Changes in the Protein Composition of the Exiguobacterium sibiricum Membrane with Decreasing Temperature: a Proteomic Analysis

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

For the first time, the proteins of the membrane fraction isolated from the psychrotrophic bacterium Exiguobacterium sibiricum were analyzed using the label-free quantitative chromatography-mass spectrometry. Comparison of the samples from cells cultured at 10°C and at room temperature revealed significant differences in the content of many proteins involved in important physiological processes, including DNA and RNA binding proteins, membrane transporters, proteins providing protection against osmotic and oxidative stress, and others. The results of the work contribute to understanding of mechanisms of the processes occurring in the cell membranes of psychrotrophic bacteria at low temperatures, and complement existing ideas about the adaptation strategies of microorganisms living in permafrost deposits. The data obtained can also be used to search for potential biocatalysts with activity at low temperatures.

About the authors

L. E Petrovskaya

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, RAS; Moscow Institute of Physics and Technology

Email: lpetr65@yahoo.com
Moscow, Russia; Dolgoprudny, Russia

R. H Ziganshin

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, RAS

Moscow, Russia

E. A Kryukova

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, RAS

Moscow, Russia

E. V Spirina

Institute of Physical, Chemical and Biological Problems of Soil Science, RAS

Pushchino, Russia

E. M Rivkina

Institute of Physical, Chemical and Biological Problems of Soil Science, RAS

Pushchino, Russia

S. A Siletsky

Research Institute of Physical and Chemical Biology named after A.N. Belozersky, Lomonosov Moscow State University; Lomonosov Moscow State University, Faculty of Bioengineering and Bioinformatics

Moscow, Russia; Moscow, Russia

D. A Dolgikh

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, RAS; Lomonosov Moscow State University, Faculty of Biology

Moscow, Russia; Moscow, Russia

M. P Kirpichnikov

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, RAS; Lomonosov Moscow State University, Faculty of Biology

