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Summary: Bacteriophages encode host‐acquired functional genes known as auxiliary metabolic genes (AMGs). Photosynthesis AMGs are commonly found in marine cyanobacteria‐infecting Myoviridae and Podoviridae cyanophages, but their ecology remains understudied in freshwater environments. To advance knowledge of this issue, we analysed viral metagenomes collected in the summertime for four years from five lakes and two estuarine locations interconnected by the Chattahoochee River, Southeast USA. Sequences representing ten different AMGs were recovered and found to be prevalent in all sites. Most freshwater AMGs were 10‐fold less abundant than estuarine and marine AMGs and were encoded by novel Myoviridae and Podoviridae cyanophage genera. Notably, several of the corresponding viral genomes showed endemism to a specific province along the river. This translated into psbA gene phylogenetic clustering patterns that matched a marine vs. freshwater origin indicating that psbA may serve as a robust classification and source‐tracking biomarker. Genomes classified in a novel viral lineage represented by isolate S‐EIVl contained psbA, which is unprecedented for this lineage. Collectively, our findings indicated that the acquisition of photosynthesis AMGs is a widespread strategy used by cyanophages in aquatic ecosystems, and further indicated the existence of viral provinces in which certain viral species and/or genotypes are locally abundant. [ABSTRACT FROM AUTHOR]

Predicting elemental cycles and maintaining water quality under increasing anthropogenic influence requires knowledge of the spatial drivers of river microbiomes. However, understanding of the core microbial processes governing river biogeochemistry is hindered by a lack of genome-resolved functional insights and sampling across multiple rivers. Here we used a community science effort to accelerate the sampling, sequencing and genome-resolved analyses of river microbiomes to create the Genome Resolved Open Watersheds database (GROWdb). GROWdb profiles the identity, distribution, function and expression of microbial genomes across river surface waters covering 90% of United States watersheds. Specifically, GROWdb encompasses microbial lineages from 27 phyla, including novel members from 10 families and 128 genera, and defines the core river microbiome at the genome level. GROWdb analyses coupled to extensive geospatial information reveals local and regional drivers of microbial community structuring, while also presenting foundational hypotheses about ecosystem function. Building on the previously conceived River Continuum Concept 1 , we layer on microbial functional trait expression, which suggests that the structure and function of river microbiomes is predictable. We make GROWdb available through various collaborative cyberinfrastructures 2,3 , so that it can be widely accessed across disciplines for watershed predictive modelling and microbiome-based management practices., Competing Interests: Competing interests: The authors declare no competing interests., (© 2024. The Author(s).)