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Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires.

Zmasek CM, Godzik A - Genome Biol. (2011)

Bottom Line: This trend is so consistent that clustering of genomes according to their functional profiles results in an organization similar to the tree of life.Furthermore, our results indicate that metabolic functions lost during animal evolution are likely being replaced by the metabolic capabilities of symbiotic organisms such as gut microbes.While protein domain gains and losses are common throughout eukaryote evolution, losses oftentimes outweigh gains and lead to significant differences in functional profiles.

View Article: PubMed Central - HTML - PubMed

Affiliation: Program in Bioinformatics and Systems Biology, Sanford-Burnham Medical Research Institute, La Jolla, CA 92037, USA.

ABSTRACT

Background: Genome size and complexity, as measured by the number of genes or protein domains, is remarkably similar in most extant eukaryotes and generally exhibits no correlation with their morphological complexity. Underlying trends in the evolution of the functional content and capabilities of different eukaryotic genomes might be hidden by simultaneous gains and losses of genes.

Results: We reconstructed the domain repertoires of putative ancestral species at major divergence points, including the last eukaryotic common ancestor (LECA). We show that, surprisingly, during eukaryotic evolution domain losses in general outnumber domain gains. Only at the base of the animal and the vertebrate sub-trees do domain gains outnumber domain losses. The observed gain/loss balance has a distinct functional bias, most strikingly seen during animal evolution, where most of the gains represent domains involved in regulation and most of the losses represent domains with metabolic functions. This trend is so consistent that clustering of genomes according to their functional profiles results in an organization similar to the tree of life. Furthermore, our results indicate that metabolic functions lost during animal evolution are likely being replaced by the metabolic capabilities of symbiotic organisms such as gut microbes.

Conclusions: While protein domain gains and losses are common throughout eukaryote evolution, losses oftentimes outweigh gains and lead to significant differences in functional profiles. Results presented here provide additional arguments for a complex last eukaryotic common ancestor, but also show a general trend of losses in metabolic capabilities and gain in regulatory complexity during the rise of animals.

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An overview of a current model of eukaryote evolution [30,67]. Numbers in brackets indicate the number of genomes from each branch analyzed in this work.
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Figure 1: An overview of a current model of eukaryote evolution [30,67]. Numbers in brackets indicate the number of genomes from each branch analyzed in this work.

Mentions: We analyzed complete sets of predicted proteins for 114 eukaryotic genomes, including 73 from opisthokonta (38 metazoa, 1 choanoflagellate, and 34 fungi), 3 from amoebozoa, 17 from archaeplastida, 16 from chromalveolata, and 5 from excavate, thus covering 5 of the 6 eukaryotic 'supergroups' [30,31] (we were unable to obtain any complete genomes for the 'supergroup' Rhizaria [32]), for the presence of protein domains, as defined by Pfam [25] (Figure 1; Additional file 1) The number of distinct protein domains varies from roughly 2,000 in the free living unicellular ciliate Paramecium tetraurelia to 3,140 in one of the simplest multicellular animals, Trichoplax adhaerens, to about 4,240 in humans (Figure 2c; for detailed counts see Additional files 2, 3, and 4). These numbers follow the expected trend of genomes of more complex organisms containing more domains; however, they include many apparent contradictions where more morphologically complex organisms contain fewer domains than less complex ones. To understand the evolutionary history of the observed domain distribution in extant species, we reconstructed the domain content of ancestral genomes, specifically those lying at internal nodes corresponding to major branching points in the evolution of eukaryotes. Since independent evolution of the same domain more than once is highly unlikely, we used Dollo parsimony, which, when applied to domain content, states that each domain can be gained only once, and seeks to minimize domain losses, to reconstruct the Pfam domain repertoire of ancestral eukaryotes [33-38] (Figure 2).


Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires.

Zmasek CM, Godzik A - Genome Biol. (2011)

An overview of a current model of eukaryote evolution [30,67]. Numbers in brackets indicate the number of genomes from each branch analyzed in this work.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3091302&req=5

Figure 1: An overview of a current model of eukaryote evolution [30,67]. Numbers in brackets indicate the number of genomes from each branch analyzed in this work.
Mentions: We analyzed complete sets of predicted proteins for 114 eukaryotic genomes, including 73 from opisthokonta (38 metazoa, 1 choanoflagellate, and 34 fungi), 3 from amoebozoa, 17 from archaeplastida, 16 from chromalveolata, and 5 from excavate, thus covering 5 of the 6 eukaryotic 'supergroups' [30,31] (we were unable to obtain any complete genomes for the 'supergroup' Rhizaria [32]), for the presence of protein domains, as defined by Pfam [25] (Figure 1; Additional file 1) The number of distinct protein domains varies from roughly 2,000 in the free living unicellular ciliate Paramecium tetraurelia to 3,140 in one of the simplest multicellular animals, Trichoplax adhaerens, to about 4,240 in humans (Figure 2c; for detailed counts see Additional files 2, 3, and 4). These numbers follow the expected trend of genomes of more complex organisms containing more domains; however, they include many apparent contradictions where more morphologically complex organisms contain fewer domains than less complex ones. To understand the evolutionary history of the observed domain distribution in extant species, we reconstructed the domain content of ancestral genomes, specifically those lying at internal nodes corresponding to major branching points in the evolution of eukaryotes. Since independent evolution of the same domain more than once is highly unlikely, we used Dollo parsimony, which, when applied to domain content, states that each domain can be gained only once, and seeks to minimize domain losses, to reconstruct the Pfam domain repertoire of ancestral eukaryotes [33-38] (Figure 2).

Bottom Line: This trend is so consistent that clustering of genomes according to their functional profiles results in an organization similar to the tree of life.Furthermore, our results indicate that metabolic functions lost during animal evolution are likely being replaced by the metabolic capabilities of symbiotic organisms such as gut microbes.While protein domain gains and losses are common throughout eukaryote evolution, losses oftentimes outweigh gains and lead to significant differences in functional profiles.

View Article: PubMed Central - HTML - PubMed

Affiliation: Program in Bioinformatics and Systems Biology, Sanford-Burnham Medical Research Institute, La Jolla, CA 92037, USA.

ABSTRACT

Background: Genome size and complexity, as measured by the number of genes or protein domains, is remarkably similar in most extant eukaryotes and generally exhibits no correlation with their morphological complexity. Underlying trends in the evolution of the functional content and capabilities of different eukaryotic genomes might be hidden by simultaneous gains and losses of genes.

Results: We reconstructed the domain repertoires of putative ancestral species at major divergence points, including the last eukaryotic common ancestor (LECA). We show that, surprisingly, during eukaryotic evolution domain losses in general outnumber domain gains. Only at the base of the animal and the vertebrate sub-trees do domain gains outnumber domain losses. The observed gain/loss balance has a distinct functional bias, most strikingly seen during animal evolution, where most of the gains represent domains involved in regulation and most of the losses represent domains with metabolic functions. This trend is so consistent that clustering of genomes according to their functional profiles results in an organization similar to the tree of life. Furthermore, our results indicate that metabolic functions lost during animal evolution are likely being replaced by the metabolic capabilities of symbiotic organisms such as gut microbes.

Conclusions: While protein domain gains and losses are common throughout eukaryote evolution, losses oftentimes outweigh gains and lead to significant differences in functional profiles. Results presented here provide additional arguments for a complex last eukaryotic common ancestor, but also show a general trend of losses in metabolic capabilities and gain in regulatory complexity during the rise of animals.

Show MeSH