Functional analysis of three sulfide:Quinone oxidoreductase homologs in Chlorobaculum tepidum

Journal of Bacteriology

Volumn 191, Issue 3, 2009, Pages 1026-1034

  Chan, Leong Keat ^a   Morgan Kiss, Rachael M ^a,b   Hanson, Thomas E ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b MIAMI UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HISTIDINE; OXIDOREDUCTASE; SULFIDE; SULFIDE QUNINONE OXIDOREDUCTASE; UBIQUINONE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SULFIDE QUINONE REDUCTASE;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHLOROBACULUM TEPIDUM; CHLOROBIUM; CONTROLLED STUDY; ENZYME ACTIVITY; GENE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY; CHLOROBI; ENZYMOLOGY; GENETICS; IMMUNOBLOTTING; METABOLISM; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS); CHLOROBACULUM TEPIDUM;

BACTERIAL PROTEINS; CHLOROBI; ELECTROPHORESIS, POLYACRYLAMIDE GEL; IMMUNOBLOTTING; MUTATION; QUINONE REDUCTASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SULFIDES;

EID: 63449095472     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01154-08     Document Type: Article

References (60)

1. Arieli, B., Y. Shahak, D. Taglicht, G. Hauska, and E. Padan. 1994. Purification and characterization of sulfide-quinone reductase, a novel enzyme driving anoxygenic photosynthesis in Oscillatoria limnetica. J. Biol. Chem. 269:5705-5711.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. Green Publishing Associates and Wiley Interscience, New York, NY.
3. Bardischewsky, F., A. Quentmeier, and C. G. Friedrich. 2006. The flavoprotein SoxF functions in chemotrophic thiosulfate oxidation of Paracoccus pantotrophus in vivo and in vitro. FEMS Microbiol. Lett. 258:121-126.
4. Bronstein, M., M. Schutz, G. Hauska, E. Padan, and Y. Shahak. 2000. Cyanobacterial sulfide-quinone reductase: cloning and heterologous expression. J. Bacteriol. 182:3336-3344.
5. Cai, Y., and C. P. Wolk. Use of a conditionally lethal gene in anabaena sp. strain Pcc 7120 to select for double recombinants and to entrap insertion sequences. J. Bacteriol. 172:3138-3145.
6. Chan, L.-K., R. Morgan-Kiss, and T. E. Hanson. 2008. Genetic and proteomic studies of sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum), p. 357-373. In R. Hell, C. Dahl, D. Knaff, and T. Leustek (ed.), Sulfur metabolism in phototrophic organisms. Springer, New York, NY.
7. Chan, L.-K., R. Morgan-Kiss, and T. E. Hanson. 2008. Sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum): genetic and proteomic analyses, p. 117-126. In C. Dahl and C. G. Friedrich (ed.), Microbial sulfur metabolism. Springer, Berlin, Germany.
8. Chan, L.K., T. S. Weber, R. M. Morgan-Kiss, and T. E. Hanson. 2008. A genomic region required for phototrophic thiosulfate oxidation in the green sulfur bacterium Chlorobium tepidum (syn. Chlorobaculum tepidum). Microbiology 154:818-829.
9. Chen, Z. W., M. Koh, G. Van Driessche, J. J. Van Beeumen, R. G. Bartsch, T. E. Meyer, M. A. Cusanovich, and F. S. Mathews. 1994. The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science 266:430-432.
10. Dahl, C. 2008. Inorganic sulfur compounds as electron donors in purple sulfur bacteria, p. 289-317. In R. Hell, C. Dahl, D. Knaff, and T. Leustek (ed.). Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, The Netherlands.
