Quantitative proteomic analysis of the heat stress response in Clostridium difficile strain 630

Journal of Proteome Research

Volumn 10, Issue 9, 2011, Pages 3880-3890

  Jain, Shailesh ^a   Graham, Ciaren ^a,b   Graham, Robert L J ^a,c   McMullan, Geoff ^a   Ternan, Nigel G ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

adaptation; Clostridium difficile; heat stress; iTRAQ; multidimensional; proteomics

Indexed keywords

4 AMINOBUTYRIC ACID; CARRIER PROTEIN; CHAPERONIN; ENDOPEPTIDASE CLP; HEAT SHOCK PROTEIN; HYDROGENASE; PEPTIDOGLYCAN; PROTEIN; PROTEIN DNAK; PROTEIN HTPG; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CLOSTRIDIUM DIFFICILE; GLYCOLYSIS; GLYCOPROTEIN SYNTHESIS; HEAT STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS;

BACTERIAL PROTEINS; CLOSTRIDIUM DIFFICILE; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; PROTEOMICS; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY;

CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE 630;

EID: 80052509484     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200327t     Document Type: Article

References (98)

1. Battistuzzi, F. U.; Feijao, A.; Hedges, S. B. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land BMC Evol. Biol. 2004, 4, 44
2. Wilkinson, S. R.; Young, D. I.; Morris, J. G.; Young, M. Molecular-genetics and the initiation of solventogenesis in Clostridium- berijerinckii (formerly Clostridium-acetobutylicum) NCIMB-8052 FEMS Microbiol. Rev. 1995, 17, 275-285
3. Nolling, J.; Breton, G.; Omelchenko, M. V.; Makarova, K. S.; Zeng, Q. D.; Gibson, R.; Lee, H. M.; Dubois, J.; Qiu, D. Y.; Hitti, J.; Wolf, Y. I.; Tatusov, R. L.; Sabathe, F.; Doucette-Stamm, L.; Soucaille, P.; Daly, M. J.; Bennett, G. N.; Koonin, E. V.; Smith, D. R. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum J. Bacteriol. 2001, 183, 4823-4838 (Pubitemid 32708967)
4. Lee, S. M.; Cho, M. O.; Park, C. H.; Chung, Y.-C.; Kim, J. H.; Sang, B.-I.; Um, Y. Continuous butanol production using suspended and immobilized Clostridium beijerinckii NCIMB 8052 with supplementary butyrate Energy Fuels 2008, 22, 3459-3464
5. Tamaru, Y.; Miyake, H.; Kuroda, K.; Ueda, M.; Doi, R. Comparative genomics of the mesophilic cellulosome-producing Clostridium cellulovorans and its application to biofuel production via consolidated bioprocessing Environ. Technol. 2010, 31, 889-903
6. Bartlett, J. G. Narrative review: The new epidemic of Clostridium difficile -associated enteric disease Ann. Intern. Med. 2006, 145, 758-764 (Pubitemid 351650356)
7. Sheth, A. N.; Wiersma, P.; Atrubin, D.; Dubey, V.; Zink, D.; Skinner, G.; Doerr, F.; Juliao, P.; Gonzalez, G.; Burnett, C.; Drenzek, C.; Shuler, C.; Austin, J.; Ellis, A.; Maslanka, S.; Sobel, J. International Outbreak of Severe Botulism with Prolonged Toxemia Caused by Commercial Carrot Juice Clin. Inf. Dis. 2008, 47, 1245-1251
