Skip to main content
SpringerLink
Log in

Methylophaga muralis Bur 1, a haloalkaliphilic methylotroph isolated from the Khilganta soda lake (Southern Transbaikalia, Buryat Republic)

  • Experimental Articles
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

A haloalkaliphilic restricted facultative methylotroph, strain Bur 1, which used methanol, methylated amines, and fructose as carbon and energy sources, was isolated from the soda Lake Khilganta (Buryat Republic, Russia). The cells were gram-negative non-spore-forming, motile rods reproducing by binary fission. The organism was aerobic, reduced nitrates to nitrites. Growth occurred at temperatures from 4 to 37°C (optimum at 25–29°C), pH 7.5–10.5 (optimum at 8.5–9.5), and NaCl concentration in the medium from 0.05 to 10.0% NaCl (optimum at 3–4%). Ectoine, glutamate, and sucrose were accumulated as osmoprotectants. Activity of the enzymes of de novo ectoine biosynthesis were detected. The organism utilized C1 compounds via the KDPG variant of the ribulose monophosphate pathway. The DNA G + C content was 44.67 mol %. Based on the similarity of the 16S rRNA gene sequences (94.7–99.1%) and the results of DNA–DNA hybridization (24–74%) with type strains of the neutrophilic and alkaliphilic Methylophaga species, the isolate was identified as Methylophaga muralis Bur 1 (VKM B-3046 = DSM 103617). The genome of M. muralis Bur 1 contained 2585 protein-encoding genes; 634 proteins with unidentified functions were predicted. Three rRNAs (5S, 16S, and 23S) and 38 tRNAs were identified. Apart from the mxaFJGIRSACKLDEH classical cluster of methanol oxidation genes, the xoxF gene was found. Methylamine was oxidized to formaldehyde by methylamine dehydrogenase and via the N-methylglutamate pathway. Orthologs of type III glutamine synthetases were revealed in the genome. The operons of ectoine and sucrose biosynthesis, ectRABC-ask and sps-spp-fruK-ams, were found. The genomes of M. muralis Bur 1 and M. lonarensis MPLT, unlike that of M. nitratireducenticrescens JAM1T, were found to contain the genes encoding the proteins of bicarbonate transport.

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

Similar content being viewed by others

References

  • Antony, C.P., Doronina, N.V., Boden, R., Trotsenko, Y.A., Shouche, Y.S., and Murrell J.C., Methylophaga lonarensis sp. nov., a moderately haloalkaliphilic methylotroph isolated from the soda lake sediments of a meteorite impact crater, Int. J. Syst. Evol. Microbiol., 2012, vol. 62, pp. 1613–1618.

    Article  CAS  PubMed  Google Scholar 

  • Boden, R., Emended description of the genus Methylophaga Janvier et al. 1985, Int. J. Syst. Evol. Microbiol., 2012, vol. 62, pp. 1644–1646.

    Article  PubMed  Google Scholar 

  • Boden, R., Ferriera, S., Johnson, J., Kelly, D.P., Murrell, J.C., and Schäfer, H., Draft genome sequence of the chemolithoheterotrophic, halophilic methylotroph Methylophaga thiooxydans DMS010, J. Bacteriol., 2011, vol. 193, pp. 3154–3155.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boden, R., Kelly, D.P., Murrell, J.C., and Schäfer, H., Oxidation of dimethylsulfide to tetrathionate by Methylophaga thiooxidans sp. nov.: a new link in the sulfur cycle, Environ. Microbiol., 2010, vol. 12, pp. 2688–2699.

    CAS  PubMed  Google Scholar 

  • But, S.Y., Khmelenina, V.N., Reshetnikov, A.S., Mustakhimov, I.I., Kalyuzhnaya, M.G., and Trotsenko, Y.A., Sucrose metabolism in halotolerant methanotroph Methylomicrobium alcaliphilum 20Z, Arch. Microbiol., 2015, vol. 197, pp. 471–480.

    Article  CAS  PubMed  Google Scholar 

  • De Zwart, J.M.M., Nelisse, P.N., and Kuenen, J.G., Isolation and characterization of Methylophaga sulfidovorans sp. nov.: an obligately methylotrophic, aerobic, dimethylsulfide oxidizing bacterium from a microbial mat, FEMS Microbiol. Ecol., 1996, vol. 20, pp. 261–270.

