Skip to main content

Advertisement

SpringerLink
Log in

Mitochondrial adaptations to utilize hydrogen sulfide for energy and signaling

  • Review
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Sulfur is a versatile molecule with oxidation states ranging from −2 to +6. From the beginning, sulfur has been inexorably entwined with the evolution of organisms. Reduced sulfur, prevalent in the prebiotic Earth and supplied from interstellar sources, was an integral component of early life as it could provide energy through oxidization, even in a weakly oxidizing environment, and it spontaneously reacted with iron to form iron–sulfur clusters that became the earliest biological catalysts and structural components of cells. The ability to cycle sulfur between reduced and oxidized states may have been key in the great endosymbiotic event that incorporated a sulfide-oxidizing α-protobacteria into a host sulfide-reducing Archea, resulting in the eukaryotic cell. As eukaryotes slowly adapted from a sulfidic and anoxic (euxinic) world to one that was highly oxidizing, numerous mechanisms developed to deal with increasing oxidants; namely, oxygen, and decreasing sulfide. Because there is rarely any reduced sulfur in the present-day environment, sulfur was historically ignored by biologists, except for an occasional report of sulfide toxicity. Twenty-five years ago, it became evident that the organisms in sulfide-rich environments could synthesize ATP from sulfide, 10 years later came the realization that animals might use sulfide as a signaling molecule, and only within the last 4 years did it become apparent that even mammals could derive energy from sulfide generated in the gastrointestinal tract. It has also become evident that, even in the present-day oxic environment, cells can exploit the redox chemistry of sulfide, most notably as a physiological transducer of oxygen availability. This review will examine how the legacy of sulfide metabolism has shaped natural selection and how some of these ancient biochemical pathways are still employed by modern-day eukaryotes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066–1071

    PubMed  CAS  Google Scholar 

  • Ackermann M, Kubitza M, Maier K, Brawanski A, Hauska G, Pina AL (2011) The vertebrate homolog of sulfide-quinone reductase is expressed in mitochondria of neuronal tissues. Neuroscience 199:1–12

    Google Scholar 

  • Amend JP, Shock EL (2001) Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and bacteria. FEMS Microbiol Rev 25:175–243

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bagarinao T, Vetter RD (1990) Oxidative detoxification of sulfide by mitochondria of the California killifish, Fundulus parvipinnis and the speckled sanddab, Citharichthys stigmaeus. J Comp Physiol 160:519–527

    CAS  Google Scholar 

  • Balaban CL, Rodriguez JV, Guibert EE (2011) Delivery of the bioactive gas hydrogen sulfide during cold preservation of rat liver: effects on hepatic function in an ex vivo model. Artif Organs 35:508–515

    Article  PubMed  CAS  Google Scholar 

  • Balazy M, Yousef IA, Harpp DN, Park J (2003) Identification of carbonyl sulfide and sulfur dioxide in porcine coronary artery by gas chromatography/mass spectrometry, possible relevance to EDHF. Biochem Biophys Res Commun 311:728–734

    Article  PubMed  CAS  Google Scholar 

  • Bartholomew TC, Powell GM, Dodgson KS, Curtis CG (1980) Oxidation of sodium sulphide by rat liver, lungs and kidney. Biochem Pharmacol 29:2431–2437

    Article  PubMed  CAS  Google Scholar 

  • Bernstein M (2006) Prebiotic materials from on and off the early Earth. Philos Trans R Soc Lond B Biol Sci 361:1689–1700

    Article  PubMed  CAS  Google Scholar 

  • Blachier F, Davila AM, Mimoun S, Benetti PH, Atanasiu C, Andriamihaja M, Benamouzig R, Bouillaud F, Tome D (2010) Luminal sulfide and large intestine mucosa: friend or foe? Amino Acids 39:335–347

    Article  PubMed  CAS  Google Scholar 

  • Blackstone E, Roth MB (2007) Suspended animation-like state protects mice from lethal hypoxia. Shock 27:370–372

    Article  PubMed  CAS  Google Scholar 

  • Blackstone E, Morrison M, Roth MB (2005) H2S induces a suspended animation-like state in mice. Science 308:518

    Article  PubMed  CAS  Google Scholar 

  • Blazejak A, Erseus C, Amann R, Dubilier N (2005) Coexistence of bacterial sulfide oxidizers, sulfate reducers, and spirochetes in a gutless worm (Oligochaeta) from the Peru margin. Appl Environ Microbiol 71:1553–1561