11. Dahl, C., S. Engels, A. S. Pott-Sperling, A. Schulte, J. Sander, Y. Lubbe, O. Deuster, and D. C. Brune. 2005. Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J. Bacteriol. 187: 1392-1404.
12. Dahl, C., G. Rákhely, A. S. Pott-Sperling, B. Fodor, M. Takács, A. Tóth, M. Kraeling, K. Gyorfi, Á. Kovács, J. Tusz, and K. L. Kovács. 1999. Genes involved in hydrogen and sulfur metabolism in phototrophic sulfur bacteria. FEMS Microbiol. Lett. 180:317-324.
13. Dennis, J. J., and G. J. Zylstra. 1998. Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl. Environ. Microbiol. 64:2710-2715.
14. Friedrich, C. G., F. Bardischewsky, D. Rother, A. Quentmeier, and J. Fischer. 2005. Prokaryotic sulfur oxidation. Curr. Opin. Microbiol. 8:253-259.
15. Friedrich, C. G., D. Rother, F. Bardischewsky, A. Quentmeier, and J. Fischer. 2001. Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl. Environ. Microbiol. 67:2873-2882.
16. Frigaard, N., and D. Bryant. 2008. Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria, p. 337-355. In R. Hell, C. Dahl, D. Knaff. and T. Leustek (ed.), Sulfur metabolism in phototrophic organisms. Springer, New York, NY.
17. Frigaard, N.-U., and D. A. Bryant. 2008. Genomic and evolutionary perspectives on sulfur metabolism in green sulfur bacteria, p. 60-76. In C. Dahl and C. G. Friedrich (ed.), Microbial sulfur metabolism. Springer. New York. NY.
18. Frigaard, N.-U., S. Takaichi, M. Hirota, K. Shimada, and K. Matsuura. 1997. Quinones in chlorosomes of green sulfur bacteria and their role in the redox-dependent fluorescence studied in chlorosome-like bacteriochlorophyll c aggregates. Arch. Microbiol. 167:343-349.
19. Frigaard, N. U., H. Li, K. J. Milks, and D. A. Bryant. 2004. Nine mutants of Chlorobium tepidum each unable to synthesize a different chlorosome protein still assemble functional chlorosomes. J. Bacteriol. 186:646-653.
20. Griesbeck, C., G. Hauska, and M. Schutz. 2000. Biological sulfide-oxidation: sulfide-quinone reductase (SQR). the primary reaction, p. 129-203. In S. G. Pandalai (ed.). Recent research developments in microbiology. Research Signpost, Trivandrum, India.
21. Grieshaber, M. K., and S. Volkel. 1998. Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu. Rev. Physiol. 60:33-53.
22. Gruber, T. M., and D. A. Bryant. 1998. Characterization of the group 1 and group 2 sigma factors of the green sulfur bacterium Chlorobium tepidum and the green non-sulfur bacterium Chloroflexus aurantiacus. Arch. Microbiol. 170:285-296.
23. Hanson, T. E., and F. R. Tabita. 2003. Insights into the stress response and sulfur metabolism revealed by proteome analysis of a Chlorobium tepidum mutant lacking the Rubisco-like protein. Photosynth. Res. 78:231-248.
24. Hanson, T. E., and F. R. Tabita. 2001. A ribulose-1.5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc. Natl. Acad. Sci. USA 98:4397-4402.
25. Heising, S., L. Richter, W. Ludwig, and B. Schink. 1999. Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a "Geospirillum" sp. strain. Arch. Microbiol. 172:116-124.
26. Hohmann-Marriott, M. F., and R. E. Blankenship. 2007. Hypothesis on chlorosome biogenesis in green photosynthetic bacteria. FEBS Lett. 581: 800-803.
27. Imhoff, J. F. 2003. Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and FMO (Fenna-Matthews-Olson protein) gene sequences. Int. J. Syst. Evol. Microbiol. 53:941-951.
