Skip to main content
SpringerLink
Log in

Diversity of copper proteins and copper homeostasis systems in Melioribacter roseus, a facultatively anaerobic thermophilic member of the new phylum Ignavibacteriae

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

Abstract

The genome of Melioribacter roseus, one of the two members of the recently described phylum Ignavibacteriae, was screened for genes encoding proteins associated with copper transport or containing copper as a cofactor, and the effect of Cu2+ concentration in the medium on M. roseus growth was investigated. Genomic analysis revealed a variety of copper-containing oxidoreductases in this facultative anaerobe. Three ATPases responsible for copper transport were identified. One of them (MROS_1511) is probably involved in the assembly of copper-containing cytochrome c oxidase, while two others (MROS_0327 and MROS_0791) probably carry out a detoxification function. The presence of several copper-containing oxidoreductases and copper homeostasis systems in M. roseus is in agreement with the previously hypothesized origin of the phylum Ignavibacteriae from an aerobic ancestor common with Bacteroidetes and Chlorobi.

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

  1. Ridge, P.G., Zhang, Y., and Gladyshev, V.N., Comparative genomic analyses of copper transporters and cuproproteomes reveal evolutionary dynamics of copper utilization and its link to oxygen, PLoS ONE, 2008, vol. 3, no. 1, e1378.

    Article  PubMed Central  PubMed  Google Scholar 

  2. Saito, M.A., Sigman, D.M., and Morel, F.M.M., The bioinorganic chemistry of the ancient ocean: the coevolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean-Proterozoic boundary?, Inorg. Chim. Acta, 2003, vol. 356, pp. 308–318.

    Article  CAS  Google Scholar 

  3. Solioz, M. and Stoyanov, J.V., Copper homeostasis in Enterococcus hirae, FEMS Microbiol. Rev., 2003, vol. 27, pp. 183–195.

    Article  CAS  PubMed  Google Scholar 

  4. Jordan, K.I., Natale, D.A., Koonin, E.V., and Galperin, M.Y., Independent evolution of heavy metal-associated domains in copper chaperones and coppertransporting ATPases, J. Mol. Evol., 2001, vol. 53, no. 6, pp. 622–633.

    Article  CAS  PubMed  Google Scholar 

  5. Magnani, D. and Solioz, M., How bacteria handle copper, in Molecular Microbiology of Heavy Metals, Nies, D.H. and Silver, S., Eds., Heidelberg: Springer, 2007, pp. 259–285.

    Chapter  Google Scholar 

  6. Saier, M.H., Jr., Yen, M.R., Noto, K., Tamang, D.G., and Elkan, C., The transporter classification database: recent advances, Nucleic Acids Res., 2009, vol. 37 (Database issue):D274–D2788.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Nies, D.H., Efflux-mediated heavy metal resistance in prokaryotes, FEMS Microbiol. Rev., 2003, vol. 27, nos. 2–3, pp. 313–339.

    Article  CAS  PubMed  Google Scholar 

  8. Podosokorskaya, O.A., Kadnikov, V.V., Gavrilov, S.N., Mardanov, A.V., Merkel, A.Y., Karnachuk, O.V., Ravin, N.V., Bonch-Osmolovskaya, E.A., and Kublanov, I.V., Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae, Environ. Microbiol, 2013, vol. 5, no. 6, pp. 1759–1771.

    Article  Google Scholar 

  9. Gupta, R.S. and Lorenzini, E., Phylogeny and molecular signatures (conserved proteins and indels) that are specific for the Bacteroidetes and Chlorobi species, BMC Evol. Biol., 2007, vol. 7, pp. 71–89.

    Article  PubMed Central  PubMed  Google Scholar 

  10. Iino, T., Mori, K., Uchino, Y., Nakagawa, T., Harayama, S., and Suzuki, K.I., Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria, Int. J. Syst. Evol. Microbiol., 2010, vol. 60, no. 6, pp. 1376–1382.

    Article  CAS  PubMed  Google Scholar 

  11. Liu, Z., Frigaard, N-U., Vogl, K., Iino, T., Ohkuma, M., Overmann, J., and Bryant, D.A., Complete genome of Ignavibacterium album, a metabolically versatile, flagellated, facultative anaerobe from the phylum Chlorobi, Front. Microbiol., 2012, vol. 3, pp. 185–200.

    PubMed Central  CAS  PubMed  Google Scholar 

  12. Solioz, M. and Vulpe, C., CPX-type ATPases: a class of P-type ATPases that pump heavy metals, Trends Biochem. Sci., 1996, vol. 21, no. 7, pp. 237–241.