    Article  PubMed  CAS  Google Scholar 

  • Booker SJ, Cicchillo RM, Grove TL (2007) Self-sacrifice in radical S-adenosylmethionine proteins. Curr Opin Chem Biol 11:543–552

    Article  PubMed  CAS  Google Scholar 

  • Bouillaud F, Blachier F (2011) Mitochondria and sulfide: a very old story of poisoning, feeding and signaling? Antioxid Redox Signal 15:379–391

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ, Mattson MP (2010) Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid Redox Signal 13:1763–1811

    Google Scholar 

  • Calvert JW, Elston M, Nicholson CK, Gundewar S, Jha S, Elrod JW, Ramachandran A, Lefer DJ (2010) Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice. Circulation 122:11–19

    Article  PubMed  Google Scholar 

  • Chattopadhyay M, Kodela R, Olson KR Kashfi K (2012) NOSH-asprin (NBS-1120), a novel nitric oxide- and hydrogen sulfide-releasing hybrid is a potent inhibitor of colon cancer cell growth in vitro and in a xenograft mouse model. Biochem Biophys Res Commun. doi:org/10.1016/j.bbrc.2012.02.051

  • Chengelis CP, Neal RA (1979) Hepatic carbonyl sulfide metabolism. Biochim Biophys Res Commun 3:993–999

    Article  Google Scholar 

  • Cherney MM, Zhang Y, Solomonson M, Weiner JH, James MN (2010) Crystal structure of sulfide:quinone oxidoreductase from Acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J Mol Biol 398:292–305

    Article  PubMed  CAS  Google Scholar 

  • Cleaves HJ, Chalmers JH, Lazcano A, Miller SL, Bada JL (2008) A reassessment of prebiotic organic synthesis in neutral planetary atmospheres. Orig Life Evol Biosph 38:105–115

    Article  PubMed  CAS  Google Scholar 

  • Collman JP, Ghosh S, Dey A, Decreau RA (2009) Using a functional enzyme model to understand the chemistry behind hydrogen sulfide induced hibernation. Proc Natl Acad Sci USA 106:22090–22095

    Article  PubMed  CAS  Google Scholar 

  • Cooper CE, Brown GC (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J Bioenerg Biomembr 40:533–539

    Article  PubMed  CAS  Google Scholar 

  • Curtis CG, Bartholomew TC, Rose FA, Dodgson KS (1972) Detoxication of sodium 35 S-sulphide in the rat. Biochem Pharmacol 21:2313–2321

    Article  PubMed  CAS  Google Scholar 

  • Davidov Y, Jurkevitch E (2009) Predation between prokaryotes and the origin of eukaryotes. BioEssays 31:748–757

    Article  PubMed  CAS  Google Scholar 

  • de Souza-Barros F, Vieyra A (2007) Mineral interface in extreme habitats: a niche for primitive molecular evolution for the appearance of different forms of life on Earth. Comp Biochem Physiol C: Toxicol Pharmacol 146:10–21

    Article  CAS  Google Scholar 

  • DeLeon ER, Stoy GF, Olson KR (2011) Passive loss of hydrogen sulfide in biological experiments. Anal Biochem 421:203–207

    Google Scholar 

  • Di Meo I, Fagiolari G, Prelle A, Viscomi C, Zeviani M, Tiranti V (2011) Chronic exposure to sulfide causes accelerated degradation of cytochrome C oxidase in ethylmalonic encephalopathy. Antioxid Redox Signal 15:353–362

    Article  PubMed  CAS  Google Scholar 

  • Doeller JE, Gaschen BK, Parrino VV, Kraus DW (1999) Chemolithoheterotrophy in a metazoan tissue: sulfide supports cellular work in ciliated mussel gills. J Exp Biol 202(Pt 14):1953–1961

    PubMed  CAS  Google Scholar 

  • Doeller JE, Grieshaber MK, Kraus DW (2001) Chemolithoheterotrophy in a metazoan tissue: thiosulfate production matches ATP demand in ciliated mussel gills. J Exp Biol 204:3755–3764

    PubMed  CAS  Google Scholar 

  • Doeller JE, Isbell TS, Benavides G, Koenitzer J, Patel H, Patel RP, Lancaster JR Jr, Darley-Usmar VM, Kraus DW (2005) Polarographic measurement of hydrogen sulfide production and consumption by mammalian tissues. Anal Biochem 341:40–51

