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. 2020 Oct 16;12(10):1173.
doi: 10.3390/v12101173.

Diversity of tRNA Clusters in the Chloroviruses

Affiliations

Diversity of tRNA Clusters in the Chloroviruses

Garry A Duncan et al. Viruses. .

Abstract

Viruses rely on their host's translation machinery for the synthesis of their own proteins. Problems belie viral translation when the host has a codon usage bias (CUB) that is different from an infecting virus due to differences in the GC content between the host and virus genomes. Here, we examine the hypothesis that chloroviruses adapted to host CUB by acquisition and selection of tRNAs that at least partially favor their own CUB. The genomes of 41 chloroviruses comprising three clades, each infecting a different algal host, have been sequenced, assembled and annotated. All 41 viruses not only encode tRNAs, but their tRNA genes are located in clusters. While differences were observed between clades and even within clades, seven tRNA genes were common to all three clades of chloroviruses, including the tRNAArg gene, which was found in all 41 chloroviruses. By comparing the codon usage of one chlorovirus algal host, in which the genome has been sequenced and annotated (67% GC content), to that of two of its viruses (40% GC content), we found that the viruses were able to at least partially overcome the host's CUB by encoding tRNAs that recognize AU-rich codons. Evidence presented herein supports the hypothesis that a chlorovirus tRNA cluster was present in the most recent common ancestor (MRCA) prior to divergence into three clades. In addition, the MRCA encoded a putative isoleucine lysidine synthase (TilS) that remains in 39/41 chloroviruses examined herein, suggesting a strong evolutionary pressure to retain the gene. TilS alters the anticodon of tRNAMet that normally recognizes AUG to then recognize AUA, a codon for isoleucine. This is advantageous to the chloroviruses because the AUA codon is 12-13 times more common in the chloroviruses than their host, further helping the chloroviruses to overcome CUB. Among large DNA viruses infecting eukaryotes, the presence of tRNA genes and tRNA clusters appear to be most common in the Phycodnaviridae and, to a lesser extent, in the Mimiviridae.

Keywords: algal viruses; chloroviruses; codon usage bias (CUB); tRNA clusters; tRNAs.

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Conflict of interest statement

The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Simplified diagram of tRNA anticodon base pairing with the mRNA codon. The tRNAMet anticodon 3′ UAC 5′ recognizes the codon 5′ AUG 3′ (left figure). The enzyme tRNA isoleucine lysidine synthase (TilS) attaches lysine to the 5′ cytosine of the tRNA, which becomes lysidine. Lysidine base pairs with adenine. As such, the modified tRNA now recognizes the isoleucine codon AUA.
Figure 2
Figure 2
Phylogram of three concatenated tRNA genes—tRNAGly, tRNATyr, and tRNAArg—using the maximum likelihood tree building algorithm with 100 bootstraps using the online website: phylogeny.fr. The concatenated sequences were aligned by MUSCLE; the alignment was curated by the Gblocks program. Parsimony and distance (BioNJ) phylogenetic tree-building algorithms were also used (100 bootstraps) and produced similar tree branching topologies. The numbers on the tree represent supported bootstrap values (i.e., percentage of bootstrap replicates that produced the same tree branch). The following chloroviruses were not included in the analysis because they lacked one of the three tRNA genes that were concatenated: PBCV-1, NE-JV-1, AR158, NE-JV-4, GM0701.1, and MN0810.1.

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