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Proposed function of alternative oxidase in mitochondrial sulphide oxidation detoxification in the Echiuran worm, Urechis unicinctus

Published online by Cambridge University Press:  22 July 2013

Jian Huang ,
Litao Zhang ,
Jinlong Li ,
Xiaoli Shi  and
Zhifeng Zhang
Jian Huang
Affiliation:
Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, Qingdao 266003, China
Litao Zhang
Affiliation:
Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, Qingdao 266003, China
Jinlong Li
Affiliation:
Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, Qingdao 266003, China
Xiaoli Shi
Affiliation:
Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, Qingdao 266003, China
Zhifeng Zhang*
Affiliation:
Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, Qingdao 266003, China
*
Correspondence should be addressed to: Z. Zhang, Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, Qingdao 266003, China email: zzfp107@ouc.edu.cn.
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Abstract

Alternative oxidase (AOX), a ubiquinol oxidase, introduces a branch pathway to the respiratory electron transport chain (ETC), bypassing complexes III and IV and catalysing the cyanide-resistant reduction of oxygen to water without translocation of protons across the inner mitochondrial membrane. Thus, it functions as a non-energy-conserving member of respiratory ETC. Previous studies of AOX focused on plants and some fungi, whereas data on animals are limited. In this study, full-length AOX cDNA was cloned from the Echiuran worm, Urechis unicinctus, a marine benthic invertebrate. In addition, mRNA expression pattern of combined activity of cytochrome c oxidase (CCO) in the body wall and hindgut of the worm exposed in sulphide (50 µM and 150 µM) was measured. The results revealed that AOX mRNA expression increased in a time- and concentration-dependent manner in both tissues, was significantly increased at 48 h, and continuously increased with time. In contrast, the activity of CCO decreased significantly at 24 h and was inhibited at 48 h during exposure to 150 µM sulphide. The present data indicate the expression of AOX mRNA depended on the sulphide concentration present as well as being influenced by the physical condition of the worm, especially the CCO activity.

Keywords

alternative oxidasecytochrome c oxidasesulphideUrechis unicinctus
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 8 , December 2013 , pp. 2145 - 2154
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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Footnotes

