The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses

Abstract

The giant mimiviruses challenged the well-established concept of viruses, blurring the roots of the tree of life, mainly due to their genetic content. Along with other nucleo-cytoplasmic large DNA viruses, they compose a new proposed order-named Megavirales-whose origin and evolution generate heated debate in the scientific community. The presence of an arsenal of genes not widespread in the virosphere related to important steps of the translational process, including transfer RNAs, aminoacyl-tRNA synthetases, and translation factors for peptide synthesis, constitutes an important element of this debate. In this review, we highlight the main findings to date about the translational machinery of the mimiviruses and compare their distribution along the distinct members of the family Mimiviridae. Furthermore, we discuss how the presence and/or absence of the translation-related genes among mimiviruses raises important insights to boost the debate on their origin and evolutionary history.

Fig 1

Schematic view of mimiviruses’ aaRS (A) and tRNA (B) and codon/amino acid usage (C). The distribution of these genes follows a clear pattern of diversity among Mimiviridae: viral genomes with a wealthy aaRS and tRNA gene set (e.g., some lineage C isolates) contain all types of aaRS/tRNAs found in the rest of the family. This indicates a gradual inter- or intra-lineages gene loss throughout the evolution of different mimiviruses. The codon and amino acid usage analysis shows a clear difference between mimiviruses and Acanthamoeba castellanii patterns.

Fig 2. Phylogeny reconstruction of mimiviruses’ aaRS.

The unrooted trees were generated using MEGA 7 with the maximum likelihood method based on all aaRS found in mimiviruses. The trees were obtained after the alignment of the 100 best hits found in Genbank after BLASTing Megavirus chilensis aaRS predicted aa against all databases. Bacteria or Eukarya taxon, when present, were condensed from the outermost branch presenting bootstrap value >90. Mimiviruses of lineages A (grey), B (blue), and C (green) are highlighted. In all trees but the TyrRS tree, mimiviruses do not cluster inside cellular organism’s branches. The bottom–right shows some evolutionary scenarios related to mimivirus evolution that considers their hosts and translation-related genetic data set.