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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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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.
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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.

Mentions: Sequences of fungal proteins annotated as OXPHOS components were retrieved from the KEGG database [11] and used as queries for blastp searches against the proteins encoded in 60 fully-sequenced fungal genomes (see figure 1 and Methods section). A phylogenetic analysis was performed on each set of homologous proteins to derive a phylogenetic tree. This tree was used to establish orthology and paralogy relationships using a species-overlap algorithm that has been described earlier [12]. This phylogeny-based approach to orthology detection, approaches more closely the original definition of orthology and reflects more appropriately the complex evolutionary relationships within protein families [13,14]. The presence of the different components of the respiratory pathway in the species surveyed is summarized in figures 2, 3 and 4. Overall, our results agree with those reported by Lavin et. al in the 27 species that both surveys have in common [9]. That the two approaches render so similar results, indicates that, despite using different approaches both methods have a similar stringency in the detection of OXPHOS components in this taxonomic range. In addition, our study extends the information on the distribution of components of the respiratory pathway to 33 additional species. The main advantage of our approach, however, is more qualitative than quantitative. By performing phylogenetic analyses on every protein family, we can readily obtain information on duplication events affecting components of the respiratory pathway, an important evolutionary process that was ignored in the previous study. Recognizing gene duplications is important, since this process is considered one of the main processes that drive functional innovation [15]. Our study reveals that duplication events have affected the OXPHOS pathway extensively. Overall, we detect duplications in 76% of the families surveyed. These results were similar (duplications in 75% of the families surveyed), when more stringent cut-offs for homology detection were applied (see figures S1, S2 and S3 in the additional file 1). Such high proportion of duplications is not the result of errors in the annotation or assembly of the genomes. We controlled for this by inspecting manually every duplication case to discard dubious cases. Moreover, even when species-specific duplications in which duplicates had more than 95% identity at the nucleotide level or all duplications from the recently assembled genomes Postia placenta and Puccina graminis were not taken into account, the fraction of OXPHOS families with a duplication event remained high (71% and 74%, respectively). Zygomycota, in particular, present the highest proportion of duplicated proteins in the OXPHOS pathway. For instance, we found duplications in 60% of the genes involved in Rhizopus oryzae OXPHOS pathway. A large percentage of these duplications (82%) can be mapped specifically to the R. oryzae lineage or to the lineage preceding the separation of R. oryzae and Phycomyces blakesleeanus and thus are specific of Zygomycota species. This large amount of lineage specific duplications seems to be general in R. oryzae and P. blakesleeanus (unpublished observation from our group). An interesting possibility is that the ancestors of these organisms underwent a Whole Genome Duplication (WGD) event, similar to that described for Saccharomyces [16]. This possibility has recently been confirmed for R. oryzae [17], in a comprehensive study that catalogues duplicated regions where the gene order is conserved. Consistently with our results, a duplication of nearly all subunits of the protein complexes associated with respiratory electron transport chains is detected, although our phylogeny-based approach detects additional, more ancestral, duplications that are not associated to the WGD event.


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)

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

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

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.
Mentions: Sequences of fungal proteins annotated as OXPHOS components were retrieved from the KEGG database [11] and used as queries for blastp searches against the proteins encoded in 60 fully-sequenced fungal genomes (see figure 1 and Methods section). A phylogenetic analysis was performed on each set of homologous proteins to derive a phylogenetic tree. This tree was used to establish orthology and paralogy relationships using a species-overlap algorithm that has been described earlier [12]. This phylogeny-based approach to orthology detection, approaches more closely the original definition of orthology and reflects more appropriately the complex evolutionary relationships within protein families [13,14]. The presence of the different components of the respiratory pathway in the species surveyed is summarized in figures 2, 3 and 4. Overall, our results agree with those reported by Lavin et. al in the 27 species that both surveys have in common [9]. That the two approaches render so similar results, indicates that, despite using different approaches both methods have a similar stringency in the detection of OXPHOS components in this taxonomic range. In addition, our study extends the information on the distribution of components of the respiratory pathway to 33 additional species. The main advantage of our approach, however, is more qualitative than quantitative. By performing phylogenetic analyses on every protein family, we can readily obtain information on duplication events affecting components of the respiratory pathway, an important evolutionary process that was ignored in the previous study. Recognizing gene duplications is important, since this process is considered one of the main processes that drive functional innovation [15]. Our study reveals that duplication events have affected the OXPHOS pathway extensively. Overall, we detect duplications in 76% of the families surveyed. These results were similar (duplications in 75% of the families surveyed), when more stringent cut-offs for homology detection were applied (see figures S1, S2 and S3 in the additional file 1). Such high proportion of duplications is not the result of errors in the annotation or assembly of the genomes. We controlled for this by inspecting manually every duplication case to discard dubious cases. Moreover, even when species-specific duplications in which duplicates had more than 95% identity at the nucleotide level or all duplications from the recently assembled genomes Postia placenta and Puccina graminis were not taken into account, the fraction of OXPHOS families with a duplication event remained high (71% and 74%, respectively). Zygomycota, in particular, present the highest proportion of duplicated proteins in the OXPHOS pathway. For instance, we found duplications in 60% of the genes involved in Rhizopus oryzae OXPHOS pathway. A large percentage of these duplications (82%) can be mapped specifically to the R. oryzae lineage or to the lineage preceding the separation of R. oryzae and Phycomyces blakesleeanus and thus are specific of Zygomycota species. This large amount of lineage specific duplications seems to be general in R. oryzae and P. blakesleeanus (unpublished observation from our group). An interesting possibility is that the ancestors of these organisms underwent a Whole Genome Duplication (WGD) event, similar to that described for Saccharomyces [16]. This possibility has recently been confirmed for R. oryzae [17], in a comprehensive study that catalogues duplicated regions where the gene order is conserved. Consistently with our results, a duplication of nearly all subunits of the protein complexes associated with respiratory electron transport chains is detected, although our phylogeny-based approach detects additional, more ancestral, duplications that are not associated to the WGD event.

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