Skip to main content
SpringerLink
Log in

Distribution and Potential Ecophysiological Roles of Multiple GroEL Chaperonins in Pink-Pigmented Facultative Methylotrophs

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

The distribution and phylogeny of the GroEL chaperonin genes in the type strains of all described species of pink-pigmented methylotrophic bacteria (PPFM) belonging to the genera Methylobacterium and Methylorubrum were analyzed. Half of the bacterial strains tested (38 out of 69) were found to possess multiple groEL genes. Analysis of their translated amino acid sequences and promoter regions preceding the groESL operons that include them demonstrated that the GroEL chaperonins of these methylotrophs form three similarity groups typical of PPFM. The largest of these (GroEL1) combines, apparently, essential housekeeping chaperonins, and the other two consist of additional separately clustered proteins that differ in the composition of the elements regulating their gene expression. The strains encoding proteins of the GroEL2 group were isolated from various environments, including those contaminated with industrially produced C1-compounds, while bacteria possessing GroEL3-like chaperonins are predominantly plant symbionts. It has been proposed that GroEL3 proteins may be involved in phytosymbiotic processes, whereas GroEL2 chaperonins can participate in response to specific stresses experienced by host cells in their habitats. At the same time, the GroEL chaperonin of Methylobacterium brachiatum B0021T, atypical for PPFM, seem to be intended for folding of dinuclear iron monooxygenase, in whose gene cluster it is encoded. Further testing of these assumptions should elucidate the roles of multiple GroEL chaperonins in PPFM and allow more complete use of their biotechnological potential as plant growth stimulants and biodegradation/bioremediation agents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

REFERENCES

  1. Alessa, O., Ogura, Y., Fujitani, Y., Takami, H., Hayashi, T., Sahin, N., and Tani, A., Comprehensive comparative genomics and phenotyping of Methylobacterium species, Front. Microbiol., 2021, vol. 12, p. 740610.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J., Basic local alignment search tool, J. Mol. Biol., 1990, vol. 215, no. 3, pp. 403–410.

    Article  CAS  PubMed  Google Scholar 

  3. Ashraf, W., Mihdhir, A., and Murrell, C.J., Bacterial oxidation of propane, FEMS Microbiol. Lett., 1994, vol. 122, nos. 1−2, pp. 1−6.

    Article  CAS  PubMed  Google Scholar 

  4. Aslam, Z., Lee, C.S., Kim, K.H., Im, W.T., Ten, L.N., and Lee, S.T., Methylobacterium jeotgali sp. nov., a non-pigmented, facultatively methylotrophic bacterium isolated from jeotgal, a traditional Korean fermented seafood, Int. J. Syst. Evol. Microbiol., 2007, vol. 57, no. 3, pp. 566–571.

    Article  CAS  PubMed  Google Scholar 

  5. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A., Dvorkin, M., Kulikov, A., Lesin, V., Nikolenko, S., Pham, S., Prjibelski, A., Pyshkin, A., Sirotkin, A., Vyahhi, N., Tesler, G., Alekseyev, M., and Pevzner, P., SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing, J. Computat. Biol.: a Journal of Computat. Mol. Cell Biol., 2012, vol. 19, no. 5, pp. 455–477.

    CAS  Google Scholar 

  6. Barnett, M.J., Bittner, A.N., Toman, C.J., Oke, V., and Long, S.R., Dual RpoH sigma factors and transcriptional plasticity in a symbiotic bacterium, J. Bacteriol., 2012, vol. 194, no. 18, pp. 4983–4994.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bolger, A.M., Lohse, M., and Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 2014, vol. 30, no. 15, pp. 2114–2120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bordel, S., Crombie, A.T., Muñoz, R., and Murrell, J.C., Genome scale metabolic model of the versatile methanotroph Methylocella silvestris, Microb. Cell. Fact., 2020, vol. 19, p. 144.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chongcharoen, R., Smith, F.J., Flint, K.P., and Dalton, H., Adaptation and acclimatization to formaldehyde in methylotrophs capable of high-concentration formaldehyde detoxification, Microbiology (SGM), 2005, vol. 151, no. 8, pp. 2615–2622.