8. Stabler, R. A.; He, M.; Dawson, L.; Martin, M.; Valiente, E.; Corton, C.; Lawley, T. D.; Sebaihia, M.; Quail, M. A.; Rose, G.; Gerding, D. N.; Gibert, M.; Popoff, M. R.; Parkhill, J.; Dougan, G.; Wren, B. W. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium BMC Genome Biol. 2009, 10, R102
9. Dubberke, E. R.; Reske, K. A.; Noble-Wang, J.; Thompson, A.; Killgore, G.; Mayfield, J.; Camins, B.; Woeltje, K.; McDonald, J. R.; McDonald, L. C.; Fraser, V. J. Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities Am. J. Infect. Control 2007, 35, 315-318 (Pubitemid 46907328)
10. Poutanen, S. M.; Simor, A. E. Clostridium difficile -associated diarrhea in adults Can. Med. Assoc. J. 2004, 171, 51-58 (Pubitemid 38925121)
11. Voth, D. E.; Ballard, J. D. Clostridium difficile toxins: Mechanism of action and role in disease Clin. Microbiol. Rev. 2005, 18, 247-263 (Pubitemid 40548293)
12. Johnson, S. Recurrent Clostridium difficile infection: A review of risk factors, treatments, and outcomes J. Infect. 2009, 58, 403-410
13. McFarland, L. V. Update on the changing epidemiology of Clostridium difficile -associated disease Nat. Clin. Pract. Gastroenterolo. Hepatol. 2008, 5, 40-48
14. Pepin, J.; Saheb, N.; Coulombe, M. A.; Alary, M. E.; Corriveau, M. P.; Authier, S.; Leblanc, M.; Rivard, G.; Bettez, M.; Primeau, V.; Nguyen, M.; Jacob, C. E.; Lanthier, L. Emergence of fluoroquinolones as the predominant risk factor for Clostridium difficile -associated diarrhea: A cohort study during an epidemic in Quebec Clin. Inf. Dis. 2005, 41, 1254-1260 (Pubitemid 41532667)
15. McDonald, L. C.; Killgore, G. E.; Thompson, A.; Owens, R. C.; Kazakova, S. V.; Sambol, S. P.; Johnson, S.; Gerding, D. N. An epidemic, toxin gene-variant strain of Clostridium difficile New Engl. J. Med. 2005, 353, 2433-2441 (Pubitemid 41770164)
16. Sebaihia, M.; Wren, B. W.; Mullany, P.; Fairweather, N. F.; Minton, N. P.; Stabler, R.; Thomson, N. R.; Roberts, A. P.; Cerdeno-Tarraga, A. M.; Wang, H.; Holden, M. T.; Wright, A.; Churcher, C.; Quail, M. A.; Baker, S.; Bason, N.; Brooks, K.; Chillingworth, T.; Cronin, A.; Davis, P.; Dowd, L.; Fraser, A.; Feltwell, T.; Hance, Z.; Holroyd, S.; Jagels, K.; Moule, S.; Mungall, K.; Price, C.; Rabbinowitsch, E.; Sharp, S.; Simmonds, M.; Stevens, K.; Unwin, L.; Whithead, S.; Dupuy, B.; Dougan, G.; Barrell, B.; Parkhill, J. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome Nat. Genet. 2006, 38, 779-786 (Pubitemid 43980598)
17. He, M.; Sebaihia, M.; Lawley, T. D.; Stabler, R. A.; Dawson, L. F.; Martin, M. J.; Holt, K. E.; Seth-Smith, H. M. B.; Quail, M. A.; Rance, R.; Brooks, K.; Churcher, C.; Harris, D.; Bentley, S. D.; Burrows, C.; Clark, L.; Corton, C.; Murray, V.; Rose, G.; Thurston, S.; van Tonder, A.; Walker, D.; Wren, B. W.; Dougan, G.; Parkhill, J. Evolutionary dynamics of Clostridium difficile over short and long time scales Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 7527-7532
