Past and present giant viruses diversity explored through permafrost metagenomics

Abstract

Giant viruses are abundant in aquatic environments and ecologically important through the metabolic reprogramming of their hosts. Lesser is known about giant viruses from soil although two of them, belonging to different families, were reactivated from 30,000-y-old Siberian permafrost samples, suggesting an untapped diversity of Nucleocytoviricota in this environment. Through permafrost metagenomics, we reveal a high heterogeneity in the abundance of giant viruses representing up to 12% of the total community in one sample. Pithoviridae and Orpheoviridae-like viruses were the most important contributors, followed by Mimiviridae. A comparison to other terrestrial metagenomes confirmed that the diversity pattern in these samples is quite unique. In contrast, Pandoraviridae sequences remained scarce. Using a stringent methodology, we were able to assemble large genomes, including a complete circular 1.6 Mb Pithoviridae-like from a 42,000-y-old sample. The uncovered Pithoviridae diversity also provided insights into the family evolution. The phylogenetic reconstruction of specific functions not only revealed gene transfers between cells and viruses, but also between viruses from different families. Finally, the extensive annotation of the permafrost viral sequences revealed a patchwork of predicted functions amidst an even larger reservoir of anonymous genes of unknown functions.