A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya

Abstract

DNA topoisomerase IB (TopoIB) was thought for a long time to be a eukaryotic specific enzyme. A shorter version was then found in viruses and later on in several bacteria, but not in archaea. Here, we show that a eukaryotic-like TopoIB is present in the recently sequenced genomes of two archaea of the newly proposed phylum Thaumarchaeota. Phylogenetic analyses suggest that a TopoIB was present in the last common ancestor of Archaea and Eucarya. This finding indicates that the last common ancestor of Archaea and Eucarya may have harboured a DNA genome.

Figure 1

A. Schematic representation of the domain organisation of Topo IB sequences from three eucarya, two thaumarchaeota, two bacteria and three viruses (the multiple alignment of these sequences is provided as Additional Files 1). Coloured boxes delineate the putative functional domains according to the PFAM database : Topoisom_I_N (PF02919, Eukaryotic DNA topoisomerase I, DNA binding fragment) in red, Topoisom_I (PF01028, Eukaryotic DNA topoisomerase I, catalytic core) in blue and virDNA-Topo-I_N (PF09266, Viral DNA topoisomerase I, N-terminal) in light-green. The N-ter regions of viral Topo IB is similar in size and share conserved residues with bacterial and mimiviral homologues, suggesting the presence of a virDNA-Topo-I_N-like domain in these sequences (in dark-green). B. Alternative evolutionary scenarios explaining the presence of Topo IB in Thaumarchaeota. Filled blue diamonds indicate the presence of a Topo IB coding gene. Empty blue diamonds indicate a Topo IB coding gene that were present in the ancestor of the corresponding lineage and lost during its evolution. Blue crosses indicate the loss events of Topo IB coding genes. (a) A Topo IB coding gene was acquired by the ancestor of Thaumarchaeota via horizontal gene transfer (blue arrow) from a eukaryotic lineage. (b), (c) and (d) A Topo IB coding gene was present in the ancestor of Archaea and Eucarya and was subsequently lost in the ancestor of Crenarchaeota and Euryarchaeota, in agreement with a thaumarchaeal rooting of the archaeal tree (B). The Topo IB coding gene was independently lost in the ancestors of Euryarchaeota and Crenarchaeota according to an euryarchaeal or crenarchaeal rooting of the archaeal tree (C and D).

Figure 2

Unrooted maximum likelihood phylogenetic tree of 151 Topo IB sequences. Numbers at branches represent bootstrap proportions. The scale bar represents the average number of substitutions per site.