Ecology of prokaryotic DNA viruses in a highly-impacted coastal lagoon revealed through comparative and temporal metagenomics

ABSTRACT Coastal lagoons are highly productive ecosystems, yet their prokaryotic viruses remain poorly studied. The Mar Menor, a hypersaline coastal lagoon in south-eastern Spain, is under strong anthropogenic pressure from continuous agricultural runoff, leading to severe eutrophication. To assess the impact of these unique conditions on viral assemblages, we analyzed a three-year metagenomic time series of picoplankton communities. We reconstructed the lagoon’s prokaryotic DNA viral communities and compared them with their counterparts in open Mediterranean Sea waters to reveal how environmental variability shapes their structure. Viral communities in the Mar Menor showed higher vOTU relative abundances and diversities, and were distinct from those offshore. Temporally, community structure was correlated with water transparency and silicate concentration. The putative hosts of the lagoon viruses were copiotrophic rather than oligotrophic compared to the open sea, and their composition shifted in response to episodic environmental disturbances. Temperate virus levels did not consistently support either the piggyback-the-winner or refugium models, spatially or temporally, indicating that viral replication strategies are governed by factors more complex than trophic status or environmental variability alone. Auxiliary viral genes (AVGs) encoding 2-oxoglutarate/Fe(II)-dependent oxygenase and DNA methyltransferase emerged as potential relevant functions in the lagoon, as they were more frequent than in the Mediterranean Sea. Similarly to targeted hosts, AVG-specific temporal relative abundance patterns were strongly shaped by local disturbances. This study provides the first metagenomic insight into viruses of the Mar Menor, revealing viral ecology in a dynamic, eutrophic lagoon, with implications for predictive models of nutrient cycling.