Viruses are a vital part of the aquatic food web and hold a profound role in carbon and energy cycling at different trophic levels. Despite the rising interest in aquatic viruses, very few studies were conducted in estuaries, where freshwater and marine communities meet along the salinity gradient. We present a paired analysis of metagenomic and metatranscriptomic data focusing on the viral fraction derived from seasonal sampling between May 2021 and November 2022 in one of Europe's largest estuaries, the temperate mesotidal Elbe River downstream of Hamburg. Our results reveal a sharp delineation of viral communities along specific salinity niches and provide evidence for their adaptation. This implicates viruses as a structural component of microbial and phytoplankton ecology across the estuary. We provide a detailed overview of the spatiotemporal distribution of viruses, including taxonomy and hosts, which emphasizes the role of giant viruses (Megaviricetes) in waters of lower salinity and RNA viruses in marine environments. We identify, besides salinity, total dissolved phosphate and temperature as the main drivers of estuarine viral communities. We find a broad spectrum of metabolic pathways, potentially altered by viruses via auxiliary metabolic genes. Potential metabolisms impacted included the underlying carbon processes like photosynthesis or methane metabolism, but may also extend to some xenobiotics and antibiotics metabolisms in this anthropogenically altered estuary. This is the first detailed molecular study of viruses in the Elbe Estuary, shedding light on viral communities and their ecological roles in controlling microbial populations at the base of the estuarine food web.

Estuaries are blue carbon loci, storing and exchanging carbon between aquatic, atmospheric, and terrestrial environments. Estuarine particles facilitate the transformation and transport of organic matter. The fate of particulate organic matter in estuaries is driven by structural changes in polymers that modify buoyancy, determining the proportions of sinking and suspended particles. In the open ocean and coastal ecosystems, the microbial composition and function of sinking and suspended particles differ, impacting carbon remineralization and sedimentation rates. We leverage 190 metagenomes and 73 metatranscriptomes to assess free-living, sinking, and suspended particle-associated microbial composition and function across the Elbe estuary. The salinity gradient in the Elbe estuary is the primary driver of microbiome composition and function. Transparent exopolymer particles (TEP) production was localized to freshwater, with seemingly no TEP-associated organisms detected above 20 practical salinity units (PSU). We observed differences in the function of free-living and particle-associated microbial communities, with diazotrophs enriched on particles. We observed that sinking particles may better support methanogenesis, and suspended particles showed signs of continued primary and secondary production. From this, we conclude that activities such as dredging, which resuspend sediment, will exacerbate carbon turnover and greenhouse gas emissions, and reduced dredging may lower greenhouse gas (GHG) emissions in the Elbe estuary. Many of these GHG linking processes are inhibited by salinity due to the osmosensitivity of methanogens and methanotrophs along the estuary. Changes in sea level and precipitation rates will likely directly interact with activities such as dredging, with as yet uncertain impacts on microbial carbon processing and storage.