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.
Homologues of the functional modules of the complex are
also found in
other bacterial electron transfer and ion transport proteins. This
implies
that complex I most probably originated by fusion of preexisting
protein
assemblies constituting modules for electron transfer and proton
transport.
Sequence comparisons revealed that complex I evolved from electron
transfer
proteins (the progenitors of NuoB and D, E. coli nomenclature), which
are
also present in nowadays soluble hydrogenases. The combination with the
progenitors of the ferredoxin NuoI, the quinone-binding protein NuoH,
the
ion-translocating protein NuoL and a protein of yet unknown function
(NuoC)
gave rise to a common ancestor of complex I and a family of
membrane-bound
multisubunit hydrogenases. This ancestral enzyme might have worked
already
as a proton-pumping hydrogen:ferredoxin oxidoreductase.
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
1) 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.
2) 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.
3) 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.
4) 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.
5) 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., submitted.
Unrooted phylogenetic tress of subunits:
NuoB - GIF
13 kB
NuoD - GIF
11 kB
NuoH - GIF
15 kB
