Expansion of the genomic and functional diversity of global ocean giant viruses

Abstract

Giant viruses (GVs) play crucial roles in the global ocean microbial food web and biogeochemistry by infecting protists. Traditionally, insights into GV ecology and functions have been limited to culture-based studies. However, recent metagenomic advances have uncovered over 1,800 new GV genomes from the world's oceans. While this rapid increase in genomic information marks an impressive advance for the field, it is nowhere close to the extensive genomic information available for other marine entities - e.g., prokaryotes and their 'virome'. Addressing this gap, we present 230 novel, high-quality GV genomes and 398 partial genomes from nine global ocean datasets using an open-source bioinformatic workflow we developed. Notably, we identified numerous GV genomes from the Baltic Sea, offering insights into their phylogenomics, metabolic potential, and environmental drivers in one of the largest brackish water ecosystems. We discovered new GV functions, including photosynthetic proteins, and identified a significant functional divide between the Imitervirales and Algavirales orders. Additionally, we evaluated best practices for GV genome recovery from metagenomic datasets through a case study on the Baltic Sea dataset. Our study significantly expands the marine GV genomic and functional diversity, broadening our understanding of their roles in the food web and biogeochemistry.