18. Clostridium difficile ribotyping network for England and Northern Ireland 2008/09 report; London, 2009.
19. Janvilisri, T.; Scaria, J.; Thompson, A. D.; Nicholson, A.; Limbago, B. M.; Arroyo, L. G.; Songer, J. G.; Grohn, Y. T.; Chang, Y. F. Microarray identification of Clostridium difficile core components and divergent regions associated with host origin J. Bacteriol. 2009, 191, 3881-3891
20. Heap, J. T.; Kuehne, S. A.; Ehsaana, M.; Cartman, S. T.; Cooksley, C. M.; Scott, J. C.; Minton, N. P. The ClosTron: Mutagenesis in Clostridium refined and streamlined J. Microbiol. Meth. 2010, 80, 49-55
21. Jain, S.; Graham, R. L. J.; McMullan, G.; Ternan, N. G. Proteomic analysis of the insoluble subproteome of Clostridium difficile strain 630 FEMS Microbiol. Lett. 2010, 312, 151-159
22. Marsden, G. L.; Davis, I. J.; Wright, V. J.; Sebaihia, M.; Kuijper, E. J.; Minton, N. P. Array comparative hybridisation reveals a high degree of similarity between UK and European clinical isolates of hypervirulent Clostridium difficile BMC Genomics 2010, 11, 389
23. Emerson, J. E.; Stabler, R. A.; Wren, B. W.; Fairweather, N. F. Microarray analysis of the transcriptional responses of Clostridium difficile to environmental and antibiotic stress J. Med. Microbiol. 2008, 57, 757-64 (Pubitemid 351842069)
24. Bradford, M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
25. Unwin, R. D.; Pierce, A.; Watson, R. B.; Sternberg, D. W.; Whetton, A. D. Quantitative proteomic analysis using isobaric protein tags enables rapid comparison of changes in transcript and protein levels in transformed cells Mol. Cell. Proteomics 2005, 4, 924-935 (Pubitemid 41309150)
26. Unwin, R. D.; Smith, D. L.; Blinco, D.; Wilson, C. L.; Miller, C. J.; Evans, C. A.; Jaworska, E.; Baldwin, S. A.; Barnes, K.; Pierce, A.; Spooncer, E.; Whetton, A. D. Quantitative proteomics reveals posttranslational control as a regulatory factor in primary hematopoietic stem cells Blood 2006, 107, 4687-4694 (Pubitemid 43882616)
27. Dobbin, E.; Graham, C.; Freeburn, R. W.; Unwin, R. D.; Griffiths, J. R.; Pierce, A.; Whetton, A. D.; Wheadon, H. Proteomic analysis reveals a novel mechanism induced by the leukaemic oncogene Tel/PDGFRβ in stem cells: Activation of the interferon response pathways Stem Cell Res. 2010, 5, 226-243
28. Williamson, A. J. K.; Smith, D. L.; Blinco, D.; Unwin, R. D.; Pearson, S.; Wilson, C.; Miller, C.; Lancashire, L.; Lacaud, G.; Kouskoff, V.; Whetton, A. D. Quantitative Proteomics analysis demonstrates post-transcriptional regulation of embryonic stem cell differentiation to hematopoiesis Mol. Cell. Proteomics 2008, 7, 459-472 (Pubitemid 351472457)
29. Muthukrishnan, G.; Quinn, G. A.; Lamers, R. P.; Diaz, C.; Cole, A. L.; Chen, S.; Cole, A. M. Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage J. Proteome Res. 2011, 10, 2064-2078
30. Soares, N. C.; Cabral, M. P.; Gayoso, C.; Mallo, S.; Rodriguez-Velo, P.; Fernández-Moreira, E.; Bou, G. Associating Growth-phase-related changes in the proteome of Acinetobacter baumannii with increased resistance to oxidative stress J. Proteome Res. 2010, 9, 1951-1964
31. Zhao, Z.; Stanley, B. A.; Zhang, W.; Assmann, S. M. ABA-regulated g protein signaling in arabidopsis guard cells: A proteomic perspective J. Proteome Res. 2010, 9, 1637-1647
32. Han, D.; Moon, S.; Kim, H.; Choi, S.-E.; Lee, S.-J.; Park, K. S.; Jun, H.; Kang, Y.; Kim, Y. Detection of differential proteomes associated with the development of type 2 diabetes in the zucker rat model using the iTRAQ technique J. Proteome Res. 2011, 10, 564-577