    Article  PubMed  CAS  Google Scholar 

  • Dombkowski RA, Naylor MG, Shoemaker E, Smith M, DeLeon ER, Stoy GF, Gao Y, Olson KR (2011) Hydrogen sulfide (H2S) and hypoxia inhibit salmonid gastrointestinal motility: evidence for H2S as an oxygen sensor. J Exp Biol 214:4030–4040

    Google Scholar 

  • Dorman DC, Moulin FJ, McManus BE, Mahle KC, James RA, Struve MF (2002) Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol Sci 65:18–25

    Article  PubMed  CAS  Google Scholar 

  • Drousiotou A, DiMeo I, Mineri R, Georgiou T, Stylianidou G, Tiranti V (2011) Ethylmalonic encephalopathy: application of improved biochemical and molecular diagnostic approaches. Clin Genet 79:385–390

    Article  PubMed  CAS  Google Scholar 

  • Dubilier N, Mulders C, Ferdelman T, de BD, Pernthaler A, Klein M, Wagner M, Erseus C, Thiermann F, Krieger J, Giere O, Amann R (2001) Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411:298–302

    Article  PubMed  CAS  Google Scholar 

  • Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740

    Article  PubMed  CAS  Google Scholar 

  • Elliot S, Lu E, Rowland FS (1987) Carbonyl sulfide hydrolysis as a source of hydrogen sulfide in open ocean seawater. Geophys Res Lett 14:131–134

    Article  Google Scholar 

  • Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630

    Article  PubMed  CAS  Google Scholar 

  • Erwin DH (2006) Extinction: how life on Earth nearly ended 250 million years ago. Princeton University Press, Princeton

    Google Scholar 

  • Fenchel TM, Riedl RJ (1970) The sulfide system: a new biotic community underneath the oxidized layer of marine sand bottoms. Mar Biol 7:255–268

    Article  CAS  Google Scholar 

  • Flannigan KL, McCoy KD, Wallace JL (2011) Eukaryotic and prokaryotic contributions to colonic hydrogen sulfide synthesis. Am J Physiol Gastrointest Liver Physiol 301:G188–G193

    Article  PubMed  CAS  Google Scholar 

  • Furne J, Springfield J, Koenig T, DeMaster E, Levitt MD (2001) Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa. Biochem Pharmacol 62:255–259

    Article  PubMed  CAS  Google Scholar 

  • Furne J, Saeed A, Levitt MD (2008) Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values. Am J Physiol Regul Integr Comp Physiol 295:R1479–R1485

    Article  PubMed  CAS  Google Scholar 

  • Giordano C, Viscomi C, Orlandi M, Papoff P, Spalice A, Burlina A, Di M, I, Tiranti V, Leuzzi V, d’Amati G, Zeviani M (2011) Morphologic evidence of diffuse vascular damage in human and in the experimental model of ethylmalonic encephalopathy. J Inherit Metab Dis. doi:10.1007/s10545-011-9408-3

  • Gorr TA, Wichmann D, Hu J, Hermes-Lima M, Welker AF, Terwilliger N, Wren JF, Viney M, Morris S, Nilsson GE, Deten A, Soliz J, Gassmann M (2010) Hypoxia tolerance in animals: biology and application. Physiol Biochem Zool 83:733–752

    Article  PubMed  CAS  Google Scholar 

  • Goubern M, Andriamihaja M, Nubel T, Blachier F, Bouillaud F (2007) Sulfide, the first inorganic substrate for human cells. FASEB J 21:1699–1706

    Article  PubMed  CAS  Google Scholar 

  • Griesbeck C, Hauska G, Schültz M (2000) Biological sulfide oxidation: sulfide-quinone reductase (SQR), the primary reaction. In: Pandalai SG (ed) Recent research developments in microbiology. Research Signpost, Trivandrum, pp 179–203

    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 

  • Guidotti TL (2010) Hydrogen sulfide: advances in understanding human toxicity. Int J Toxicol 29:569–581

    Google Scholar 

  • He G, Shankar RA, Chzhan M, Samouilov A, Kuppusamy P, Zweier JL (1999) Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. Proc Natl Acad Sci USA 96:4586–4591

    Article  PubMed  CAS  Google Scholar 

  • Hildebrandt TM (2011) Modulation of sulfide oxidation and toxicity in rat mitochondria by dehydroascorbic acid. Biochim Biophys Acta 1807:1206–1213

