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

Marcet-Houben M, Marceddu G, Gabaldón T - BMC Evol. Biol. (2009)

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Comparative Genomics, Centre for Genomics Regulation, 08003 Barcelona, Spain. mmarcet@crg.es

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.

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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.
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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.

Mentions: Our results confirm earlier findings of a complete loss of the OXPHOS pathway in microsporidia [18] and the absence of most components of Complex I in Schizosaccharomyces and Saccharomycetales [4]. We are able to find most of the subunits of complex I in the Taphrinomycotina species Pneumocystis carinii, suggesting that the event of gene loss occurred after the diversification of Pneumocystis and Schizosaccharomyces lineages. The apparent multiple absences of Complex I subunits, and those of other complexes, in P. carinii is probably related to a low coverage of the genome sequence for this organism. Similarly, the presence of a complete repertoire of Complex I subunits in all species in the Candida cluster and the lack of this complex in all surveyed species from the Saccharomyces/Kluyveromyces clade, situates the loss of Complex I in the latter lineage. Remarkably, the two independent losses of Complex I in the Taphrinomycotina and Saccharomyces/Kluyveromyces clades are concomitant with independent expansions of their alternative NADH dehydrogenases repertoire by virtue of gene duplications. Alternative NADH dehydrogenases bypass Complex I electron transport, oxidizing NADH without pumping of protons. The duplication of alternative NADH dehydrogenases (Figure 5) might have provided a selective advantage for yeast species using predominantly fermentative metabolism, due to adaptation to anaerobic environments. Excess of NADH causes a problem under fermentative anaerobic growth, since it prevents further oxidation of substrates due to a lack of a sufficient NAD+ pool to accept electrons. Thus, the diversification of pathways to further oxidize NADH would have been beneficial in such conditions. The loss of Complex I in the same evolutionary periods might also be related to adaptation to fermentative growth. It is unclear which of the processes preceded the other or whether both processes were concomitant. A higher taxon sampling within the Saccharomycotina and Taphrinomycotina might help to solve this issue in the future. Also coupled with Complex I loss, and in line with adaptations to anaerobic environments in the abovementioned lineages, we observe the loss of alternative oxidases.


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

Marcet-Houben M, Marceddu G, Gabaldón T - BMC Evol. Biol. (2009)

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.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2803194&req=5

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.
Mentions: Our results confirm earlier findings of a complete loss of the OXPHOS pathway in microsporidia [18] and the absence of most components of Complex I in Schizosaccharomyces and Saccharomycetales [4]. We are able to find most of the subunits of complex I in the Taphrinomycotina species Pneumocystis carinii, suggesting that the event of gene loss occurred after the diversification of Pneumocystis and Schizosaccharomyces lineages. The apparent multiple absences of Complex I subunits, and those of other complexes, in P. carinii is probably related to a low coverage of the genome sequence for this organism. Similarly, the presence of a complete repertoire of Complex I subunits in all species in the Candida cluster and the lack of this complex in all surveyed species from the Saccharomyces/Kluyveromyces clade, situates the loss of Complex I in the latter lineage. Remarkably, the two independent losses of Complex I in the Taphrinomycotina and Saccharomyces/Kluyveromyces clades are concomitant with independent expansions of their alternative NADH dehydrogenases repertoire by virtue of gene duplications. Alternative NADH dehydrogenases bypass Complex I electron transport, oxidizing NADH without pumping of protons. The duplication of alternative NADH dehydrogenases (Figure 5) might have provided a selective advantage for yeast species using predominantly fermentative metabolism, due to adaptation to anaerobic environments. Excess of NADH causes a problem under fermentative anaerobic growth, since it prevents further oxidation of substrates due to a lack of a sufficient NAD+ pool to accept electrons. Thus, the diversification of pathways to further oxidize NADH would have been beneficial in such conditions. The loss of Complex I in the same evolutionary periods might also be related to adaptation to fermentative growth. It is unclear which of the processes preceded the other or whether both processes were concomitant. A higher taxon sampling within the Saccharomycotina and Taphrinomycotina might help to solve this issue in the future. Also coupled with Complex I loss, and in line with adaptations to anaerobic environments in the abovementioned lineages, we observe the loss of alternative oxidases.

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Comparative Genomics, Centre for Genomics Regulation, 08003 Barcelona, Spain. mmarcet@crg.es

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.

Show MeSH
Related in: MedlinePlus