The membrane qmoABC complex interacts directly with the dissimilatory adenosine 5′-phosphosulfate reductase in sulfate reducing bacteria

Frontiers in Microbiology

Volumn 3, Issue APR, 2012, Pages

  Ramos, Ana Raquel ^a   Keller, Kimberly L ^b,c   Wall, Judy D ^b,c   Cardoso Pereira, Inês A ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b University of Missouri   (United States)

^c Ecosystems and Networks Integrated with Genes and Molecular Assemblies   (United States)

Author keywords

Electron bifurcation; Membrane complex; Protein protein interactions; Sulfate reducing bacteria; Sulfur oxidizing bacteria; Surface plasmon resonance

Indexed keywords

EID: 84871719363     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00137     Document Type: Article

References (45)

1. Barton, L. L., and Fauque, G. D. (2009). Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv. Appl. Microbiol. 68, 41-98.
2. Bashir, Q., Scanu, S., and Ubbink, M. (2011). Dynamics in electron transfer protein complexes. FEES J. 278, 1391-1400.
3. Chan, L. K., Weber, T. S., Morgan-Kiss, R. M., and Hanson, T. E. (2008). A genomic region required for pho-totrophic thiosulfate oxidation in the green sulfur bacterium Chloro-bium tepidum (syn. Chlorobacu-lutn tepidum). Microbiology 154, 818-829.
4. Chen, L., Le Gall, J., and Xavier, A. V. (1994). Purification, characterization and properties of an NADH oxidase from Desulfovibrio vulgaris (Hildenborough) and its coupling to adenylyl phosphosulfate reductase. Biochem. Biophys. Res. Commun. 203, 839-844.
5. Chhabra, S. R., Butland, G., Elias, D. A., Chandonia, J. M., Fok, O. Y., Juba, T. R., Gorur, A., Allen, S., Leung, C. M., Keller, K. L, Reveco, S., Zane, G. M., Semkiw, E., Prathapam, R., Gold, B., Singer, M., Ouellet, M., Szakal, E. D., Jorgens, D., Price, M. N., Witkowska, H. E., Beller, H. R., Arkin, A. P., Hazen, T. C, Biggin, M. D., Auer, M., Wall, J. D., and Keasling, J. D. (2011a). Generalized schemes for high-throughput manipulation of the Desulfovibrio vulgaris genome. Appl. Environ. Microbiol. 77, 7595-7604.
6. Chhabra, S. R., Joachimiak, M. P., Pet-zold, C. J., Zane, G. M., Price, M. N., Reveco, S. A., Fok, V., Johanson, A. R., Batth, T. S., Singer, M., Chandonia, J. M., Joyner, D., Hazen, T. C, Arkin, A. P., Wall, J. D., Singh,A. K., and Keasling, J. D. (2011b). Towards a rigorous network of protein-protein interactions of the model sulfate reducer Desulfovibrio vulgaris Hildenborough. PLoS ONE 6, e21470. doi:10.1371/jour-nal.pone.0021470
7. Costa, K. C, Wong, P. M., Wang, T., Lie, T. J., Dodsworth, J. A., Swanson, L, Burn, J. A., Hackett, M., and Leigh, J.A. (2010). Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase. Proc. Natl. Acad. Sci. U.S.A. 107, 11050-11055.
8. Frigaard, N. U., and Dahl, C. (2009). Sulfur metabolism in phototrophic sulfur bacteria. Adv. Microb. Physiol. 54, 103-200.
9. Fritz, G., Biichert, T., Huber, H., Stet-ter, K. O., and Kroneck, P. M. H. (2000). Adenylylsulfate reductases from archaea and bacteria are1:1 αβ-heterodimeric iron-sulfur flavoenzymes-high similarity of molecular properties emphasizes their central role in sulfur metabolism. FEBS Lett. 473, 63-66.
10. Fritz, G., Biichert, T., and Kroneck, P. M. H. (2002a). The function of the [4Fe-4S] clusters and FAD in bacterial and archaeal adenylylsulfate reductases. Evidence for flavin-catalyzed reduction of adenosine 5;-phosphosulfate. J. Biol. Chem. 277, 26066-26073.
