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Methacrylate-Reducing Activity of Anaerobic Bacteria Anaeromyxobacter dehalogenans and Denitrovibrio acetiphilus

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Abstract

Periplasmic methacrylate-reducing activity was shown for anaerobic acetate-oxidizing gram-negative bacteria Anaeromyxobacter dehalogenans 2CP-1Т (class Deltaproteobacteria) and Denitrovibrio acetiphilus DSM 12809Т (class Deferribacteres), both possessing homologous genes for methacrylate redox system components. No acrylate reductase activity was revealed in these bacteria. A. dehalogenans and D. acetiphilus were also found to reduce fumarate, exhibiting periplasmic and intracellular fumarate reductase activity, respectively. D. acetiphilus was found to possess nitrate reductase activity of periplasmic and intracellular localization. The possible correspondence between reductase activities and the hypothetical proteins genes in the known genomes of A. dehalogenans and D. acetiphilus are discussed.

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REFERENCES

  1. Arkhipova, O.V. and Akimenko V.K., Unsaturated organic acids as terminal electron acceptors for reductase chains of anaerobic bacteria, Microbiology (Moscow), 2005, vol. 74, pp. 629–639.

    Article  CAS  Google Scholar 

  2. Arkhipova, O.V., Troshina, O.Yu., and Mikulinskaya, G.V., Spatial model of the anaerobic methylacrylate reductase system, Vestn. TvGU, Ser. Biol. Ekol., 2017, no. 2, pp. 306‒323.

  3. Arkhipova, O.V., Chuvochina, M.S., and Trutko, S.M., Cytochromes c of the anaerobic methacrylate reducer Geobacter sulfurreducens AM-1, Microbiology (Moscow), 2009, vol. 78, pp. 296–303.

    Article  CAS  Google Scholar 

  4. Arkhipova, O.V., Meer, M., Mikoulinskaia, G.V., Zakharova, M.V., Galushko, A.S., Akimenko, V.K., and Kondrashov, F.A., Recent origin of the methacrylate redox system in Geobacter sulfurreducens AM-1 through horizontal gene transfer, PLoS One, 2015, vol. 10, no. 5. e0125888. https://doi.org/10.1371/journal.pone.0125888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bagos, P.G., Nikolaou, E.P., Liakopoulos, T.D., and Tsirigos, K.D., Combined prediction of Tat and Sec signal peptides with hidden Markov models, Bioinform., 2010, vol. 26, pp. 2811‒2817. https://doi.org/10.1093/bioinformatics/btq530

    Article  CAS  Google Scholar 

  6. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.

    Article  CAS  Google Scholar 

  7. Craske, A. and Ferguson S.J., The respiratory nitrate reductase from Paracoccus denitrificans. Molecular characterisation and kinetic properties, Eur. J. Biochem., 1986, vol. 158, pp. 429‒436.

    Article  CAS  PubMed  Google Scholar 

  8. Curson, A.R.J., Burns, O.J., Voget, S., Daniel, R., Todd, J.D., McInnis, K., Wexler, M., and Johnston, A.W.B., Screening of metagenomic and genomic libraries reveals three classes of bacterial enzymes that overcome the toxicity of acrylate, PLoS One, 2014, vol. 9, no. 5. e97660. doi 10.1371

  9. Denton, K., Atkinson, M.M., Borenstein, S.P., Carlson, A., Carroll, T., Cullity, K., DeMarsico, C., Ello-witz, D., Gialtouridis, A., Gore, R., Herleikson, A., Ling, A.Y., Martin, R., McMahan, K., Naksukpaiboon, P., et al., Identification of a possible respiratory arsenate reductase in Denitrovibrio acetiphilus, a member of the phylum Deferribacteres, Arch. Microbiol., 2013, vol. 195, pp. 661–670. https://doi.org/10.1007/s00203-013-0915-5

    Article  CAS  PubMed  Google Scholar 

  10. Galushko, A.S., Mikulinskaya, O.V., Laurinavichus, K.S., Obraztsova, A.Ya., and Akimenko, V.K., Periplasmic location of methacrylate reductase in cells of the strictly anaerobic bacterial strain AM-1, Microbiology (Moscow), 1996, vol. 65, pp. 432‒435.

    Google Scholar 

  11. Galushko, A.S., Obraztsova, A.Ya., Shtarkman, N.B., Laurinavichus, K.S., and Akimenko, V.K., An anaerobic acetate-oxidizing bacterium capable of transforming methacrylic acid, Dokl. Biol. Sci., 1994, vol. 335, pp. 122‒123.

    Google Scholar 

  12. Gross, R., Simon, J., and Kröger, A., Periplasmatic methacrylate reductase activity in Wolinella succinogenes, Arch. Microbiol., 2001, vol. 176, pp. 310–313.

    Article  CAS  PubMed  Google Scholar 

  13. Helenius, A. and Simons, K., Solubilization of membranes by detergents, Biochem. Biophys. Acta, 1975, vol. 415, pp. 29‒79.

    CAS  PubMed  Google Scholar 

  14. Kiss, H., Lang, E., Lapidus, A., Copeland, A., Nolan, M., Del Rio, T.G., Chen, F., Lucas, S., Tice, H., Cheng, J.-F., Han, C., Goodwin, L., Pitluck, S., Liolios, K., Pati, A., et al., Complete genome sequence of Denitrovibrio acetiphilus type strain (N2460T), Stand. Genomic Sci., 2010, vol. 2, pp. 270‒279. https://doi.org/10.4056/sigs.892105

    Article  PubMed  PubMed Central  Google Scholar 

  15. Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 1970, vol. 227, pp. 680–685.

