Viral lysis and host reprogramming impact carbohydrate, amino acid, and osmolyte cycling in salt-marsh tidal creek sediments

Salt marshes are highly productive ecosystems where microbial communities drive key transformations of organic matter at rates often exceeding those of oceanic and inland environments. Viruses are recognized as important drivers and regulators of global biogeochemical cycling, yet their diversity, host range, and functional roles in salt marsh ecosystems remain largely unresolved. To address these gaps, we investigated how viral lysis and host reprogramming can affect microbe-mediated organic matter transformations in a salt marsh of the Venice lagoon (Italy). Focusing on tidal creek surface sediments, we reconstructed 311 metagenome-assembled genomes (MAGs), built corresponding genome-scale metabolic models (GEMs) individually constrained with 121 metabolites detected in the sediments, and identified 3537 viral populations (vOTUs) across 10 samples. To assess the impact of viral lysis, we inferred prokaryotic hosts for 243 vOTUs and analysed host metabolism through MAG pathway analysis and GEM flux modelling across 13 bacterial orders, thus highlighting a negative impact on polysaccharide degradation, organic nitrogen mineralization, and organosulphur mineralization/volatilization processes. For host metabolic reprogramming, we characterized a subset of 50 auxiliary viral genes (AVGs) by mapping them to GEM reactions and analysing their stoichiometry, directionality, and pathway context, outlining two dominant strategies: resource scavenging through nucleotide-sugar biosynthesis, amino acid utilization, and sulphate assimilation; functional host maintenance through cofactor biosynthesis, electron transport, and energy production through carbonyl-compound utilization. Our findings provide a mechanistic view of the viral influence on organic matter transformations in salt marsh sediments and confirm viruses as key players in salt marsh biogeochemistry.