    Article  Google Scholar 

  • Doronina, N.V., Darmaeva, T.D., and Trotsenko, Y.A., Methylophaga alcalica sp. nov., a novel alkaliphilic and moderately halophilic, obligately methylotrophic bacterium from the East Mongolian saline soda lake, Int. J. Syst. Evol. Microbiol., 2003a, vol. 53, pp. 223–229.

    Article  CAS  PubMed  Google Scholar 

  • Doronina, N.V., Darmaeva, Ts.D., and Trotsenko, Y.A., Methylophaga natronica sp. nov., a new alkaliphilic and moderately halophilic, restricted-facultative methylotrophic bacterium from soda lake of the Southern Transbaikal region, Syst. Appl. Microbiol., 2003b, vol. 26, pp. 382–389.

    Article  CAS  PubMed  Google Scholar 

  • Doronina, N.V., Gogleva, A.A., and Trotsenko, Y.A., Methylophilus glucosoxydans sp. nov., a restricted facultative methylotroph from rice rhizosphere, Int. J. Syst. Evol. Microbiol., 2012, vol. 62, pp. 196–201.

    Article  CAS  PubMed  Google Scholar 

  • Doronina, N.V., Lee, T.D., Ivanova, E.G., and Trotsenko, Y.A., Methylophaga murata sp. nov.: a haloalkaliphilic aerobic methylotroph from deteriorating marble, Microbiology (Moscow), 2005, vol. 74, no. 4, pp. 440–447.

    Article  CAS  Google Scholar 

  • Doronina, N.V., Li, T.D., Ivanova, E.G., and Trotsenko, Y.A. Methylophaga muralis sp. nov. in List of New Names and new combinations previously effectively, but not validly, published, validation list no. 138, Int. J. Syst. Evol. Microbiol., 2011, vol. 61, pp. 475–476.

    Article  Google Scholar 

  • Doronina, N.V., Trotsenko, Y.A., and Tourova, T.P. Methylarcula marina gen. nov., sp. nov. and Methylarcula terricola sp. nov.: novel aerobic, moderately halophilic, facultatively methylotrophic bacteria from coastal saline environments, Int. J. Syst. Evol. Microbiol., 2000, vol. 50, pp. 1849–1859.

    Article  CAS  PubMed  Google Scholar 

  • Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucl. Acids. Symp. Ser., Oxford Univ. Press. 1999, no. 41, pp. 95–98.

    CAS  Google Scholar 

  • Han, G.H., Kim, W., Chun, J., and Kim, S.W., Draft genome sequence of Methylophaga aminisulfidivorans MPT, J. Bacteriol., 2011, vol. 193, p. 4265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janvier, M., Frehel, C., Grimont, F., and Gasser, F., Methylophaga marina gen. nov., sp. nov. and Methylophaga thalassica sp. nov., marine methylotrophs, Int. J. Syst. Bacteriol., 1985, vol. 35, pp. 131–139.

    Article  CAS  Google Scholar 

  • Kim, H.G., Doronina, N.V., Trotsenko, Y.A., and Kim, S.W., Methylophaga aminisulfidivorans sp. nov., a restricted facultatively methylotrophic marine bacterium, Int. J. Syst. Evol. Microbiol., 2007, vol. 57, pp. 2096–2101.

    Article  CAS  PubMed  Google Scholar 

  • Kumada, Y., Benson, D.R., Hillemann, D., Hosted, T.J., Rochefort, D.A., Thompson, C.J., Wohlleben, W., and Tateno, Y., Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes (gene duplication/molecular evolution/pre-prokaryote-eukaryote evolution), Proc. Natl. Acad. Sci. U. S. A., 1993, vol. 90, pp. 3009–3013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Markowitz, V.M., Chen, I.-M.A., Palaniappan, K., Chu, K., Szeto, E., Grechkin, Y., Ratner, A., Jacob, B., Huang, J., Williams, P., Huntemann, M., Anderson, I., Mavromatis, K., Ivanova, N.N., and Kyrpides, N.C., IMG: the integrated microbial genomes database and comparative analysis system, Nucl. Acids Res., 2012, vol. 40. Database issue: D123–129.

    Article  CAS  PubMed  Google Scholar 

  • Marmur, J.A., A procedure for the isolation of deoxyribonucleic acid from microorganisms, J. Mol. Biol., 1961, vol. 3, pp. 208–218.

