Abstract
An aerobic hyperthermophilic CO-oxidizing archaeon, Sulfolobus sp. strain ETSY, was isolated and characterized. Presently, it is the only known representative of both hyperthermophiles and Archaea that is capable of aerobic oxidation of CO, a gas of global importance for atmospheric chemistry and of local importance as one of the substrates for the microbial communities of hydrothermal vents. In the genome of Sulfolobus sp. ETSY we found genetic determinants of aerobic CO oxidation: a coxFMSLDE gene cluster and two separately located coxG genes. We also found such gene clusters in the genomes of certain strains of Sulfolobus islandicus and Sulfolobus solfataricus. On the phylogenetic tree of large subunits of aerobic CO-dehydrogenases (CoxLs), these proteins of Sulfolobus representatives formed a compact cluster within one of the branches formed by bacterial form I CoxLs. Thus we argue that the ability to oxidize CO aerobically was acquired by Sulfolobus ancestor from Bacteria relatively late in the evolution, presumably after the formation of the atmosphere with a high oxygen content.
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Brady, A.L., Sharp, C.E., Grasby, S.E., and Dunfield, P.F., Anaerobic carboxydotrophic bacteria in geothermal springs identified using stable isotope probing, Front. Microbiol., 2015, vol. 6, 897.
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T.L., BLAST+: architecture and applications, BMC Bioinformatics, 2009, vol. 10, 421.
Fuhrmann, S., Ferner, M., Jeffke, T., Henne, A., Gottschalk, G., and Meyer, O., Complete nucleotide sequence of the circular megaplasmid pHCG3 of Oligotropha carboxidovorans: function in the chemolithoautotrophic utilization of CO, H2 and CO2, Gene, 2003, vol. 322, pp. 67–75.
Huber, H., Prangishvili, D., Sulfolobales, in Prokaryotes, 3d ed., Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K. H., and Stackebrandt, E., Eds., Syngapure: Springer, 2006, vol. 3, pp. 23–51
Huson, D.H. and Scornavacca, C., Dendroscope 3–an interactive viewer for rooted phylogenetic trees and networks, Syst. Biol., 2012, vol. 61, pp. 1061–1067.
IPCC Climate Change 2001, The Scientific Basis. Contribution of Working Group 1 to the Third Assessment Report of the Intergovernmental Panel on Climate Change. New York: Cambridge University Press, 2001.
Katoh, K., Misawa, K., Kuma, K., and Miyata, T., MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 2002, vol. 30, pp. 3059–3066.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. and Drummond, A., Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data, Bioinformatics, 2012, vol. 28, pp. 1647–1649.
Kevbrin, V.V. and Zavarzin, G.A., The effect of sulfur compounds on the growth of the halophilic homoacetic bacterium Acetohalobium arabaticum, Mikrobiologiya, 1992, vol. 61, pp. 812–817 (in Russian).
King, C.E., Diversity and activity of aerobic thermophilic carbon monoxide oxidizing Bacteria on Kilauea volcano, Hawaii, Doctoral Dissertation, Louisiana State University. 2013.
King, C.E. and King, G.M., Description of Thermogemmatispora carboxidivorans sp. nov., a carbon-monoxide-oxidizing member of the class Ktedonobacteria isolated from a geothermally heated biofilm, and analysis of carbon monoxide oxidation by members of the class Ktedonobacteria, Int. J. Syst. Evol. Microbiol., 2014a, vol. 64, pp. 1244–1251.
King, C.E. and King, G.M., Thermomicrobium carboxidum sp. nov., and Thermorudis peleae gen. nov., sp. nov., carbon monoxide-oxidizing bacteria isolated from geothermally heated biofilms, Int. J. Syst. Evol. Microbiol., 2014b, vol. 64, pp. 2586–2592.
King, G.M. and Weber, C.F., Distribution, diversity and ecology of aerobic CO-oxidizing bacteria, Nat. Microbiol. Rev., 2007, vol. 5, pp. 107–118.
Kochetkova, T.V., Rusanov, I.I., Pimenov, N.V., Kolganova, T.V., Lebedinsky, A.V., Bonch-Osmolovskaya, E.A., and Sokolova, T.G., Anaerobic transformation of carbon monoxide by microbial communities of Kamchatka hot springs, Extremophiles, 2011, vol. 15, pp. 319–325.
Krüger, B. and Meyer, O., Thermophilic bacilli growing with carbon monoxide, Arch. Microbiol., 1984, vol. 139, pp. 402–408.
Markowitz, V.M., Chen, I.M., 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, Nucleic Acids Res., 2012, vol. 40 (Database issue), pp. D115–D122.
Marmur, J., A procedure for the isolation of deoxyribonucleic acid from microorganisms, J. Mol. Biol., 1961, vol. 3, pp. 208–218.
Martínez-Alonso, S., Deeter, M.N., Worden, H.M., Clerbaux, C., Mao, D., and Gille, J. C. First satellite identification of volcanic carbon monoxide, Geophys. Res. Lett., 2012, vol. 39, no. 21, L21809.