Moscow, Russia; Moscow, Russia

References

  1. Tarnocai C. // In: Permafrost Soils / Ed. Margesin R. Berlin, Heidelberg: Springer, 2009. P. 3–16. https://doi.org/10.1007/978-3-540-69371-0_1
  2. Gilichinsky D.A., Rivkina E.M. // In: Encyclopedia of Geobiology. Encyclopedia of Earth Sciences Series / Eds. Reitner J., Thiel V. Dordrecht: Springer, 2011. P. 726–732. https://doi.org/10.1007/978-1-4020-9212-1_162
  3. Jansson J.K., Tas N. // Nat. Rev. Microbiol. 2014. V. 12. P. 414–425. https://doi.org/10.1038/nrmicro3262
  4. Rivkina E., Laurinavichius K., McGrath J., Tiedje J., Shcherbakova V., Gilichinsky D. // Adv. Space Res. 2004. V. 33. P. 1215–1221. https://doi.org/10.1016/j.asr.2003.06.024
  5. Vishnivetskaya T.A., Petrova M.A., Urbance J., Ponder M., Moyer C.L., Gilichinsky D.A., Tiedje J.M. // Astrobiology. 2006. V. 6. P. 400–414. https://doi.org/10.1089/ast.2006.6.400
  6. Rodrigues D.F., Goris J., Vishnivetskaya T., Gilichinsky D., Thomashow M.F., Tiedje J.M. // Extremophiles. 2006. V. 10. P. 285–294. https://doi.org/10.1007/s00792-005-0497-5
  7. Rodrigues D.F., Ivanova N., He Z., Huebner M., Zhou J., Tiedje J.M. // BMC Genomics. 2008. V. 9. P. 547. https://doi.org/10.1186/1471-2164-9-547
  8. Qiu Y., Vishnivetskaya T.A., Lubman D.M. // In: Permafrost Soils / Ed. Margesin R. Berlin, Heidelberg: Springer, 2009. P. 169–181. https://doi.org/10.1007/978-3-540-69371-0_12
  9. Petrovskaya L.E., Siletsky S.A., Mamedov M.D., Lukashev E.P., Balashov S.P., Dolgikh D.A., Kirpichnikov M.P. // Biochemistry (Moscow). 2023. V. 88. P. 1544–1554. https://doi.org/10.1134/s0006297923100103
  10. Petrovskaya L.E., Lukashev E.P., Chupin V.V., Sychev S.V., Lyukmanova E.N., Kryukova E.A., Ziganshin R.H., Spirina E.V., Rivkina E.M., Khatypov R.A., Erokhina L.G., Gilichinsky D.A., Shuvalov V.A., Kirpichnikov M.P. // FEBS Lett. 2010. V. 584. P. 4193–4196. https://doi.org/10.1016/j.febslet.2010.09.005
  11. Berlina Y.Y., Petrovskaya L.E., Kryukova E.A., Shingarova L.N., Gapizov S.S., Kryukova M.V., Rivkina E.M., Kirpichnikov M.P., Dolgikh D.A. // Biomolecules. 2021. V. 11. P. 1229. https://doi.org/10.3390/biom11081229
  12. Gangoiti J., Pijning T., Dijkhuizen L. // Appl. Environ. Microbiol. 2016. V. 82. P. 756–766. https://doi.org/10.1128/AEM.03420-15
  13. Löwe J., Ingram A.A., Gröger H. // Bioorg. Med. Chem. 2018. V. 26. P. 1387–1392. https://doi.org/10.1016/j.bmc.2017.12.005
  14. Konings W.N., Albers S.-V., Koning S., Driessen A.J.M. // Antonie Van Leeuwenhoek. 2002. V. 81. P. 61–72. https://doi.org/10.1023/A:1020573408652
  15. Soufi B., Macek B. // Int. J. Med. Microbiol. 2015. V. 305. P. 203–208. https://doi.org/10.1016/j.ijmm.2014.12.017
  16. Rodrigues D.F., Tiedje J.M. // Appl. Environ. Microbiol. 2008. V. 74. P. 1677–1686. https://doi.org/10.1128/AEM.02000-07
  17. Collins T., Margesin R. // Appl. Microbiol. Biotechnol. 2019. V. 103. P. 2857–2871. https://doi.org/10.1007/s00253-019-09659-5
  18. Seixas A.F., Quendera A.P., Sousa J.P., Silva A.F.Q., Arraiano C.M., Andrade J.M. // Front. Genet. 2022. V. 12. Р. 821535. https://doi.org/10.3389/fgene.2021.821535
  19. Ezraty B., Gennaris A., Barras F., Collet J.-F. // Nat. Rev. Microbiol. 2017. V. 15. P. 385–396. https://doi.org/10.1038/nrmicro.2017.26
  20. Molloy M.P., Herbert B.R., Slade M.B., Rabilloud T., Nouwens A.S., Williams K.L., Gooley A.A. // Eur. J. Biochem. 2000. V. 267. P. 2871–2881. https://doi.org/10.1046/j.1432-1327.2000.01296.x
