Growth pattern and partial proteome of Mycobacterium avium subsp. paratuberculosis during the stress response to hypoxia and nutrient starvation

Veterinary Microbiology

Volumn 133, Issue 4, 2009, Pages 344-357

  Gumber, Sanjeev ^a   Taylor, Deborah L ^a   Marsh, Ian B ^a   Whittington, Richard J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Growth; Mycobacterium avium subsp.; Paratuberculosis; Proteome; Stress response; Survival

Indexed keywords

BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; OXYGEN; PROTEOME;

ANIMALIA; BOS; CORYNEBACTERINEAE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; OVIS ARIES;

EID: 58149088853     PISSN: 03781135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetmic.2008.07.021     Document Type: Article

References (43)

1. Archuleta R.J., Yvonne Hoppes P., and Primm T.P. Mycobacterium avium enters a state of metabolic dormancy in response to starvation. Tuberculosis (Edinb) 85 (2005) 147-158
2. Behr M.A., Schroeder B.G., Brinkman J.N., Slayden R.A., and Barry III C.E. A point mutation in the mma3 gene is responsible for impaired methoxymycolic acid production in Mycobacterium bovis BCG strains obtained after 1927. J. Bacteriol. 182 (2000) 3394-3399
3. Betts J.C., Lukey P.T., Robb L.C., McAdam R.A., and Duncan K. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43 (2002) 717-731
4. Blum H., Beier H., and Gross H. Improved silver staining of plant proteins. RNA and DNA in polyacrylamide gels. Electrophoresis 8 (1987) 93-99
5. Boon C., and Dick T. Mycobacterium bovis BCG response regulator essential for hypoxic dormancy. J. Bacteriol. 184 (2002) 6760-6767
6. Bush R.D., Toribio J.A., and Windsor P. Losses of adult sheep due to ovine Johne's disease in 12 infected flocks over a 3-year period. Aust. Vet. J. 84 (2006) 246-253
7. Chatterji D., and Ojha A.K. Revisiting the stringent response, ppGpp and starvation signaling. Curr. Opin. Microbiol. 4 (2001) 160-165
8. Dohmann K., Strommenger B., Stevenson K., De Juan L., Stratmann J., Kapur V., Bull T.J., and Gerlach G.F. Characterization of genetic differences between Mycobacterium avium subsp. paratuberculosis type i and type ii isolates. J. Clin. Microbiol. 41 (2003) 5215-5223
9. Dosanjh N.S., Rawat M., Chung J.H., and Av-Gay Y. Thiol specific oxidative stress response in Mycobacteria. FEMS Microbiol. Lett. 249 (2005) 87-94
10. Dziejman M., and Mekalanos J.J. Two-component signal transduction and its role in the expression of bacterial virulence factors. In: Hoch J.A., and Silhavy T.J. (Eds). Two-component Signal Transduction (1995), American Society for Microbiology, Washington, DC 305-317
11. Gatlin C.L., Kleemann G.R., Hays L.G., Link A.J., and Yates III J.R. Protein identification at the low femtomole level from silver-stained gels using a new fritless electrospray interface for liquid chromatography-microspray and nanospray mass spectrometry. Anal. Biochem. 263 (1998) 93-101
12. Gumber S., Taylor D.L., and Whittington R.J. Protein extraction from Mycobacterium avium subsp. paratuberculosis: comparison of methods for analysis by sodium dodecyl sulphate polyacrylamide gel electrophoresis, native PAGE and surface enhanced laser desorption/ionization time of flight mass spectrometry. J. Microbiol. Methods 68 (2007) 115-127
13. Gupta S., Pandit S.B., Srinivasan N., and Chatterji D. Proteomics analysis of carbon-starved Mycobacterium smegmatis: induction of Dps-like protein. Protein Eng. 15 (2002) 503-512
14. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
15. Locht C., Hougardy J.M., Rouanet C., Place S., and Mascart F. Heparin-binding hemagglutinin, from an extrapulmonary dissemination factor to a powerful diagnostic and protective antigen against tuberculosis. Tuberculosis (Edinb) 86 (2006) 303-309
16. Marchler-Bauer A., Anderson J.B., Cherukuri P.F., DeWeese-Scott C., Geer L.Y., Gwadz M., He S., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Liebert C.A., Liu C., Lu F., Marchler G.H., Mullokandov M., Shoemaker B.A., Simonyan V., Song J.S., Thiessen P.A., Yamashita R.A., Yin J.J., Zhang D., and Bryant S.H. CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res. 33 (2005) D192-196
17. Marsh I., Whittington R., and Cousins D. PCR-restriction endonuclease analysis for identification and strain typing of Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium based on polymorphisms in IS1311. Mol. Cell Probes 13 (1999) 115-126
18. Marsh I.B., Bannantine J.P., Paustian M.L., Tizard M.L., Kapur V., and Whittington R.J. Genomic comparison of Mycobacterium avium subsp. paratuberculosis sheep and cattle strains by microarray hybridization. J. Bacteriol. 188 (2006) 2290-2293
19. Marsh I.B., and Whittington R.J. Deletion of an mmpL gene and multiple associated genes from the genome of the S strain of Mycobacterium avium subsp. paratuberculosis identified by representational difference analysis and in silico analysis. Mol. Cell. Probes 19 (2005) 371-384
