Advertisement

Applied Microbiology and Biotechnology

, Volume 102, Issue 12, pp 5133–5147 | Cite as

A novel enzyme of type VI sulfide:quinone oxidoreductases in purple sulfur photosynthetic bacteria

  • Ágnes Duzs
  • András Tóth
  • Brigitta Németh
  • Tímea Balogh
  • Péter B. Kós
  • Gábor Rákhely
Biotechnologically relevant enzymes and proteins
  • 268 Downloads

Abstract

Sulfide detoxification can be catalyzed by ancient membrane-bound flavoproteins, sulfide:quinone oxidoreductases (Sqr), which have important roles in sulfide homeostasis and sulfide-dependent energy conservation processes by transferring electrons from sulfide to respiratory or photosynthetic membrane electron flow. Sqr enzymes have been categorized into six groups. Several members of the groups I, II, III, and V are well-known, but type IV and VI Sqrs are, as yet, uncharacterized or hardly characterized at all. Here, we report detailed characterization of a type VI sulfide:quinone oxidoreductase (TrSqrF) from a purple sulfur bacterium, Thiocapsa roseopersicina. Phylogenetic analysis classified this enzyme in a special group composed of SqrFs of endosymbionts, while a weaker relationship could be observed with SqrF of Chlorobaculum tepidum which is the only type VI enzyme characterized so far. Directed mutagenesis experiments showed that TrSqrF contributed substantially to the sulfide:quinone oxidoreductase activity of the membranes. Expression of the sqrF gene could be induced by sulfide. Homologous recombinant TrSqrF protein was expressed and purified from the membranes of a SqrF-deleted T. roseopersicina strain. The purified protein contains redox-active covalently bound FAD cofactor. The recombinant TrSqrF enzyme catalyzes sulfur-dependent quinone reduction and prefers ubiquinone-type quinone compounds. Kinetic parameters of TrSqrF show that the affinity of the enzyme is similar to duroquinone and decylubiquinone, but the reaction has substantially lower activation energy with decylubiquinone, indicating that the quinone structure has an effect on the catalytic process. TrSqrF enzyme affinity for sulfide is low, therefore, in agreement with the gene expressional analyis, SqrF could play a role in energy-conserving sulfide oxidation at high sulfide concentrations. TrSqrF is a good model enzyme for the subgroup of type VI Sqrs of endosymbionts and its characterization might provide deeper insight into the molecular details of the ancient, anoxic, energy-gaining processes using sulfide as an electron donor.

Keywords

Sulfide:quinone oxidoreductase (Sqr) Sulfur metabolism Quinone reduction Purple sulfur photosynthetic bacteria Enzyme kinetics Anoxic energy gaining 

Notes

Acknowledgements

The authors gratefully thank Klára Katonáné Lehoczky for excellent technical assistance. This research was supported by the European Union and the State of Hungary, co-financed by the European Social Fund in the framework of TÁMOP 4.2.4. A/2-11-1-2012-0001 “National Excellence Program.” This work was supported by the European Union and European Regional Development Fund (GINOP-2.3.2-15-2016-00001).

Funding

This study was funded by the European Union and co-financed by the European Social Fund (grant agreement no. TÁMOP-4.2.4.A/2-11/1-2012-0001 “National Excellence Program”) and by the GINOP-2.3.2-15-2016-00001 grant.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

The research presented did not involve any human participants.

Supplementary material

253_2018_8973_MOESM1_ESM.pdf (388 kb)
ESM 1 (PDF 388 kb)