    Article  CAS  PubMed  Google Scholar 

  10. Crombie, A.T. and Murrel, J.C., Trace-gas metabolic versatility of the facultative methanotroph Methylocella silvestris, Nature, 2014, vol. 510, pp. 148–151.

    Article  CAS  PubMed  Google Scholar 

  11. Csáki, R., Bodrossy, L., Klem, J., Murrell, J.C., and Kovács, K.L., Genes involved in the copper-dependent regulation of soluble methane monooxygenase of Methylococcus capsulatus (Bath): cloning, sequencing and mutational analysis, Microbiology (SGM), 2003, vol. 149, pp. 785–1795.

    Article  Google Scholar 

  12. De Marco, P., Pacheco, C.C., Figueiredo, A.R., and Moradas-Ferreira, P., Novel pollutant-resistant methylotrophic bacteria for use in bioremediation, FEMS Microbiol. Lett., 2004, vol. 234, no. 1, pp. 75–80.

    Article  CAS  PubMed  Google Scholar 

  13. Doronina, N.V., Torgonskaya, M.L., Fedorov, D.N., and Trotsenko, Y.A., Aerobic methylobacteria as promising objects of modern biotechnology, Appl. Biochem. Microbiol., 2015, vol. 51, pp. 125–134.

    Article  CAS  Google Scholar 

  14. Dourado, M.N., Aparecida Camargo Neves, A., Santos, D.S., and Araújo, W.L., Biotechnological and agronomic potential of endophytic pink-pigmented methylotrophic Methylobacterium spp., BioMed Res. Int., 2015, vol. 2015, p. 909016.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Eschinimaev, B.Ts., Tsyrenzhapova, I.S., Khmelenina, V.N., and Trotsenko Yu.A., Measurement of the content of the osmoprotectant ectoine in methylotrophic bacteria by means of normal-phase high performance liquid chromatography, Appl. Biochem. Microbiol., 2007, vol. 43, no. 2, pp. 193–196.

    Article  Google Scholar 

  16. Fedorov, D.N., Doronina, N.V., and Trotsenko, Y.A., Phytosymbiosis of aerobic methylobacteria: new facts and views, Microbiology (Moscow), 2011, vol. 80, pp. 443–454.

    Article  CAS  Google Scholar 

  17. Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap, Evolution, 1985, vol. 39, no. 4, pp. 783–791.

    Article  PubMed  Google Scholar 

  18. Firsova, Y.E. and Torgonskaya, M.L., Different roles of two groEL homologues in methylotrophic utiliser of dichloromethane Methylorubrum extorquens DM4, A. van Leeuwenhoek, 2020, vol. 113, no. 1, pp. 101–116.

    Article  CAS  Google Scholar 

  19. Fraaije, M.W., Wu, J., Heuts, D.P., van Hellemond, E.W., Spelberg, J.H., and Janssen, D.B., Discovery of a thermostable Baeyer-Villiger monooxygenase by genome mining, Appl. Microbiol. Biotechnol., 2005, vol. 66, no. 4, pp. 393–400.

    Article  CAS  PubMed  Google Scholar 

  20. Furuya, T., Hayashi, M., Semba, H., and Kino, K., The mycobacterial binuclear iron monooxygenases require a specific chaperonin-like protein for functional expression in a heterologous host, FEBS J., 2013, vol. 280, no. 3, pp. 817–826.

    Article  CAS  PubMed  Google Scholar 

  21. Furuya, T., Nakao, T., and Kino, K., Catalytic function of the mycobacterial binuclear iron monooxygenase in acetone metabolism, FEMS Microbiol. Lett., 2015, vol. 362, no. 19, p. fnv136.

    Article  PubMed  Google Scholar 

  22. Goyal, K., Qamra, R., and Mande, S.C., Multiple gene duplication and rapid evolution in the groEL gene: functional implications, J. Mol. Evol., 2006, vol. 63, pp. 781–787.

    Article  CAS  PubMed  Google Scholar 

  23. Green, P.N. and Ardley, J.K., Review of the genus Methylobacterium and closely related organisms: a proposal that some Methylobacterium species be reclassified into a new genus, Methylorubrum gen. nov., Int. J. Syst. Evol. Microbiol., 2018, vol. 68, no. 9, pp. 2727–2748.

