Virus-encoded metabolism may support environmental stress adaptation of microbial hosts in an estuarine hypoxic zone

Hypoxic zones in estuaries threaten the ecological balance and the productivity in coastal areas. However, it is poorly understood how viruses regulate metabolic processes of their microbial hosts to adapt to the hypoxic environment, and consequently impact the biogeochemical cycles in hypoxic zones. In this study, the diversity and functional potentials of the bacterial, archaeal and viral communities of a hypoxic zone at the Pearl River Estuary was characterized along with local environmental factors, with a particular focus on viral auxiliary metabolic genes (AMGs). The viral community derived from the virion fraction and the cellular fraction of the seawater were distinctly different, with the cellular fraction generating fewer unique viruses, but more types of AMGs. Overall, more AMGs were identified in samples with higher dissolved oxygen levels. Globally conserved AMGs were infrequently observed in the current samples, suggesting a certain level of adaptation of AMGs to the local environment. There were strong correlations in abundances among cyanobacteria, cyanophages, and photosynthesis AMGs, suggesting potential viral participation in estuarine primary production. Many AMGs involved in nutrient limitation endurance were found, potentially assisting their host with phosphorus, iron and B family vitamin shortages. Although putative hosts were predicted for the viruses, the functionality of their AMGs appears to be a better predictor of their distribution than the hosts they infect. Our study provides a functional insight into the viral community in poorly researched estuarine hypoxic zones, and sheds light on the potential interactions of viruses with their microbial hosts for co-adaptation to this unique environment.