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hildebrandt TM, Grieshaber MK (2008b) 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 

  • Hill BC, Woon TC, Nicholls P, Peterson J, Greenwood C, Thomson AJ (1984) Interactions of sulphide and other ligands with cytochrome c oxidase. An electron-paramagnetic-resonance study. Biochem J 224:591–600

    PubMed  CAS  Google Scholar 

  • Holland HD (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B Biol Sci 361:903–915

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ishigami M, Hiraki K, Umemura K, Ogasawara Y, Ishii K, Kimura H (2009) A source of hydrogen sulfide and a mechanism of its release in the brain. Antioxid Redox Signal 11:205–214

    Article  PubMed  CAS  Google Scholar 

  • Jeroschewski P, Steuckart CKM (1996) An amperometric microsensor for the determination of H2S in aquatic environments. Anal Chem 68:4351–4357

    Article  CAS  Google Scholar 

  • Jiang B, Tang G, Cao K, Wu L, Wang R (2010) Molecular mechanism for H(2)S-induced activation of K(ATP) channels. Antioxid Redox Signal 12:1167–1178

    Article  PubMed  CAS  Google Scholar 

  • Johnson JE (1981) The lifetime of carbonyl sulfide in the troposphere. Geophys Res Lett 8:938–940

    Article  CAS  Google Scholar 

  • Kajimura M, Fukuda R, Bateman RM, Yamamoto T, Suematsu M (2010) Interactions of multiple gas-transducing systems: hallmarks and uncertainties of CO, NO, and H2S gas biology. Antioxid Redox Signal 13:157–192

    Article  PubMed  CAS  Google Scholar 

  • Kamboures MA, Blake DR, Cooper DM, Newcomb RL, Barker M, Larson JK, Meinardi S, Nussbaum E, Rowland FS (2005) Breath sulfides and pulmonary function in cystic fibrosis. Proc Natl Acad Sci USA 102:15762–15767

    Article  PubMed  CAS  Google Scholar 

  • Kilburn KH, Thrasher JD, Gray MR (2010) Low-level hydrogen sulfide and central nervous system dysfunction. Toxicol Ind Health 26:387–405

    Article  PubMed  CAS  Google Scholar 

  • Kraus DW, Doeller JE (2004) Sulfide consumption by mussel gill mitochondria is not strictly tied to oxygen reduction: measurements using a novel polargraphic sulfide sensor. J Exp Biol 207:3667–3679

    Article  PubMed  CAS  Google Scholar 

  • Kump LR (2008) The rise of atmospheric oxygen. Nature 451:277–278

    Google Scholar 

  • Kurland CG, Andersson SG (2000) Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev 64:786–820

    Article  PubMed  CAS  Google Scholar 

  • Lagoutte E, Mimoun S, Andriamihaja M, Chaumontet C, Blachier F, Bouillaud F (2010) Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim Biophys Acta 1797:1500–1511

    Article  PubMed  CAS  Google Scholar 

  • Leman L, Orgel L, Ghadird MR (2004) Carbonyl sulfide-mediated prebiotic formation of peptides. Science 306:283–286

    Article  PubMed  CAS  Google Scholar 

  • Leschelle X, Goubern M, Andriamihaja M, Blottiere HM, Couplan E, Gonzalez-Barroso MD, Petit C, Pagniez A, Chaumontet C, Mignotte B, Bouillaud F, Blachier F (2005) Adaptative metabolic response of human colonic epithelial cells to the adverse effects of the luminal compound sulfide. Biochim Biophys Acta 1725:201–212

    Article  PubMed  CAS  Google Scholar 

  • Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831–838

    Article  PubMed  CAS  Google Scholar 

  • Linden DR, Levitt MD, Farrugia G, Szurszewski JH (2010) Endogenous production of H2S in the gastrointestinal tract: still in search of a physiologic function. Antioxid Redox Signal 12:1135–1146

    Article  PubMed  CAS  Google Scholar 

  • Linden DR, Furne J, Stoltz GJ, bdel-Rehim MS, Levitt MD, Szurszewski JH (2011) Sulfide quinone reductase contributes to hydrogen sulfide metabolism in murine peripheral tissues but not in the central nervous system. Br J Pharmacol 165:2178–2190

