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.
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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.
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.
Solioz, M. and Stoyanov, J.V., Copper homeostasis in Enterococcus hirae, FEMS Microbiol. Rev., 2003, vol. 27, pp. 183–195.
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.
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.
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.
Nies, D.H., Efflux-mediated heavy metal resistance in prokaryotes, FEMS Microbiol. Rev., 2003, vol. 27, nos. 2–3, pp. 313–339.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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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.
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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
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DOI: https://doi.org/10.1134/S0026261715020058