríguez-García, A.; Barreiro, C.; Santos-Beneit, F.; Sola-Landa, A.; Martin, J. F. Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a DeltaphoP mutant Proteomics 2007, 7 (14) 2410-2429
26. Novotna, J.; Vohradsky, J.; Berndt, P.; Gramajo, H.; Langen, H.; Li, X. M.; Minas, W.; Orsaria, L.; Roeder, D.; Thompson, C. J. 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. 2003, 48 (5) 1289-1303
27. Akanuma, G.; Hara, H.; Ohnishi, Y.; Horinouchi, S. Dynamic changes in the extracellular proteome caused by absence of a pleiotropic regulator AdpA in Streptomyces griseus Mol. Microbiol. 2009, 73 (5) 898-912
28. Birko, Z.; Swiatek, M.; Szajli, E.; Medzihradszky, K. F.; Vijgenboom, E.; Penyige, A.; Keseru, J.; van Wezel, G. P.; Biro, S. Lack of A-factor Production Induces the Expression of Nutrient Scavenging and Stress-related Proteins in Streptomyces griseus Mol. Cell. Proteomics 2009, 8 (10) 2396-2403
29. Jayapal, K. P.; Philp, R. J.; Kok, Y. J.; Yap, M. G.; Sherman, D. H.; Griffin, T. J.; Hu, W. S. Uncovering genes with divergent mRNA-protein dynamics in Streptomyces coelicolor PLoS One 2008, 3 e2097
30. Nieselt, K.; Battke, F.; Herbig, A.; Bruheim, P.; Wentzel, A.; Jakobsen, O. M.; Sletta, H.; Alam, M. T.; Merlo, M. E.; Moore, J.; Omara, W.; Morrissey, E. R.; Hermosillo, M. J.; Rodriguez-Garcia, A.; Nentwich, M.; Thomas, L.; Legaie, R.; Gaze, W. H.; Challis, G. L.; Jansen, R. C.; Dijkhuizen, J.; Rand, D. A.; Wild, D. L.; Bonin, M.; Reuther, J.; Wohlleben, W.; Smith, M. C.; Burroughs, N. J.; Martin, J. F.; Hodgson, D. A.; Takano, E.; Breitling, R.; Ellingsen, T. E.; Wellington, E. M. The dynamic architecture of the metabolic switch in Streptomyces coelicolor BMC Genomics 2010, 11, 10
31. Novella, I. S.; Barbes, C.; Sanchez, J. Sporulation of Streptomyces antibioticus ETHZ 7451 in liquid culture Can. J. Microbiol. 1992, 38 (8) 769-773
32. Quiros, L. M.; Hardisson, C.; Salas, J. A. Isolation and properties of Streptomyces spore membranes J. Bacteriol. 1986, 165 (3) 923-928
33. Fernandez, M.; Sanchez, J. Nuclease activities and cell death processes associated with the developmenton solid cultures of Streptomyces antibioticus ETH7451 Microbiology 2002, 148 (2) 405-412
34. Bradford, M. M. A rapid and sensitive for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
35. Lowry, O. H.; Rosenbrough, N. J.; Farr, A. L.; Randall, R. J. Protein measurement with the Folin phenol reagent J. Biol. Chem. 1951, 193 (1) 265-275
36. Sachon, E.; Mohammed, S.; Bache, N.; Jensen, O. N. Phosphopeptide quantitation using amine-reactive isobaric tagging reagents and tandem mass spectrometry: application to proteins isolated by gel electrophoresis Rapid Commun. Mass Spectrom. 2006, 20 (7) 1127-1134
37. Bezdek, J. C. Pattern Recognition with Fuzzy Objective Function Algorithms; Plenum Press: New York, 1981.
38. Xie, X. L.; Beni, G. A validity measure for fuzzy clustering IEEE Trans. Pattern Anal. Mach. Intell. 1991, 13 (8) 841-847
39. Schwaömmle, V.; Jensen, O. N. A simple and fast method to determine the parameters for fuzzy c-means cluster validation. Quant. Methods, submitted for publication, 2010. DOI: arXiv:1004.1307v1.
40. Tahlan, K.; Yu, Z.; Xu, Y.; Davidson, A. R.; Nodwell, J. R. Ligand recognition by ActR, a TetR-like regulator of actinorhodin export J. Mol. Biol. 2008, 383 (4) 753-761
41. Ou, X.; Zhang, B.; Zhang, L.; Zhao, G.; Ding, X. Characterization of rrdA, a TetR family protein gene involved in the regulation of secondary metabolism in Streptomyces coelicolor Appl. Environ. Microbiol. 2009, 75 (7) 2158-216
42. Duong, C. T.; Lee, H. N.; Choi, S. S.; Lee, S. Y. Functional Expression of SAV3818, a Putative TetR-Family Transcriptional Regulatory Gene from Streptomyces avermitilis, Stimulates Antibiotic Production in Streptomyces Species J. Microbiol. Biotechnol. 2009, 19 (2) 136-139
43. Chahal, H. K.; Dai, Y.; Saini, A.; Ayala-Castro, C.; Outten, F. W. The SufBCD Fe-S scaffold complex interacts with SufA for Fe-S cluster transfer Biochemistry 2009, 48 (44) 10644-10653
44. Errington, J. Septation and chromosome segregation during sporulation in Bacillus subtilis Curr. Opin. Microbiol. 2001, 4, 660-666
45. Chater, K. F.; Chandra, G. The use of the rare UUA codon to define "expression space" for genes involved in secondary metabolism, development and environmental adaptation in Streptomyces J. Microbiol. 2008, 46 (1) 1-11
46. Willey, J. M.; Santamaria, R. I.; Guijarro, J.; Geistlich, M.; Losick, R. Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor Cell 1991, 65 (4) 641-650
47. Willey, J. M.; Schwedock, J.; Losick, R. Multiple extracellular signals govern the production of a morphogenetic protein involved in aerial mycelium formation by Streptomyces coelicolor Genes Dev. 1993, 7 (5) 895-903
48. Nguyen, K. T.; Willey, J. M.; Nguyen, L. D.; Nguyen, L. T.; Viollier, P. H.; Thompson, C. J. A central regulator of morphological differentiation in the multicellular bacterium Streptomyces coelicolor Mol. Microbiol. 2002, 46 (5) 1223-1238
49. Nodwell, J. R.; McGovern, K.; Losick, R. An oligopeptide permease responsible for the import of an extracellular signaling molecule governing aerial mycelium formation in Streptomyces coelicolor Mol. Microbiol. 1996, 22 (5) 881-893
50. Nodwell, J. R.; Losick, R. Purification of an extracellular signaling molecule involved in aerial mycelium formation by Streptomyces coelicolor J. Bacteriol. 1998, 180 (5) 334-1337
51. Bignell, D. R.; Warawa, J. L.; Strap, J. L.; Chater, K. F. Study of the bldG locus suggests that an anti-anti-sigma factor and an anti-sigma factor may be involved in Streptomyces coelicolor antibiotic production and sporulation Microbiology 2000, 146 (9) 2161-2173