    Google Scholar 

  • Lopez-Barneo J, Nurse CA, Nilsson GE, Buck LT, Gassmann M, Bogdanova AY (2010) First aid kit for hypoxic survival: sensors and strategies. Physiol Biochem Zool 83:753–763

    Article  PubMed  CAS  Google Scholar 

  • Madden JA, Ahlf SB, Dantuma MW, Olson KR, Roerig DL (2011) Precursors and inhibitors of hydrogen sulfide symphysis affect acute hypoxic pulmonary vasoconstriction in the intact lung. J Appl Physiol 112:411–418

    Google Scholar 

  • 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 USA 106:9625–9630

    Article  PubMed  CAS  Google Scholar 

  • Marcia M, Ermler U, Peng G, Michel H (2010) A new structure-based classification of sulfide:quinone oxidoreductases. Proteins 78:1073–1083

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Russell MJ (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans R Soc Lond B Biol Sci 358:59–83

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Russell MJ (2007) On the origin of biochemistry at an alkaline hydrothermal vent. Philos Trans R Soc Lond B Biol Sci 362:1887–1925

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Rotte C, Hoffmeister M, Theissen U, Gelius-Dietrich G, Ahr S, Henze K (2003) Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 55:193–204

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Baross J, Kelley D, Russell MJ (2008) Hydrothermal vents and the origin of life. Nat Rev Microbiol 6:805–814

    PubMed  CAS  Google Scholar 

  • Mathew ND, Schlipalius DI, Ebert PR (2011) Sulfurous gases as biological messengers and toxins: Comparative genetics of their metabolism in model organisms. J Toxicol. doi:10.1155/2011/394970

  • Mentel M, Martin W (2010) Anaerobic animals from an ancient, anoxic ecological niche. BMC Biol 8:32

    Article  PubMed  CAS  Google Scholar 

  • Mikami Y, Shibuya N, Kimura Y, Nagahara N, Ogasawara Y, Kimura H (2011) Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem J 439:479–485

    Article  PubMed  CAS  Google Scholar 

  • Miller SL, Urey HC (1959) Organic compound synthesis on the primitive Earth. Science 130:245–251

    Article  PubMed  CAS  Google Scholar 

  • Morii D, Miyagatani Y, Nakamae N, Murao M, Taniyama K (2010) Japanese experience of hydrogen sulfide: the suicide craze in 2008. J Occup Med Toxicol 5:28–30

    Article  PubMed  CAS  Google Scholar 

  • Nicholson CK, Calvert JW (2010) Hydrogen sulfide and ischemia–reperfusion injury. Pharmacol Res 62:289–297

    Article  PubMed  CAS  Google Scholar 

  • Olson KR (2009) Is hydrogen sulfide a circulating “gasotransmitter” in vertebrate blood? Biochim Biophys Acta 1787:856–863

    Article  PubMed  CAS  Google Scholar 

  • Olson KR (2011a) A practical look at the chemistry and biology of hydrogen sulfide. Antioxid Redox Signal. doi:10.1089/ars.2011.4401

  • Olson KR (2011b) Hydrogen sulfide is an oxygen sensor in the carotid body. Respir Physiol Neurobiol 179:103–110

    Google Scholar 

  • Olson KR (2011c) The therapeutic potential of hydrogen sulfide: separating hype from hope. Am J Physiol Regul Integr Comp Physiol 301:R297–R312

    Article  PubMed  CAS  Google Scholar 

  • Olson KR, Whitfield NL (2010) Hydrogen sulfide and oxygen sensing in the cardiovascular system. Antioxid Redox Signal 12:1219–1234

    Article  PubMed  CAS  Google Scholar 

  • Olson KR, Dombkowski RA, Russell MJ, Doellman MM, Head SK, Whitfield NL, Madden JA (2006) Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation. J Exp Biol 209:4011–4023

    Article  PubMed  CAS  Google Scholar 

  • Olson KR, Healy M, Qin J, Skovgaard N, Vulesevic B, Duff DW, Whitfield NL, Yang G, Wang R, Perry SF (2008) Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors. Am J Physiol Regul Integr Comp Physiol 295:R669–R680

    Article  PubMed  CAS  Google Scholar 

  • Olson KR, Whitfield NL, Bearden SE, St Leger J, Nilson E, Gao Y, Madden JA (2010) Hypoxic pulmonary vasodilation: a paradigm shift with a hydrogen sulfide mechanism. Am J Physiol Regul Integr Comp Physiol 298:R51–R60

