A dinoflagellate-infecting giant virus with a micron-length tail

Abstract

Viral infection is a ubiquitous source of marine plankton mortality, but relatively few viruses that infect phytoplankton have been characterized. Here we describe a virus, PelV-1, with unusual morphological and genomic features that infects a dinoflagellate, Pelagodinium sp. Both host and virus were isolated from the epipelagic zone in the North Pacific Subtropical Gyre. PelV-1 has a [~]200 nm capsid size, and the virion variably exhibits two appendages, the presence and length of which may reflect different stages of virion maturity or artifacts of sample preparation. The appendages are a thinner 30 nm-wide tail-like structure that can extend to 2.3 {micro}m -- the longest virus appendage described to date-- and a shorter, thicker (>40-70 nm) protrusion, which appears to emerge from a star-shaped capsid opening directly opposite the attachment point of the long, thin tail. Sequencing and assembly of material in a purified lysate generated a high-coverage (> 4,000x) genome of 459 kb (33.8% GC). A second, distinct genome of 504 kb (25.8% GC) was also assembled, but had low read coverage (< 24x), suggesting the presence of a low-abundance, co-cultured virus (co-PelV). Phylogenetic analysis indicates that both PelV-1 and co-PelV are members of Mesomimiviridae. They contain various genes for the metabolism of amino acids (e.g., asparagine synthase), carbohydrates (e.g., epimerase, glycosyl hydrolase, aconitate hydratase, succinate dehydrogenase of the TCA cycle), and lipids (e.g., phospholipases), as well as other noteworthy genes (e.g., light-harvesting complex, rhodopsin, ion channel, sugar transporters, aquaporin). PelV-1 also has ORFs most similar to tail fiber genes of Synechococcus phage and other tail domain-containing protein homologs. The ecological advantages that might be conferred by the extraordinarily long tail and metabolic genes of PelV-1 is unknown, but this isolate expands the scope of morphological and metabolic diversity of viruses and suggests many more unusual marine viruses await discovery. Author summaryGiant viruses challenged our traditional views of virology due to their large size and the presence of hundreds of auxiliary metabolic genes. But despite the immense giant virus diversity discovered through sequencing, few isolates were described, and those were primarily viruses that infect amoeba host and rarely from phytoplankton. This hampers our understanding of marine host-virus interaction and thus the impact of viruses on the ocean ecosystem. Here we provide genomic and morphological characterization of a novel dinoflagellate giant virus (PelV-1) and a second co-occurring, albeit low abundance, virus (co-PelV). Dinoflagellates are vital in marine symbiosis and algal blooms but only two giant virus isolates have been described with no available genomic resources to date. Thus, this is a significant contribution to the literature on dinoflagellate viruses. Among the notable features of PelV-1 are its unique micron-length tail appendage, phagocytosis-like entry mechanism and its varied auxiliary metabolic genes including photosynthesis and energy generating genes.