28. Kaneko, T., and S. Tabata. 1997. Complete genome structure of the unicellular cyanobacterium Synechocystis sp. PCC6803. Plant Cell Physiol. 38: 1171-1176.
29. Kim, H., H. Li, J. A. Maresca, D. A. Bryant, and S. Savikhin. 2007. Triplet exciton formation as a novel photoprotection mechanism in chlorosomes of Chlorobium tepidum. Biophys. J. 93:192-201.
30. Kjaer, B., N. U. Frigaard, F. Yang, B. Zybailov, M. Miller, J. H. Golbeck, and H. V. Scheller. 1998. Menaquinone-7 in the reaction center complex of the green sulfur bacterium Chlorobium vibrioforme functions as the electron acceptor A1. Biochemistry 37:3237-3242.
31. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
32. ΔΔCT method. Methods 25:402-408.
33. Luo, Q., L. R. Krumholz, F. Z. Najar, A. D. Peacock, B. A. Roe, D. C. White, and M. S. Elshahed. 2005. Diversity of the microeukaryotic community in sulfide-rich Zodletone Spring (Oklahoma). Appl. Environ. Microbiol. 71: 6175-6184.
34. Maresca, J. A., S. P. Romberger, and D. A. Bryant. 2008. Isorenieratene biosynthesis in green sulfur bacteria requires the cooperative actions of two carotenoid cyclases. J. Bacteriol. 190:6384-6391.
35. Meeks, J. C., J. Elhai, T. Thiel, M. Potts, F. Larimer, J. Lamerdin, P. Predki, and R Atlas. 2001. An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth. Res. 70:85-106.
36. Morgan-Kiss, R. M., and J. E. Cronan. 2004. The Escherichia coli fadK (ydiD) gene encodes an anerobically regulated short chain acyl-CoA synthetase. J. Biol. Chem. 279:37324-37333.
37. Morton, R. A. 1965. Biochemistry of quinones. Academic Press, London. United Kingdom.
38. Mukhopadhyay, B., E. F. Johnson, and M. J. Ascano. 1999. Conditions for vigorous growth on sulfide and reactor-scale cultivation protocols for the thermophilic green sulfur bacterium Chlorobium tepidum. Appl. Environ. Microbiol. 65:301-306.
39. Nakamura, Y., T. Kaneko, S. Sato, M. Ikeuchi, H. Katoh, S. Sasamoto, A. Watanabe, M. Iriguchi, K. Kawashima, T. Kimura, Y. Kishida, C. Kiyokawa, M. Kohara, M. Matsumoto, A. Matsuno, N. Nakazaki, S. Shimpo, M. Sugimoto, C. Takeuchi, M. Yamada, and S. Tabata. 2002. Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res. 9:123-130.
40. Nakamura, Y., T. Kaneko, S. Sato, M. Mimuro, H. Miyashita, T. Tsuchiya, S. Sasamoto, A. Watanabe, K. Kawashima, Y. Kishida, C. Kiyokawa, M. Kohara, M. Matsumoto, A. Matsuno, N. Nakazaki, S. Shimpo, C. Takeuchi, M. Yamada, and S. Tabata. 2003. Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thvlakoids. DNA Res. 10:137-145.
41. Oh-oka, H., and R E. Blankenship. 2004. Green bacteria: secondary electron donor (cytochromes), p. 321-324. In W. J. Lennarz and M. D. Lane (ed.), Encyclopedia of biological chemistry, vol. 2. Elsevier, Boston, MA.
42. Quentmeier, A., P. Hellwig, F. Bardischewsky, R. Wichmann, and C. G. Friedrich. 2004. Sulfide dehydrogenase activity of the monomeric flavoprotein SoxE of Pam coccus pa ntotrophus. Biochemistry 43:14696-14703.
43. Reinartz, M., J. Tschape, T. Bruser, H. G. Truper, and C. Dahl. 1998. Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch. Microbiol. 170:59-68.
