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

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.

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.

Figure 2

Domain gains and losses during eukaryote evolution. (a) Inferred domainome sizes for ancestral genomes on the path from the LECA to mammals are shown on the left. (b) The numbers of gained protein domains per branch (edge), inferred by Dollo parsimony, are shown in green, whereas inferred losses are shown in red. (c) The numbers of distinct domains per genome in extant species are shown on the right side; for groups of species represented as triangles, these numbers are averages. Species, or groups of species, that are mostly parasitic are shown in grey. For more detailed data see Additional files 3 and 4. This figure was made using 'gathering' cutoffs provided by Pfam; for a corresponding figure using a E-value cutoff of 10^-8, see Additional file 13.

Figure 3

Dynamics of genomes during animal evolution. The functional contents of inferred ancestral genomes from the LECA to hominids (humans and great apes) are shown. (a) GO categories involved in various aspects of regulation. (b) GO categories involved in various aspects of metabolism (for detailed results see Additional files 5 and 6). Divergence time estimates are based on the fossil record and thus are minimum time constrains [39,68,69]. Geological periods are indicated on both panels ('Ed' stands for Ediacaran period and 'Cz' for Cenozoic era).

Figure 4

Classifying eukaryotes by the functional profiles of their genomes. A two-dimensional plot of regulatory function versus catalytic activity percentages for ancestral and extant domainomes.