    Article  CAS  PubMed  Google Scholar 

  24. Hayer-Hartl, M., Bracher, A., and Hartl, F.U., The Gro-EL–GroES chaperonin machine: a nano-cage for protein folding, Trends Biochem. Sci., 2016, vol. 41, no. 1, pp. 62–76.

    Article  CAS  PubMed  Google Scholar 

  25. Hecker, M., Schumann, W., and Völker, U., Heat-shock and general stress response in Bacillus subtilis, Mol. Microbiol., 1996, vol. 19, no. 3, pp. 417–428.

    Article  CAS  PubMed  Google Scholar 

  26. Hendrickson, E.L., Beck, D.A.C., Wang, T., Lidstrom, M.E., Hackett, M., and Chistoserdova, L., Expressed genome of Methylobacillus flagellatus as defined through comprehensive proteomics and new insights into methylotrophy, J. Bacteriol., 2010, vol. 192, no. 19, pp. 4859–4867.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hördt, A., López, M.G., Meier-Kolthoff, J.P., Schleuning, M., Weinhold, L.-M., Tindall, B. J., Gronow, S., Kyrpides, N.C., Woyke, T., and Göker, M., Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria, Front. Mi-robiol., 2020, vol. 11, p. 468.

    Article  Google Scholar 

  28. Iguchi, H., Yurimoto H., and Sakai Y., Soluble and particulate methanemonooxygenase gene clusters of the type I methanotrophy Methylovulum miyakonense HT12, FEMS Microbiol. Lett., 2010, vol. 312, pp. 71–76.

    Article  CAS  PubMed  Google Scholar 

  29. Jones, D.T., Taylor, W.R., and Thornton J.M., The rapid generation of mutation data matrices from protein sequenc-es, Comput. Appl. Biosci., 1992, vol. 8, pp. 275–282.

    CAS  PubMed  Google Scholar 

  30. Jourand, P., Giraud, E., Bena, G., Sy, A., Willems, A., Gillis, M., Dreyfus, B., and de Lajudie, P., Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively me-thylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria, Int. J. Syst. Evol. Microbiol., 2004, vol. 54, no. 6, pp. 2269–2273.

    Article  CAS  PubMed  Google Scholar 

  31. Kato, Y., Asahara, M., Goto, K., Kasai, H., and Yokota, A., Methylobacterium persicinum sp. nov., Methylobacterium komagatae sp. nov., Methylobacterium brachiatum sp. nov., Methylobacterium tardum sp. nov. and Methylobacterium gregans sp. nov., isolated from freshwater, Int. J. Syst. Evol. Microbiol., 2008, vol. 58, no. 5, pp. 1134–1141.

    Article  CAS  PubMed  Google Scholar 

  32. Kerner, M.J., Naylor, D.J., Ishihama, Y., Maier, T., Chang, H.-H., Stines, A.P., Georgopoulos, C., Frish-man, D., Hayer-Hartl, M., Mann, M., and Hartl, F.U., Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli, Cell, 2005, vol. 122, no. 2, pp. 209–220.

    Article  CAS  PubMed  Google Scholar 

  33. Kotani, T., Yamamoto, T., Yurimoto, H., Sakai, Y., and Kato, N., Propane monooxygenase and NAD+-dependent secondary alcohol dehydrogenase in propane metabolism by Gordonia sp. strain TY-5, J. Bacteriol., 2003, vol. 185, no. 24, pp. 7120–7128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kotani, T., Yurimoto, H., Kato, N., and Sakai, Y., Novel acetone metabolism in a propane-utilizing bacterium, Gordonia sp. strain TY-5, J. Bacteriol., 2007, vol. 189, no. 3, pp. 886–893.

