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

Chrysophytes are widespread nanoflagellate protists in aquatic ecosystems with diverse trophic strategies ranging from phototrophy to phagotrophy. Molecular evidence has suggested that chrysophytes are commonly infected by giant viruses, but no isolates of such viruses have been reported. Here, we describe the chrysophyte-infecting virus Chrysophyceae Clade H virus SA1 (ChrysoHV). Both mixotrophic host and virus were isolated from surface waters in the subtropical 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, thin tail extending 1,200 (± 240) nm in length. This morphology has not been previously observed in other virus isolates or environmental surveys. The sequenced, assembled genome is 1.19 Mbp, and phylogenetic analysis places ChrysoHV as the third cultivated member of the Aliimimivirinae subfamily in the Mimiviridae family of giant viruses. ChrysoHV is the first cultivated member of Aliimimivirinae to encode a rhodopsin, and the most similar rhodopsin sequences from cultivated organisms derive from marine bacteria in the genus Pelagibacter. The rhodopsin homolog in ChrysoHV may thus represent a new lineage of viral rhodopsins. The ChrysoHV genome also contains nine genes, mostly related to nutrient uptake, with the closest known homologs in the marine cyanobacterium Prochlorococcus. Therefore, lateral gene transfer may be occurring between abundant marine bacterial clades and giant viruses, a process that may be promoted by phagotrophic mixotrophs as both giant viruses and bacterial prey are taken into the cell.