Viral ecogenomics across oxic and anoxic zones of the Yongle Blue Hole.

Background: Deep ocean blue holes are characterized by distinct physicochemical gradients and complex biological processes, and Yongle Blue Hole (YBH) in the South China Sea (SCS) is the world's deepest (301 m) underwater cavern with unique environmental characteristics. So far, studies investigated the bacterial community structure with different lifestyles of the YBH; however, our understanding of viruses in the YBH remains limited. Here, we utilized a metagenomic approach to investigate viral communities in both the "viral fraction" and "cellular fraction" of seawater samples in oxic and anoxic zones within YBH.

Results: A total of 1,730 viral operational taxonomic units (vOTUs) were identified, with over 70% affiliated with the classes Caudoviricetes and Megaviricetes, particularly within the families Kyanoviridae, Phycodnaviridae and Mimiviridae. Gene-sharing network analyses indicated that the deeper anoxic layers contain a high proportion of novel viral genera, while the oxic layer's viral genera overlap with those found in the open water samples from SCS. Virus-linked prokaryotic hosts predominantly belong to the phyla Patescibacteria, Desulfobacterota, and Planctomycetota. Notably, the detected putative auxiliary metabolic genes (AMGs) suggest that these viruses may influence photosynthetic and chemosynthetic pathways, as well as methane, nitrogen, and sulfur metabolisms, especially with several high-abundance AMGs potentially involved in prokaryotic assimilatory sulfur reduction.

Conclusions: Together, these findings highlight the potential ecological roles and diversity of viral communities within YBH and shedding light on niche-separated viral speciation.