33. Graham, R.L.J.; Sharma, M. K.; Ternan, N. G.; Weatherly, D. B.; Tarleton, R. L.; McMullan, G. A semi-quantitative GeLC-MS analysis of temporal proteome expression in the emerging nosocomial pathogen Ochrobactrum anthropi BMC Genome Biol. 2007, 8, R110
34. Gardy, J. L.; Laird, M. R.; Chen, F.; Rey, S.; Walsh, C. J.; Ester, M.; Brinkman, F. S. L. Psortb v.2.0: Expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis Bioinformatics 2005, 21, 617-623 (Pubitemid 40424787)
35. Bendtsen, J.; Nielsen, H.; von Heijne, G.; Brunak, S. Improved prediction of signal peptides: Signalp 3.0 J. Mol. Biol. 2004, 340, 783-795 (Pubitemid 38829638)
36. Bendtsen, J.; Kiemer, L.; Fausboll, A.; Brunak, S. Non-classical protein secretion in bacteria BMC Microbiol. 2005, 5, 58
37. Matsuda, K.; Tsuji, H.; Asahara, T.; Kado, Y.; Nomoto, K. Sensitive quantitative detection of commensal bacteria by rRNA-targeted reverse transcription-PCR Appl. Environ. Microbiol. 2007, 73, 32-39 (Pubitemid 46079932)
38. Lemèe, L.; Bourgeois, I.; Ruffin, E.; Collignon, A.; Lemeland, J. F.; Pons, J. L. Multilocus sequence analysis and comparative evolution of virulence-associated genes and housekeeping genes of Clostridium difficile Microbiology-SGM 2005, 151, 3171-3180 (Pubitemid 41488902)
39. Lemèe, L.; Dhalluin, A.; Pestel-Caron, M.; Lemeland, J.; Pons, J. Multilocus sequence typing analysis of human and animal Clostridium difficile isolates of various toxigenic types J. Clin. Microbiol. 2004, 42, 2609-2617 (Pubitemid 38747511)
40. Karlsson, S.; Dupuy, B.; Mukherjee, K.; Norin, E.; Burman, L. G.; Åkerlund, T. Expression of Clostridium difficile Toxins A and B and their sigma factor TcdD is controlled by temperature Infect. Immun. 2003, 71, 1784-1793 (Pubitemid 36368707)
41. Janvilisri, T; Scaria, J.; Chang, Y. F. Transcriptional profiling of Clostridium difficile and Caco-2 cells during infection J. Inf. Dis. 2010, 202, 282-290
42. Wright, A.; Wait, R.; Begum, S.; Crossett, B.; Nagy, J.; Brown, K.; Fairweather, N. Proteomic analysis of cell surface proteins from Clostridium difficile Proteomics 2005, 5, 2443-2452 (Pubitemid 40835415)
43. Lawley, T. D.; Croucher, N. J.; Yu, L.; Clare, S.; Sebaihia, M.; Goulding, D.; Pickard, D. J.; Parkhill, J.; Choudhary, J.; Dougan, G. Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores J. Bacteriol. 2009, 191, 5377-5386
44. Kachman, M. T.; Hurley, M. C.; Thiele, T.; Srinivas, G.; Aronoff, D. M. Comparative analysis of the extracellular proteomes of two Clostridium sordellii strains exhibiting contrasting virulence Anaerobe 2010, 16, 454-460
45. Sengupta, N.; Alam, S. I.; Kumar, B.; Kumar, R. B.; Gautam, V.; Kumar, S.; Singh, L. Comparative proteomic analysis of extracellular proteins of Clostridium perfringens Type A and Type C strains Inf. Immun. 2010, 78, 3957-3968
46. Alam, S. I.; Bansod, S.; Kumar, R. B.; Sengupta, N.; Singh, L. Differential proteomic analysis of Clostridium perfringens ATCC13124; identification of dominant, surface and structure associated proteins BMC Microbiol. 2009, 9 Art. No. 162
47. Bartlett, J. G. Historical perspectives on studies of Clostridium difficile and C. difficile infection Clin. Infect. Dis. 2008, 48 (Suppl 1) s4-s11
48. Rosen, R.; Ron, E. Z. Proteome analysis in the study of bacterial heat shock response Mass. Spectrom. Rev. 2002, 21, 244-265
49. Ross, P. L.; Huang, Y. L. N.; Marchese, J. N.; Williamson, B.; Parker, K.; Hattan, S.; Khainovski, N.; Pillai, S.; Dey, S.; Daniels, S.; Purkayastha, S.; Juhasz, P.; Martin, S.; Bartlet-Jones, M.; He, F.; Jacobson, A.; Pappin, D. J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents Mol. Cell. Proteomics 2004, 3, 1154-1169
