Coccolithoviruses: A Review of Cross-Kingdom Genomic Thievery and Metabolic Thuggery

Abstract

Coccolithoviruses (Phycodnaviridae) infect and lyse the most ubiquitous and successful coccolithophorid in modern oceans, Emiliania huxleyi. So far, the genomes of 13 of these giant lytic viruses (i.e., Emiliania huxleyi viruses-EhVs) have been sequenced, assembled, and annotated. Here, we performed an in-depth comparison of their genomes to try and contextualize the ecological and evolutionary traits of these viruses. The genomes of these EhVs have from 444 to 548 coding sequences (CDSs). Presence/absence analysis of CDSs identified putative genes with particular ecological significance, namely sialidase, phosphate permease, and sphingolipid biosynthesis. The viruses clustered into distinct clades, based on their DNA polymerase gene as well as full genome comparisons. We discuss the use of such clustering and suggest that a gene-by-gene investigation approach may be more useful when the goal is to reveal differences related to functionally important genes. A multi domain "Best BLAST hit" analysis revealed that 84% of the EhV genes have closer similarities to the domain Eukarya. However, 16% of the EhV CDSs were very similar to bacterial genes, contributing to the idea that a significant portion of the gene flow in the planktonic world inter-crosses the domains of life.

Keywords: E. huxleyi; coccolithovirus; domains of life; genome comparison; horizontal gene transfer.

Figure 1

Phylogenetic analysis of coccolithoviruses based on their DNA polymerase and serine palmitoyltransferase (SPT) genes. The evolutionary history of 13 EhV strains was inferred based on the 2604 bp long SPT (I and II) and 2921 bp long DNA polymerase (III and IV) genes, using the Neighbor-Joining (I and III) and Maximum Likelihood (II and IV) methods. Note that EhV-18 and EhV-145 are absent from the serine palmitoyltransferase tree due to the full length SPT protein being split over two separate genes in their respective genomes. Based on the DNA polymerase phylogeny, the EhVs cluster into two main clades: A and B (green). Clade A is further divided into sub-clusters A1 (red), A2 (yellow), and A3 (purple). The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches. The evolutionary distances were computed using the Tamura-Nei method and are in the units of the number of base substitutions per site.

Figure 2

Whole genome alignment of sequenced coccolithovirus genomes. The genomes were aligned using MAUVE, in relation to the non-gapped backbone genome of EhV-86. Syntenous blocks are indicated in the same colours and the lines that connect them indicate the position of each block in relation to the same block of genes in the genome of EhV-86. The small red lines on each genome represent the exact positions of the gaps that separate the different contigs within each draft genome. The genomes are ordered based on their DNA polymerase phylogeny (Figure 1), based on the ANI analysis of this study (Table 2), and based on previously published microarray data that puts them into the aforementioned groups and sub-clades [20].

Figure 3

“Best BLAST hit” analysis of coccolithovirus CDSs in relation to the three domains of life: Eukarya, Bacteria and Archaea. Predicted genes within EhV genomes were BLASTp analyzed against possible hits in the three domains of life using a gene BitScore of >50 (A); and >100 (B). Further EhV gene hits analysis to the taxonomic level of “order” in Eukarya (C); and Bacteria (D) was performed using a BitScore of >100.