    Article  CAS  PubMed  Google Scholar 

  35. Kumar, C.S., Mande, S.C., and Mahajan, G., Multiple chaperonins in bacteria – novel functions and non-canonical behaviors, Cell Stress Chaperones, 2015, vol. 20, no. 4, pp. 555–574.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K., MEGA X: molecular evolutionary genetics analysis across computing platforms, Mol. Biol. Evol., 2018, vol. 35, no. 6, pp. 1547.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. López-Leal, G., Tabche, M.L., Castillo-Ramírez, S., Mendoza-Vargas, A., Ramírez-Romero, M.A., and Dávila, G., RNA-Seq analysis of the multipartite genome of Rhizobium etli CE3 shows different replicon contributions under heat and saline shock, BMC Genomics, 2014, vol. 15, no. 1, pp. 1–15.

    Article  Google Scholar 

  38. Lu, X., Xu, B., Sun, H., Wei, J., Chi H., Khan, N.U., Wang, X., Wang, X., and Huang, F., Impact of bacterial chaperonin GroEL–GroES on bacteriorhodopsin folding and membrane integration, Biophys. Rep., 2019, vol. 5, no. 3, pp. 133–144.

    Article  CAS  Google Scholar 

  39. Mizobata, T. and Kawata, Y., The versatile mutational “repertoire” of Escherichia coli GroEL, a multidomain chaperonin nanomachine, Biophys. Rev., 2018, vol. 10, pp. 631–640.

    Article  CAS  PubMed  Google Scholar 

  40. Muller, E.E.L., Hourcade, E., Louhichi-Jelail, Y., Hammann, P., Vuilleumier, S., and Bringel, F., Functional genomics of dichloromethane utilization in Methylobacterium extorquens DM4, Environ. Microbiol., 2011, vol. 13, no. 9, pp. 2518–2535.

    Article  CAS  PubMed  Google Scholar 

  41. Narberhaus, F., Käser, R., Nocker, A., and Hennecke, H., A novel DNA element that controls bacterial heat shock gene expression, Mol. Microbiol., 1998, vol. 28, no. 2, pp. 315–323.

    Article  CAS  PubMed  Google Scholar 

  42. Nei, M. and Kumar, S., Molecular Evolution and Phylogenetics, Oxford Univ. Press, 2000.

    Book  Google Scholar 

  43. Pasternak, G. and Kolwzan, B., Surface tension and toxicity changes during biodegradation of carbazole by newly isolated methylotrophic strain Methylobacterium sp. GPE1, Int. Biodeter. Biodegr., 2013, vol. 84, pp. 143–149.

    Article  CAS  Google Scholar 

  44. Roncarati, D. and Scarlato, V., Regulation of heat-shock genes in bacteria: from signal sensing to gene expression output, FEMS Microbiol. Rev., 2017, vol. 41, no. 4, pp. 549–574.

    Article  CAS  PubMed  Google Scholar 

  45. Rzhetsky, A. and Nei, M., A simple method for estimating and testing minimum-evolution trees, Mol. Biol. Evol., 1992, vol. 9, no. 5, pp. 945–967.

    CAS  Google Scholar 

  46. Saitou, N. and Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. B-iol. Evol., 1987, vol. 4, no. 4, pp. 406–425.

    CAS  Google Scholar 

  47. Sluis, M.K., Larsen, R.A., Krum, J.G., Anderson, R., Metcalf, W.W., and Ensign, S.A., Biochemical, molecular, and genetic analyses of the acetone carboxylases from Xanthobacter autotrophicus strain Py2 and Rhodobacter capsulatus strain B10, J. Bacteriol., 2002, vol. 184, no. 11, pp. 2969–2977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Stafford, G.P., Scanlan, J., McDonald, I.R., and Murrell, J.C., rpoN, mmoR and mmoG, genes involved in regulating the expression of soluble methane monooxygenase in Methylosinus trichosporium OB3b, Microbiology (SGM), 2003, vol. 149, no. 7, pp. 1771–1784.

    Article  CAS  PubMed  Google Scholar 

  49. Tatusova, T., DiCuccio, M., Badretdin, A., Chetvernin, V., Nawrocki, E. P., Zaslavsky, L., Lomsadze A., Pruitt K.D., Borodovsky M., and Ostell, J., NCBI prokaryotic genome annotation pipeline, Nucl. Ac. Res., 2016, vol. 44, no. 14, pp. 6614–6624.

    Article  CAS  Google Scholar 

  50. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmou-gin, F., and Higgins, D.G., The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucl. Ac. Res., 1997, vol. 725, no. 24, pp. 4876–4882.

