Functional determinism amid taxonomic stochasticity: insights into rules governing the assembly of algal-microbial...

Marine algal-microbial symbioses constitute essential functional units that drive ocean biogeochemical cycles and trigger harmful algal blooms. Yet, a long-standing controversy persists regarding the mechanisms of algal-microbial symbiose assembly, specifically whether phycosphere microbiota are predominantly shaped by deterministic algal-driven selection or by stochastic environmental processes, with no definitive resolution to date. Here, we examined phycosphere communities associated with a series of Skeletonema strains, tracking their taxonomic and functional dynamics across successive growth stages. Despite pronounced taxonomic diversity, reflected in distinct community compositions, successional trajectories, and microbial networks, shotgun metagenomic analyses revealed highly conserved functional repertoires across samples, with consistently abundant core pathways, including amino acid biosynthesis, secondary metabolite and antibiotic production, and ABC transport systems. Statistical analyses further revealed a marked decoupling of taxonomy and function, with functional redundancy enabling taxonomically distinct lineages to perform equivalent metabolic roles. Based on these findings, we propose a dual assembly model in which deterministic algal host-driven selection constrains functional composition, while stochastic processes govern species-level membership. This "function-first, taxonomy-stochastic" paradigm reconciles opposing assembly theories, underscores functional resilience in the face of taxonomic turnover, and provides a conceptual foundation for the rational design of synthetic algal-microbial consortia in marine biotechnological applications.IMPORTANCEMarine algae live in close association with diverse microorganisms that influence nutrient cycling and ecosystem stability. Yet, how these algal-microbial partnerships assemble and maintain functional integrity remains unresolved. Using Skeletonema as a model, this study demonstrates that while the microbial species surrounding different algal strains vary greatly, their metabolic functions remain remarkably consistent. This finding reveals that algal hosts deterministically shape the functional needs of their microbiome, whereas the specific bacterial members fulfilling those roles are interchangeable. Such a "function-first" organization explains how algal-microbial symbioses persist despite environmental fluctuations. Understanding these assembly rules not only advances our knowledge of marine microbial ecology but also provides a conceptual foundation for engineering stable and resilient algal-microbial consortia for sustainable ocean biotechnologies.