50. Aggarwal, K.; Choe, L. H.; Lee, K. H. Shotgun proteomics using the iTRAQ isobaric tags Brief. Funct. Genomics Proteomics 2006, 5, 112-120 (Pubitemid 46403004)
51. Chong, P. K.; Gan, C. S.; Pham, T. K.; Wright, P. C. Isobaric tags for relative and absolute quantitation (iTRAQ) reproducibility: Implication of multiple injections J. Proteome Res. 2006, 5, 1232-1240 (Pubitemid 43727802)
52. Graham, R. L. J.; Graham, C.; McMullan, G. Microbial proteomics: a mass spectrometry primer for biologists Microb. Cell. Fact. 2007, 6, 26
53. Danielsen, M.; Hornshøj, H.; Siggers, R. H.; Jensen, B. B.; van Kessel, A. G.; Bendixen, E. Effects of bacterial colonization on the porcine intestinal proteome J. Proteome Res. 2007, 6, 2596-2604 (Pubitemid 47122354)
54. Leuko, S.; Raftery, M. J.; Burns, B. P.; Walter, M. R.; Neilan, B. A. Global protein-level responses of Halobacterium salinarum NRC-1 to prolonged changes in external sodium chloride concentrations J. Proteome Res. 2009, 8, 2218-2225
55. Eshghi, A.; Cullen, P. A.; Cowen, L.; Zuerner, R. L.; Cameron, C. E. Global proteome analysis of Leptospira interrogans J. Proteome Res. 2009, 8, 4564-4578
56. Pham, T. K.; Roy, S.; Noirel, J.; Douglas, I.; Wright, P,C.; Stafford, G. P. A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia Proteomics 2010, 10, 3130-3141
57. Pham, T. K.; Sierocinski, P.; van der Oost, J.; Wright, P. C. Quantitative proteomic analysis of Sulfolobus solfataricus membrane proteins J. Proteome Res. 2010, 5, 1165-1172
58. Graham, R. L. J.; Pollock, C. E.; Ternan, N. G.; McMullan, G. Top-down proteomic analysis of the soluble sub-proteome of the obligate thermophile, Geobacillus thermoleovorans T80: Insights into its cellular processes J. Proteome Res. 2006, 5, 822-828
59. Graham, R. L. J.; O'Loughlin, S. N.; Pollock, C. E.; Ternan, N. G.; Weatherly, D. B.; Jackson, P. J.; Tarleton, R. L.; McMullan, G. A combined shotgun and multidimensional proteomic analysis of the insoluble subproteome of the obligate thermophile, Geobacillus thermoleovorans T80 J. Proteome Res. 2006, 5, 2465-2473 (Pubitemid 44330841)
60. Graham, R. L. J.; Pollock, C. E.; O'Loughlin, S. N.; Ternan, N. G.; Weatherly, D. B.; Jackson, P. J.; Tarleton, R. L.; McMullan, G Multidimensional analysis of the insoluble sub-proteome of Oceanobacillus iheyensis HTE831, an alkaliphilic and halotolerant deep-sea bacterium isolated from the Iheya ridge Proteomics 2007, 7, 82-91 (Pubitemid 46173718)
61. Moszer, I.; Jones, L. M.; Moreira, S.; Fabry, C.; Danchin, A. SubtiList: the reference database for the Bacillus subtilis genome Nucleic Acids Res. 2002, 30, 62-65 (Pubitemid 34679505)
62. Lechat, P.; Hummel, L.; Rousseau, S.; Moszer, I. GenoList: an integrated environment for comparative analysis of microbial genomes Nucleic Acids Res. 2008, 36 (Database issue) D469-474
63. Djordjevic, M. A.; Chen, H. C.; Natera, S.; Van Noorden, G.; Menzel, C.; Taylor, S.; Renard, C.; Geiger, O.; Weller, G. F. A global analysis of protein expression profiles in Sinorhizobium meliloti: discovery of new genes for nodule occupancy and stress adaptation Plant-Microbe Interact. 2003, 16, 508-524 (Pubitemid 36610723)
64. Karp, P. D.; Ouzounis, C. A.; Moore-Kochlacs, C.; Goldovsky, L.; Kaipa, P.; Ahren, D.; Tsoka, S.; Darzentas, N.; Kunin, V.; Lopez-Bigas, N. Expansion of the BioCyc collection of pathway/genome databases to 160 genomes Nucleic Acids Res. 2005, 19, 6083-6089 (Pubitemid 41742547)