  21. Cao Y., Pan Y., Huang H., Jin X., Levin E.J., Kloss B., Zhou M. // Nature. 2013. V. 496. P. 317–322. https://doi.org/10.1038/nature12056
  22. Pech M., Karim Z., Yamamoto H., Kitakawa M., Qin Y., Nierhaus K.H. // Proc. Natl. Acad. Sci. USA. 2011. V. 108. P. 3199–3203. https://doi.org/10.1073/pnas.1012994108
  23. Weber M.H.W., Marahiel M.A. // Sci. Prog. 2003. V. 86. P. 9–75. https://doi.org/10.3184/003685003783238707
  24. Kato J., Suzuki H., Ikeda H. // J. Biol. Chem. 1992. V. 267. P. 25676–25684. https://doi.org/10.1016/S0021-9258(18)35660-6
  25. Zhang Y., Burkhardt D.H., Rouskin S., Li G.-W., Weissman J.S., Gross C.A. // Mol. Cell. 2018. V. 70. P. 274–286.e7. https://doi.org/10.1016/j.molcel.2018.02.035
  26. Owttrim G.W. // RNA Biol. 2013. V. 10. P. 96–110. https://doi.org/10.4161/rna.22638
  27. Pavankumar T.L., Rai N., Pandey P.K., Vincent N. // DNA. 2024. V. 4. P. 455–472. https://doi.org/10.3390/dna4040031
  28. Starosta A.L., Lassak J., Jung K., Wilson D.N. // FEMS Microbiol. Rev. 2014. V. 38. P. 1172–1201. https://doi.org/10.1111/1574-6976.12083
  29. Gruffaz C., Smirnov A. // Front. Mol. Biosci. 2023. V. 10. Р. 1263433. https://doi.org/10.3389/fmolb.2023.1263433
  30. Wood A., Irving S.E., Bennison D.J., Corrigan R.M. // PLoS Genet. 2019. V. 15. P. e1008346. https://doi.org/10.1371/journal.pgen.1008346
  31. Njenga R., Boele J., Öztürk Y., Koch H.-G. // J. Biol. Chem. 2023. V. 299. Р. 105163. https://doi.org/10.1016/j.jbc.2023.105163
  32. Hederstedt L. // Biochemistry (Moscow). 2021. V. 86. P. 8–21. https://doi.org/10.1134/S0006297921010028
  33. Seel W., Flegler A., Zunabovic-Pichler M., Lipski A. // J. Bacteriol. 2018. V. 200. Р. e00148-18. https://doi.org/10.1128/jb.00148-18
  34. Jeckelmann J.-M., Erni B. // In: Bacterial Cell Walls Membranes / Ed. Kuhn A. Cham: Springer Int. Publ., 2019. P. 223–274. https://doi.org/10.1007/978-3-030-18768-2_8
  35. Trincone A. // Molecules. 2018. V. 23. P. 901. https://doi.org/10.3390/molecules23040901
  36. Mascher T. // FEMS Microbiol. Lett. 2006. V. 264. P. 133–144. https://doi.org/10.1111/j.1574-6968.2006.00444.x
  37. George N.L., Orlando B.J. // Nat. Commun. 2023. V. 14. P. 3896. https://doi.org/10.1038/s41467-023-39678-w
  38. Suntharalingam P., Senadheera M.D., Mair R.W., Lé-vesque C.M., Cvitkovitch D.G. // J. Bacteriol. 2009. V. 191. P. 2973–2984. https://doi.org/10.1128/jb.01563-08
  39. Hsu J.-L., Chen H.-C., Peng H.-L., Chang H.-Y. // J. Biol. Chem. 2008. V. 283. P. 9933–9944. https://doi.org/10.1074/jbc.M708836200
  40. Claverys J.-P., Prudhomme M., Martin B. // Annu. Rev. Microbiol. 2006. V. 60. P. 451–475. https://doi.org/10.1146/annurev.micro.60.080805.142139
  41. Erill I., Campoy S., Barbé J. // FEMS Microbiol. Rev. 2007. V. 31. P. 637–656. https://doi.org/10.1111/j.1574-6976.2007.00082.x
  42. Schulz A., Schumann W. // J. Bacteriol. 1996. V. 178. P. 1088–1093. https://doi.org/10.1128/jb.178.4.1088-1093.1996
  43. Prabudiansyah I., Driessen A.J.M. // In: Protein Sugar Export Assembly Gram-positives / Eds. Bagnoli F., Rappuoli R. Cham: Springer Int. Publ., 2017. P. 45–67. https://doi.org/10.1007/82_2016_9
  44. Imam S., Chen Z., Roos D.S., Pohlschröder M. // PLoS One. 2011. V. 6. P. e28919. https://doi.org/10.1371/journal.pone.0028919
  45. Jin F., Conrad J.C., Gibiansky M.L., Wong G.C.L. // Proc. Natl. Acad. Sci. USA. 2011. V. 108. P. 12617– 12622. https://doi.org/10.1073/pnas.1105073108
