Journal of Comparative Physiology B

, Volume 182, Issue 7, pp 881–897 | Cite as

Mitochondrial adaptations to utilize hydrogen sulfide for energy and signaling

Review

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.

Keywords

H2S metabolism Evolution H2S toxicity Sulfur: quinone: oxidoreductase  Oxygen sensing 

Notes

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.

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Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Indiana University School of Medicine South BendSouth BendUSA

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