Comparative genomics of the oxidative phosphorylation system in fungi José L. Lavín, José A. Oguiza, Lucía Ramírez, Antonio G. Pisabarro * Departamento de Producción Agraria, Universidad Pública de Navarra, 31006 Pamplona, Spain article info Article history: Received 31 January 2008 Accepted 18 June 2008 Available online 3 July 2008 Keywords: Comparative genomics Mitochondria OXPHOS Genomic analysis Mitochondrial genome Nuclear genome abstract In this study, we have carried out an in silico analysis of the available mitochondrial and nuclear genomes of fungi in order to identify the oxidative phosphorylation (OXPHOS) proteome, the complete set of pro- teins that perform the OXPHOS in mitochondria. The presence of OXPHOS proteins has been investigated in 27 nuclear and 52 mitochondrial genomes of fungi. Comparative genomics reveals a high conservation of the OXPHOS system within each fungal phyla, and notable differences between the OXPHOS proteo- mes of the fungal phyla. The most striking differences concerned Complexes I and V. The absence of Com- plex I has been previously described in various species of Ascomycota and Microsporidia, and the NDUFB4 and NURM accessory subunits of Complex I appear to be specific of fungi belonging to the sub- phylum Pezizomycotina. In addition, the Complex V essential subunit ATP14 appears to be specific of two subphyla of Ascomycota: the Saccharomycotina and Pezizomycotina. Ó 2008 Elsevier Inc. All rights reserved. 1. Introduction Mitochondria are essential for energy production of all eukaryotic respiring cells (Ryan and Hoogenraad, 2007; Saraste, 1999). It is widely accepted that these eukaryotic organelles are derived from the capture of an a-Proteobacterial endosymbi- ont by a nucleus-containing eukaryotic host introducing the oxi- dative phosphorylation (OXPHOS) system into eukaryotes (Kurland and Andersson, 2000; Lang et al., 1999). The mitochon- drial genome is a remnant of the endosymbiont’s genome and the majority of the mitochondrial proteome is encoded by the nuclear genome, synthesized in the cytosol and selectively im- ported into the organelle. In the OXPHOS system, consisting of the mitochondrial respira- tory pathway and the ATP synthase, electrons are transferred from NADH to molecular oxygen and this electron transfer is coupled to proton translocation across the inner mitochondrial membrane that is used to generate cellular energy in the form of adenosine triphosphate (ATP) (Saraste, 1999). The OXPHOS system contains large enzyme complexes formed by a combination of subunits en- coded by both the mitochondrial and nuclear genomes (D ´ Elia et al., 2006; Garesse and Vallejo, 2001). This metabolic pathway is orga- nized in five multipolypeptide complexes embedded in the lipid bi- layer of the inner mitochondrial membrane: NADH dehydrogenase (Complex I), succinate dehydrogenase (Complex II), cytochrome bc1 (Complex III), cytochrome c oxidase (COX, Complex IV), and ATP synthase (Complex V). Some of the OXPHOS complexes phys- ically associate with each other to form supramolecular structures termed OXPHOS supercomplexes or respirosomes (Boekema and Braun, 2007). Mitochondrial genome encodes only a limited num- ber of the essential components of Complexes I, III, IV and V (Burger et al., 1996; Gray et al., 2001). Complex I is a large multi- subunit enzyme containing a core of 14 central subunits and a var- iable number of accessory subunits found specifically in the eukaryotic Complex I (Gabaldón et al., 2005). Seven subunits of the eukaryotic core Complex I are nuclearly encoded, and the other seven subunits are mitochondrially encoded (Cardol et al., 2004, 2005; Gabaldón et al., 2005; Videira and Duarte, 2002). Complex II contains only four nuclearly encoded polypeptides, and Complex III is an oligomeric membrane protein. Cytochrome c (CYTC) is a small heme protein that mediates the electron transfer between Complexes III and IV. Complex V catalyzes the final step of OX- PHOS, and separates into a hydrophilic subcomplex F 0 involved in proton translocation and a hydrophobic subcomplex F 1 that cat- alyzes ATP synthesis (Velours and Arselin, 2000). The OXPHOS sys- tem is strictly dependent on oxygen, and during conditions of oxygen deprivation ATP synthesis is halted, eventually resulting in cell death. However, yeast and some other eukaryotes can sur- vive by fermentation in the absence of oxygen. The kingdom Fungi comprise morphologically and biochemi- cally diverse eukaryotic organisms that are divided in five phyla: Ascomycota, Basidiomycota, Glomeromycota, Zygomycota and Chytridiomycota (James et al., 2006). The majority of characterized fungi contain mitochondria, and frequently fungal mitochondria have additional OXPHOS components such as alternative oxidase (AOX) and/or alternative NAD(P)H dehydrogenases (Joseph-Horne 1087-1845/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.fgb.2008.06.005 * Corresponding author. Fax: +34 948 169732. E-mail address: gpisabarro@unavarra.es (A.G. Pisabarro). Fungal Genetics and Biology 45 (2008) 1248–1256 Contents lists available at ScienceDirect Fungal Genetics and Biology journal homepage: www.elsevier.com/locate/yfgbi