    Article  CAS  PubMed  Google Scholar 

  16. Logan, B., Exoelectrogenic bacteria that power microbial fuel cells, Nature Rev. Microbiol., 2009, vol. 7, pp. 375–383. doi 10.1038/nrmicrо2113

  17. Lovley, D.R., Powering microbes with electricity: direct electron transfer from electrodes to microbes, Env. Microbiol. Rep., 2010. https://doi.org/10.1111/j.1758-2229.2010.00211.x

  18. Methe, B.A., Nelson, K.E., Eisen, J.A., Paulsen, I.T., Nelson, W., Heidelberg, J.F., Wu, D., Wu, M., Ward, N., Beanan, M.J., Dodson, R.J., Madupu, R., Brinkac, L.M., Daugherty, S.C., DeBoy, R.T., et al., Genome of Geobacter sulfurreducens: metal reduction in subsurface environments, Science, 2003, vol. 302, pp. 1967–1969.

    Article  CAS  PubMed  Google Scholar 

  19. Mikoulinskaia (Arkhipova), O., Akimenko, V., Galushko, A., Thauer, R., and Hedderich, R., Cytochrome c-dependent methacrylate reductase from Geobacter sulfurreducens AM-1, Eur. J. Biochem., 1999, vol. 263, pp. 346‒352.

  20. Myhr, S. and Torsvik, T., Denitrovibrio acetiphilus, a novel genus and species of dissimilatory nitrate-reducing bacterium isolated from an oil reservoir model column, Int. J. Syst. Evol. Microbiol., 2000, vol. 50, pp. 1611–1619.

    Article  CAS  PubMed  Google Scholar 

  21. Nissen, S., Liu, X., Chourey, K., Hettich, R.L., Wagner, D.D., Pfiffner, S.M., and Loffler, F.E., Comparative c-type cytochrome expressionanalysis in Shewanella oneidensis strain MR-1 and Anaeromyxobacter dehalogenans strain 2CP-C grown with soluble and insoluble oxidized metal electron acceptors, Biochem. Soc. Trans., 2012, vol. 40, pp. 1204‒2010.

    Article  CAS  PubMed  Google Scholar 

  22. Sanford, R.A., Cole, J.R., and Tiedje, J.M., Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium, Appl. Environ. Microbiol., 2002, vol. 68, pp. 893–900.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Sanford, R.A., Wu, Q., Sung, Y., Thomas, S.H., Amos, B.K., Prince, E.K., and Löffler, F.E., Hexavalent uranium supports growth of Anaeromyxobacter dehalogenans and Geobacter spp. with lower than predicted biomass yields, Environ. Microbiol., 2007, vol. 9, pp. 2885–2893.

    Article  CAS  PubMed  Google Scholar 

  24. Seitz, H.-J. and Cypionka, H., Chemolithotrophic growth of Desulfovibrio desulfuricans with hydrogen coupled to ammoniofication of nitrate or nitrite, Arch. Microbiol., 1986, vol. 146, pp. 63‒67.

    Article  CAS  Google Scholar 

  25. Shi, L., Fredrickson, J.K., and Zachara, J.M., Genomic analyses of bacterial porin-cytochrome gene clusters, Front Microbiol., 2014, vol. 5, article 657. https://doi.org/10.3389/fmicb.2014.00657

    Article  PubMed  PubMed Central  Google Scholar 

  26. Strycharz, S.M., Gannon, S.M., Boles, A.R., Franks, A.E., Nevin, K.P., and Lovley, D.R., Reductive dechlorination of 2-chlorophenol by Anaeromyxobacter dehalogenans with an electrode serving as the electron donor, Environ. Microbiol. Rep., 2010, vol. 2, pp. 289–294. doi 10.1111/j.1758-2229.2009.00118.x

  27. Szewzyk, R. and Pfennig, N., Complete oxidation of catechol by the strictly anaerobic sulfate-reducing Desulfobacterium catecholicum sp. nov., Arch. Microbiol., 1987, vol. 147, pp. 163‒168.

    Article  CAS  Google Scholar 

  28. Thomas, S.H., Wagner, R.D., Arakaki, A.K., Skolnick, J., Kirby, J.R., Shimkets, L.J., Sanford, R.A., and Löffler, F.E., The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-Proteobacteria, PLoS One, 2008, vol. 3, no. 5. e2103. https://doi.org/https://doi.org/10.1371/journal.pone.0002103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Van der Westen, H.M., Mayhew, S.G., and Veeger, C., Separation of hydrogenase from intact cells of Desulfovibrio vulgaris, FEBS Lett., 1978, vol. 86, pp. 122–126.

  30. Zeikus, J.G., Fuchs, G., Kenealy, W., and Thauer, R.K., Oxidoreductases involved in cell carbon synthesis of Methanobacterium thermoautotrophicum, J. Bacteriol., 1977, vol. 132, pp. 604‒613.

    CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

This work was supported by the Russian Foundation for Basic Research, project no. 17-04-01068 “The Anaerobic Enzyme System, Reducing Methacrylate.” We are grateful to Prof. F.A. Kondrashov (Institute of Science and Technology, Austria) for his help in the acquisition of cultures from DSMZ.

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Correspondence to O. V. Arkhipova.

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The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Translated by E. Babchenko

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Arkhipova, O.V., Biryukova, E.N., Abashina, T.N. et al. Methacrylate-Reducing Activity of Anaerobic Bacteria Anaeromyxobacter dehalogenans and Denitrovibrio acetiphilus. Microbiology 88, 137–145 (2019). https://doi.org/10.1134/S0026261719020024

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