Host Range and Coding Potential of Eukaryotic Giant Viruses

Abstract

Giant viruses are a group of eukaryotic double-stranded DNA viruses with large virion and genome size that challenged the traditional view of virus. Newly isolated strains and sequenced genomes in the last two decades have substantially advanced our knowledge of their host diversity, gene functions, and evolutionary history. Giant viruses are now known to infect hosts from all major supergroups in the eukaryotic tree of life, which predominantly comprises microbial organisms. The seven well-recognized viral clades (taxonomic families) have drastically different host range. Mimiviridae and Phycodnaviridae, both with notable intrafamilial genome variation and high abundance in environmental samples, have members that infect the most diverse eukaryotic lineages. Laboratory experiments and comparative genomics have shed light on the unprecedented functional potential of giant viruses, encoding proteins for genetic information flow, energy metabolism, synthesis of biomolecules, membrane transport, and sensing that allow for sophisticated control of intracellular conditions and cell-environment interactions. Evolutionary genomics can illuminate how current and past hosts shape viral gene repertoires, although it becomes more obscure with divergent sequences and deep phylogenies. Continued works to characterize giant viruses from marine and other environments will further contribute to our understanding of their host range, coding potential, and virus-host coevolution.

Keywords: Nucleo-Cytoplasmic Large DNA Viruses (NCLDVs); algae; auxiliary genes; cophylogeny; gene repertoire; genome evolution; host switch; lateral gene transfers; protists; virus-encoded metabolism.

Figure 1

Cophylogenetic relationships between giant viruses and eukaryotes. Virus-host connections are mapped onto reference trees summarizing giant virus phylogenies based on up to 10 putatively vertically inherited core genes [13,14,37,42,43] and phylogenetic relationships across the eukaryotic tree of life [27,44,45,46,47,48,49,50]. The seven commonly delineated giant virus clades (seven families with two nested families) are divided into subfamilial lineages, each of which comprises one or more viral strains with known hosts (Table S1), with a schematic diagram of virion morphology, if known, and the average genome size across strains (proportional to the circle area; Table S1) shown. Names in double quotes correspond to non-monophyletic groupings. * Giant viruses are also known to infect the SAR lineages dictyochophytes (Stramenopila) [51,52], dinoflagellates (Alveolata) [53], and chlorarachniophytes (Rhizaria) [52], but their phylogenetic positions in the virus reference tree are less certain.