Dynamic Transcriptional Landscape of under Cold Stress.

Artem S Grigorov, Yulia V Skvortsova, Oksana S Bychenko, Leonid V Aseev, Ludmila S Koledinskaya, Irina V Boni, Tatyana L Azhikina
Author Information
  1. Artem S Grigorov: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow 117997, Russia.
  2. Yulia V Skvortsova: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow 117997, Russia.
  3. Oksana S Bychenko: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow 117997, Russia.
  4. Leonid V Aseev: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow 117997, Russia.
  5. Ludmila S Koledinskaya: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow 117997, Russia.
  6. Irina V Boni: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow 117997, Russia.
  7. Tatyana L Azhikina: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow 117997, Russia. ORCID

Abstract

Bacterial adaptation to cold stress requires wide transcriptional reprogramming. However, the knowledge of molecular mechanisms underlying the cold stress response of mycobacteria is limited. We conducted comparative transcriptomic analysis of subjected to cold shock. The growth of cultivated at 37 °C was arrested just after exposure to cold (acclimation phase) but later (by 24 h) was resumed at a much slower rate (adaptation phase). Transcriptomic analyses revealed distinct gene expression patterns corresponding to the two phases. During the acclimation phase, differential expression was observed for genes associated with cell wall remodeling, starvation response, and osmotic pressure stress, in parallel with global changes in the expression of transcription factors and the downregulation of ribosomal genes, suggesting an energy-saving strategy to support survival. At the adaptation phase, the expression profiles were recovered, indicating restoration of the processes repressed earlier. Comparison of transcriptional responses in with those in other bacteria revealed unique adaptation strategies developed by mycobacteria. Our findings shed light on the molecular mechanisms underlying survival under cold stress. Further research should clarify whether the discovered transcriptional mechanisms exist in other mycobacterial species, including pathogenic , which could be important for transmission control.

