A horizontal connectivity mode in coastal oceans: transport overrides stratification to govern microbiome network stability

Coastal ecosystems are critical biogeochemical reactors and biodiversity reservoirs, yet the mechanisms governing the community connectivity and stability of their foundational microbiomes remain poorly understood, particularly in anthropogenically influenced coastal oceans. Here, we systematically analyzed prokaryotic and microeukaryotic communities along both vertical and horizontal gradients in the Bohai-Yellow Sea, a model anthropogenically influenced and multi-stressed coastal ocean. We found that horizontal gradients, primarily driven by distance to coastline and latitudinal transitions, surpassed vertical gradients as the principal force governing microbial community assembly, connectivity, and stability. These horizontal factors overwhelmingly shaped microbial diversity, niche breadth, and biogeographic patterns, with prokaryotes displaying broader environmental adaptability and stronger cross-regional dispersal potential than microeukaryotes. Consequently, prokaryotes maintained higher spatial connectivity than microeukaryotes across both dimensions. This prokaryotic connectivity advantage was most pronounced within intermediate water masses. In contrast, vertical connectivity weakened with intensified water column stratification from the well-mixed Bohai Sea to the hydrographically complex South Yellow Sea. Horizontal gradients directly steered microbial co-occurrence network properties, driving a depth-dependent decline in network complexity and stability. This regional disparity was further underscored by distinct stability trade-offs: the semi-enclosed Bohai Sea fostered robust, modular networks, whereas the Yellow Sea systems formed highly connected but less modular, and thus more vulnerable, network architectures. Our findings reveal a dominant horizontal connectivity mode in coastal microbiomes, establishing a mechanistic link between large-scale environmental gradients and microbial network stability. This is a crucial advance for predicting ecological responses to anthropogenic and climate perturbations in vulnerable coastal zones. IMPORTANCE: Coastal microbial communities drive global biogeochemical cycles, yet the principles governing their large-scale connectivity and microbial network stability remain elusive, particularly in anthropogenic disturbances regions. Focusing on the Bohai-Yellow Sea system, we establish that horizontal transport processes, modulated by land-sea exchange and latitudinal gradients, override vertical stratification as the dominant force structuring microbial assembly and interaction networks. We demonstrate that prokaryotes possess a stronger horizontal dispersal advantage than microeukaryotes, sustaining higher connectivity through intermediate water layers. This horizontal connectivity governs microbial network stability. Networks shift from robust, prokaryote-driven modular architectures in shallow coastal waters to fragile, microeukaryote-dominated patterns in deeper, stratified regions. These findings define a "horizontal connectivity mode" as a central organizing principle for coastal microbiomes, moving beyond descriptive biogeography to provide a mechanistic framework for predicting community resilience to anthropogenic and climate forcing.