    Article  Google Scholar 

  51. Torgonskaya, M.L., Doronina, N.V., Hourcade, E., Trotsenko, Y.A., and Vuilleumier, S., Chloride-associated adaptive response in aerobic methylotrophic dichloromethane-utilising bacteria, J. Basic Microbiol., 2011, vol. 51, no. 3, pp. 296–303.

    Article  CAS  PubMed  Google Scholar 

  52. Tosu, P., Luepromchai, E., and Suttinun, O., Activation and immobilization of phenol-degrading bacteria on oil palm residues for enhancing phenols degradation in treated palm oil mill effluent, Environ. Eng. Res., 2015, vol. 20, no. 2, pp. 141–148.

    Article  Google Scholar 

  53. Tsagkari, E. and Sloan, W.T., Impact of Methylobacterium in the drinking water microbiome on removal of trihalomethanes, Int. Biodeter. Biodegr., 2019, vol. 141, pp. 10–16.

    Article  CAS  Google Scholar 

  54. Van Aken, B., Yoon, J.M., and Schnoor, J.L., Biodegradation of nitro-substituted explosives 2,4,6-trinitrotoluene, hexahydro-1,3,5-trinitro-1,3,5-triazine, and octahydro-1,3,5,7-tetranitro-1,3,5-tetrazocine by a phytosymbiotic Methylobacterium sp. associated with poplar tissues (Populus deltoides x nigra DN34), Appl. Environ. Microbiol., 2004, vol. 70, no. 1, pp. 508–517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Van Dien, S.J., Okubo, Y., Hough, M.T., Korotkova, N., Taitano, T., and Lidstrom, M.E., Reconstruction of C3 and C4 metabolism in Methylobacterium extorquens AM1 using transposon mutagenesis, Microbiology (SCM), 2003, vol. 149, no. 3, pp. 601–609.

    Article  CAS  PubMed  Google Scholar 

  56. Vorholt, J.A., Microbial life in the phyllosphere, Nature Rev. Microbiol., 2012, vol. 10, no. 12, pp. 828–840.

    Article  CAS  Google Scholar 

  57. Vuilleumier, S., Coping with a halogenated one-carbon diet: aerobic dichloromethane-mineralising bacteria, in Biotechnology for the Environment: Strategy and Fundamentals, 2002, pp.105–130.

    Google Scholar 

  58. Zuckerkandl, E. and Pauling, L., Evolutionary divergence and convergence in proteins, in Evolving Genes and Proteins, Bryson, V. and Vogel, H.J., Eds., New York: Academic, 1965. pp 97–166.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are very grateful to Prof. Akio Tani (Institute of Plant Science and Resources, Okayama University, Okayama, Japan) for kindly providing the type strain of Methylobacterium brachiatum.

Funding

The study was supported by the Russian Science Foundation (grant 23-24-00377, https://rscf.ru/en/project/23-24-00377/).

Author information

Authors and Affiliations

  1. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Federal Research Center “Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences”, 142290, Pushchino, Russia

    M. L. Torgonskaya, Y. E. Firsova, G. A. Ekimova & N. V. Agafonova

  2. SciBear OU, 10115, Tallinn, Estonia

    D. S. Grouzdev

Authors
  1. M. L. Torgonskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. E. Firsova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. A. Ekimova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. S. Grouzdev
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. V. Agafonova
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MLT and NVA analysed the available genomes and coordinated the study. YEF and GAE cultivated Methylobacterium brachiatum B0021T and tested its growth with new substrates, DSG performed sequencing and annotation of its genome. All authors contributed to data analysis. MLT and NVA wrote the main manuscript text. The final manuscript was reviewed and approved by all authors.

Corresponding author

Correspondence to N. V. Agafonova.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Torgonskaya, M.L., Firsova, Y.E., Ekimova, G.A. et al. Distribution and Potential Ecophysiological Roles of Multiple GroEL Chaperonins in Pink-Pigmented Facultative Methylotrophs. Microbiology 93, 14–27 (2024). https://doi.org/10.1134/S0026261723601768

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261723601768

Keywords:

Search

Navigation