Evolution of codon usage in the smallest photosynthetic eukaryotes and their giant viruses

Abstract

Prasinoviruses are among the largest viruses (>200 kb) and encode several hundreds of protein coding genes, including most genes of the DNA replication machinery and several genes involved in transcription and translation, as well as transfer RNAs (tRNAs). They can infect and lyse small eukaryotic planktonic marine green algae, thereby affecting global algal population dynamics. Here, we investigate the causes of codon usage bias (CUB) in one prasinovirus, OtV5, and its host Ostreococcus tauri, during a viral infection using microarray expression data. We show that 1) CUB in the host and in the viral genes increases with expression levels and 2) optimal codons use those tRNAs encoded by the most abundant host tRNA genes, supporting the notion of translational optimization by natural selection. We find evidence that viral tRNA genes complement the host tRNA pool for those viral amino acids whose host tRNAs are in short supply. We further discuss the coevolution of CUB in hosts and prasinoviruses by comparing optimal codons in three evolutionary diverged host-virus-specific pairs whose complete genome sequences are known.

Keywords: NCLDV; Ostreococcus; codon usage bias; microarray; picoeukaryote; selection; tRNA.

Fig. 1.—

Principal component analysis of codon prevalence of the six prasinoviruses and the four Mamiellophyceae genomes, divided according to normal chromosomes (Ota, Olu, Bpra, and Mpu), low GC regions of the big outlier chromosome (Ota-BOC, Olu-BOC, Bpra-BOC, and Mpu-BOC), and small outlier chromosome (Ota-SOC, Olu-SOC, Bpra-SOC, and Mpu-SOC). Prasinoviruses are represented in red. We also projected codons on the two principal axes, 4-fold degenerate codons are blue, 3-fold degenerate codons are green, and 2-fold degenerate codons are pink.

Fig. 2.—

CUB, measured as Ncp, as a function of expression levels in Ostreococcus tauri, Kruskal–Wallis analysis of variance, P < 10⁻¹⁰ (A) and OtV5, 10 h postinfection, P < 0.01 (B). Host and viral data include genes longer than 200 codons, and gene expression classes have been defined to have an equal number of genes between classes.

Fig. 3.—

Proportion of host tRNA gene per viral AA, depending on whether the viral AA have a cognate viral tRNA (with tRNA) or not (without tRNA).