  46. Schuhmacher J.S., Thormann K.M., Bange G. // FEMS Microbiol. Rev. 2015. V. 39. P. 812–822. https://doi.org/10.1093/femsre/fuv034
  47. Herrou J., Willett J.W., Czyż D.M., Babnigg G., Kim Y., Crosson S. // J. Bacteriol. 2017. V. 199. P. e00746-16. https://doi.org/10.1128/jb.00746-16
  48. Rismondo J., Schulz L.M. // Microorganisms. 2021. V. 9. P. 163. https://doi.org/10.3390/microorganisms9010163
  49. Zhang D., Zhu Z., Li Y., Li X., Guan Z., Zheng J. // mSystems. 2021. V. 6. P. e0038321. https://doi.org/10.1128/msystems.00383-21
  50. Shabayek S., Bauer R., Mauerer S., Mizaikoff B., Spellerberg B. // Mol. Microbiol. 2016. V. 100. P. 589– 606. https://doi.org/10.1111/mmi.13335
  51. Sleator R.D., Hill C. // FEMS Microbiol. Rev. 2002. V. 26. P. 49–71. https://doi.org/10.1111/j.1574-6976.2002.tb00598.x
  52. Wendel B. M. ,Pi H. ,Krüger L., Herzberg C., Stülke J., Helmann J. D. / / mBio. 2022. V. 13. P. e00092-22. https://doi.org/10.1128/mbio.00092-22
  53. Lesniak J., Barton W.A., Nikolov D.B. // Protein Sci. 2003. V. 12. P. 2838–2843. https://doi.org/10.1110/ps.03375603
  54. Saikolappan S., Das K., Sasindran S.J., Jagannath C., Dhandayuthapani S. // Tuberculosis. 2011. V. 91. P. S119–S127. https://doi.org/10.1016/j.tube.2011.10.021
  55. Goto S., Kawamoto J., Sato S.B., Iki T., Watanabe I., Kudo K., Esaki N., Kurihara T. // AMB Expr. 2015. V. 5. P. 11. https://doi.org/10.1186/s13568-015-0098-3
  56. Sajjad W., Din G., Rafiq M., Iqbal A., Khan S., Zada S., Ali B., Kang S. // Extremophiles. 2020. V. 24. P. 447– 473. https://doi.org/10.1007/s00792-020-01180-2
  57. Tribelli P.M., López N.I. // Life. 2018. V. 8. P. 8. https://doi.org/10.3390/life8010008
  58. Sauvage E., Kerff F., Terrak M., Ayala J.A., Charlier P. // FEMS Microbiol. Rev. 2008. V. 32. P. 234– 258. https://doi.org/10.1111/j.1574-6976.2008.00105.x
  59. Martinez-Bond E.A., Soriano B.M., Williams A.H. // Curr. Opin. Struct. Biol. 2022. V. 77. P. 102480. https://doi.org/10.1016/j.sbi.2022.102480
  60. Shih Y.-L., Rothfield L. // Microbiol. Mol. Biol. Rev. 2006. V. 70. P. 729–754. https://doi.org/10.1128/mmbr.00017-06
  61. Meziane-Cherif D., Stogios P.J., Evdokimova E., Savchenko A., Courvalin P. // Proc. Natl. Acad. Sci. USA. 2014. V. 111. P. 5872–5877. https://doi.org/10.1073/pnas.1402259111
  62. Brown S., Santa Maria J.P., Walker S. // Annu. Rev. Microbiol. 2013. V. 67. P. 313–336. https://doi.org/10.1146/annurev-micro-092412-155620
  63. Ting L., Williams T.J., Cowley M.J., Lauro F.M., Guilhaus M., Raftery M.J., Cavicchioli R. // Environ. Microbiol. 2010. V. 12. P. 2658–2676. https://doi.org/10.1111/j.1462-2920.2010.02235.x
  64. Lambert C., Poullion T., Zhang Q., Schmitt A., Masse J.-M., Gloux K., Poyart C., Fouet A. // PLoS One. 2023. V. 18. P. e0284402. https://doi.org/10.1371/journal.pone.0284402
  65. Gabrielska J., Gruszecki W.I. // Biochim. Biophys. Acta Biomembr. 1996. V. 1285. P. 167–174. https://doi.org/10.1016/S0005-2736(96)00152-6
  66. Rappsilber J., Mann M., Ishihama Y. // Nat. Protoc. 2007. V. 2. P. 1896–1906. https://doi.org/10.1038/nprot.2007.261
  67. Tyanova S., Temu T., Cox J. // Nat. Protoc. 2016. V. 11. P. 2301–2319. https://doi.org/10.1038/nprot.2016.136
  68. Tyanova S., Temu T., Sinitcyn P., Carlson A., Hein M.Y., Geiger T., Mann M., Cox J. // Nat. Methods. 2016. V. 13. P. 731–740. https://doi.org/10.1038/nmeth.3901

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2025 Russian Academy of Sciences