    Article  CAS  PubMed  Google Scholar 

  13. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res., 2000, vol. 25, no. 17, pp. 3389–3402.

    Article  Google Scholar 

  14. 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, no. 10, pp. 2731–2739.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Ying, H., Beifang, N., Ying, G., Limin, F., and Weizhong, L., CD-HIT Suite: a web server for clustering and comparing biological sequences, Bioinformatics, 2010, vol. 26, pp. 680–682.

    Article  Google Scholar 

  16. Chan, H., Babayan, V., Blyumin, E., Gandhi, C., Hak, K., Harake, D., Kumar, K., Lee, P., Li, T.T., Liu, H.Y., Tung, Lo T.C., Meyer, C.J., Stanford, S., Zamora, K.S., and Saier, M.H., Jr., The P-type ATPase superfamily, J. Mol. Microbiol. Biotechnol., 2010, vol. 19, nos. 1–2, pp. 5–104.

    Article  CAS  PubMed  Google Scholar 

  17. Franke, S., Grass, G., Rensing, C., and Nies, D.H., Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli, J. Bacteriol., 2003, vol. 185, no. 13, pp. 3804–3812.

    Article  PubMed Central  PubMed  Google Scholar 

  18. Lamrabet, O., Pieulle, L., Aubert, C., Mouhamar, F., Stocker, P., Dolla, A., and Brasseur, D., Oxygen reduction in the strict anaerobe Desulfovibrio vulgaris Hildenborough: characterization of two membranebound oxygen reductases, Microbiology (UK), 2011, vol. 157, pp. 2720–2732.

    Article  CAS  Google Scholar 

  19. Karnachuk, O.V., Sasaki, K., Gerasimchuk, A.L., Sukhanova, O., Ivasenko, D.A., Kaksonen, A.H., Puhakka, J.A., and Tuovinen, O.H., Precipitation of Cu-sulfides by copper-tolerant Desulfovibrio isolates, Geomicrobiol. J., 2008, vol. 25, no. 5, pp. 219–227.

    Article  CAS  Google Scholar 

  20. Karnachuk, O.V., Kurochkina, S.Yu., Nicomrat, D., Frank, Yu.A., Ivasenko, D.A., Phyllipenko, E.A., and Tuovinen, O.H., Copper resistance in Desulfovibrio strain R2, Antonie van Leeuwenhoek, 2003, vol. 83, no. 1, pp. 99–106.

    Article  CAS  PubMed  Google Scholar 

  21. Madsen, J.H., Burmølle, M., Hansen, L.H., Sørensen, S.J. The interconnection between biofilm formation and horizontal gene transfer, FEMS Immunol. Med. Microbiol., 2012, vol. 65, no. 2, pp. 183–195.

    Article  CAS  PubMed  Google Scholar 

  22. Liu, Z., Klatt, C.G., Ludwig, M., Rusch, D.B., Jensen, S.I., Kühl, M., Ward, D.M., and Bryant, D., ‘Candidatus Thermochlorobacter aerophilum’: an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics, ISME J., 2012, vol. 6, pp. 1869–1882.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. 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 Press, 1965, pp. 97–166.

    Chapter  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Physiology and Biotechnology, Tomsk State University, Tomsk, Russia

    O. V. Karnachuk, M. R. Avakyan & Yu. A. Frank

  2. Winogradsky Institute of Microbiology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7, k. 2, Moscow, 117312, Russia

    S. N. Gavrilov, O. A. Podosokorskaya, E. A. Bonch-Osmolovskaya & I. V. Kublanov

Authors
  1. O. V. Karnachuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. N. Gavrilov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. R. Avakyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. A. Podosokorskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu. A. Frank
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. A. Bonch-Osmolovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. I. V. Kublanov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to O. V. Karnachuk or I. V. Kublanov.

Additional information

Original Russian Text © O.V. Karnachuk, S.N. Gavrilov, M.R. Avakyan, O.A. Podosokorskaya, Yu.A. Frank, E.A. Bonch-Osmolovskaya, I.V. Kublanov, 2015, published in Mikrobiologiya, 2015, Vol. 84, No. 2, pp. 165–174.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karnachuk, O.V., Gavrilov, S.N., Avakyan, M.R. et al. Diversity of copper proteins and copper homeostasis systems in Melioribacter roseus, a facultatively anaerobic thermophilic member of the new phylum Ignavibacteriae . Microbiology 84, 135–143 (2015). https://doi.org/10.1134/S0026261715020058

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261715020058

Keywords

Search

Navigation