Evidence for the acquisition of a proteorhodopsin-like rhodopsin by a chrysophyte-infecting giant virus

Chrysophytes are nanoflagellate protists widespread in aquatic ecosystems with diverse trophic roles as primary producers and bacterivores. Molecular evidence suggests that chrysophytes are commonly infected by giant viruses, but isolates of such virus-host systems have not been reported. Here, we describe the first cultivated chrysophyte-infecting virus, Chrysophyceae Clade H virus SA1 (ChrysoHV), isolated along with its phago-mixotrophic host alga from surface waters in the tropical North Pacific Ocean. The ChrysoHV capsid (290 ± 40 nm diameter) is associated with a loose, sac-like membrane that extends its effective diameter (720 ± 120 nm) and presents a long (1,200 ± 240 nm), thin (20 ± 2 nm), flexible tail, a morphology unlike any virion yet described. The assembled genome is 1.19 Mbp. Phylogenetic analysis places ChrysoHV as the third cultivated member of the Aliimimivirinae subfamily in the Mimiviridae family of giant viruses. The ChrysoHV genome encodes two heliorhodopsins and one proteorhodopsin. Proteorhodopsins are well-known light-driven proton pumps in bacteria but have not been previously reported in a viral genome. The predicted viral proteorhodopsin structure suggests it may not have a functional retinal binding site, implying a light-independent function. The genome also encodes two ribosomal proteins and nine genes with closest known homologs in marine cyanobacteria, most annotated as encoding proteins involved in nutrient uptake. This unusual virus could serve as a model system for exploring viral rhodopsin functions, and its genome suggests that phagotrophic protists may serve as an intracellular market for gene exchange between infecting viruses and ingested bacterial prey.