Phylogeny of complex I

by Thorsten Friedrich and Dierk Scheide

The proton-pumping NADH:ubiquinone oxidoreductase is the first of the respiratory chain complexes providing the proton motive force required for energy consuming processes like the synthesis of ATP. The complex is found in many bacteria and in the mitochondria of most eucaryotes. The bacterial complex, in general, consists of 14 different subunits and works as NADH dehydrogenase. It has been brought into mitochondria by endosymbiosis. The mitochondrial complex contains in addition to the homologues of these 14 subunits at least 28 accessory proteins which do not directly participate in the electron and proton transport function.

A homologous complex which has 11 subunits in common with the respiratory complex I exists in cyanobacteria and chloroplasts. This complex most likely works as a NAD(P)H:plastoquinone oxidoreductase or ferredoxin:plastoquinone oxidoreductase being involved in a cyclic photosynthetic electron transport. Homologues of this 11 subunits are also present in archaea. The archaeal complex contains additional subunits which work as a F420H2 dehydrogenase.

Upon evolutionary division, the membrane-bound hydrogenases were equipped with individual substrate binding proteins and a few with other membraneous subunits. The progenitor of complex I lost its [NiFe] active site but most likely gained a quinone binding site. The membrane part of the complex was equipped with further membrane proteins by triplication of the transporter subunit NuoL and acquisition of the subunits NuoA, J and K. Homologues of this subunits are also found in bacterial Na+/H+- and K+ /H+-antiporters. Thus, the common ancestor of donor:quinone oxidoreductases of bacteria, archaea, mitochondria and chloroplasts emerged. This complex of eleven subunits might have worked as a ferredoxin:quinone oxidoreductase, but due to its more sophisticated membrane part, may have achieved a higher efficiency of energy transduction resulting in the H+/e- stoichiometry of 2. The eleven polypeptides of this complex most likely constitute the structural framework for proton translocation and quinone binding in the complex of all three domains of life.

Adaption of the NADH dehydrogenase module (NuoE, F, and G) led to the formation of the proton-pumping NADH:ubiquinone oxidoreductase present in bacteria and mitochondria. The NADH dehydrogenase module is also present in various bacterial and archaeal NAD(P)+-depending hydrogenases and formate dehydrogenases. Because these are soluble, non-energy converting enzymes, it is unlikely that this module contributes to energy coupling in complex I. Adaption of the F420H2 dehydrogenase subunit to the ancestral donor:quinone oxidoreductase led to the formation of the archaeal F420H2:quinone oxidoreductase. It remains an open question whether the complex I homologue of cyanobacteria was equipped with the NAD(P)H dehydrogenase module or the ferredoxin:NADPH reductase as a new electron input module or whether it evolved by alterations of the already existing hydrogenase module.

References

• Friedrich, T., Weidner, U., Nehls, U., Fecke, W., Schneider, R. & Weiss, H. (1993). Attempts to Define Distinct Parts of NADH:Ubiquinone Oxidoreductase (Complex I). J. Bioenerget. Biomembr. 25, 331.

• Friedrich, T., Steinmüller, K. & Weiss, H. (1995). The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett. 367, 107-111.

• Friedrich, T. & Weiss, H. (1996). Origin and Evolution of the proton-pumping NADH:ubiquinone oxidoreductase (complex I). In: Origin and evolution of biological energy conversion. (Baltscheffsky, H., ed.) New York: VCH Publishers, pp.205-220.

• Friedrich, T. & Weiss, H. (1997). Modular evolution of the Respiratory NADH:Ubiquinone Oxidoreductase and the Origin of its Modules. J. theoret. Biol. 187, 529-541.

• Friedrich, T. & Scheide, D. (2000). The respiratory complex I of Bacteria, Archaea, and Eucarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett. (2000), 479, 1-5.

• Friedrich, T. (2001). Complex I: A chimera of redox and conformation driven proton-pump ?. J. Bioenerget.Biomembr. 33, 169-177.