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Metabolic Potential of Sulfobacillus thermotolerans: Pathways for Assimilation of Nitrogen Compounds and the Possibility of Lithotrophic Growth in the Presence of Molecular Hydrogen

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Abstract

Sulfobacillus thermotolerans predominates in communities of acidophilic chemolithotrophic microorganisms and is of practical importance to biotechnologies for sulfide minerals processing. This is the first report on the presence of the genes encoding a quinone-binding [Fe-Ni] hydrogenase in S. thermotole-rans genome; this microorganism is therefore potentially capable of lithotrophic growth in the presence of molecular hydrogen. Components of the pathways for nitrogen compounds assimilation by S. thermotolerans probably include two assimilatory nitrate reductases, while NO dioxygenase and nitronate monooxygenases are probably involved in detoxication of nitric oxide and nitrocompounds. Research on the pathways of assimilation and detoxication of nitrogen compounds, as well as on alternative electron donors and acceptors in sulfobacilli will improve our understanding of the interactions within acidophilic chemolithotrophic communities in nature and industry.

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REFERENCES

  1. Bogdanova, T.I., Tsaplina, I.A., Kondrat’eva, T.F., Duda, V.I., Suzina, N.E., Melamud, V.S., Tourova, T.P., and Karavaiko, G.I., Sulfobacillus thermotolerans sp. nov., a thermotolerant, chemolithotrophic bacterium, Int. J. Syst. Evol. Microbiol., 2006, vol. 56, pp. 1039–1042.

    Article  CAS  Google Scholar 

  2. Bridge, T.A.M. and Johnson, D.B., Reduction of soluble iron and reductive dissolution of ferric iron-containing minerals by moderately thermophilic iron-oxidizing bacteria, Appl. Environ. Microbiol., 1998, vol. 64, pp. 2181–2186.

    Article  CAS  Google Scholar 

  3. Brierley, C.L. and Brierley, J.A., Progress in bioleaching: part B: applications of microbial processes by the minerals industries, Appl. Microbiol. Biotechnol., 2013, vol. 97, pp. 7543–7552.

    Article  CAS  Google Scholar 

  4. Bulaev, A., Belyi, A., Panyushkina, A., Solopova, N., and Pivovarova, T., Microbial population of industrial biooxidation reactors, Solid State Phenomena, 2017, vol. 262, pp. 48–52.

    Article  Google Scholar 

  5. Bulaev, A.G., Pivovarova, T.A., Melamud, V.S., Bumazhkin, B.K., Patutina, E.O., Kolganova, T.V., Kuzne-tsov, B.B., and Kondrat’eva, T.F., Changes in the species composition of a thermotolerant community of acidophilic chemolithotrophic microorganisms upon switching to the oxidation of a new energy substrate, Microbiology (Moscow), 2012, vol. 81, pp. 391–396.

    Article  CAS  Google Scholar 

  6. Dopson, M. and Lindström, E.B., Analysis of community composition during moderately thermophilic bioleaching of pyrite, arsenical pyrite, and chalcopyrite, Microb. Ecol., 2004, vol. 48, pp. 19–28.

    Article  CAS  Google Scholar 

  7. Francis, K., Smitherman, C., Nishino, S.F., Spain, J.C., and Gadda, G., The biochemistry of the metabolic poison propionate 3-nitronate and its conjugate acid, 3-nitropropionate, IUBMB Life, 2013, vol. 65, pp. 759–768.

    Article  CAS  Google Scholar 

  8. Gadda, G. and Francis, K., Nitronate monooxygenase, a model for anionic flavin semiquinone intermediates in oxidative catalysis, Arch. Biochem. Biophys., 2010, vol. 493, pp. 53–61.

    Article  CAS  Google Scholar 

  9. Gardner, P.R., Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases, J. Inorg. Biochem., 2005, vol. 99, pp. 247–266.

    Article  CAS  Google Scholar 

  10. Hedrich, S. and Johnson, D.B., Aerobic and anaerobic oxidation of hydrogen by acidophilic bacteria, FEMS Microbiol. Lett., 2013, vol. 349, pp. 40–45.

    CAS  PubMed  Google Scholar 

  11. Johnson, D.B., Joulian, C., d’Hugues, P., and Hallberg, K.B., Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations, Extremophiles, 2008, vol. 12, pp. 789–798.

    Article  CAS  Google Scholar 

  12. Justice, N.B, Norman, A., Brown, C.T., Singh, A., Thomas, B.C., and Banfield, J.F., Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms, BMC Genomics, 2014, vol. 15, p. 1107. https://doi.org/10.1186/1471-2164-15-1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M., KEGG as a reference resource for gene and protein annotation, Nucleic Acids Res., 2016, vol. 44, no. D1, pp. D457–D462.

    Article  CAS  Google Scholar 

  14. Karavaiko, G.I., Krasil’nikova, E.N., Tsaplina, I.A., and Zakharchuk, L.M., Growth and carbohydrate metabolism of sulfobacilli, Microbiology (Moscow), 2001, vol. 70, pp. 245–250.