*

Joint first authors

References

REFERENCES

Abramson, J., Riistama, S., Larsson, G., Jasaitis, A., Svensson-Ek, M., Laakkonen, L., Puustinen, A., Iwata, S. and Wikstrom, M. (2000) The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nature Structural and Molecular Biology 7, 910–917.Google Scholar
Affonso, E.G. and Rantin, F.T. (2005) Respiratory responses of the air-breathing fish Hoplosternum littorale to hypoxia and hydrogen sulfide. Comparative Biochemistry and Physiology 141C, 275–280.Google Scholar
Affonso, E.G., Polez, V.L., Correa, C.F., Mazon, A.F., Araujo, M.R., Moraes, G. and Rantin, F.T. (2004) Physiological responses to sulfide toxicity by the air-breathing catfish, Hoplosternum littorale (Siluriformes, Callichthyidae). Comparative Biochemistry and Physiology 139C, 251–257.Google Scholar
Affourtit, C., Albury, M.S., Crichton, P.G. and Moore, A.L. (2002) Exploring the molecular nature of alternative oxidase regulation and catalysis. FEBS Letters 510, 121–126.Google Scholar
Albury, M.S., Affourtit, C., Crichton, P.G. and Moore, A.L. (2002) Structure of the plant alternative oxidase. Site-directed mutagenesis provides new information on the active site and membrane topology. Journal of Biological Chemistry 277, 1190–1194.Google Scholar
Albury, M.S., Elliott, C. and Moore, A.L. (2010) Ubiquinol-binding site in the alternative oxidase: mutagenesis reveals features important for substrate binding and inhibition. Biochimica et Biophysica Acta (BBA)—Bioenergetics 1797, 1933–1939.Google Scholar
Attene-Ramos, M.S., Wagner, E.D., Gaskins, H.R. and Plewa, M.J. (2007) Hydrogen sulfide induces direct radical-associated DNA damage. Molecular Cancer Research 5, 455–459.Google Scholar
Bagarinao, T. (1992) Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquatic Toxicology 24, 21–62.Google Scholar
Bailly, X. and Vinogradov, S. (2005) The sulfide binding function of annelid hemoglobins: relic of an old biosystem? Journal of Inorganic Biochemistry 99, 142–150.Google Scholar
Berthold, D.A., Andersson, M.E. and Nordlund, P. (2000) New insight into the structure and function of the alternative oxidase. Biochimica et Biophysica Acta (BBA)—Bioenergetics 1460, 241–254.Google Scholar
Berthold, D.A., Voevodskaya, N., Stenmark, P., Graslund, A. and Nordlund, P. (2002) EPR studies of the mitochondrial alternative oxidase. Evidence for a diiron carboxylate center. Journal of Biological Chemistry 277, 43608–43614.Google Scholar
Buchner, T., Abele, D. and Pörtner, H.O. (2001) Oxyconformity in the intertidal worm Sipunculus nudus: the mitochondrial background and energetic consequences. Comparative Biochemistry and Physiology 129B, 109–120.Google Scholar
Cooper, C. and Brown, G. (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. Journal of Bioenergetics and Biomembranes 40, 533–539.Google Scholar
Eghbal, M.A., Pennefather, P.S. and O'Brien, P.J. (2004) H2S cytotoxicity mechanism involves reactive oxygen species formation and mitochondrial depolarisation. Toxicology 203, 69–76.Google Scholar
Fernandez-Ayala, D.J., Sanz, A., Vartiainen, S., Kemppainen, K.K., Babusiak, M., Mustalahti, E., Costa, R., Tuomela, T., Zeviani, M., Chung, J., O'Dell, K.M., Rustin, P. and Jacobs, H.T. (2009) Expression of the Ciona intestinalis alternative oxidase (AOX) in Drosophila complements defects in mitochondrial oxidative phosphorylation. Cell Metabolism 9, 449–460.Google Scholar
Grieshaber, M.K. and Völkel, S. (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annual Review of Physiology 60, 33–53.Google Scholar
Goffredi, S.K., Childress, J.J., Desaulniers, N.T., Lallier, F.J. (1997) Sulfide acquisition by the vent worm Riftia pachyptila appears to be via uptake of HS−, rather than H2S. Journal of Experimental Biology 200, 2609–2616.Google Scholar
Gomes, C.M., Le Gall, J., Xavier, A.V. and Teixeira, M. (2001) Could a diiron-containing four-helix-bundle protein have been a primitive oxygen reductase? ChemBioChem 2, 583–587.Google Scholar
Hakkaart, G.A., Dassa, E.P., Jacobs, H.T. and Rustin, P. (2006) Allotopic expression of a mitochondrial alternative oxidase confers cyanide resistance to human cell respiration. EMBO Reports 7, 341–345.Google Scholar
Hand, S.C. and Somero, G.N. (1983) Energy metabolism pathways of hydrothermal vent animals: adaptations to a food-rich and sulfide-rich deep-sea environment. Biological Bulletin. Marine Biological Laboratory, Woods Hole 165, 167–181.Google Scholar
Hildebrandt, T.M. and Grieshaber, M.K. (2008a) Redox regulation of mitochondrial sulfide oxidation in the lugworm, Arenicola marina . Journal of Experimental Biology 211, 2617–2623.Google Scholar
Hildebrandt, T.M. and Grieshaber, M.K. (2008b) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS Journal 275, 3352–3361.Google Scholar
