Dynamic microbiome turnover and glycerol-3-phosphate-linked metabolic adjustments underlie resilience to desiccation in intertidal algae.

Abstract

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.