    Article  CAS  Google Scholar 

  15. Kondrat’eva, N.F., Pivovarova, T.A., Tsaplina, I.A., Fomchenko, N.V., Murav’ev, M.I., Melamud, V.S., and Bulaev, A.G., Diversity of the communities of acidophilic chemolithotrophic microorganisms in natural and technogenic ecosystems, Microbiology (Moscow), 2012, vol. 81, pp. 1–24.

    Article  Google Scholar 

  16. Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870–1874.

    Article  CAS  Google Scholar 

  17. Lin, K.-H., Liao, B.-Y., Chang, H.-W., Huang, S.-W., Chang, T.-Y., Yang, C.-Y., Wang, Y.-B., Lin, Y.-T. K., Wu, Y.-W., Tang, S.-L., and Yu, H.-T., Metabolic characteristics of dominant microbes and key rare species from an acidic hot spring in Taiwan revealed by metagenomics, BMC Genomics, 2015, vol. 16, p. 1029. https://doi.org/10.1186/s12864-015-2230-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Panyushkina, A.E., Babenko, V.V., Nikitina, A.S., Selezneva, O.V., Tsaplina, I.A., Letarova, M.A., Kostryukova, E.S., and Letarov, A.V., Sulfobacillus thermotolerans: new insights into resistance and metabolic capacities of acidophilic chemolithotrophs, Sci. Rep., 2019. In press.

  19. Panyushkina, A.E., Tsaplina, I.A., Grigor’eva, N.V., and Kondrat’eva, T.F., Thermoacidophilic microbial community oxidizing the gold-bearing flotation concentrate of a pyrite-arsenopyrite ore, Microbiology (Moscow), 2014, vol. 83, pp. 539–549.

    Article  CAS  Google Scholar 

  20. Panyushkina, A.E., Tsaplina, I.A., Kondrat’eva, T.F., Belyi, A.V., and Bulaev, A.G., Physiological and morphological characteristics of acidophilic bacteria Leptospirillum ferriphilum and Acidithiobacillus thiooxidans, members of the chemolithotrophic microbial consortium, Microbiology (Moscow), 2018, vol. 87, pp. 326–338.

    Article  CAS  Google Scholar 

  21. Parry, R., Nishino, S., and Spain, J., Naturally-occurring nitro compounds, Nat. Prod. Rep., 2011, vol. 28, pp. 152–167.

    Article  CAS  Google Scholar 

  22. Tan, G.L., Shu, W.S., Hallberg, K.B., Li, F., Lan, C.Y., Zhou, W.H., and Huang, L.N., Culturable and molecular phylogenetic diversity of microorganisms in an open-dumped, extremely acidic Pb/Zn mine tailings, Extremophiles, 2008, vol. 12, pp. 657–664.

    Article  CAS  Google Scholar 

  23. Tsaplina, I.A., Zhuravleva, A.E., Bogdanova, T.I., Kondrat’eva, T.F., Krasil’nikova, E.N., Egorova, M.A., Zakharchuk, L.M., Suzina, N.E., Duda, V.I., and Stadnichuk, I.N., Phenotypic properties of Sulfobacillus thermotolerans: Comparative aspects, Microbiology (Moscow), 2008, vol. 77, pp. 654–664.

    Article  CAS  Google Scholar 

  24. Tsaplina, I.A., Zhuravleva, A.E., Egorova, M.A., Bogdanova, T.I., Krasil’nikova, E.N., Zakharchuk, L.M., and Kondrat’eva, T.F., Response to oxygen limitation in bacteria of the genus Sulfobacillus,Microbiology (Moscow), 2010, vol. 79, pp. 13–22.

    Article  CAS  Google Scholar 

  25. Vignais, P.M. and Billoud, B., Occurrence, classification, and biological function of hydrogenases: an overview, Chem. Rev., 2007, vol. 107, pp. 4206–4272.

    Article  CAS  Google Scholar 

  26. Zhang, X., Liu, X., Liang, Y., Guo, X., Xiao, Y., Ma, L., Miao, B., Liu, H., Peng, D., Huang, W., Zhang, Y., and Yin, H., Adaptive evolution of extreme acidophile Sulfobacillus thermosulfidooxidans potentially driven by horizontal gene transfer and gene loss, Appl. Environ. Microbiol., 2017, vol. 83, p. e03098-16. https://doi.org/10.1128/AEM.03098-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zhuravleva, A.E., Ismailov, A.D., and Tsaplina, I.A., Electron donors at oxidative phosphorylation in bacteria of the genus Sulfobacillus,Microbiology (Moscow), 2009, vol. 78, pp. 811–814.

    Article  CAS  Google Scholar 

  28. 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 

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This study was supported by the Ministry of Science and Higher Education of the Russian Federation.

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Correspondence to A. E. Panyushkina.

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The author declares no conflict of interest. This article does not contain any studies involving animals or human participants performed by the author.

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Panyushkina, A.E. Metabolic Potential of Sulfobacillus thermotolerans: Pathways for Assimilation of Nitrogen Compounds and the Possibility of Lithotrophic Growth in the Presence of Molecular Hydrogen. Microbiology 88, 759–763 (2019). https://doi.org/10.1134/S0026261719060134

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