Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta

Symbiosis between reef-building corals and unicellular algae (Symbiodiniaceae) fuels the growth and productivity of corals reefs. Capacity for Symbiodiniaceae to fix inorganic carbon (Ci) and translocate carbon compounds to the host is central to coral health, but how these processes change for corals thriving in environmental extremes remains largely unresolved. We investigate how a model coral— Pocillopora acuta— persists from a reef habitat into an adjacent extreme mangrove lagoon on the Great Barrier Reef. We combine respirometry and photophysiology measurements, Symbiodiniaceae genotyping, and 13 C labelling to compare P. acuta metabolic performance across habitats, in relation to the Ci uptake and translocation capacity by symbionts’ autotrophy. We show that differences in P. acuta metabolic strategies across habitats align with a shift in dominant host-associated Symbiodiniaceae taxon, from Cladocopium in the reef to Durusdinium in the mangroves. This shift corresponded with a change in “photosynthetic strategy”, with P. acuta in the mangroves utilising absorbed light for photochemistry over non-photochemical quenching. Mangrove corals translocated similar proportions of carbon compared to the reefs, despite a lower Ci uptake. These trends indicate that coral survival in mangrove environments occurs through sustained translocation rate of organic compounds from coral symbionts to host.