Cyanophage tRNAs may have a role in cross-infectivity of oceanic Prochlorococcus and Synechococcus hosts

Abstract

Marine cyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant photosynthetic prokaryotes in oceanic environments, and are key contributors to global CO(2) fixation, chlorophyll biomass and primary production. Cyanophages, viruses infecting cyanobacteria, are a major force in the ecology of their hosts. These phages contribute greatly to cyanobacterial mortality, therefore acting as a powerful selective force upon their hosts. Phage reproduction is based on utilization of the host transcription and translation mechanisms; therefore, differences in the G+C genomic content between cyanophages and their hosts could be a limiting factor for the translation of cyanophage genes. On the basis of comprehensive genomic analyses conducted in this study, we suggest that cyanophages of the Myoviridae family, which can infect both Prochlorococcus and Synechococcus, overcome this limitation by carrying additional sets of tRNAs in their genomes accommodating AT-rich codons. Whereas the tRNA genes are less needed when infecting their Prochlorococcus hosts, which possess a similar G+C content to the cyanophage, the additional tRNAs may increase the overall translational efficiency of their genes when infecting a Synechococcus host (with high G+C content), therefore potentially enabling the infection of multiple hosts.

Figure 1

A clustered distance matrix based on CU (a) and NU (b) profiles. Colors range from blue, indicating close distances, and red, representing great distances. Color bar is given. Phage and host names are given: red labels indicate Prochlorococcus, blue labels indicate Synechococcus and black represents the phages.

Figure 2

Distribution of phage tRNAs within cyanomyophage genomes. Genetic table presents the distribution of tRNA isoacceptors within the phage genomes. Phage tRNAs are denoted by their optimal complementary codon. Colors correspond to the number of appearances of each tRNA in the genomes studied.

Figure 3

Phage codon frequencies compared with the codon frequencies of their hosts for four phage–host interactions: (a) Syn19 compared with NATL2A, a low %GC Prochlorococcus host; (b) Syn19 compared with MIT9303, a relatively high %GC Prochlorococcus host; (c) Syn19 compared with WH7803, a Synechococcus host; and (d) Syn19 compared with WH8102, a Synechococcus host. Each triangle stands for a specific codon; red triangles correspond to tCC. The regions between the lower and the upper quartile representing the distances of the triangle to the diagonal are shaded in gray.

Figure 4

Distribution of genes encoding for hypothetical proteins in phage genomes sorted according to the distance between the phage gene and the host CU grouped into 10 groups (bins). Bins are marked from 1 to 10 corresponding to groups of genes having the highest to the lowest distance from the host CU, respectively. Each bin contains an equal number of genes. The height of the bar denotes the average number of hypothetical genes in each bin calculated from all studied genomes; error bars correspond to s.d.'s. Cyan bars represent the results obtained from phages associated with Synechococcus hosts, whereas red bars illustrate the results obtained from phages associated with Prochlorococcus hosts. Probabilities of the gene enrichment calculated based on the hypergeometric distribution test are detailed in Supplementary Table S2. The colour reproduction of this figure is available at the ISME journal online.

Figure 5

(Left) Heat map representing the tRCI values calculated for all ORFs in the Syn19 genome. Color bar is shown on the left of the heat map. The tRCI values are calculated independently for each of the Syn19 known hosts. Vertical lines represent the tRCI values of the gene, calculated relative to the specific host, listed on the right. (right) Example showing the ranking of the tRCI of the Syn19 gp16 gene (pointed by arrows in the heat map) when calculated for the five different hosts. tRCI values were sorted and ranked for each host from the highest tRCI (100th percentile) to the lowest (1st percentile) and grouped into 10 bins. As demonstrated, the same gene can obtain a different tRCI value that can be ranked differently and grouped in a different bin depending on the phage–host interactions.

Figure 6

hli (a) and cpeT (b) enrichment in genomes sorted according to tRCI values and grouped into 10 bins from the most distant tRCI values (bin 1) to the least distant (bin 10). P-values for the hypergeometric distribution test are detailed in Supplementary Table S3. The colour reproduction of this figure is available at the ISME journal online.

Figure 7

Phage tRNA gene copy number plotted against the difference in G+C content between the phage and its most distant host (in terms of NU). Black triangles stand for cyanomyophages (wide host range), gray circles represent cyanopodophages (narrow host range).