    Article  PubMed  CAS  Google Scholar 

  • Paris D, Svoronos N, Bruno TJ (2002) Carbonyl sulfide: a review of its chemistry and properties. Ind Eng Chem Res 41:5321–5336

    Article  CAS  Google Scholar 

  • Parker ET, Cleaves HJ, Callahan MP, Dworkin JP, Glavin DP, Lazcano A, Bada JL (2011a) Prebiotic synthesis of methionine and other sulfur-containing organic compounds on the primitive Earth: a contemporary reassessment based on an unpublished 1958 Stanley Miller experiment. Orig Life Evol Biosph 41:201–212

    Article  PubMed  CAS  Google Scholar 

  • Parker ET, Cleaves HJ, Dworkin JP, Glavin DP, Callahan M, Aubrey A, Lazcano A, Bada JL (2011b) Primordial synthesis of amines and amino acids in a 1958 Miller H2S-rich spark discharge experiment. Proc Natl Acad Sci USA 108:5526–5531

    Article  PubMed  CAS  Google Scholar 

  • Parrino V, Kraus DW, Doeller JE (2000) ATP production from the oxidation of sulfide in gill mitochondria of the ribbed mussel Geukensia demissa. J Exp Biol 203:2209–2218

    PubMed  CAS  Google Scholar 

  • Peng YJ, Nanduri J, Raghuraman G, Souvannakitti D, Gadalla MM, Kumar GK, Snyder SH, Prabhakar NR (2010) H2S mediates O2 sensing in the carotid body. Proc Natl Acad Sci USA 107:10719–10724

    Article  PubMed  CAS  Google Scholar 

  • Petersen CL (1977) The effect of inhibitors on the oxygen kinetics of cytochrome c oxidase. Biochim Biophys Acta 460:299–307

    Article  PubMed  CAS  Google Scholar 

  • Poulton SW, Fralick PW, Canfield DE (2004) The transition to a sulphidic ocean approximately 1.84 billion years ago. Nature 431:173–177

    Article  PubMed  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 

  • Pratt AJ (2011) Prebiological evolution and the metabolic origins of life. Artif Life 17:203–217

    Article  PubMed  Google Scholar 

  • Ruehland C, Blazejak A, Lott C, Loy A, Erseus C, Dubilier N (2008) Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean Sea grass sediments. Environ Microbiol 10:3404–3416

    Article  PubMed  CAS  Google Scholar 

  • Schenk S, Kesselmeier J, Anders E (2004) How does the exchange of one oxygen atom with sulfur affect the catalytic cycle of carbonic anhydrase? Chemistry 10:3091–3105

    Article  PubMed  CAS  Google Scholar 

  • Searcy DG (2003) Metabolic integration during the evolutionary origin of mitochondria. Cell Res 13:229–238

    Article  PubMed  CAS  Google Scholar 

  • Searcy DG, Lee SH (1998) Sulfur reduction by human erythrocytes. J Exp Zool 282:310–322

    Article  PubMed  CAS  Google Scholar 

  • Sehnert SS, Jiang L, Burdick JF, Risby TH (2002) Breath biomarkers for detection of human liver diseases: preliminary study. Biomarkers 7:174–187

    Article  PubMed  CAS  Google Scholar 

  • Sheftel A, Stehling O, Lill R (2010) Iron–sulfur proteins in health and disease. Trends Endocrinol Metab 21:302–314

    Article  PubMed  CAS  Google Scholar 

  • Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11:703–714

    Article  PubMed  CAS  Google Scholar 

  • Studer SM, Orens JB, Rosas I, Krishnan JA, Cope KA, Yang S, Conte JV, Becker PB, Risby TH (2001) Patterns and significance of exhaled-breath biomarkers in lung transplant recipients with acute allograft rejection. J Heart Lung Transplant 20:1158–1166

    Article  PubMed  CAS  Google Scholar 

  • Szklarczyk R, Huynen MA (2010) Mosaic origin of the mitochondrial proteome. Proteomics 10:4012–4024

    Article  PubMed  CAS  Google Scholar 

  • Takamiya S, Fukuda K, Nakamura T, Aoki T, Sugiyama H (2010) Paragonimus westermani possesses aerobic and anaerobic mitochondria in different tissues, adapting to fluctuating oxygen tension in microaerobic habitats. Int J Parasitol 40:1651–1658

