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Tolerance to extreme dehydration has emerged across the tree of life, yet current understanding relies heavily on terrestrial host traits. Marine lineages facing rapid, tide-driven hydration oscillations remain largely unexplored. We used Pyropia haitanensis as a model to determine if intertidal resilience arises from a coordinated holobiont strategy. We integrated time-resolved microbiome profiling and metagenomics. Mechanisms were validated through multi-omics of desiccation-stressed bacterial isolates, inoculation, and antibiotic-depletion experiments, and host physiological assessment. Rapid drying reshaped the microbiome through selective loss of osmosensitive taxa and occupation by stress-tolerant lineages, whereas rehydration promoted selective recolonization and network recovery. Metagenomic analysis revealed enrichment of functional potential for microbial antioxidant, osmoprotective, and extracellular polysaccharide pathways, alongside enrichment of glycerol-3-phosphate (G3P) ABC transporter modules. Host G3P secretion increased, creating a selective nutrient niche that recruited symbionts possessing specialized G3P transporters. Inoculation and microbiota-depletion experiments established a causal role for the microbiome in host resilience. Keystone isolates Sulfitobacter sp. and Alteromonas sp. utilized host-derived G3P to fuel complementary protective mechanisms, with their combination outperforming either taxon alone. These findings highlight an integrated host-microbiome partnership shaped by tidal filtering, a cross-domain strategy that buffers hydration stress and supports intertidal resilience and mariculture practices.
Wang et al. (Thu,) studied this question.