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

Abstract

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), 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 for 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. ImportanceChrysophytes are abundant eukaryotic phytoplankton with trophic strategies ranging from photosynthesis to phagotrophy. They serve as models of mixotrophy among aquatic protists, but no chrysophyte-infecting viruses had been isolated, leaving a gap in experimental virus-host systems for a major class of protists. This study reports on the characterization of the first isolated chrysophyte-infecting virus, ChrysoHV. The virion morphology is unusual, having a loose membranous sac around a large capsid and a long filamentous tail. The genome contains genes for ribosomal proteins, a rarity in eukaryotic viruses, and multiple genes with homologs in common marine bacteria, one of which is a type of rhodopsin never before reported in a virus. We hypothesize that phago-mixotrophs, through infections and ingestion, may facilitate lateral gene exchange between eukaryote-infecting viruses and bacteria, entities that might not otherwise directly interact. The results expand the observed morphological diversity among viruses and the catalog of known virus genes.