A Phylogenomic Census of Molecular Functions Identifies Modern Thermophilic Archaea as the Most Ancient Form of Cellular Life

Abstract

The origins of diversified life remain mysterious despite considerable efforts devoted to untangling the roots of the universal tree of life. Here we reconstructed phylogenies that described the evolution of molecular functions and the evolution of species directly from a genomic census of gene ontology (GO) definitions. We sampled 249 free-living genomes spanning organisms in the three superkingdoms of life, Archaea, Bacteria, and Eukarya, and used the abundance of GO terms as molecular characters to produce rooted phylogenetic trees. Results revealed an early thermophilic origin of Archaea that was followed by genome reduction events in microbial superkingdoms. Eukaryal genomes displayed extraordinary functional diversity and were enriched with hundreds of novel molecular activities not detected in the akaryotic microbial cells. Remarkably, the majority of these novel functions appeared quite late in evolution, synchronized with the diversification of the eukaryal superkingdom. The distribution of GO terms in superkingdoms confirms that Archaea appears to be the simplest and most ancient form of cellular life, while Eukarya is the most diverse and recent.

The natural history of molecular functions inferred from an extensive phylogenomic analysis of gene ontology data

“…Relatively new level 1 GO terms were not uniquely present in Archaea (there is no A taxonomic group), suggesting that the BE and E groups increased novel functional activities during evolution, the likely result of bacterial biodiversity and eukaryal multicellularity. Data in Venn taxonomic group distributions is consistent with a scenario in which functions evolved from a complex and rich ancestor of extant life, producing archaeal functionomes first by massive genome streamlining [21]. Eukarya unique terms appeared in the very late phase of the timeline (0.86 ≤ nd ≤1).…”

“…This simple observation reveals a progression of functional complexity that follows the order, Archaea, Bacteria and Eukarya. The order matches the rise of superkingdoms inferred from molecular structures [30] and functions [21]. It is unlikely that this progression is due to quality of GO data, since GO coverage for Archaea (57%) was not far away from that of Bacteria and Eukarya (60%) [21].…”

“…The order matches the rise of superkingdoms inferred from molecular structures [30] and functions [21]. It is unlikely that this progression is due to quality of GO data, since GO coverage for Archaea (57%) was not far away from that of Bacteria and Eukarya (60%) [21]. Remarkably, the timelines show Eukarya unfolding an extremely rich toolkit of functions when compared to the other superkingdoms.…”

“…However, the method was successfully applied to other studies [7, 8, 17, 21]. Moreover, genomic abundance has several advantages over other character types (including presence/absence) and the topologies of resulting ToFs are less affected by HGT or recruitment [62].…”

The aspartate aminotransferase-like domain of Firmicutes MocR transcriptional regulators

“…It can be therefore conjectured that either horizontal transfer (Garcia-Vallve et al, 2000) or gene duplication of an ancestral gene coding for a type-I enzyme, followed by the fusion with the ancient HTH domain (Aravind et al, 2005), initiated the evolution of the MocR family. This picture is compatible with a recent survey suggesting that thermophilic Archaea are the most ancient form of cellular life (Nasir et al, 2014) and, therefore, may represent the original source of the ancestral AAT-like enzyme. However, no MocR-like regulators are found in the Archaea genomes available (results not shown).…”