References

  1. Arieli B, Shahak Y, Taglicht D, Hauska G, Padan E (1994) Purification and characterization of sulfide-quinone reductase, a novel enzyme driving anoxygenic photosynthesis in Oscillatoria limnetica. J Biol Chem 269:5705–5711PubMedGoogle Scholar
  2. Bogorov LV (1974) The properties of Thiocapsa roseopersicina, strain BBS, isolated from an estuary of the White Sea. Mikrobiologiia 43:326–332PubMedGoogle Scholar
  3. Brito JA, Sousa FL, Stelter M, Bandeiras TM, Vonrhein C, Teixeira M, Pereira MM, Archer M (2009) Structural and functional insights into sulfide:quinone oxidoreductase. Biochemistry 48:5613–5622.  https://doi.org/10.1021/bi9003827 CrossRefPubMedGoogle Scholar
  4. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25:1327–1333.  https://doi.org/10.1002/elps.200305844 CrossRefPubMedGoogle Scholar
  5. Chan LK, Morgan-Kiss RM, Hanson TE (2009) Functional analysis of three sulfide:quinone oxidoreductase homologs in Chlorobaculum tepidum. J Bacteriol 191:1026–1034.  https://doi.org/10.1128/JB.01154-08 CrossRefPubMedGoogle Scholar
  6. Chen ZW, Koh M, Van Driessche G, Van Beeumen JJ, Bartsch RG, Meyer TE, Cusanovich MA, Mathews FS (1994) The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science 266:430–432CrossRefPubMedGoogle Scholar
  7. Cherney MM, Zhang Y, Solomonson M, Weiner JH, James MNG (2010) Crystal structure of sulfide:quinone oxidoreductase from Acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J Mol Biol 398:292–305.  https://doi.org/10.1016/j.jmb.2010.03.018 CrossRefPubMedGoogle Scholar
  8. Dahl C (2008) Inorganic sulfur compounds as electron donors in purple sulfur bacteria. In: Hell R, Dahl C, Knaff D, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer Netherlands, Dordrecht, pp 289–317CrossRefGoogle Scholar
  9. Dahl C, Rakhely G, Pott-Sperling AS, Fodor B, Takacs M, Toth A, Kraeling M, Győrfi K, Kovacs A, Tusz J, Kovacs KL (1999) Genes involved in hydrogen and sulfur metabolism in phototrophic sulfur bacteria. FEMS Microbiol Lett 180:317–324CrossRefPubMedGoogle Scholar
  10. Degli Esposti M, Lenaz G, Izzo G, Papa S (1982) Kinetics and sidedness of ubiquinol-cytochrome c reductase in beef-heart mitochondria. FEBS Lett.  https://doi.org/10.1016/0014-5793(82)80713-8
  11. Ding H, Moksa MM, Hirst M, Beatty JT (2014) Draft genome sequences of six Rhodobacter capsulatus strains, YW1, YW2, B6, Y262, R121, and DE442. Genome Announc.  https://doi.org/10.1128/genomeA.00050-14
  12. Dorf R, Bishop R (2011) Modern control systems, 11th edn. Pearson Prentice Hall, Upper Saddle River, New JerseyGoogle Scholar
  13. Eddie BJ, Hanson TE (2013) Chlorobaculum tepidum TLS displays a complex transcriptional response to sulfide addition. J Bacteriol 195:399–408.  https://doi.org/10.1128/JB.01342-12 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fodor B, Rakhely G, AT K, Kovacs KL (2001) Transposon mutagenesis in purple sulfur photosynthetic bacteria: identification of hypF, encoding a protein capable of processing [NiFe] hydrogenases in alpha, beta, and gamma subdivisions of the proteobacteria. Appl Environ Microbiol 67:2476–2483. doi:  https://doi.org/10.1128/AEM.67.6.2476-2483.2001
  15. Friedrich CG, Rother D, Bardischewsky F, Ouentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882.  https://doi.org/10.1128/AEM.67.7.2873-2882.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Frigaard N-U, Bryant DA (2008a) Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria. In: Hell R, Dahl C, Knaff D, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer Netherlands, Dordrecht, pp 337–355CrossRefGoogle Scholar
  17. Frigaard N-U, Bryant DA (2008b) Genomic and evolutionary perspectives on sulfur metabolism in green sulfur bacteria. In: Dahl C, Friedrich CG (eds) Microbial sulfur metabolism. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 60–76CrossRefGoogle Scholar
