Skip to main content
SpringerLink
Log in

Comparative analysis of the N-terminal sequence of Geobacter sulfurreducens AM-1 methacrylate reductase

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

Abstract

Comparative analyses of the amino acid sequence of the N-terminus of methacrylate reductase (50 kDa) from the anaerobic bacterium Geobacter sulfurreducens AM-1 revealed significant similarity to the sites of flavocytochromes c and flavin-containing proteins of anaerobic bacteria from the genera Anaero-myxobacter, Campylobacter, Desulfatibacillum, Desulfuromonas, Geobacter, Parasutterella, Shewanella, Sulfurospirillum, Sutterella, and Wolinella (belonging to four classes of the Proteobacteria), Denitrovibrio of the phylum Deferribacteres, Desulfitobacterium of the phylum Firmicutes, Eggerthella and Slackia of the phylum Actinobacteria, and Spirochaeta of the phylum Spirochaetes. High homology was also revealed between the methacrylate reductase amino acid sequence and the flavoproteins of aerobic bacteria Frankia and Gordonia from the phylum Actinobacteria and of the archaeon Haloterrigena turkmenica from the phylum Euryarchaeota. Among 11 Geobacter strains with known genomes, only G. lovleyi SZ capable of chlororespiration was found to contain an amino acid fragment of flavocytochrome c with pronounced similarity (80%) to the N-terminus of methacrylate reductase. The physiological properties common to these bacteria are discussed. Molecular masses and the hypothetical functions and localization of the homologous proteins are analyzed. The grouping of proteins according to the phylogenetic affiliation of their owners is discussed. Hypotheses concerning the distribution and evolutionary role of such proteins in microorganisms are suggested.

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. Caccavo, F.J.R., Lonergan, D.J., Lovley, D.R., Davis, M., Stolz, J.F., and McInerney, M.J., Geobacter sulfurreducens sp. nov., a Hydrogen- and Acetate-Oxidizing Dissimilatory Metal-Reducing Microorganism, Appl. Environ. Microbiol., 1994, vol. 60, no. 10, pp. 3752–3759.

    PubMed  CAS  Google Scholar 

  2. Nevin, K.P., Holmes, D.E., Woodard, T.L., Hinlein, E.S., Ostendorf, D.W., and Lovley, D.R., Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., Two Novel Fe(III)-Reducing Subsurface Isolates, Int. J. Syst. Evol. Microbiol., 2005, vol. 55, pp. 1667–1674.

    Article  PubMed  CAS  Google Scholar 

  3. Sung, Y., Fletcher, K.E., Ritalahti, K.M., Apkarian, R.P., Ramos-Hernández, N., Sanford, R.A., Mesbah, N.M., and Löffler, F.E., Geobacter lovleyi sp. nov. Strain SZ, a Novel Metal-Reducing and Tetrachloroethene-Dechlorinating Bacterium, Appl. Environ. Microbiol., 2006, vol. 72, no. 4, pp. 2775–2782.

    Article  PubMed  CAS  Google Scholar 

  4. Amos, B.K., Sung, Y., Fletcher, K.E., Gentry, T.J., Wu, W.-M., Criddle, C.S., Zhou, J., and Löffler, F.E., Detection and Quantification of Geobacter lovleyi Strain SZ: Implications for Bioremediation at Tetrachloroethene- and Uranium-Impacted Sites, Appl. Environ. Microbiol., 2007, vol. 73, no. 21, pp. 6898–6904.

    Article  PubMed  CAS  Google Scholar 

  5. Lovley, D.R., Powering Microbes with Electricity: Direct Electron Transfer from Electrodes to Microbes, Environ. Microbiol. Rep., 2010. doi: 10.1111/j.1758-2229.2010.00211.x

  6. Galushko, A.S., Obraztsova, A.Ya., Shtarkman, N.B., Laurinavichyus, K.S., and Akimenko, V.K., An Anaerobic Acetate-Oxidizing Bacterium Transforming Methacrylic Acid, DAN. Ser. Biol., 1994, vol. 335, no. 3, pp. 382–384.

    CAS  Google Scholar 

  7. Mikoulinskaia (Arkhipova), O.V., Akimenko, V.K., Galushko, A.S., Thauer, R.K., and Hedderich, R., Cytochrome c-Dependent Methacrylate Reductase from Geobacter sulfurreducens AM-1, Eur. J. Biochem., 1999, vol. 263, pp. 346–352.

    Article  PubMed  CAS  Google Scholar 

  8. Arkhipova, O.V. and Akimenko, V.K., Unsaturated Organic Acids as Terminal Electron Acceptors for Reductase Chains of Anaerobic Bacteria, Microbiology, 2005, vol. 74, no. 6, pp. 629–639.

    Article  CAS  Google Scholar 

  9. Arkhipova, O.V., Chuvochina, M.S., and Trutko, S.M., Cytochromes c of the Anaerobic Methacrylate Reducer Geobacter sulfurreducens AM-1, Microbiology, 2009, vol. 78, no. 3, pp. 296–303.