Joyner-Matos, J., Predmore, B.L., Stein, J.R., Leeuwenburgh, C. and Julian, D. (2010) Hydrogen sulfide induces oxidative damage to RNA and DNA in a sulfide-tolerant marine invertebrate. Physiological and Biochemical Zoology 83, 356–365.Google Scholar
Julian, D., Wieting, S.L., Seto, S.L., Bogan, M.R. and Arp, A.J. (1999) Thiosulfate elimination and permeability in a sulfide-adapted marine invertebrate. Physiological and Biochemical Zoology 72, 416–425.Google Scholar
Kabil, O. and Banerjee, R. (2010) Redox biochemistry of hydrogen sulfide. Journal of Biological Chemistry 285, 21903–21907.Google Scholar
Kraus, D., Doeller, J. and Powell, C. (1996) Sulfide may directly modify cytoplasmic hemoglobin deoxygenation in Solemya reidi gills. Journal of Experimental Biology 199, 1343–1352.Google Scholar
Ma, Y.B., Zhang, Z.F., Shao, M.Y., Kang, K.H., Tan, Z. and Li, J.L. (2010) Sulfide:quinone oxidoreductase from echiuran worm Urechis unicinctus . Marine Biotechnology 13, 1–15.Google Scholar
Maréchal, A., Kido, Y., Kita, K., Moore, A.L. and Rich, P.R. (2009) Three redox states of Trypanosoma brucei alternative oxidase identified by infrared spectroscopy and electrochemistry. Journal of Biological Chemistry 284, 31827–31833.Google Scholar
McDonald, A.E., Vanlerberghe, G. and Staples, J.F. (2009) Alternative oxidase in animals: unique characteristics and taxonomic distribution. Journal of Experimental Biology 212, 2627–2634.Google Scholar
Millero, F.J., Plese, T. and Fernandez, M. (1988) The dissociation of hydrogen sulfide in seawater. Limnology and Oceanography 33, 69–74.Google Scholar
Moore, A.L. and Albury, M.S. (2008) Further insights into the structure of the alternative oxidase: from plants to parasites. Biochemical Society Transactions 036, 1022–1026.Google Scholar
Moore, A.L., Carre, J.E., Affourtit, C., Albury, M.S., Crichton, P.G., Kita, K. and Heathcote, P. (2008) Compelling EPR evidence that the alternative oxidase is a diiron carboxylate protein. Biochimica et Biophysica Acta 1777, 327–330.Google Scholar
Muller, M., Mentel, M., van Hellemond, J.J., Henze, K., Woehle, C., Gould, S.B., Yu, R.Y., van der Giezen, M., Tielens, A.G.M., Martin, W.F. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiology and Molecular Biology Reviews 76, 444–495.Google Scholar
Nicholls, P. (1975) The effect of sulfide on cytochrome aa3. Isosteric and allosteric shifts of the reduced α-peak. Biochimica et Biophysica Acta 396, 24–35.Google Scholar
Oeschger, R. and Storey, K.B. (1990) Regulation of glycolytic enzymes in the marine invertebrate Halicryptus spinulosus (Priapulida) during environmental anoxia and exposure to hydrogen sulfide. Marine Biology 106, 261–266.Google Scholar
Pichaud, N., Rioux, P. and Blier, P.U. (2012) In situ quantification of mitochondrial respiration in permeabilized fibers of a marine invertebrate with low aerobic capacity. Comparative Biochemistry and Physiology 161A, 429–35.Google Scholar
Powell, M.A. and Somero, G.N. (1986) Hydrogen sulfide oxidation is coupled to oxidative phosphorylation in mitochondria of Solemya reidi . Science 233, 563–566.CrossRefGoogle ScholarPubMed
Schroff, G. (1977) Anaerobic reduction of fumarate in the body wall musculature of Arenicola marina (Polychaeta). Comparative Biochemistry and Physiology 116B, 325–336.Google Scholar
Sluse, F.E. and Jarmuszkiewicz, W. (1998) Alternative oxidase in the branched mitochondrial respiratory network: an overview on structure, function, regulation, and role. Brazilian Journal of Medical and Biological Research 31, 733–747.Google Scholar
Taniguchi, E., Matsunami, M., Kimura, T., Yonezawa, D., Ishiki, T., Sekiguchi, F., Nishikawa, H., Maeda, Y., Ishikura, H. and Kawabata, A. (2009) Rhodanese, but not cystathionine-gamma-lyase, is associated with dextran sulfate sodium-evoked colitis in mice: a sign of impaired colonic sulfide detoxification? Toxicology 264, 96–103.Google Scholar
Theissen, U. and Martin, W. (2008) Sulfide: quinone oxidoreductase (SQR) from the lugworm Arenicola marina shows cyanide- and thioredoxin-dependent activity. FEBS Journal 275, 1131–1139.Google Scholar
Tiranti, V., Viscomi, C., Hildebrandt, T., Di Meo, I., Mineri, R., Tiveron, C.D., Levitt, M., Prelle, A., Fagiolari, G., Rimoldi, M. and Zeviani, M. (2009) Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nature Medicine 15, 200–205.Google Scholar
Truong, D.H., Eghbal, M.A., Hindmarsh, W., Roth, S.H. and O'Brien, P.J. (2006) Molecular mechanisms of hydrogen sulfide toxicity. Drug Metabolism Reviews 38, 733–744.Google Scholar
Völkel, S. and Grieshaber, M.K. (1996) Mitochondrial sulfide oxidation in Arenicola marina: evidence for alternative electron pathways. European Journal of Biochemistry 235, 231–237.Google Scholar
Vanlerberghe, G.C. and McIntosh, L. (1997) Alternative oxidase: from gene to function. Annual Review of Plant Physiology and Plant Molecular Biology 48, 703–734.Google Scholar