  18. Gardebrecht A, Markert S, Sievert SM, Felbeck H, Thurmer A, Albrecht D, Wollherr A, Kabisch J, Le Bris N, Lehmann R, Daniel R, Liesegang H, Hecker M, Schweder T (2012) Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics. ISME J 6:766–776.  https://doi.org/10.1038/ismej.2011.137 CrossRefPubMedGoogle Scholar
  19. Gregersen LH, Bryant DA, Frigaard N-U (2011) Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front Microbiol 2:116.  https://doi.org/10.3389/fmicb.2011.00116 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Griesbeck C, Schutz M, Schodl T, Bathe S, Nausch L, Mederer N, Vielreicher M, Hauska G (2002) Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565CrossRefPubMedGoogle Scholar
  21. Herrero M, de Lorenzo V, Timmis KN (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172:6557–6567CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379.  https://doi.org/10.1093/bioinformatics/14.4.378 CrossRefPubMedGoogle Scholar
  23. Holkenbrink C, Barbas SO, Mellerup A, Otaki H, Frigaard NU (2011) Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system. Microbiology 157:1229–1239.  https://doi.org/10.1099/mic.0.044669-0 CrossRefPubMedGoogle Scholar
  24. Hosoki R, Matsuki N, Kimura H (1997) The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237:527–531.  https://doi.org/10.1006/bbrc.1997.6878 CrossRefPubMedGoogle Scholar
  25. Imhoff JF (1984) Quinones of phototrophic purple bacteria. FEMS Microbiol Lett 25:85–89.  https://doi.org/10.1111/j.1574-6968.1984.tb01381.x CrossRefGoogle Scholar
  26. Jackson MR, Melideo SL, Jorns MS (2012) Human sulfide:quinone oxidoreductase catalyzes the first step in hydrogen sulfide metabolism and produces a sulfane sulfur metabolite. Biochemistry 51:6804–6815.  https://doi.org/10.1021/bi300778t CrossRefPubMedGoogle Scholar
  27. Karplus PA, Schulz GE (1987) Refined structure of glutathione reductase at 1.54 A resolution. J Mol Biol 195:701–729CrossRefPubMedGoogle Scholar
  28. Keen NT, Tamaki S, Kobayashi D, Trollinger D (1988) Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene.  https://doi.org/10.1016/0378-1119(88)90117-5
  29. Kimura H (2002) Hydrogen sulfide as a neuromodulator. Mol Neurobiol 26:013–020.  https://doi.org/10.1385/MN:26:1:013 CrossRefGoogle Scholar
  30. Kós PB, Deák Z, Cheregi O, Vass I (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta Bioenerg 1777:74–83CrossRefGoogle Scholar
  31. Kovacs AT, Rakhely G, Kovacs KL (2003) Genes involved in the biosynthesis of photosynthetic pigments in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl Environ Microbiol 69:3093–3102CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kröger A (1978) Determination of contents and redox states of ubiquinone and menaquinone. Methods Enzymol 53:579–591CrossRefPubMedGoogle Scholar
  33. Kuwahara H, Yoshida T, Takaki Y, Shimamura S, Nishi S, Harada M, Matsuyama K, Takishita K, Kawato M, Uematsu K, Fujiwara Y, Sato T, Kato C, Kitagawa M, Kato I, Maruyama T (2007) Reduced genome of the thioautotrophic intracellular symbiont in a Deep-Sea Clam, Calyptogena okutanii. Curr Biol 17:881–886.  https://doi.org/10.1016/j.cub.2007.04.039 CrossRefPubMedGoogle Scholar
  34. Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320.  https://doi.org/10.1093/molbev/msn067 CrossRefPubMedGoogle Scholar
  35. Lencina AM, Ding Z, Schurig-Briccio LA, Gennis RB (2013) Characterization of the type III sulfide:quinone oxidoreductase from Caldivirga maquilingensis and its membrane binding. Biochim Biophys Acta Bioenerg 1827:266–275.  https://doi.org/10.1016/j.bbabio.2012.10.010 CrossRefGoogle Scholar
  36. Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51:169–187.  https://doi.org/10.1146/annurev-pharmtox-010510-100505 CrossRefPubMedGoogle Scholar
