Phylogenomics of the oxidative phosphorylation in fungi reveals extensive gene duplication followed by functional divergence

Abstract

Background: Oxidative phosphorylation is central to the energy metabolism of the cell. Due to adaptation to different life-styles and environments, fungal species have shaped their respiratory pathways in the course of evolution. To identify the main mechanisms behind the evolution of respiratory pathways, we conducted a phylogenomics survey of oxidative phosphorylation components in the genomes of sixty fungal species.

Results: Besides clarifying orthology and paralogy relationships among respiratory proteins, our results reveal three parallel losses of the entire complex I, two of which are coupled to duplications in alternative dehydrogenases. Duplications in respiratory proteins have been common, affecting 76% of the protein families surveyed. We detect several instances of paralogs of genes coding for subunits of respiratory complexes that have been recruited to other multi-protein complexes inside and outside the mitochondrion, emphasizing the role of evolutionary tinkering.

Conclusions: Processes of gene loss and gene duplication followed by functional divergence have been rampant in the evolution of fungal respiration. Overall, the core proteins of the respiratory pathways are conserved in most lineages, with major changes affecting the lineages of microsporidia, Schizosaccharomyces and Saccharomyces/Kluyveromyces due to adaptation to anaerobic life-styles. We did not observe specific adaptations of the respiratory metabolism common to all pathogenic species.

Figure 1

Species table. List of species and their corresponding three-letter codes used in the analysis. The tree on the left represents the fungal species tree as described by a recent analysis [7]. The names of the major fungal taxa, as provided by the source database, are indicated to the right of the tree. A list of synonyms for this species names is provided in the additional file 1. Sources of the sequences are: JGI http://www.jgi.doe.gov, Broad Institute http://broad.mit.edu, YGOB http://wolfe.gen.tcd.ie/ygob, SGD http://www.yeastgenome.org, Fungal Genomes http://fungalgenomes.org, Genolevures http://www.genolevures.org/, integr8 http://www.ebi.ac.uk/integr8, Candida genome database http://www.candidagenome.org, NCBI http://www.ncbi.nlm.nih.gov.

Figure 2

Complex I. Phylogenetic distribution across 60 fungal species of Complex I subunits. Absences of a corresponding ortholog in a given species is indicated with a blank square or a crossed green square. Crossed green squares indicate that no ortholog was found but at least one paralog is present. Presence of orthologs is indicated with uncrossed green squares. The different colour intensities correspond to the number of homologs of the query protein found in that specific genome. The species are ordered according to their phylogenetic position in the fungal species tree [7].

Figure 3

Complex II-III-IV. Phylogenetic distribution across 60 fungal species of subunits from Complexes II, III and IV subunits. Symbols and codes as in figure 2.

Figure 4

Complex V-Alternative oxidases and dehydrogenases. Phylogenetic distribution across 60 fungal species of Complex V and alternative oxidases and dehydrogenases. Symbols and codes as in figure 2.

Figure 5

Phylogenetic tree representing the evolution of the alternative dehydrogenase protein family. The model used was WAG and approximate Likelihood (aLRT) support of the tree partitions is indicated if lower than 0.9. Duplications involving S. cerevisiae were marked with coloured boxes, while those involving N. crassa are indicated with white boxes. The species name is followed by the protein name according to the database from which the sequences where retrieved. Functional annotations were taken from Saccharomyces Genome Database (S. cerevisiae) [39] and the Broad Institute (N. crassa). This tree represents a subset of the sequences used in the analysis, the tree with the full set of sequences can be accessed in the additional file 1.

Figure 6

Phylogenetic tree representing the evolution of the ACPM protein family. The model used was WAG and approximate Likelihood (aLRT) support of the tree partitions is indicated. This tree represents a subset of the sequences used in the analysis, the tree with the full set of sequences can be accessed in the additional file 1.