65. Carranza, P.; Grunau, A.; Schneider, T.; Hartmann, I.; Lehner, A.; Stephan, R.; Gehrig, P.; Grossmann, J.; Groebel, K.; Hoelzle, L. E.; Eberl, L.; Riedel, K. A gel-free quantitative proteomics approach to investigate temperature adaptation of the food-borne pathogen Cronobacter turicensis 3032 Proteomics 2010, 10, 3248-3261
66. Hecker, M.; Schumann, W.; Volker, U. Heat-shock and general stress response in Bacillus subtilis Mol. Microbiol. 1996, 19, 417-428 (Pubitemid 26052132)
67. Hennequin, C.; Collignon, A.; Karjalainen, T. Analysis of expression of GroEL (Hsp60) of Clostridium difficile in response to stress Microb. Pathog. 2001, 31 (5) 255-260 (Pubitemid 33096070)
68. Homuth, G.; Mogk, A.; Schumann, W. Post-transcriptional regulation of the Bacillus subtilis dnaK operon Mol. Microbiol. 1999, 32, 1183-1197 (Pubitemid 29286659)
69. Derré, I.; Rapoport, G.; Devine, K.; Rose, M.; Msadek, T. ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis Mol. Microbiol. 1999, 32, 581-593 (Pubitemid 29233902)
70. Watanabe, Y. H.; Nakazaki, Y.; Suno, R.; Yoshida, M. Stability of the two wings of the coiled-coil domain of ClpB chaperone is critical for its disaggregation activity Biochem. J. 2010, 421, 71-77
71. Msadek, T.; Dartois, V.; Kunst, F.; Herbaud, M. L.; Denizot, F.; Rapoport, G. ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation Mol. Microbiol. 1998, 27, 899-914 (Pubitemid 28254941)
72. Versteeg, S.; Escher, A.; Wende, A.; Schumann, W. Regulation of the Bacillus subtilis heat shock gene htpG is under positive control J. Bacteriol. 2003, 185, 466-474 (Pubitemid 36070472)
73. Nielsen, A. K.; Breüner, A.; Krzystanek, M.; Andersen, J. T.; Poulsen, T. A.; Olsen, P. B.; Mijakovic, I.; Rasmussen, M. D. Global transcriptional analysis of Bacillus licheniformis reveals an overlap between heat shock and iron limitation stimulon J. Mol. Microbiol. Biotechnol. 2010, 18, 162-173
74. Motojima-Miyazaki, Y.; Yoshida, M.; Motojima, F. Ribosomal protein L2 associates with E. coli HtpG and activates its ATPase activity Biochem. Biophys. Res. Commun. 2010, 400, 241-245
75. Darmon, E.; Noone, D.; Masson, A.; Bron, S.; Kuipers, O. P.; Devine, K. M.; van-Dij, J. M. A novel class of heat and secretion stress-responsive genes is controlled by the autoregulated cssrs two-component system of Bacillus subtilis J. Bacteriol. 2002, 184, 5661-5671
76. Ron, E. Editorial: an update on the bacterial stress response Res. Microbiol. 2009, 160, 243-244
77. Imlay, J. A. How obligatory is anaerobiosis? Mol. Microbiol. 2008, 68, 801-804 (Pubitemid 351581069)
78. Rodrigues, R.; Vicente, J. B.; Félix, R.; Oliveira, S.; Teixeira, M.; Rodrigues-Pousada, C. Desulfovibrio gigas flavodiiron protein affords protection against nitrosative stress in vivo J. Bacteriol. 2006, 188, 2745-2751
79. Hillmann, F.; Fischer, R.-J.; Bahl, H. The rubrerythrin-like protein Hsp21 of Clostridium acetobutylicum is a general stress protein Arch. Microbiol. 2006, 185, 270-276
80. May, A.; Hillmann, F.; Riebe, O.; Fischer, R.-J.; Bahl, H. A rubrerythrin-like oxidative stress protein of Clostridium acetobutylicum is encoded by a duplicated gene and identical to the heat shock protein Hsp21 FEMS Microbiol. Lett. 2006, 238, 249-254 (Pubitemid 39164556)
81. Hillmann, F.; Riebe, O.; Fischer, R.-J.; Mot, A.; Caranto, J. D.; Kurtz, D. M., Jr.; Bahl, H. Reductive dioxygen scavenging by flavo-diiron proteins of Clostridium acetobutylicum FEBS Lett. 2009, 583, 241-245
82. Meyer, J. [FeFe] hydrogenases and their evolution: a genomic perspective Cell. Mol. Life Sci. 2007, 64, 1063-1084 (Pubitemid 46684546)
83. Buckel, W. Special Clostridial Enzymes and fermentation pathways. In Handbook on Clostridia; Dürre, P., Ed.; CRC Press: Boca Raton, FL, 2005; pp 177-220.