  37. Lloyd D (2006) Hydrogen sulfide: clandestine microbial messenger? Trends Microbiol 14:456–462.  https://doi.org/10.1016/j.tim.2006.08.003 CrossRefPubMedGoogle Scholar
  38. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  39. Ma Y-B, Zhang Z-F, Shao M-Y, Kang K-H, Shi X-L, Dong Y-P, Li J-L (2012) Response of sulfide:quinone oxidoreductase to sulfide exposure in the echiuran worm Urechis unicinctus. Mar Biotechnol (NY) 14:245–251.  https://doi.org/10.1007/s10126-011-9408-1 CrossRefGoogle Scholar
  40. Macheroux P (1999) UV-visible spectroscopy as a tool to study flavoproteins. In: Chapman SK, Reid GA (eds) Flavoprotein protocols. Humana Press, Totowa, NJ, pp 1–7Google Scholar
  41. Marcia M, Ermler U, Peng G, Michel H (2009) The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. Proc Natl Acad Sci U S A 106:9625–9630.  https://doi.org/10.1073/pnas.0904165106 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Marcia M, Ermler U, Peng G, Michel H (2010a) A new structure-based classification of sulfide:quinone oxidoreductases. Proteins 78:1073–1083.  https://doi.org/10.1002/prot.22665 CrossRefPubMedGoogle Scholar
  43. Marcia M, Langer JD, Parcej D, Vogel V, Peng G, Michel H (2010b) Characterizing a monotopic membrane enzyme. Biochemical, enzymatic and crystallization studies on Aquifex aeolicus sulfide:quinone oxidoreductase. Biochim Biophys Acta 1798:2114–2123.  https://doi.org/10.1016/j.bbamem.2010.07.033 CrossRefPubMedGoogle Scholar
  44. Miura T, Kusada H, Kamagata Y, Hanada S, Kimura N (2013) Genome sequence of the multiple-beta-lactam-antibiotic-resistant bacterium Acidovorax sp. strain MR-S7. Genome Announc.  https://doi.org/10.1128/genomeA.00412-13
  45. Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W, Gazi SK, Barrow RK, Yang G, Wang R, Snyder SH (2009) H2S signals through protein S-sulfhydration. Sci signal 2:ra72.  https://doi.org/10.1126/scisignal.2000464 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Nagy CI, Vass I, Rakhely G, Vass IZ, Toth A, Duzs A, Peca L, Kruk J, Kos PB (2014) Coregulated genes link sulfide:quinone oxidoreductase and arsenic metabolism in Synechocystis sp. strain PCC6803. J Bacteriol 196:3430–3440.  https://doi.org/10.1128/JB.01864-14 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Nakagawa S, Shimamura S, Takaki Y, Suzuki Y, Murakami S, Watanabe T, Fujiyoshi S, Mino S, Sawabe T, Maeda T, Makita H, Nemoto S, Nishimura S-I, Watanabe H, Watsuji T, Takai K (2014) Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont. ISME J 8:40–51.  https://doi.org/10.1038/ismej.2013.131 CrossRefPubMedGoogle Scholar
  48. Nitschke W, Liebl U, Matsuura K, Kramer DM (1995) Membrane-bound c-type cytochromes in Heliobacillus mobilis. In vivo study of the hemes involved in electron donation to the photosynthetic reaction center. Biochemistry 34:11831–11839CrossRefPubMedGoogle Scholar
  49. Nübel T, Klughammer C, Huber R, Hauska G, Schutz M (2000) Sulfide:quinone oxidoreductase in membranes of the hyperthermophilic bacterium Aquifex aeolicus (VF5). Arch Microbiol 173:233–244CrossRefPubMedGoogle Scholar
  50. Palágyi-Mészáros L (2006) The Thiocapsa roseopersicina genome project and the use of results in the hydrogenase research. Acta Biol Szeged 50:169Google Scholar
  51. Palágyi-Mészáros LS, Maróti J, Latinovics D, Balogh T, Klement É, Medzihradszky KF, Rákhely G, Kovács KL (2009) Electron-transfer subunits of the NiFe hydrogenases in Thiocapsa roseopersicina BBS. FEBS J 276:164–174.  https://doi.org/10.1111/j.1742-4658.2008.06770.x CrossRefPubMedGoogle Scholar
  52. Pfennig N (1961) Eine vollsynthetische Nährlösung zur selektiven Anreicherung einiger Schwefelpurpurbakter. Naturwissenschaften 48:136CrossRefGoogle Scholar
