Ocean warming indirectly affects seagrass performance through effects on sediment microbial communities

Belowground microbes are increasingly recognised as mediators of plant responses to stress, but it remains unclear whether the thermal histories of marine plants and their associated belowground microbes influence plant performance under ocean warming. We conducted a common-garden field experiment at a long-term warmed site in Lake Macquarie (NSW, Australia, > 30 yr, 1-3°C warming), to test the effects of sediment origin (ambient vs warm-origin), plant origin (ambient vs warm-origin) and microbial disruption (intact vs disrupted rhizosphere and bulk sediment microbial communities) on seagrass (Zostera muelleri) performance. Both plant origins had lower aboveground biomass in intact warm-origin sediments, but warm-origin plants recovered when bulk sediment microbial communities were disrupted, indicating that warming-altered sediment microbial communities can suppress seagrass performance. Disrupted warm-origin sediments were enriched in sulphide-oxidising bacteria, which likely contributed to enhanced performance. In warm-origin sediments, rhizosphere bacterial communities were similar across plant origins, indicating that sediments shape rhizosphere bacterial assembly. Rhizosphere microbial disruption had no effect on plant performance. We show that ocean warming can shape sediment microbial communities in ways that suppress seagrass performance, suggesting that sediment microbial communities can override plant thermal history and act as hidden constraints on seagrass tolerance to warming.