44. Rother, D., H. J. Henrich, A. Quentmeier, F. Bardischewsky, and C. G. Friedrich. 2001. Novel genes of the sox gene cluster, mutagenesis of the flavoprotein SoxF, and evidence for a general sulfur-oxidizing system in Paracoccus pantotrophus GB17. J. Bacteriol. 183:4499-4508.
45. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
46. Schütz, M., I. Maldener, C. Griesbeck, and G. Hauska. 1999. Sulfide-quinone reductase from Rhodobacter capsulatus: requirement for growth, periplasmic localization, and extension of gene sequence analysis. J. Bacteriol. 181:6516-6523.
47. Schütz, M., Y. Shahak, E. Padan, and G. Hauska. 1997. Sulfide-quinone reductase from Rhodobacter capsulatus. Purification, cloning, and expression. J. Biol. Chem. 272:9890-9894.
48. Shahak, Y. 2008. Sulfide oxidation from cyanobacteria to humans: sulfide-quinone oxidoreductase (SQR). p. 319-335. In R. Hell. C. Dahl, D. Knaff, and T. Leustek (ed.), Sulfur metabolism in phototrophic organisms. Springer. Dordrecht, The Netherlands.
49. Shahak, Y., B. Arieli, B. Binder, and E. Padan. 1987. Sulfide-dependent photosynthetic electron flow coupled to proton translocation in thylakoids of the cyanobacterium Oscillatoria limnetica. Arch. Biochem. Biophys. 259:605-615.
50. Shahak, Y., B. Arieli, E. Padan, and G. Hauska. 1992. Sulfide quinone reductase (SQR) activity in Chlorobium. FEBS Lett. 299:127-130.
51. Shahak, Y., C. Klughammer, U. Schreiber, E. Padan, I. Herrman, and G. Hauska. 1994. Sulfide-quinone and sulfide-cytochrome reduction in Rhodobacter capsulatus. Photosynth. Res. 39:175-181.
52. Shahak, Y., M. Schütz, M. Bronstein, C. Griesbeck, G. Hauska, and E. Padan. 1999. Sulfide-dependent anoxygenic photosynthesis in prokaiyotes - sulfide-quinone reductase (SQR), the initial step, p. 217-228. In G. A. Peschek. W. L. Loffelhardt. and G. Schmetterer (ed.). The phototrophic prokaryotes. Kluwer Academic/Plenum, New York. NY.
53. Shen, N., L. Dagasan, D. Sledjeski, and R. M. Weiner. 1989. Major outer membrane proteins unique to reproductive cells of Hyphomonas jannaschiana. J. Bacteriol. 171:2226-2228.
54. Takashima, T., T. Nishiki, and Y. Konishi. 2000. Anaerobic oxidation of dissolved hydrogen sulfide in continuous culture of the phototrophic bacterium Prosthecochloris aestuarii. J. Biosci. Bioeng. 89:247-251.
55. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. Mega4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
56. Theissen, U., M. Hoffmeister, M. Grieshaber, and W. Martin. 2003. Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol. Biol. Evol. 20:1564-1574.
57. Vassilieva, E. V., M. L. Antonkine, B. L. Zybailov, F. Yang, C. U. Jakobs, J. H. Golbeck, and D. A. Bryant. 2001. Electron transfer may occur in the chlorosome envelope: the Csml and CsmJ proteins of chlorosomes are 2Fe-2S ferredoxins. Biochemistry 40:464-473.
58. Wahlund, T. M., and M. T. Madigan. 1995. Genetic transfer by conjugation in the thermophilic green sulfur bacterium Chlorobium tepidum. J. Bacteriol. 177:2583-2588.
59. Wahlund, T. M., C. R. Woese, R. W. Castenholz, and M. T. Madigan. 1991. A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch. Microbiol. 156: 81-90.
60. Wakai, S., M. Kikumoto, T. Kanao, and K. Kamimura. 2004. Involvement of sulfide:quinone oxidoreductase in sulfur oxidation of an acidophilic iron-oxidizing bacterium, Acidithiobacillus ferrooxidans NASF-1. Biosci. Biotechnol. Biochem. 68:2519-2528.