  53. Pham VH, Yong J-J, Park S-J, Yoon D-N, Chung W-H, Rhee S-K (2008) Molecular analysis of the diversity of the sulfide:quinone reductase (sqr) gene in sediment environments. Microbiology 154:3112–3121.  https://doi.org/10.1099/mic.0.2008/018580-0 CrossRefPubMedGoogle Scholar
  54. Rakhely G, Colbeau A, Garin J, Vignais PM, Kovacs KL (1998) Unusual organization of the genes coding for HydSL, the stable [NiFe]hydrogenase in the photosynthetic bacterium Thiocapsa roseopersicina BBS. J Bacteriol 180:1460–1465PubMedPubMedCentralGoogle Scholar
  55. Rakhely G, Kovacs AT, Maroti G, Fodor BD, Csanadi G, Latinovics D, Kovacs KL (2004) Cyanobacterial-type, heteropentameric, NAD+−reducing NiFe hydrogenase in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl Environ Microbiol 70:722–728CrossRefPubMedPubMedCentralGoogle Scholar
  56. Reinartz M, Tschape J, Bruser T, Truper HG, Dahl C (1998) Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch Microbiol 170:59–68CrossRefPubMedGoogle Scholar
  57. Schäfer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69–73CrossRefPubMedGoogle Scholar
  58. Schoepp-Cothenet B, Lieutaud C, Baymann F, Verméglio A, Friedrich T, Kramer DM, Nitschke W (2009) Menaquinone as pool quinone in a purple bacterium. Proc Natl Acad Sci U S A 106:8549–8554.  https://doi.org/10.1073/pnas.0813173106 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Schutz M, Shahak Y, Padan E, Hauska G (1997) Sulfide-quinone reductase from Rhodobacter capsulatus. Purification, cloning, and expression. J Biol Chem 272:9890–9894CrossRefPubMedGoogle Scholar
  60. Schutz M, Maldener I, Griesbeck C, Hauska G (1999) Sulfide-quinone reductase from Rhodobacter capsulatus: requirement for growth, periplasmic localization, and extension of gene sequence analysis. J Bacteriol 181:6516–6523PubMedPubMedCentralGoogle Scholar
  61. Shahak Y, Hauska G (2008) Sulfide oxidation from cyanobacteria to humans: sulfide–quinone oxidoreductase (Sqr). In: Hell R, Dahl C, Knaff D, Leustek T (eds) Advances in photosynthesis and respiration. Springer Netherlands, Dordrecht, pp 319–335Google Scholar
  62. Shahak Y, Arieli B, Binder B, Padan E (1987) Sulfide-dependent photosynthetic electron flow coupled to proton translocation in thylakoids of the cyanobacterium Oscillatoria limnetica. Arch Biochem Biophys 259:605–615CrossRefPubMedGoogle Scholar
  63. Shahak Y, Arieli B, Padan E, Hauska G (1992) Sulfide quinone reductase (SQR) activity in Chlorobium. FEBS Lett 299:127–130CrossRefPubMedGoogle Scholar
  64. Shibata H, Suzuki K, Kobayashi S (2007) Menaquinone reduction by an HMT2-like sulfide dehydrogenase from Bacillus stearothermophilus. Can J Microbiol 53:1091–1100.  https://doi.org/10.1139/W07-077 CrossRefPubMedGoogle Scholar
  65. Shuman KE, Hanson TE (2016) A sulfide:quinone oxidoreductase from Chlorobaculum tepidum displays unusual kinetic properties. FEMS Microbiol Lett fnw 100.  https://doi.org/10.1093/femsle/fnw100
  66. Soballe B, Poole RK (2008) Microbial ubiquinones: multiple roles in respiration, gene regulation and oxidative stress management. Microbiology 145:1817–1830.  https://doi.org/10.1099/13500872-145-8-1817 CrossRefGoogle Scholar
  67. Stanton TB, Jensen NS (1993) Purification and characterization of NADH oxidase from Serpulina (Treponema) hyodysenteriae. J Bacteriol 175:2980–2987CrossRefPubMedPubMedCentralGoogle Scholar
  68. Szabo C (2016) Gasotransmitters in cancer: from pathophysiology to experimental therapy. Nat Rev Drug Discov 15:185–203.  https://doi.org/10.1038/nrd.2015.1 CrossRefPubMedGoogle Scholar
  69. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Tengölcs R, Mészáros L, Győri E, Doffkay Z, Kovács KL, Rákhely G (2014) Connection between the membrane electron transport system and Hyn hydrogenase in the purple sulfur bacterium, Thiocapsa roseopersicina BBS. Biochim Biophys Acta Bioenerg 1837:1691–1698.  https://doi.org/10.1016/j.bbabio.2014.07.021 CrossRefGoogle Scholar