84. Gao, H.; Wang, Y.; Liu, X.; Yan, T.; Wu, L.; Alm, E.; Arkin, A.; Thompson, D. K.; Zhou, J. Global Transcriptome Analysis of the Heat Shock Response of Shewanella oneidensis J. Bacteriol. 2004, 186, 7796-7803 (Pubitemid 39463746)
85. Graentzdoerffer, A.; Rauh, D.; Pich, A.; Andreesen, J. R. Molecular and biochemical characterization of two tungsten- and selenium-containing formate dehydrogenases from Eubacterium acidaminophilum that are associated with components of an iron-only hydrogenase Arch. Microbiol. 2003, 179, 116-130 (Pubitemid 36241196)
86. Zindel, U.; Freudenberg, W.; Rieth, M.; Andreesen, J. R.; Schnell, J.; Widdel, F. Eubacterium acidaminophilum sp. nov., a versatile amino acid-degrading anaerobe producing or utilizing H-2 or formate-description and enzymatic studies Arch. Microbiol. 1988, 150, 254-266
87. Janssen, H.; Döring, C.; Ehrenreich, A.; Voigt, B.; Hecker, M.; Bahl, H.; Fischer, R. J. A proteomic and transcriptional view of acidogenic and solventogenic steady-state cells of Clostridium acetobutylicum in a chemostat culture Appl. Microbiol. Biotechnol. 2010, 87, 2209-2206
88. Soderberg, M. A.; Cianciotto, N. P. A Legionella pneumophila peptidyl-prolyl cis-trans isomerase present in culture supernatants is necessary for optimal growth at low temperatures Appl. Environ. Microbiol. 2008, 74, 1634-1638 (Pubitemid 351358460)
89. Göthel, S. F.; Scholz, C.; Schmid, F. X.; Marahiel, M. A. Cyclophilin and trigger factor from Bacillus subtilis catalyze in vitro protein folding and are necessary for viability under starvation conditions Biochemistry 1998, 37, 13392-13399 (Pubitemid 28449584)
90. Bang, N.; Pecht, A.; Raddatz, G.; Scior, T.; Solbach, W.; Brune, K.; Pahl, A. Prolyl isomerases in a minimal cell-Catalysis of protein folding by trigger factor from Mycoplasma genitalium Eur. J. Biochem. 2000, 267, 3270-3280 (Pubitemid 30341155)
91. Maki, Y.; Yoshida, H.; Wada, A. Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary phase Escherichia coli Genes Cells 2000, 5, 965-974 (Pubitemid 32156740)
92. Agafonov, D. E.; Spirin, A. S. The ribosome-associated inhibitor A reduces translation errors Biochem. Biophys. Res. Commun. 2004, 320, 354-358 (Pubitemid 38798873)
93. Bubunenko, M.; Baker, T.; Court, D. L. Essentiality of ribosomal and transcription antitermination proteins analyzed by systematic gene replacement in Escherichia coli J. Bacteriol. 2007, 189, 2844-2853 (Pubitemid 46556067)
94. Rudd, K. E. EcoGene: a genome sequence database for Escherichia coli K-12 Nucl. Acids. Res. 2000, 28, 60-64 (Pubitemid 30047714)
95. Ghosh, J.; Basu, A.; Pal, S.; Chowdhuri, S.; Bhattacharya, A.; Pal, D.; Chattoraj, D. K.; DasGupta, C. Ribosome-DnaK interactions in relation to protein folding Mol. Microbiol. 2003, 48, 1679-1692 (Pubitemid 36751070)
96. Yonekura, K.; Maki, S.; Morgan, D. G.; DeRosier, D. J.; Vonderviszt, F.; Imada, K.; Namba, K. The bacterial flagellar cap as the rotary promoter of flagellin self-assembly Science 2000, 290, 2148-2152 (Pubitemid 32001595)
97. Zhao, K.; Liu, M. Z.; Burgess, R. R. Adaptation in bacterial flagellar and motility systems: from regulon members to 'foraging'-like behavior in E-coli Nucl. Acids Res. 2007, 35, 4441-4452 (Pubitemid 47244595)
98. Gibbons, H. S.; Wolschendorf, F.; Abshire, M.; Niederweis, M.; Braünstein, M. Identification of two Mycobacterium smegmatis lipoproteins exported by a SecA2-dependent pathway J. Bacteriol. 2007, 189, 5090-5100 (Pubitemid 47076055)