1887

Abstract

Further understanding of the physiological states of and other mycobacteria was sought through comparisons with the genomic properties and macromolecular compositions of A3(2), grown at 30 °C, and B/r, grown at 37 °C. A frame of reference was established based on quantitative relationships observed between specific growth rates () of cells and their macromolecular compositions. The concept of a schematic cell based on transcription/translation coupling, average genes and average proteins was developed to provide an instantaneous view of macromolecular synthesis carried out by cells growing at their maximum rate. It was inferred that the ultra-fast growth of results from its ability to increase the average number of rRNA () operons per cell through polyploidy, thereby increasing its capacity for ribosome synthesis. The maximum growth rate of was deduced to be limited by the rate of uptake and consumption of nutrients providing energy. Three characteristic properties of A3(2) growing optimally (=0·30 h) were identified. First, the rate of DNA replication was found to approach the rate reported for (=1·73 h); secondly, all operons were calculated to be fully engaged in precursor-rRNA synthesis; thirdly, compared with , protein synthesis was found to depend on higher concentrations of ribosomes and lower concentrations of aminoacyl-tRNA and EF-Tu. An equation was derived for B/r relating to the number of operons per genome. Values of =0·69 h and =1·00 h were obtained respectively for cells with one or two operons per genome. Using the author's equation relating the number of operons per genome to maximum growth rate, it is expected that with one operon should be capable of growing much faster than it actually does. Therefore, it is suggested that the high number of insertion sequences in this species attenuates growth rate to still lower values.

Keyword(s): RNAP, RNA polymerase
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26560-0
2004-05-01
2020-08-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/5/mic1501413.html?itemId=/content/journal/micro/10.1099/mic.0.26560-0&mimeType=html&fmt=ahah

