|Dennis G. Searcy
Professor of University of Massachusetts
Cellular Evolution and Physiology
Molecular sequence data indicate that mitochondria originated from purple sulfide-oxidizing bacteria and the cytoplasm originated from sulfur-reducing Archaea. Thus, both the mitochondria and cytoplasm evolved from sulfur-specialists. We hypothesize that the initial symbiosis was between a host cell that produced H2S and a bacterial symbiont that oxidized it.
If such an hypothesis is true, then sulfur metabolism is a primitive shared feature of all eukaryotes, and vestiges of it may still be present in modern cells. Our observations confirm that. We have found that mitochondria are avid sulfide oxidizers, and can couple the process to ATP production. That contradicts the widespread view that sulfide is simply a metabolic poison
In regard to cytoplasmic metabolism, all cells tested (animals, plants, fungi, and various protists) vigorously produced H2S. To observe this, it is necessary to prevent mitochondrial sulfide consumption, and that was done either by removing the O2, or by using inhibitors such as cyanide, or by cellular fractionation. In those conditions the eukaryotic cytoplasms did indeed produce H2S. In a mitochondrion-free cytoplasmic fraction, sulfide production occurred even in aerobic condtions, and that was an unexpected, remarkable observation.
Current research involves the "Sulfidostat", an instrument designed to measure sulfide consumption at concentrations as low as 10-12 M sulfide. That is crucial because even 1 µM sulfide can inhibit respiration, explaining why mitochondrial sulfide consumption had not been described previously.
Questions remain such as: (1) Cells can produce H2S even without added sulfur, indicating that a reservoir of reducible sulfur exists. If so, what is its chemical nature, and how much is there? (2) What enzyme produces the H2S, and what is the electron donor? (3) In typical eukaryotic cells, does sulfur cycle endlessly between cytoplasm and mitochondria? (4) What are the benefits of sulfur reduction? Is it a form of mineral respiration in which sulfur can substitute for O2, at least to some degree?
Searcy, D.G. and M.A. Peterson. 2004. Hydrogen sulfide consumption measured at low steady state concentrations using a Sulfidostat. Anal. Biochem. 324: 269-275.
Searcy, D.G. 2003. Metabolic integration during the evolutionary origin of mitochondria. Cell Research 13: 229-238.
Searcy, D. G. 2001. Nutritional syntrophies and consortia as models for the origin of mitochondria. In: Symbiosis: Mechanisms and Model Systems. J. Seckbach, ed., Kluwer Academic Publishers, Dordrecht. Pps. 163-183.
Yong, R. and D.G. Searcy. 2001. Hydrogen sulfide oxidation by rooster liver mitochondria. Comp. Biochem. Physiol. B 129: 129-137.
Searcy, D.G. and S.H. Lee. 1998. Sulfur reduction by human red blood cells. J. Exp. Zool. 282: 310-322.
Searcy, D.G., S.H. Lee, D. Gleeson, R. Yong, K. Abderazzaq, and G. Dowd. 1998. Mitochondrial origin by sulfur symbiosis. In: From Symbiosis to Eukaryotism - ENDOCYROBIOLOGY VII (E. Wagner et al., eds), Geneva University Press, p. 43-51.
Searcy, D.G., J.P. Whitehead, and M.J. Maroney. 1995. Interaction of Cu,Zn superoxide dismutase with hydrogen sulfide. Arch. Biochem. Biophys. 318: 251-263.
Searcy, D.G. 1992. Origins of mitochondria and chloroplasts from sulfur-based symbioses. In Origins and Evolution of Prokaryotic and Eukaryotic Cells, H. Hartman and K. Matsuno, eds., World Scientific Publishing, Singapore, pps. 47-87.
Searcy, D.G. and W.G. Hixon. 1991. Cytoskeletal origins in sulfur-metabolizing archaebacteria. BioSystems 25: 1-11 and BioSystems 29: 151-160.
Searcy, D.G. 1987. Phylogenetic and phenotypic relationships between the eukaryotic nucleocytoplasm and thermophilic archaebacteria. Ann. NY Acad. Sci. 503: 168-179.
Searcy, D.G. 1986. The Archaebacterial Histone "HTa". In: Bacterial Chromatin, C.O. Gualerzi and C.L. Pon, eds. Springer-Verlag, Berlin, pp. 175-184.
Stein, D.B. and D.G. Searcy. 1978. Physiologically important stabilization of DNA by a prokaryotic histone-like protein. Science 202: 219-221.