    Article  CAS  Google Scholar 

  • Mustakhimov, I.I., Reshetnikov, A.S., Khmelenina, V.N., and Trotsenko, Y.A., Regulatory mechanisms of biosynthesis of ectoins in halophilic bacteria, Microbiology (Moscow), 2010, vol. 79, no. 5, pp. 595–604.

    Article  Google Scholar 

  • Peters, P., Galinski, E.A., and Trüper, H.G., The biosynthesis of ectoine, FEMS Microbiol. Lett., 1990, vol. 71, pp. 157–162.

    Article  CAS  Google Scholar 

  • Poroshina, M.N., Doronina, N.V., Kaparullina, E.N., Kovalevskaya, N.P., and Trotsenko, Yu.A., Halophilic and halotolerant aerobic methylobacteria from the technogenic Solikamsk biotopes, Microbiology (Moscow), 2013, vol. 82, no. 4, pp. 490–498.

    Article  CAS  Google Scholar 

  • Reshetnikov, A.S., Khmelenina, V.N., and Trotsenko, Yu.A., Ectoine biosynthesis genes identification in moderate halophilic alphaproteobacteria Methylarcula marina, Microbiology (Moscow), 2010, vol. 79, no. 6, pp. 859–860.

    Article  CAS  Google Scholar 

  • Seemann, T., Prokka: rapid prokaryotic genome annotation, Bioinformatics, 2014, vol. 30, pp. 2068–2069.

    Article  CAS  PubMed  Google Scholar 

  • Shetty, S.A., Marathe, N.P., Munot, H., Antony, C.P., Dhotre, D.P., Murrell, J.C., and Shouche, Y.S., Draft genome sequence of Methylophaga lonarensis MPLT, a haloalkaliphilic (non-methane-utilizing) methylotroph, Genome Announc., 2013, vol. 1, pp. 202–213.

    Article  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol., 2011, vol. 28, pp. 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G., The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucl. Acids Res., 1997, vol. 25, pp. 4876–4882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trotsenko, Y.A., Doronina, N.V., and Govorukhina, N.I., Metabolism of non-motile obligately methylotrophic bacteria, FEMS Microbiol. Lett., 1986, vol. 3, pp. 293–297.

    Article  Google Scholar 

  • Vasilenko, O.V., Shmareva, M.N., Doronina, N.V., Tarlachkov, S.V., Mustakhimov, I.I., and Trotsenko, Y.A., Draft genome sequence of Methylophaga muralis Bur1, a haloalkaliphilic (non-methane-utilising) methylotroph from soda lake, Genome Announc., 2016, vol. 4. e01227–16.

    PubMed  PubMed Central  Google Scholar 

  • Villeneuve, C., Martineau, C., Mauffrey, F., and Villemur, R. Methylophaga nitratireducenticrescens sp. nov. and Methylophaga frappieri sp. nov., isolated from the biofilm of the methanol-fed denitrification system treating the seawater at the Montreal Biodome, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, pp. 2216–2222.

    Article  CAS  PubMed  Google Scholar 

  • Villeneuve, C., Martineau, C., Mauffrey, F., and Villemur, R., Complete genome sequences of Methylophaga sp. strain JAM1 and Methylophaga sp. strain JAM7, J. Bacteriol., 2012, vol. 194, pp. 4126–4127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Russia

    M. N. Shmareva, N. V. Doronina, S. V. Tarlachkov, O. V. Vasilenko & Yu. A. Trotsenko

Authors
  1. M. N. Shmareva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. V. Doronina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. V. Tarlachkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. V. Vasilenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu. A. Trotsenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. N. Shmareva.

Additional information

Original Russian Text © M.N. Shmareva, N.V. Doronina, S.V. Tarlachkov, O.V. Vasilenko, Yu.A. Trotsenko, 2018, published in Mikrobiologiya, 2018, Vol. 87, No. 1, pp. 23–36.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shmareva, M.N., Doronina, N.V., Tarlachkov, S.V. et al. Methylophaga muralis Bur 1, a haloalkaliphilic methylotroph isolated from the Khilganta soda lake (Southern Transbaikalia, Buryat Republic). Microbiology 87, 33–46 (2018). https://doi.org/10.1134/S0026261718010162

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261718010162

Keywords

Search

Navigation