11. Fritz, G., Roth, A., Schiffer, A., Buchert, T., Bourenkov, G., Bartunik, H. D., Huber, H., Stetter, K. O., Kroneck, P. M., and Ermler, U. (2002b). Structure of adenylylsulfate reductase from the hyperthermophilic Archaeoglobus fulgidus at 1.6-A resolution. Proc. Natl. Acad. Sci. U.S.A. 99, 1836-1841.
12. Gregersen, L. H., Bryant, D. A., and Frigaard, N. U. (2011). Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front. Mkrobiol. 2:116. doi:10.3389/fmicb.2011.00116
13. Haveman, S. A., Greene, E. A., Stil-well, C. P., Voordouw, J. K., and Voordouw, G. (2004). Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris Hildenborough by nitrite. J. Bacte-riol. 186,7944-7950.
14. Herrmann, G., Jayamani, E., Mai, G., and Buckel, W. (2008). Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J. Bacterial 190,784-791.
15. Hipp, W. M., Pott, A. S., Thum-Schmitz, N., Faath, I., Dahl, C, and Truper, H. G. (1997). Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokary-otes. Microbiology 143(Pt 9), 2891-2902.
16. Junier, P., Junier, T., Podell, S., Sims, D. R., Detter, J. C, Lykidis, A., Han, C. S., Wigginton, N. S., Gaasterland, T., and Bernier-Latmani, R. (2010). The genome of the Gram-positive metal-and sulfate-reducing bacterium Desulfototnaculutn reducens strain MI-1. Environ. Microbiol. 12, 2738-2754.
17. Raster, A. K., Moll, J., Parey, K., and Thauer, R. K. (2011). Coupling of ferredoxin and heterodisulflde reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. Proc. Natl. Acad. Sci. U.S.A. 108,2981-2986.
18. Keller, K. L, and Wall, J. D. (2011). Genetics and molecular biology of the electron flow for sulfate respiration in Desulfovibrio. Front. Microbiol. 2:135. doi:10.3389/fmicb.2011.00135
19. Keller, K. L, Wall, J. D., and Chhabra, S. (2011). Methods for engineering sulfate reducing bacteria of the genus Desulfovibrio. Meth. Enzymol. 497, 503-517.
20. Lampreia, J., Pereira, A. S., and Moura, J. J. G. (1994). Adenylylsulfate reductases from sulfate-reducing bacteria. Meth. Enzymol. 243, 241-260.
21. Li, M., and Elledge, S. J. (2007). Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat. Methods 4, 251-256.
22. Liu, M. C, and Peck, H. D. Jr. (1981). The isolation of hexa-heme cytochrome from Desulfovibrio desulfuricans and its identification as a new type of nitrite reductase. J. Biol. Chem. 256, 13159-13164.
23. Mander, G. J., Duin, E. C, Linder, D., Stetter, K. O., and Hedderich, R. (2002). Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisul-fide reductase from methanogenic archaea. Eur. J. Biochem. 269, 1895-1904.
24. Martinez-Fabregas, J., Rubio, S., Diaz-Quintana, A., Diaz-Moreno, I., and De la Rosa, M. A. (2011). Pro-teomic tools for the analysis of transient interactions between metallo-proteins. FEBS J. 278,1401-1410.
25. Meyer, B., and Kuever, J. (2007a). Phylogeny of the alpha and beta sub-units of the dissimilatory adenosine-5;-phosphosulfate (APS) reductase from sulfate-reducing prokaryotes-origin and evolution of the dis-similatory sulfate-reduction pathway. Microbiology 153, 2026-2044.
26. Meyer, B., and Kuever, J. (2007b). Molecular analysis of the distribution and phylogeny of dissimi-latory adenosine-5;-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes. Microbiology 153, 3478-3498.