Keywords

References

  1. J Biosci. 2003 Jun;28(4):363-4 [PMID: 12799482]
  2. J Bacteriol. 2010 May;192(10):2491-502 [PMID: 20233930]
  3. Cell Microbiol. 2009 Aug;11(8):1170-8 [PMID: 19438516]
  4. Nucleic Acids Res. 2011 Apr;39(8):3418-26 [PMID: 21193488]
  5. Tuberculosis (Edinb). 2022 Jan;132:102162 [PMID: 34952299]
  6. Microbiology (Reading). 2013 Dec;159(Pt 12):2437-2443 [PMID: 24068238]
  7. Annu Rev Genet. 2021 Nov 23;55:377-400 [PMID: 34530639]
  8. Proc Natl Acad Sci U S A. 2018 Aug 7;115(32):8191-8196 [PMID: 30038002]
  9. Microbiology (Reading). 2010 Jan;156(Pt 1):88-93 [PMID: 19778963]
  10. Bioinformatics. 2014 Apr 1;30(7):923-30 [PMID: 24227677]
  11. Nucleic Acids Res. 2022 Jul 5;50(W1):W216-W221 [PMID: 35325185]
  12. J Mol Biol. 2003 Sep 19;332(3):575-84 [PMID: 12963368]
  13. Nucleic Acids Res. 2017 Jan 4;45(D1):D320-D324 [PMID: 27899676]
  14. Appl Environ Microbiol. 2008 Jul;74(14):4560-3 [PMID: 18487398]
  15. Food Microbiol. 2010 Jun;27(4):493-502 [PMID: 20417398]
  16. Mol Microbiol. 2001 Feb;39(4):994-1009 [PMID: 11251819]
  17. iScience. 2021 Sep 14;24(10):103128 [PMID: 34611612]
  18. Microbiology (Reading). 2013 May;159(Pt 5):913-923 [PMID: 23475950]
  19. RNA. 2004 Feb;10(2):265-76 [PMID: 14730025]
  20. Mol Microbiol. 2002 Feb;43(3):717-31 [PMID: 11929527]
  21. J Bacteriol. 1986 Mar;165(3):849-55 [PMID: 3512525]
  22. BMC Genomics. 2021 Jan 7;22(1):28 [PMID: 33413101]
  23. Acta Crystallogr D Biol Crystallogr. 2013 Dec;69(Pt 12):2543-54 [PMID: 24311595]
  24. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  25. PLoS One. 2013 Nov 14;8(11):e79411 [PMID: 24244498]
  26. Microbiology (Reading). 2015 Mar;161(Pt 3):463-76 [PMID: 25527627]
  27. Cryobiology. 1998 Mar;36(2):75-83 [PMID: 9527869]
  28. Nature. 2013 Jul 11;499(7457):178-83 [PMID: 23823726]
  29. Int J Mol Sci. 2019 Jan 22;20(3): [PMID: 30678142]
  30. J Bacteriol. 2023 Jan 26;205(1):e0033722 [PMID: 36598232]
  31. J Bacteriol. 1997 Aug;179(16):5111-7 [PMID: 9260953]
  32. Nucleic Acids Res. 2019 May 21;47(9):4652-4662 [PMID: 30916323]
  33. Microbiol Res. 2017 Dec;205:8-18 [PMID: 28942848]
  34. mBio. 2011 Jun 14;2(3):e00100-11 [PMID: 21673191]
  35. Arch Microbiol. 2010 Feb;192(2):85-95 [PMID: 20049417]
  36. Front Cell Infect Microbiol. 2019 Jul 30;9:272 [PMID: 31428590]
  37. J Bacteriol. 2011 Dec;193(24):6824-33 [PMID: 21984791]
  38. J Biol Chem. 2006 Sep 29;281(39):28811-21 [PMID: 16895921]
  39. ACS Infect Dis. 2021 Apr 9;7(4):927-936 [PMID: 33663204]
  40. J Bacteriol. 1992 Aug;174(15):5027-35 [PMID: 1629159]
  41. Cell Mol Biol (Noisy-le-grand). 2004 Jul;50(5):605-12 [PMID: 15559977]
  42. Methods Mol Biol. 2015;1269:307-26 [PMID: 25577387]
  43. ISME J. 2012 Aug;6(8):1544-57 [PMID: 22258101]
  44. Curr Opin Microbiol. 2015 Oct;27:86-95 [PMID: 26336012]
  45. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2003-7 [PMID: 7534408]
  46. J Food Prot. 2003 Nov;66(11):2045-50 [PMID: 14627281]
  47. Microbiologyopen. 2015 Dec;4(6):896-916 [PMID: 26434659]
  48. Antimicrob Agents Chemother. 2017 Aug 24;61(9): [PMID: 28674058]
  49. Antioxid Redox Signal. 2020 Jun;32(18):1348-1366 [PMID: 31621379]
  50. Appl Environ Microbiol. 2013 Apr;79(7):2112-20 [PMID: 23354714]
  51. Cell. 2009 Jul 10;138(1):146-59 [PMID: 19596241]
  52. RNA. 2013 Jan;19(1):74-84 [PMID: 23169799]
  53. Nat Methods. 2012 Mar 04;9(4):357-9 [PMID: 22388286]
  54. J Bacteriol. 1987 May;169(5):2092-5 [PMID: 3553157]
  55. Front Microbiol. 2022 Jul 11;13:919538 [PMID: 35898907]
  56. Front Microbiol. 2017 Mar 14;8:430 [PMID: 28352263]
  57. EMBO J. 1999 Mar 15;18(6):1653-9 [PMID: 10075935]
  58. Mol Microbiol. 2019 Feb;111(2):354-372 [PMID: 30427073]
  59. Nucleic Acids Res. 2004 May 17;32(9):2751-9 [PMID: 15148362]
  60. Nucleic Acids Res. 2013 Aug;41(14):e140 [PMID: 23716638]
  61. Cell Microbiol. 2007 May;9(5):1275-83 [PMID: 17223927]
  62. Tuberculosis (Edinb). 2013 Jan;93(1):26-9 [PMID: 23291152]
  63. Nucleic Acids Res. 2014 Oct;42(18):11763-76 [PMID: 25217589]
  64. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):76-80 [PMID: 8552679]
  65. Pathog Dis. 2018 Jun 1;76(4): [PMID: 29796669]
  66. PLoS One. 2014 Apr 04;9(4):e93604 [PMID: 24705585]
  67. Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12462-7 [PMID: 9770508]
  68. J Bacteriol. 2011 Apr;193(7):1552-62 [PMID: 21296969]
  69. Bioinformatics. 2009 Aug 1;25(15):1974-5 [PMID: 19398448]
  70. J Biol Chem. 2006 Jan 20;281(3):1313-6 [PMID: 16326699]
  71. Mol Microbiol. 1997 Jan;23(2):381-6 [PMID: 9044271]
  72. Cell Stress Chaperones. 2020 Nov;25(6):1025-1032 [PMID: 32683538]
  73. Biochem Biophys Res Commun. 2010 Nov 26;402(4):693-8 [PMID: 20977881]
  74. Int J Food Microbiol. 2011 Mar 30;146(2):163-9 [PMID: 21402428]
  75. J Bacteriol. 2002 Nov;184(22):6395-402 [PMID: 12399512]
  76. Genome Biol. 2021 Apr 29;22(1):123 [PMID: 33926534]
  77. Appl Environ Microbiol. 2012 Oct;78(20):7483-6 [PMID: 22885758]
  78. J Bacteriol. 2009 Apr;191(8):2888-93 [PMID: 19218386]
  79. J Biol Chem. 2010 Jul 9;285(28):21698-707 [PMID: 20457615]
  80. Gene. 2014 Aug 15;547(1):91-7 [PMID: 24952137]
  81. mSphere. 2021 May 12;6(3): [PMID: 33980681]
  82. J Biol Chem. 2012 Jul 6;287(28):24053-63 [PMID: 22544737]
  83. J Mol Biol. 2003 Aug 15;331(3):527-39 [PMID: 12899826]

Grants

  1. 20-34-90149/Russian Foundation for Basic Research

MeSH Term

Mycobacterium smegmatis
Cold-Shock Response
Acclimatization
Cell Wall
Down-Regulation

Word Cloud

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