Complex Genomes of Early Nucleocytoviruses Revealed by Ancient Origins of Viral Aminoacyl-tRNA Synthetases

Author:

Kijima Soichiro12ORCID,Hikida Hiroyuki1ORCID,Delmont Tom O3ORCID,Gaïa Morgan3ORCID,Ogata Hiroyuki1ORCID

Affiliation:

1. Chemical Life Science, Institute for Chemical Research, Kyoto University , Uji, Kyoto 611-0011 , Japan

2. School of Life Science and Technology, Tokyo Institute of Technology , Meguro, Tokyo 152-8550 , Japan

3. Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ. Evry, Université Paris-Saclay , 91057 Evry , France

Abstract

Abstract Aminoacyl-tRNA synthetases (aaRSs), also known as tRNA ligases, are essential enzymes in translation. Owing to their functional essentiality, these enzymes are conserved in all domains of life and used as informative markers to trace the evolutionary history of cellular organisms. Unlike cellular organisms, viruses generally lack aaRSs because of their obligate parasitic nature, but several large and giant DNA viruses in the phylum Nucleocytoviricota encode aaRSs in their genomes. The discovery of viral aaRSs led to the idea that the phylogenetic analysis of aaRSs can shed light on ancient viral evolution. However, conflicting results have been reported from previous phylogenetic studies: one posited that nucleocytoviruses recently acquired their aaRSs from their host eukaryotes, while another hypothesized that the viral aaRSs have ancient origins. Here, we investigated 4,168 nucleocytovirus genomes, including metagenome-assembled genomes (MAGs) derived from large-scale metagenomic studies. In total, we identified 780 viral aaRS sequences in 273 viral genomes. We generated and examined phylogenetic trees of these aaRSs with a large set of cellular sequences to trace evolutionary relationships between viral and cellular aaRSs. The analyses suggest that the origins of some viral aaRSs predate the last common eukaryotic ancestor. Inside viral aaRS clades, we identify intricate evolutionary trajectories of viral aaRSs with horizontal transfers, losses, and displacements. Overall, these results suggest that ancestral nucleocytoviruses already developed complex genomes with an expanded set of aaRSs in the proto-eukaryotic era.

Funder

Japan Society for the Promotion of Science KAKENHI

Research Unit for Development of Global Sustainability

Kyoto University Research Coordination Alliance

International Collaborative Research Program of the Institute for Chemical Research, Kyoto University

Publisher

Oxford University Press (OUP)

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