Meyer, O., Frunzke, K., Gadkari, D., Jacobitz, S., Hugendieck, I., and Kraut, M., Utilization of carbon monoxide by aerobes–recent advances, FEMS. Microbiol. Rev., 1990, vol. 87, pp. 253–260.
Nishimura, H., Nomura, Y., Iwata, E., Sato, N., and Sako, Y., Purification and characterization of carbon monoxide dehydrogenase from the aerobic hyperthermophilic archaeon Aeropyrum pernix, Fish Sci., 2010, vol. 76, pp. 999–1006.
Nozhevnkova, A.N. and Zavarzin, G.A., Taxonomy of COoxidizing Gram-negative bacteria, Izv. Akad. Nauk SSSR, Ser. Biol., 1974, vol. 3, pp. 436–440 (in Russian).
Pelzmann, A.M., Mickoleit, F., and Meyer, O., Insights into the posttranslational assembly of the Mo-, S-and Cucontaining cluster in the active site of CO dehydrogenase of Oligotropha carboxidovorans, J. Biol. Inorg. Chem., 2014, vol. 19, pp. 1399–1414.
Petron, G., Granier, C., Khattatov, B., Yudin, V., Lamarque, J.-F., Emmons, L., Gille, J., and Edwards, D.P., Monthly CO surface sources inventory based on the 2000–2001 MOPITT satellite data, Geophys. Res. Lett., 2004, vol. 31, L21107.
Price, M.N., Dehal, P.S., and Arkin, A.P., FastTree 2–approximately maximum-likelihood trees for large alignments, PLoS One, 2010, vol. 5, e9490.
Shimodaira, H. and Hasegawa, M., Multiple comparisons of log-likelihoods with applications to phylogenetic inference, Mol. Biol. Evol., 1999, vol. 16, pp. 1114–1116.
Slepova, T.V., Hydrogenogenic carboxydotrophic prokaryotes in hot springs of Kamchatka, Cand. Sci. (Biol.) Dissertation, Moscow: Winogradsky Institute of Microbiology, 2008 (in Russian).
Sokolova, T.G., Henstra, A.M., Sipma, J., Parshina, S.N., Stams, A.J., and Lebedinsky, A.V., Diversity and ecophysiological features of thermophilic carboxydotrophic anaerobes, FEMS Microbiol. Ecol., 2009, vol. 68, pp. 131–141.
Sokolova, T. and Lebedinsky, A., CO-oxidizing anaerobic thermophilic prokaryotes, in Thermophilic Microbes in Environmental and Industrial Biotechnology. Biotechnology of thermophiles, 2nd ed., Satyanarayana, T., Littlechild, J., and Kawarabayasi, Y., Eds., Dordrecht–Heidelberg–New York–London: Springer Science + Business Media Dordrecht, 2013, pp. 203–231.
Volland, S., Rachinger, M., Strittmatter, A., Daniel, R., Gottschalk, G., and Meyer, O., Complete genome sequences of the chemolithoautotrophic Oligotropha carboxidovorans strains OM4 and OM5, J. Bacteriol., 2011, vol. 193, p. 5043.
Wolin, E.A., Wolin, M.J., and Wolfe, R.S., Formation of methane by bacterial extracts, J. Biol. Chem., 1963, vol. 238, pp. 2882–2886.
Wu, D., Raymond, J., Wu, M., Chatterji, S., and Ren, Q., Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum, PLoS One, 2009, vol. 4(1), e4207.
Yang, J., Zhou, E., Jiang, H., Li, W., Wu, G., Huang, V., Hedlund, B. P., and Dong, H., Distribution and diversity of aerobic carbon monoxide-oxidizing bacteria in geothermal springs of China, the Philippines, and the United States, Geomicrobiol. J., 2015, vol. 32, pp. 903–913.
Yoneda, Y., Kano, S.I., Yoshida, T., Ikeda, E., Fukuyama, Y., Omae, K., Kimura-Sakai, S., Daifuku, T., Watanabe, T., and Sako, Y., Detection of anaerobic carbon monoxide-oxidizing thermophiles in hydrothermal environments, FEMS Microbiol. Ecol., 2015, vol. 91(9), fiv093.
Zavarzin, G.A., Hydrogen Bacteria and Carboxydobacteria, Moscow: Nauka, 1978 (in Russian).
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Original Russian Text © T.G. Sokolova, M.M. Yakimov, N.A. Chernyh, E.Yu. Lun’kova, N.A. Kostrikina, E.A. Taranov, A.V. Lebedinskii, E.A. Bonch-Osmolovskaya, 2017, published in Mikrobiologiya, 2017, Vol. 86, No. 5, pp. 527–537.
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Sokolova, T.G., Yakimov, M.M., Chernyh, N.A. et al. Aerobic carbon monoxide oxidation in the course of growth of a hyperthermophilic archaeon, Sulfolobus sp. ETSY. Microbiology 86, 539–548 (2017). https://doi.org/10.1134/S0026261717050174
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DOI: https://doi.org/10.1134/S0026261717050174