Non-classical structures and association of the OXPHOS complexes in Euglena gracilis and Polytomella sp.

To date, the idea that the OXPHOS complexes can associate with each other in larger structures named supercomplexes [1] is generally accepted. This association can allow a more efficient transport of electrons to minimize the generation of reactive oxygen species during electron transfer reactions and can also be involved in the regulation of the mitochondrial metabolism in response to different stimuli, carbon sources or stress conditions. Recently, the arising studies outside the classical models yeast and bovine mitochondria brought to light many unusual characteristics in the ATP synthase from a wide variety of organisms. Due to this, the dimer nature of the mitochondrial ATP synthase is no longer a matter of debate. Given the large structural differences among the peripheral stator and dimerization modules of mitochondrial ATP synthases described so far, it is of relevance to study a wider number of species to gain insight into the structural diversity of their OXPHOS complexes.
Recently, our group showed that at least 41 of the non-canonical subunits reported in trypanosomes are also present in Euglena complexes along with 48 classical subunits described in other eukaryotes including green plants [2]. Further purification of the complexes I, III, IV and V by liquid chromatography after solubilization with n-β-dodecyl-maltoside and the subsequent analysis by single-particle analysis from transmission electron microscopy revealed some unusual features in Euglena respiratory complexes. In the case of complex V the structures of both the catalytic and central rotor parts are conserved while other structural features are original, including a large membrane-spanning region joining the monomers, an external peripheral stalk and a structure that goes through the membrane and reaches the inter membrane space below the c-ring [3]. Complex I also shows an unusually long matricial arm. Complex IV shows an atypical shape compared to that of the bovine one. An unusual association between complexes I and V can be observed when the membranes are extracted with the mild detergent digitonin.
Other case of atypical subunit composition is the complex V of chlorophycean algae. Each monomer of the enzyme has 17 polypeptides, eight of which are the conserved, main functional components, and nine polypeptides (Asa1 to Asa9) unique to this lineage that form the robust peripheral stalk in this complex [4]. This complex presents highly stable dimeric and tetrameric structures, and the respiratory complexes have an unusual capacity to reassociate in vitro and restore the functional respirasome.