Retroids in Archaea: Phylogeny and lateral origins

Abstract

Until recently, none of the diverse elements bearing reverse transcriptase (retroids) have been known from Archaea. However, in the recently published genomes of the acetate-utilizing archaeal methanogens, Methanosarcina acetivorans and M. mazei, several open reading frames (ORFs) are annotated as reverse transcriptase (RT). These annotations led us to the characterization of a retron and 13 retrointrons, including three twintrons, clustered at seven loci of the M. acetivorans genome, and four retrointrons at two loci of the M. mazei genome. Based on a phylogeny of the RT ORFs, we infer four lateral gene transfers (LGT) of these retroids from Bacteria to Archaea and of retrointron mobility within the Archaea genomes. Our phylogenetic analysis also identifies several novel retrons from GenBank in the bacterial groups Firmicutes, Fusobacteria, Cyanobacteria and β-Proteobacteria, as well as in M. acetivorans. The discovery of retrointrons in Archaea as a consequence of LGT from Bacteria suggests that they did not originate in the progenote and parallels the "mitochondrial seed" theory of the origin of spliceosomes. Extending the known phylogenetic distribution of retroids to Archaea is consistent with the view that they have played a significant role in evolution of genomes throughout the tree of life.