Has Sulfolobus an Archaic Respiratory System? Structure, Function and Genes of its Components

Abstract

The electron transport system of Sulfolobus acidocaldarius has been shown to act as a respiration driven proton pump. Essentially it is composed of three functional units: the NADH-and substrate dehydrogenases, caldariella quinone as a pool of bound hydrogen, and one or two terminal oxidases catalyzing its reoxidation by molecular oxygen. The latter systems contain only FeS proteins, b - and a -type cytochromes; c -type cytochromes are absent. The cytochrome aa 3 from Sulfolobus is the first heme- a containing terminal oxidase shown to act as a quinol oxidase. Its redox centers were investigated by redox potentiometry, EPR- and Raman-resonance spectroscopy, revealing a typical binuclear heme- a /Cu center, however displaying unusual structural interaction between the formyl substituents and the protein environment; the redox potentials of low and high spin centers were titrated. A cytochrome a 587 atypical for any other species emerged to contain a low spin, low potential heme- a center, mimicing the function of a b -type cytochrome and likely to be the product of the SOX -C gene from the SOX operon ( Lübben et al., 1992). The aa 3 oxidase when reconstituted into liposomes is shown to generate a proton motive force. Though Sulfolobus contains no equivalent to the bc 1 complex of classical respiratory chains, in addition to the caldariella quinol oxidase a Rieske-type FeS protein could be detected in its plasma membrane; it was isolated and characterized by EPR, strongly suggesting a participation in respiratory electron transport. Its redox potential displays significant pH dependence revealing two distinct pKs. It remains to be established whether it interacts with the aa 3 oxidase or other electron carriers. A cytochrome b 562 appears to be present constitutively in small amount, while cytochrome- b 558 is the major heme- b containing compound in the membrane of Sulfolobus . A previously envisaged function as an alternate terminal oxidase is still questionable. Recently conditions were found allowing to modulate its expression dramatically, leading to almost complete suppression of cytochrome- b 558 . Based on differential spectroscopy and redox titrations a tentative scheme of the electron transport system from Sulfolobus is proposed. Sequence comparisons are discussed with regard to the question, as to whether it resembles a primitive “archaic” precursor form of more complex “modern” respiratory systems, or whether it evolved by aquisition and adaptation of “foreign” genes.