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Response of Sulfide:Quinone Oxidoreductase to Sulfide Exposure in the Echiuran Worm Urechis unicinctus

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Abstract

Sulfide is a natural, widely distributed, poisonous substance, and sulfide:quinone oxidoreductase (SQR) is responsible for the initial oxidation of sulfide in mitochondria. In this study, we examined the response of SQR to sulfide exposure (25, 50, and 150 μM) at mRNA, protein, and enzyme activity levels in the body wall and hindgut of the echiuran worm Urechis unicinctus, a benthic organism living in marine sediments. The results revealed SQR mRNA expression during sulfide exposure in the body wall and hindgut increased in a time- and concentration-dependent manner that increased significantly at 12 h and continuously increased with time. At the protein level, SQR expression in the two tissues showed a time-dependent relationship that increased significantly at 12 h in 50 μM sulfide and 6 h in 150 μM, and then continued to increase with time while no significant increase appeared after 25 μM sulfide exposure. SQR enzyme activity in both tissues increased significantly in a time-dependent manner after 50 μM sulfide exposure. We concluded that SQR expression could be induced by sulfide exposure and that the two tissues studied have dissimilar sulfide metabolic patterns. A U. unicinctus sulfide-induced detoxification mechanism was also discussed.

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References

  • Anwar-Mohamed A, El-Kadi AOS (2009) Sulforaphane induces CYP1A1 mRNA, protein, and catalytic activity levels via an AhR-dependent pathway in murine hepatoma Hepa 1c1c7 and human HepG2 cells. Cancer Lett 275:93–101

    Article  PubMed  CAS  Google Scholar 

  • Arp AJ, Menon JG, Julian D (1995) Multiple mechanisms provide tolerance to environmental sulfide in Urechis caupo. Integr Comp Biol 35:132–144

    Article  CAS  Google Scholar 

  • Bagarinao T (1992) Sulfide as an envrionmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquat Toxicol 24:21–62

    Article  CAS  Google Scholar 

  • Bogan MR, Arp AJ (1993) Sulfide oxidation by the tissues of Urechis caupo in vitro. Amer Zool 33:83A

    Google Scholar 

  • Bogan MR, Delacroix O, Arp AJ (1992) Thiosulfate is the initial product of sulfide detoxification in Urechis caupo. Amer Zool 32:47A

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Chem 72:248–254

    CAS  Google Scholar 

  • Carrico RJ, Blumberg WE, Peisach J (1978) The reversible binding of oxygen to sulfhemoglobin. J Biol Chem 253:7212–7215

    PubMed  CAS  Google Scholar 

  • Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458

    Article  CAS  Google Scholar 

  • Eaton RA, Arp AJ (1993) Aerobic respiration during sulfide exposure in the marine echiuran worm Urechis caupo. Physiol Zool 66:1–19

    CAS  Google Scholar 

  • Evans CL (1967) The toxicity of hydrogen sulphide and other sulphides. J Exp Physiol 52:231–248

    CAS  Google Scholar 

  • Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu Rev Physiol 60:33–53

    Article  PubMed  CAS  Google Scholar 

  • Hance JM, Andrzejewski JE, Predmore BL, Dunlap KJ, Misiak KL, Julian D (2008) Cytotoxicity from sulfide exposure in a sulfide-tolerant marine invertebrate. J Exp Mar Biol 359:102–109

    Article  CAS  Google Scholar 

  • Hildebrandt TM, Grieshaber MK (2008a) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J 275:3352–3361

    Article  PubMed  CAS  Google Scholar 

  • Hildebrandt TM, Grieshaber MK (2008b) Redox regulation of mitochondrial sulfide oxidation in the lugworm, Arenicola marina. J Exp Biol 211:2617–2623

    Article  PubMed  Google Scholar 

  • Ip YK, Kuah SSL, Chew SF (2004) Strategies adopted by the mudskipper Boleophthalmus boddaerti to survive sulfide exposure in normoxia or hypoxia. Physiol Biochem Zool 77(5):824–837

    Article  PubMed  CAS  Google Scholar 

  • Joyner-Matos J, Predmore BL, Stein JR, Leeuwenburgh C, Julian D (2010) Hydrogen sulfide induces oxidative damage to RNA and DNA in a sulfide-tolerant marine invertebrate. Physiol Biochem Zool 83(2):356–365

    PubMed  CAS  Google Scholar 

  • Julian D, Wieting SL, Bogan MR, Arp AJ (1999) Thiosulfate elimination and permeability in a sulfide-adapted marine invertebrate. Physiol Biochem Zool 72(4):416–425

    Article  PubMed  CAS  Google Scholar 

  • Julian D, April KL, Patel S, Stein JR, Wohlgemuth SE (2005) Mitochondrial depolarization following hydrogen sulfide exposure in erythrocytes from a sulfide-tolerant marine invertebrate. J Exp Biol 208:4109–4122

    Article  PubMed  CAS  Google Scholar 

  • Kabil O, Banerjee R (2010) Redox biochemistry of hydrogen sulfide. J Biol Chem 285(29):21903–21907

    Article  PubMed  CAS  Google Scholar 

  • Kraus D, Doeller J, Powell C (1996) Sulfide may directly modify cytoplasmic hemoglobin deoxygenation in Solemya reidi gills. J Exp Biol 199:1343–1352

    PubMed  CAS  Google Scholar 

  • Li FL, Wang W, Zhou H (1994) Studies on the echiurans (echiura) of the yellow sea (Huanghai) and Bohai sea. Period Ocean Univ China 24:203–210 (in Chinese, with English abstract)