20. Marsh I.B., and Whittington R.J. Genomic diversity in Mycobacterium avium: Single nucleotide polymorphisms between the S and C strains of M. avium subsp. paratuberculosis and with M. a. avium. Mol. Cell. Probes 21 (2007) 66-75
21. Mukamolova G.V., Kaprelyants A.S., Kell D.B., and Young M. Adoption of the transiently non-culturable state-a bacterial survival strategy?. Adv. Microb. Physiol. 47 (2003) 65-129
22. Nyka W. Studies on the effect of starvation on mycobacteria. Infect. Immun. 9 (1974) 843-850
23. Olsen I., Reitan L.J., Holstad G., and Wiker H.G. Alkyl hydroperoxide reductases C and D are major antigens constitutively expressed by Mycobacterium avium subsp. paratuberculosis. Infect. Immun. 68 (2000) 801-808
24. Ott S.L., Wells S.J., and Wagner B.A. Herd-level economic losses associated with Johne's disease on US dairy operations. Prev. Vet. Med. 40 (1999) 179-192
25. Park H.D., Guinn K.M., Harrell M.I., Liao R., Voskuil M.I., Tompa M., Schoolnik G.K., and Sherman D.R. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol. Microbiol. 48 (2003) 833-843
26. Primm T.P., Andersen S.J., Mizrahi V., Avarbock D., Rubin H., and Barry III C.E. The stringent response of Mycobacterium tuberculosis is required for long-term survival. J. Bacteriol. 182 (2000) 4889-4898
27. Reddacliff L.A., Nicholls P.J., Vadali A., and Whittington R.J. Use of growth indices from radiometric culture for quantification of sheep strains of Mycobacterium avium subsp. paratuberculosis. Appl. Environ. Microbiol. 69 (2003) 3510-3516
28. Schlags W., Walther M., Masree M., Kratzel M., Noe C.R., and Lachmann B. Towards validating a method for two-dimensional electrophoresis/silver staining. Electrophoresis 26 (2005) 2461-2469
29. Sechi L.A., Ahmed N., Felis G.E., Dupre I., Cannas S., Fadda G., Bua A., and Zanetti S. Immunogenicity and cytoadherence of recombinant heparin binding haemagglutinin (HBHA) of Mycobacterium avium subsp. paratuberculosis: functional promiscuity or a role in virulence?. Vaccine 24 (2006) 236-243
30. Sherman D.R., Voskuil M., Schnappinger D., Liao R., Harrell M.I., and Schoolnik G.K. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystalline. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 7534-7539
31. Starck J., Kallenius G., Marklund B.I., Andersson D.I., and Akerlund T. Comparative proteome analysis of Mycobacterium tuberculosis grown under aerobic and anaerobic conditions. Microbiology 150 (2004) 3821-3829
32. Tabira Y., Ohara N., Ohara N., Kitaura H., Matsumoto S., Naito M., and Yamada T. The 16-kDa alpha-crystallin-like protein of Mycobacterium bovis BCG is produced under conditions of oxygen deficiency and is associated with ribosomes. Res. Microbiol. 149 (1998) 255-264
33. Tartaglia L.A., Storz G., and Ames B.N. Identification and molecular analysis of oxyR-regulated promoters important for the bacterial adaptation to oxidative stress. J. Mol. Biol. 210 (1989) 709-719
34. Trujillo M., Mauri P., Benazzi L., Comini M., De Palma A., Flohe L., Radi R., Stehr M., Singh M., Ursini F., and Jaeger T. The mycobacterial thioredoxin peroxidase can act as a one-cysteine-peroxiredoxin. J. Biol. Chem. 281 (2006) 20555-20566
35. Wayne L.G. Synchronized replication of Mycobacterium tuberculosis. Infect. Immun. 17 (1977) 528-530
36. Wayne L.G. Dormancy of Mycobacterium tuberculosis and latency of disease. Eur. J. Clin. Microbiol. Infect. Dis. 13 (1994) 908-914
37. Wayne L.G., and Hayes L.G. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect. Immun. 64 (1996) 2062-2069
38. Whittington R.J., Hope A.F., Marshall D.J., Taragel C.A., and Marsh I. Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis: IS900 restriction fragment length polymorphism and IS1311 polymorphism analyses of isolates from animals and a human in Australia. J. Clin. Microbiol. 38 (2000) 3240-3248
39. Whittington R.J., Marsh I., McAllister S., Turner M.J., Marshall D.J., and Fraser C.A. Evaluation of modified BACTEC 12B radiometric medium and solid media for culture of Mycobacterium avium subsp. paratuberculosis from sheep. J. Clin. Microbiol. 37 (1999) 1077-1083
40. Whittington R.J., Marsh I., Turner M.J., McAllister S., Choy E., Eamens G.J., Marshall D.J., and Ottaway S. Rapid detection of Mycobacterium paratuberculosis in clinical samples from ruminants and in spiked environmental samples by modified BACTEC 12B radiometric culture and direct confirmation by IS900 PCR. J. Clin. Microbiol. 36 (1998) 701-707
41. Whittington R.J., Marsh I.B., and Reddacliff L.A. Survival of Mycobacterium avium subsp. paratuberculosis in dam water and sediment. Appl. Environ. Microbiol. 71 (2005) 5304-5308
42. Whittington R.J., Marshall D.J., Nicholls P., Marsh I.B., and Reddacliff L.A. Survival and dormancy of Mycobacterium avium subsp. paratuberculosis in the environment. Appl. Environ. Microbiol. 70 (2004) 2989-3004
43. Whittington R.J., Reddacliff L.A., Marsh I., McAllister S., and Saunders V. Temporal patterns and quantification of excretion of Mycobacterium avium subsp. paratuberculosis in sheep with Johne's disease. Aust. Vet. J. 78 (2000) 34-37