References

  1. Armstrong J. A., D'Arcy-Hart P.. 1971; Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med134:713–740[CrossRef]
    [Google Scholar]
  2. Bentley S. D., Chater K. F., Cerdeño-Tárraga A.-M..40 other authors 2002; Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature417:141–147[CrossRef]
    [Google Scholar]
  3. Bercovier H., Kafri O., Sela S.. 1986; Mycobacteria possess a surprisingly small number of ribosomal RNA genes in relation to the size of their genome. Biochem Biophys Res Commun136:1136–1141[CrossRef]
    [Google Scholar]
  4. Bernstein J. A., Khodursky A. B., Lin P.-S., Lin-Chao S., Cohen S. N.. 2002; Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci U S A99:9697–9702[CrossRef]
    [Google Scholar]
  5. Blattner F. R., Plunket G., III, Bloch C. A..14 other authors 1997; The complete genome sequence of Escherichia coli K-12. Science277:1453–1462[CrossRef]
    [Google Scholar]
  6. Bremer H., Dennis P. P..others 1996; Modulation of chemical composition and other parameters of the cell growth rate. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp.1553–1568Edited by Neidhardt F. C.. Washington DC: American Society for Microbiology;
    [Google Scholar]
  7. Brosch R., Gordon S. V., Eiglmeier K., Garnier T., Tekaia F., Yeramian E., Cole S. T.. 2000; Genomics, biology, and evolution of the Mycobacterium tuberculosis complex. In Molecular Genetics of Mycobacteria pp.19–36Edited by Hatfull G. F., Jacobs W. R. Jr. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  8. Brosch R., Gordon S. V., Marmiesse M..12 other authors 2002; A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A99:3684–3689[CrossRef]
    [Google Scholar]
  9. Byrne R., Levin J. G., Bladen H. A., Nirenberg M. W.. 1964; The in vitro formation of a DNA–ribosome complex. Proc Natl Acad Sci U S A52:140–148[CrossRef]
    [Google Scholar]
  10. Clark H. F., Shepard C. C.. 1963; Effect of environmental temperatures on infection with Mycobacterium marinum (balnei) of mice and a number of poikilothermic species. J Bacteriol86:1057–1069
    [Google Scholar]
  11. Cole S. T., Brosch R., Parkhill J..39 other authors 1998; Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature393:537–544[CrossRef]
    [Google Scholar]
  12. Condon C., French S., Squires C., Squires C. L.. 1993; Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. EMBO J12:4305–4315
    [Google Scholar]
  13. Condon C., Liveris D., Squires C., Schwartz I., Squires C. L.. 1995; rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation. J Bacteriol177:4152–4156
    [Google Scholar]
  14. Cox R. A.. 2003; Correlation of the rate of protein synthesis and the third power of the RNA : protein ratio in Escherichia coli and Mycobacterium tuberculosis. Microbiology149:729–737[CrossRef]
    [Google Scholar]
  15. Domenech P., Menendez M. C., Garcia M. J.. 1994; Restriction fragment length polymorphism of 16S rRNA genes in the differentiation of fast-growing mycobacterial species. FEMS Microbiol Lett116:19–21[CrossRef]
    [Google Scholar]
  16. Ferrari G., Langen H., Naito M., Pieters J.. 1999; A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell97:435–447[CrossRef]
    [Google Scholar]
  17. Gonzalez-y-Merchand J. A., Colston M. J., Cox R. A.. 1999; Effects of growth conditions on the expression of mycobacterial murA and tyrS genes and contributions of their transcripts to precursor rRNA synthesis. J Bacteriol181:4617–4627
    [Google Scholar]
  18. Grunberg-Manago M.. 1999; Messenger RNA stability and its role in the control of gene expression in bacteria and phages. Annu Rev Genet33:193–227[CrossRef]
    [Google Scholar]
  19. Harshey R. M., Ramakrishnan T.. 1977; Rate of ribonucleic acid chain growth in Mycobacterium tuberculosis H37Rv. J Bacteriol129:616–622
    [Google Scholar]
  20. Helmstetter C. E..others 1996; Timing of synthetic activities in the cell cycle. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp.1627–1639Edited by Neidhardt F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  21. Helmstetter C. E., Cooper S.. 1968; DNA synthesis during the division cycle of rapidly growing E. coli B/r. J Mol Biol31:507–518[CrossRef]
    [Google Scholar]
  22. Hiriyanna K. T., Ramakrishnan T.. 1986; Deoxyribonucleic acid replication time in Mycobacterium tuberculosis H37Rv. Arch Microbiol144:105–109[CrossRef]
    [Google Scholar]
  23. Ingraham J. L., Marr J. L..others 1996; Effect of temperature, pressure, pH, and osmotic stress on growth. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp.1570–1578Edited by Neidhardt F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  24. Ingraham J. L., Maaløe O., Neidhardt F. C.. 1983; Growth of the Bacterial Cell Sunderland, MA: Sinauer Associates;
  25. Jacobsen H.. 1974; PhD thesis. University of Copenhagen;
  26. Khodursky A. R., Bernstein J. A.. 2003; Life after transcription – revisiting the fate of messenger RNA. Trends Genet19:113–115[CrossRef]
    [Google Scholar]
  27. Krummel B., Chamberlin M. J.. 1989; RNA chain initiation by Escherichia coli RNA polymerase. Structural transitions of the enzyme in early ternary complexes. Biochemistry28:7829–7842[CrossRef]
    [Google Scholar]
  28. Leroy A., Vanzo N. F., Sousa S., Dreyfus M., Carpousis A. J.. 2002; Function in Escherichia coli of the non-catalytic part of RNase E : role in the degradation of ribosome-free mRNA. Mol Microbiol45:1231–1243[CrossRef]
    [Google Scholar]
  29. Miller O. L., Hamkalo B. A., Thomas C. A. Jr. 1970; Visualization of bacterial genes in action. Science169:392–395[CrossRef]
    [Google Scholar]
  30. Neidhardt F. C..others 1996; The enteric bacterial cell and the age of bacteria. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp.1–3Edited by Neidhart F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  31. Noller H. E., Nomura M..others 1996; Ribosomes. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp.167–186Edited by Neidhardt F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  32. Régnier P., Arraiano C. M.. 2000; Degradation of mRNA in bacteria: emergence of ubiquitous features. BioEssays22:235–244[CrossRef]
    [Google Scholar]
  33. Schaechter E., Maaløe O., Kjeldgaard N. O.. 1958; Dependence on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J Gen Microbiol19:592–606[CrossRef]
    [Google Scholar]
  34. Shahab N., Flett F., Oliver S. G., Butler P. R.. 1996; Growth rate control of protein and nucleic acids in Streptomyces coelicolor A3(2) and Escherichia coli B/r. Microbiology142:1927–1935[CrossRef]
    [Google Scholar]
  35. Shepard C. C.. 1960; The experimental disease that follows the injection of human leprosy bacilli into the footpads of mice. J Exp Med112:445–454[CrossRef]
    [Google Scholar]
  36. Stent G. S.. 1964; The operon: on its third anniversary. Science144:816–820[CrossRef]
    [Google Scholar]
  37. Stewart G. R., Robertson B. D., Young D. B.. 2003; Tuberculosis: a problem with persistence. Nat Rev1:97–105
    [Google Scholar]
  38. Tonella L., Walsh B. J., Sanchez J. C..14 other authors 1998; '98 Escherichia coli SWISS-2DPAGE database update. Electrophoresis19:1960–1971[CrossRef]
    [Google Scholar]
  39. Tønjum T., Welty D. B., Jantzen E., Small P. L.. 1998; Differentiation of Mycobacterium ulcerans, M. marinum, and M.haemophilum: mapping of their relationships to M. tuberculosis by fatty acid profile analysis, DNA–DNA hybridization and 16S rRNA gene sequence analysis. J Clin Microbol35:918–925
    [Google Scholar]
  40. Verma A., Sampla A. K., Tyagi J. S.. 1999; Mycobacterium tuberculosis rrn promoters: differential usage and growth rate-dependent control. J Bacteriol181:4326–4333
    [Google Scholar]
  41. Wayne L. G.. 1994; Cultivation of Mycobacterium tuberculosis for research purposes. In Tuberculosis: Pathogenesis, Protection and Control pp.73–83Edited by Bloom B.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  42. Wayne L. G., Hayes L. G.. 1996; An in vitro model for sequential study of shift down of Mycobacterium tuberculosis through two stages of replicating persistence. Infect Immun64:2062–2069
    [Google Scholar]
  43. Wayne L. G., Kubica G. P.. 1986; The mycobacteria. In Bergey's Manual of Systematic Bacteriologyvol. 2 pp.1435–1457 Edited by Sneath P. H. A., Mair N. S., Sharpe M. E., Holt J. G.. London: Williams & Wilkins;
    [Google Scholar]
  44. Winder F. G., Rooney S. A.. 1970; Effects of nitrogenous components of the medium on the carbohydrate and nucleic acid content of Mycobacterium tuberculosis BCG. J Gen Microbiol63:29–39[CrossRef]
    [Google Scholar]
  45. Woods G. L., Washington J. A.. 1987; Mycobacteria other than Mycobacterium tuberculosis: review of microbiologic and clinical aspects. Rev Infect Dis9:275–294[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26560-0
Loading
/content/journal/micro/10.1099/mic.0.26560-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error