    CAS  Google Scholar 

  • Ma ZJ, Bao ZM, Kang KH, Yu L, Zhang ZF (2005) The changes of three components in coelomic fluid of Urechis unicinctus exposed to different concentrations of sulfide. Chin J Oceanol Limnol 23:104–109

    Article  CAS  Google Scholar 

  • Ma ZJ, Bao ZM, Wang SF, Zhang ZF (2010) Sulfide-based ATP production in Urechis unicinctus. Chin J Oceanol Limnol 28(3):521–526

    Article  CAS  Google Scholar 

  • Ma YB, Zhang ZF, Shao MY, Kang KH, Tan Z, Li JL (2011) Sulfide:quinone oxidoreductase from echiuran worm Urechis unicinctus. Mar Biotechnol 13:93–107

    Article  PubMed  CAS  Google Scholar 

  • Menon JG, Arp AJ (1992) Morphological adaptations of the respiratory hindgut of a marine echiuran worm. J Morphol 214:131–138

    Article  Google Scholar 

  • Menon JG, Arp AJ (1993) The integument of the marine echiuran worm Urechis caupo. J Morphol 185:440–454

    Google Scholar 

  • Menon JG, Arp AJ (1998) Ultrastructural evidence of detoxification in the alimentary canal of Urechis caupo. Integr Biol 117:307–317

    Google Scholar 

  • Nicholls P (1975) The effect of sulphide on cytochrome aa3 isosteric and allosteric shifts of the reduced alpha-peak. Biochim Biophys Acta 396:24–35

    Article  PubMed  CAS  Google Scholar 

  • Powell MA, Arp AJ (1989) Hydrogen sulfide oxidation by abundant nonhemoglobin heme compounds in marine invertebrates from sulfide-rich habitats. J Exp Zool 249:121–132

    Article  CAS  Google Scholar 

  • Powell MA, Somero GN (1986) Hydrogen sulfide oxidation is coupled to oxidative phosphorylation in mitochondria of Solemya reidi. Science 233:563–566

    Article  PubMed  CAS  Google Scholar 

  • Ramasamy S, Taniere P, Langman MJS, Eggo MC (2006) Sulfide-detoxifying enzymes in the human colon are decreased in cancer and upregulated in differentiation. Am J Physiol Gastrointest Liver Physiol 291(2):G288–G296

    Article  PubMed  CAS  Google Scholar 

  • Schroff G, Schöttler U (1977) Anaerobic reduction of fumarate in the body wall musculature of Arenicola marina (Polychaeta). J Comp Physiol B 116:325–336

    Article  CAS  Google Scholar 

  • Shao CX, Liu YT, Ruan HQ, Li Y, Wang HF (2010) Shotgun proteomic analysis of hibernating arctic ground squirrels. Mol Cell Proteomics 9(2):313–326

    Article  PubMed  CAS  Google Scholar 

  • Subudhia U, Chainya G (2010) Expression of hepatic antioxidant genes in l-thyroxine-induced hyperthyroid rats: regulation by vitamin E and curcumin. Chem-Biol Interact 183:304–316

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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(9):1564–1574

    Article  PubMed  CAS  Google Scholar 

  • Tiranti V, Viscomi C, Hildebrandt T, Meo ID, Mineri R, Tiveron C, Levitt MD, Prelle A, Fagiolari G, Rimoldi M, Zeviani M (2009) Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat med 15(2):200–205

    Article  PubMed  CAS  Google Scholar 

  • Völkel S, Grieshaber MK (1997) Sulphide oxidation and oxidative phosphorylation in the mitochondria of the lugworm Arenicola marina. J Exp Biol 200:83–92

    Google Scholar 

  • Wang SF, Zhang ZF, Cui H, Kang KH, Ma ZJ (2010) The effect of toxic sulfide exposure on oxygen consumption and oxidation products in Urechis unicinctus (Echiura: Urechidae). J Ocean Univ Chin 9(2):157–161

    Article  CAS  Google Scholar 

  • Wohlgemuth SE, Taylor AC, Grieshaber MK (2000) Ventilatory and metabolic responses to hypoxia and sulphide in the lugworm Arenicola marina (L.). J Exp Biol 203:3177–3188

    Google Scholar 

  • Wohlgemuth SE, Arp AJ, Bergquist D, Julian D (2007) Rapid induction and disappearance of electron-dense organelles following sulfide exposure in the marine annelid Branchioasychis americana. Inverteb Biol 126(2):163–172

    Article  Google Scholar 

  • Zhang ZF, Shao MY, Kang KH, Jin ZM (2003) Studies on the tolerating mechanism for sulfide in Urechis unicinctus (Echiura: Urechidae)-cytological observation on Urechis unicinctus in different hydrogen sulfide environment. Chin J Oceanol Limnol 21(1):86–90

    Article  CAS  Google Scholar 

  • Zhang ZF, Wang SF, Huo JG, Shao MY, Kang KH (2006) Adaptation of respiratory metabolism to sulfide exposure in Urechis unicinctus. Period Ocean Univ China 36:639–644 (in Chinese, with English abstract)

    CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to the laboratory members for experimental material preparation and technical assistance. This work was supported by the Natural Science Foundation of China (40776074 and 31072191.

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Correspondence to Zhi-Feng Zhang.

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Ma, YB., Zhang, ZF., Shao, MY. et al. Response of Sulfide:Quinone Oxidoreductase to Sulfide Exposure in the Echiuran Worm Urechis unicinctus . Mar Biotechnol 14, 245–251 (2012). https://doi.org/10.1007/s10126-011-9408-1

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