Eco-evolutionary Dynamics of Prokaryotic and Viral Communities in a Glacial Foreland

Glacial retreat zones offer an ideal natural laboratory setting to explore how soil viral and microbial communities adapt to ecosystem succession from seemingly barren substrates, particularly the evolutionary strategies underpinning microbial-viral coexistence, functional interdependencies, and the dynamics of cross-kingdom interaction. Here, we conducted a comprehensive metagenomic and viromic expedition across a 130-year glacial foreland chronosequence located on the Tibetan plateau. We identified 404 microbial operational taxonomic units (mOTUs) from metagenome-assembled genomes and 61,394 viral OTUs (vOTUs), revealing complex interaction networks involving 161 mOTUs and 3,095 vOTUs. Diverse sulfur-oxidizing (S→SO42-) bacteria (SOB) with complete conserved Dsr gene cluster (5’-DsrA-DsrB-DsrE-DsrF-DsrH-DsrC-DsrM-DsrK-fdhB/gltD-(hyp)-ttrB-dmsC-DsrN-DsrR-3’) were enriched in the early stage (0-40 year), whereas ammonia-oxidizing (NH4+→NO2-) bacterial lineage were flourished in the late stage of glacial retreat (41-130 year), suggesting the SOB facilitate the organic carbon storage and carbonates digestion during the early stage of glacial retreat. Core genes (dsrAB) in sulfur-cycling rDsr clusters exhibited significantly higher genetic diversity (p < 0.05) than accessory genes, reflecting environmental selection for metabolic plasticity. Microdiversity profiling further indicated that glacial retreat imposes divergent selection pressures: bacterial adaptation correlated with taxonomic hierarchy and functional guilds, while viral evolution depended on genome size and lifestyle. Our study dissects the intricate eco-evolutionary patterns governing microbial-viral interactions in deglaciating ecosystems, providing genomic insights into their adaptive resilience during climate-driven ecosystem succession.