27. Meyer, B., and Kuever, J. (2008).Homol-ogy modeling of dissimilatory APS reductases (AprBA) of sulfur-oxidizing and sulfate-reducing prokaryotes. PLoS ONE 3, el514. doi:10.1371/journal.pone.0001514
28. Miiller, N., Worm, P., Schink, B., Stams, A. J. M., and Plugge, C. M. (2010) Syntrophic butyrate and propionate oxidation processes: from genomes to reaction mechanisms. Environ. Microbiol. Rep. 2,489-499.
29. Muyzer, G., and Stams, A. J. M. (2008). The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 6, 441-454.
30. Nitschke, W, and Russell, M. J. (2011) Redox bifurcations: mechanisms and importance to life now, and at its origin: a widespread means of energy conversion in biology unfolds. Bioessays 34, 106-109.
31. Pereira, I. A. C. (2008). "Membrane complexes in Desulfovibrio"in Microbial Sulfur Metabolism, eds C. Friedrich and C. Dahl (Berlin: Springer-Verlag), 24-35.
32. Pereira, I. A. C, Ramos, A. R., Grein, E, Marques, M. C, da Silva, S. M., and Vesceslau, S. S. (2011). A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea. Front. Microbiol. 2:69. doi:10.3389/fmicb.2011. 00069
33. Pires, R. H., Lourenco, A. I., Morais, E, Teixeira, M., Xavier, A. V., Saraiva, L. M., and Pereira, LA. (2003). A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim. Biophys. Acta 1605,67-82.
34. Plugge, C. M., Zhang, W., Scholten, J. C,and Stams, A. J. (2011). Meta bolic flexibility of sulfate-reducing bacteria. Front. Microbiol. 2:81. 10.3389/fmicb.2011.00081
35. Rodriguez, J., Hiras, J., and Hanson, T. E. (2011). Sulfite oxidation in Chlorobaculum tepidum. Front. Microbiol. 2:112. doi:10.3389/fmicb.2011.00112
36. Rothery, R. A., Workun, G. J., and Weiner, J. H. (2008). The prokary-otic complex iron-sulfur molyb-doenzyme family. Biochim. Biophys. Acta 1778, 1897-1929.
37. Sato, Y., Kameya, M., Arai, H., Ishii, M., and Igarashi, Y. (2011). Detecting weak protein-protein interactions by modified far-western blotting. J. Biosci. Bioeng. 112, 304-307.
38. Schut, G. J., and Adams, M. W (2009) The iron-hydrogenase of Thermo-toga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J. Bacteriol. 191, 4451-4457.
39. Sieber, J. R., Sims, D. R., Han, C, Kim, E., Lykidis, A., Lapidus, A. L., McDonnald, E., Rohlin, L, Culley, D.E., Gunsalus, R., and Mclner-ney, M. J. (2010) The genome of Syntrophomonas wolfei: new insights into syntrophic metabolism and biohydrogen production, Environ. Microbiol. 12,2289-2301.
40. Simon, J., van Spanning, R. J., and Richardson, D. J. (2008). The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. Biochim. Biophys. Acta 1777, 1480-1490
41. Stams, A. J., and Plugge, C. M. (2009). Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7, 568-577.
42. Stojanowic, A., Mander, G. J., Duin, E. C, and Hedderich, R. (2003). Physiological role of the F-420-non-reducing hydrogenase (Mvh) from Methanothermobacter marburgensis. Arch. Microbiol. 180, 194-203.
43. Thauer, R. K., Raster, A. K., See-dorf, H., Buckel, W, and Hedderich, R. (2008). Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6, 579-591.
44. + reduction with NADH are coupled via an electron-bifurcating enzyme complex in Clostridium kluyveri.J. Bacteriol. 192,5115-5123.
45. Zane, G. M., Yen, H. C, and Wall, J. D. (2010). Effect of the deletion of qmoABC and the promoter-distal gene encoding a hypothetical protein on sulfate reduction in Desulfovibrio vulgaris Hildenborough. Appl. Environ. Microbiol. 76, 5500-5509.