    Article  CAS  Google Scholar 

  10. Gross, R., Simon, J., and Kröger, A., Periplasmatic Methacrylate Reductase Activity in Wolinella succinogenes, Arch. Microbiol., 2001, vol. 176, pp. 310–313.

    Article  CAS  Google Scholar 

  11. Methé, 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., Durkon, A.S., Gwinn, M., Kolonay, J.F., Sullivan, S.A., Haft, D.H., Selengut, J., Davidsen, T.M., Zafar, N., White, O., Tran, B., Romero, C., Forberger, H.A., Weidman, J., Khouri, H., Feldblyum, T.V., Utterback, T.R., Van Aken, S.E., Lovley, D.R., and Frazer, C.M., Genome of Geobacter sulfurreducens: Metal Reduction in Subsurface Environments, Science, 2003, vol. 302, pp. 1967–1969.

    Article  PubMed  Google Scholar 

  12. Aklujkar, M., Young, N.D., Holmes, D., Chavan, M., Risso, C., Kiss, H.E., Han, C.S., Land, M.L., and Lovley, D.R., The Genome of Geobacter bemidjiensis, Exemplar for the Subsurface Clade of Geobacter Species That Predominate in Fe(III)-Reducing Subsurface Environments, BMC Genomics, 2010. 11:490. doi: 10.1186/1471-2164-11-490

    Article  PubMed  Google Scholar 

  13. Nagarajan, H., Butler, J.E., Klimes, A., Qiu, Y., Zengler, K., Ward, J., Young, N.D., Methé, B.A., Palsson, B.., Lovley, D.R., and Barrett, C.L., De novo Assembly of the Complete Genome of an Enhanced Electricity-Producing Variant of Geobacter sulfurreducens Using only Short Reads, PLoS ONE, 2010, vol. 5, no. 6. e10922. doi: 10.1371/journal.pone.0010922

    Article  PubMed  Google Scholar 

  14. Aklujkar, M., Krushkal, J., DiBartolo, G., Lapidus, A., Land, M.L., and Lovley, D.R., The Genome Sequence of Geobacter metallireducens: Features of Metabolism, Physiology and Regulation Common and Dissimilar to Geobacter Sulfurreducens, BMC Microbiol., 2009. 9:109. doi: 10:1186/1471-2180-9-109

    Article  PubMed  Google Scholar 

  15. Butler, J.E., Young, N.D., and Lovley, D.R., Evolution from a Respiratory Ancestor to Fill Syntrophic and Fermentative Niches: Comparative Genomics of Six Geobacteraceae Species, BMC Genomics, 2009. 10:103 doi: 10.1186/1471-2164-10-103

    Article  PubMed  Google Scholar 

  16. 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 Acid Res., 1997, vol. 25, no. 17, pp. 3389–3402.

    Article  PubMed  CAS  Google Scholar 

  17. 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, Bioinformatics, 2010, vol. 26, no. 22, pp. 2811–2817. doi: 10.1093/bioinformatics/btq530

    Article  PubMed  CAS  Google Scholar 

  18. Tamura, K., Dudley, J., Nei, M., and Kumar, S., MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0, Mol. Biol. Evol., 2007, vol. 24, pp. 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  19. Wexler, H.M., Reeves, D., Summanen, P.H., Molitoris, E., McTeague, M., Duncan, J., Wilson, K.H., and Finegold, S.M., Sutterella wadsworthensis gen. nov., sp. nov., Bile-Resistant Microaerophilic Campylobacter gracilis-Like Clinical Isolates, Int. J. Syst. Bacteriol., 1996, vol. 46, no. 1, pp. 252–258.

    Article  PubMed  CAS  Google Scholar 

  20. Sim, W.H., Wagner, J., Cameron, D.J., Catto-Smith, A.G., Bishop, R.F., and Kirkwood, C.D., Novel Burkholderiales 23S rRNA Genes Identified in Ileal Biopsy Samples from Children: Preliminary Evidence that a Subtype Is Associated with Perianal Crohn’s Disease, J. Clin. Microbiol., 2010, vol. 48, no. 5, pp. 1939–1942.

    Article  PubMed  CAS  Google Scholar 

  21. Saunders, E., Pukall, R., Abt, B., Lapidus, A., Glavina, DelRioT., Copeland, A., Tice, H., Cheng, J.-F., Lucas, S., Chen, F., Nolan, M., Bruce, D., Goodwin, L., Pitluck, S., Ivanova, N., Mavromatis, K., Ovchinnikova, G., Pati, A., Chen, A., Palaniappan, K., Land, M., Hauser, L., Chang, Y.-J., Jeffries, C.D., Chain, P., Meincke, L., Sims, D., Brettin, T., Detter, J.C., Göker, M., Bristow, J., Eisen, J.A., Markowitz, V., Hugenholtz, P., Kyrpides, N.C., Klenk, H.-P., and Han, C., Complete Genome Sequence of Eggerthella lenta Type Strain (VPI 0255T), Standard. Genomic Sci., 2009, vol. 1, pp. 174–182.

    Article  Google Scholar 

  22. Wampler, D.A. and Ensign, S.A., Photoheterotrophic Metabolism of Acrylamide by a Newly Isolated Strain of Rhodopseudomonas palustris, Appl. Environ. Microbiol., 2005, vol. 71, no. 10, pp. 5850–5857.