  71. Theissen U, Martin W (2008) Sulfide:quinone oxidoreductase (Sqr) from the lugworm Arenicola marina shows cyanide- and thioredoxin-dependent activity. FEBS J 275:1131–1139.  https://doi.org/10.1111/j.1742-4658.2008.06273.x CrossRefPubMedGoogle Scholar
  72. Theissen U, Hoffmeister M, Grieshaber M, Martin W (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.  https://doi.org/10.1093/molbev/msg174 CrossRefPubMedGoogle Scholar
  73. Vande Weghe JG, Ow DW (1999) A fission yeast gene for mitochondrial sulfide oxidation. J Biol Chem 274:13250–13257CrossRefPubMedGoogle Scholar
  74. Valdes J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake R 2nd, Eisen JA, Holmes DS (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9:597.  https://doi.org/10.1186/1471-2164-9-597 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Wakai S, Tsujita M, Kikumoto M, Manchur MA, Kanao T, Kamimura K (2007) Purification and characterization of sulfide:quinone oxidoreductase from an acidophilic iron-oxidizing bacterium, Acidithiobacillus ferrooxidans. Biosci Biotechnol Biochem 71:2735–2742.  https://doi.org/10.1271/bbb.70332 CrossRefPubMedGoogle Scholar
  76. Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J Off Publ Fed Am Soc Exp Biol 16:1792–1798.  https://doi.org/10.1096/fj.02-0211hyp CrossRefGoogle Scholar
  77. Weissgerber T, Zigann R, Bruce D, Chang Y-J, Detter JC, Han C, Hauser L, Jeffries CD, Land M, Munk AC, Tapia R, Dahl C (2011) Complete genome sequence of Allochromatium vinosum DSM 180(T). Stand Genomic Sci 5:311–330.  https://doi.org/10.4056/sigs.2335270 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Weissgerber T, Dobler N, Polen T, Latus J, Stockdreher Y, Dahl C (2013) Genome-wide transcriptional profiling of the purple sulfur bacterium Allochromatium vinosum DSM 180T during growth on different reduced sulfur compounds. J Bacteriol 195:4231–4245.  https://doi.org/10.1128/JB.00154-13 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Weissgerber T, Sylvester M, Kroninger L, Dahl C (2014) A comparative quantitative proteomic study identifies new proteins relevant for sulfur oxidation in the purple sulfur bacterium Allochromatium vinosum. Appl Environ Microbiol 80:2279–2292.  https://doi.org/10.1128/AEM.04182-13 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wittig I, Schägger H (2005) Advantages and limitations of clear-native PAGE. Proteomics.  https://doi.org/10.1002/pmic.200500081
  81. Wittig I, Braun H-P, Schägger H (2006) Blue native PAGE. Nat Protoc 1:418–428.  https://doi.org/10.1038/nprot.2006.62 CrossRefPubMedGoogle Scholar
  82. Yan H, Du J, Tang C (2004) The possible role of hydrogen sulfide on the pathogenesis of spontaneous hypertension in rats. Biochem Biophys Res Commun 313:22–27CrossRefPubMedGoogle Scholar
  83. Zhang Y, Weiner JH (2014) Characterization of the kinetics and electron paramagnetic resonance spectroscopic properties of Acidithiobacillus ferrooxidans sulfide:quinone oxidoreductase (Sqr). Arch Biochem Biophys 564:110–119.  https://doi.org/10.1016/j.abb.2014.09.016 CrossRefPubMedGoogle Scholar
  84. Zhang Y, Qadri A, Weiner JH (2016) The quinone-binding site of Acidithiobacillus ferrooxidans sulfide : quinone oxidoreductase controls both sulfide oxidation and quinone reduction. Biochem Cell Biol 166:159–166.  https://doi.org/10.1139/bcb-2015-0097 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiotechnologyUniversity of SzegedSzegedHungary
  2. 2.Institute of Biophysics, Biological Research CentreHungarian Academy of SciencesSzegedHungary
  3. 3.Institute of Plant Biology, Biological Research CentreHungarian Academy of SciencesSzegedHungary

Personalised recommendations