Vertical transport and spatiotemporal dynamics of giant viruses in the North Pacific subtropical gyre

Nucleocytoplasmic large DNA viruses, or "giant viruses," are prevalent in marine environments, infecting diverse eukaryotic lineages and influencing the marine carbon cycle. Their genomes harbor wide range of auxiliary metabolic genes that influence biogeochemical processes. This study integrates planktonic (5-4000 m) and particle-associated (4000 m) metagenomic samples in the North Pacific Subtropical Gyre, along with particulate export flux data at 4000 m, to investigate the vertical transport of giant viruses and their correlation with carbon export through space and time. By analyzing metagenomic samples over a period of 6 years across 15 depths, we curated a database of 37 giant virus population genomes and 1496 contigs and investigated their spatiotemporal variability and functional capacity in the open ocean. We reported multiple lines of evidence supporting the viral shuttle hypothesis, including the vertical transport of giant viruses from the upper ocean to abyssal depths and their positive correlation with particulate carbon export flux at 4000 m, particularly a giant species closely related to Phaeocystis globosa virus known to infect a bloom-forming alga. We identified giant viruses encoding diverse auxilary metabolic genes, including genes associated with photosynthesis, nutrient transport, and energy metabolism. These auxiliary metabolic genes displayed depth-specific distributions, which we postulate reflect depth-specific adaptations to light-energy and nutrient-limited conditions along the water column. This study provides critical insights into biogeochemical impacts of giant viruses by identifying key giant viruses that can impact export processes and depth-specific distributions of auxiliary metabolic genes impacting biogeochemical processes along the open ocean water column.