    Article  PubMed  CAS  Google Scholar 

  • Telezhkin V, Brazier SP, Cayzac S, Muller CT, Riccardi D, Kemp PJ (2009) Hydrogen sulfide inhibits human BK(Ca) channels. Adv Exp Med Biol 648:65–72

    Article  PubMed  CAS  Google Scholar 

  • Telezhkin V, Brazier SP, Cayzac SH, Wilkinson WJ, Riccardi D, Kemp PJ (2010) Mechanism of inhibition by hydrogen sulfide of native and recombinant BKCa channels. Respir Physiol Neurobiol 172:169–178

    Article  PubMed  CAS  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 20:1564–1574

    Article  PubMed  CAS  Google Scholar 

  • Tielens AG, Rotte C, van Hellemond JJ, Martin W (2002) Mitochondria as we don’t know them. Trends Biochem Sci 27:564–572

    Article  PubMed  CAS  Google Scholar 

  • Tiranti V, Viscomi C, Hildebrandt T, Di MI, 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 15:200–205

    Article  PubMed  CAS  Google Scholar 

  • Vairavamurthy A, Manowitz B, Luther GW III, Jeon Y (1993) Oxidation state of sulfur in thiosulfate and implications for anaerobic energy metabolism. Geochim Cosmochim Acta 57:1619–1623

    Article  CAS  Google Scholar 

  • Viscomi C, Burlina AB, Dweikat I, Savoiardo M, Lamperti C, Hildebrandt T, Tiranti V, Zeviani M (2010) Combined treatment with oral metronidazole and N-acetylcysteine is effective in ethylmalonic encephalopathy. Nat Med 16:869–871

    Article  PubMed  CAS  Google Scholar 

  • Völkel S, Grieshaber MK (1996) Mitochondrial sulfide oxidation in Arenicola marina. Evidence for alternative electron pathways. Eur J Biochem 235:231–237

    Article  PubMed  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 

  • Wacey D, Kilburn MR, Saunders M, Cliff J, Brasier MD (2011) Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nat Geosci 4:698–702

    Article  CAS  Google Scholar 

  • Wächtershäuser G (2007) On the chemistry and evolution of the pioneer organism. Chem Biodivers 4:584–602

    Article  PubMed  Google Scholar 

  • Ward PD (2006) Impact from the deep. Sci Am 295:64–71

    Article  PubMed  Google Scholar 

  • Wojcicka G, Jamroz-Wisniewska A, Atanasova P, Chaldakov GN, Chylinska-Kula B, Beltowski J (2010) Differential effects of statins on endogenous H(2)S formation in perivascular adipose tissue. Pharmacol Res 63:68–76

    Google Scholar 

  • Woodall GM, Smith RL, Granville GC (2005) Proceedings of the hydrogen sulfide health research and risk assessment symposium October 31 November 2, 2000. Inhal Toxicol 17:593–639

    Article  PubMed  CAS  Google Scholar 

  • Yong R, Searcy DG (2001) Sulfide oxidation coupled to ATP synthesis in chicken liver mitochondria. Comp Biochem Physiol B: Biochem Mol Biol 129:129–137

    Article  CAS  Google Scholar 

  • Zhao W, Zhang J, Lu Y, Wang R (2001) The vasorelaxant effect of H2S as a novel endogenous KATP channel opener. EMBO J 20:6008–6016

    Article  PubMed  CAS  Google Scholar 

  • Ziurys LM (2006) The chemistry in circumstellar envelopes of evolved stars: following the origin of the elements to the origin of life. Proc Natl Acad Sci USA 103:12274–12279

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The author wishes to thank Drs. S. Wohlgemuth and A. Pratt for suggestions and comments during the development of this manuscript and the students and colleagues who have made the major contributions in this field. Supported in part by National Science Foundation Grants IOS 0641436 and IOS 1051627.

Author information

Authors and Affiliations

  1. Indiana University School of Medicine South Bend, 1234 Notre Dame Avenue, South Bend, IN, 46617, USA

    Kenneth R. Olson

Authors
  1. Kenneth R. Olson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenneth R. Olson.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olson, K.R. Mitochondrial adaptations to utilize hydrogen sulfide for energy and signaling. J Comp Physiol B 182, 881–897 (2012). https://doi.org/10.1007/s00360-012-0654-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-012-0654-y

Keywords

Search

Navigation