    Article  PubMed  CAS  Google Scholar 

  23. Alves, A.S., Paquete, C.M., Fonseca, B.M., and Louro, R.O., Exploration of the’ Cytochromome’ of Desulfuromonas acetoxidans, a Marine Bacterium Capable of Powering Microbial Fuel Cells, Metallomics, 2011, vol. 3, no. 4, pp. 349–353.

    Article  PubMed  CAS  Google Scholar 

  24. Schumacher, W., Kroneck, P.M.H., and Pfennig, N., Comparative Systematic Study on “Spirillum” 5175, Campylobacter and Wolinella Species. Description of “Spirillum” 5175 as Sulfurospirillum deleyianum gen. nov., spec. nov., Arch. Microbiol., 1992, vol. 158, pp. 287–293.

    Article  CAS  Google Scholar 

  25. Mavromatis, K., Yasawong, M., Chertkov, O., Lapidus, A., Lucas, S., Nolan, M., Glavina Del Rio, T., Tice, H., Cheng, J.-F., Pitluck, S., Liolios, K., Ivanova, N., Tapia, R., Han, C., Bruce, D., Goodwin, L., Pati, A., Chen, A., Palaniappan, K., Land, M., Hauser, L., Chang, Y.-J., Jeffries, C.D., Detter, J.C., Rohde, M., Brambilla, E., Spring, S., Göker, M., Sikorski, J., Woyke, T., Bristow, J., Eisen, J.A., Markowitz, V., Hugenholtz, P., Klenk, H.-P., and Kyrpides, N.C., Complete Genome Sequence of Spirochaeta smaragdinae Type Strain (SEBR 4228T), Standard. Genomic Sci., 2010, vol. 3, pp. 136–144.

    Google Scholar 

  26. 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, no. 2, pp. 893–900.

    Article  PubMed  CAS  Google Scholar 

  27. Nonaka, H., Keresztes, G., Shinoda, Y., Ikenaga, Y., Abe, M., Naito, K., Inatomi, K., Furukawa, K., Inui, M., and Yukawa, H., Complete Genome Sequence of the Dehalorespiring Bacterium Desulfitobacterium hafniense Y51 and Comparison with Dehalococcoides ethenogenes 195, J. Bacteriol., 2006, vol. 188, no. 6, pp. 2262–2274.

    Article  PubMed  CAS  Google Scholar 

  28. 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., Ivanova, N., Mavromatis, K., Chen, A., Palaniappan, K., Land, M., Hauser, L., Chang, Y.-J., Jeffries, C.D., Detter, J.C., Brettin, T., Spring, S., Rohde, M., Göker, M., Woyke, T., Bristow, J., Eisen, J.A., Markowitz, V., Hugenholtz, P., Kyrpides, N.C., and Klenk, H.-P., Complete Genome Sequence of Denitrovibrio acetiphilus Type Strain (N2460T), Standard. Genomic Sci., 2010, vol. 2, pp. 270–279.

    Article  Google Scholar 

  29. Miller, T.R., Franklin, M.P., and Halden, R.U., Bacterial Community Analysis of Shallow Groundwater Undergoing Sequential Anaerobic and Aerobic Chloroethene Biotransformation, FEMS Microbiol. Ecol., 2007, vol. 60, pp. 299–311.

    Article  PubMed  CAS  Google Scholar 

  30. Straub, K.L. and Schink, B., Ferrihydrite-Dependent Growth of Sulfurospirillum deleyianum through Electron Transfer via Sulfur Cycling, Appl. Environ. Microbiol., 2004, vol. 70, no. 10, pp. 5744–5749.

    Article  PubMed  CAS  Google Scholar 

  31. Zhao, J.-S., Deng, Y., Manno, D., and Hawari, J., Shewanella spp. Genomic Evolution for a Cold Marine Lifestyle and in-situ Explosive Biodegradation, PLoS ONE, 2010, vol. 5, no. 2: e9109. doi: 10.1371/journal.pone.0009109

    Article  PubMed  Google Scholar 

  32. 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. doi: 10.1371/journal.pone.0002103

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, pr. Nauki 5, Pushchino, Moscow oblast, Russia

    O. V. Arkhipova

  2. Branch of Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Pushchino, 142290, Russia

    G. V. Mikulinskaya

  3. University of Vienna, Vienna, Austria

    A. S. Galushko

Authors
  1. O. V. Arkhipova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. V. Mikulinskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. S. Galushko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. V. Arkhipova.

Additional information

Original Russian Text © O.V. Arkhipova, G.V. Mikulinskaya, A.S. Galushko, 2012, published in Mikrobiologiya, 2012, Vol. 81, No. 5, pp. 600–610.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arkhipova, O.V., Mikulinskaya, G.V. & Galushko, A.S. Comparative analysis of the N-terminal sequence of Geobacter sulfurreducens AM-1 methacrylate reductase. Microbiology 81, 555–564 (2012). https://doi.org/10.1134/S0026261712050049

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261712050049

Keywords

Search

Navigation