Extremely heat tolerant photo-symbiosis in a shallow marine benthic foraminifera

Bleaching, the loss of algal symbionts, occurs in marine photosymbiotic organisms at water temperatures minimally exceeding average summer SST (sea surface temperatures). Pre-adaptation allows organisms to persist under warmer conditions, providing the tolerance can be carried to new habitats. Here we provide evidence for the existence of such adaptation in the benthic foraminifera Pararotalia calcariformata. This species occurs at a thermally polluted site in the Mediterranean, where water temperatures reach a maxima daily average of 36 °C during the summer. To test whether this occurrence represents a widespread adaptation, we conducted manipulative experiments exposing this species from an unpolluted site to elevated temperatures (20-42 °C). It was kept in co-culture with the more thermally sensitive foraminifera Amphistegina lobifera in two experiments (20-36 °C). Reduced photosynthetic activity in A. lobifera occurred at 32 °C whereas photochemical stress in P. calcariformata was first observed during exposure to 36 °C. Pararotalia calcariformata survived all treatment conditions and grew under 36 °C. The photosymbiosis in P. calcariformata is unusually thermally tolerant. These observations imply that marine eukaryote-eukaryote photosymbiosis can respond to elevated temperatures by drawing on a pool of naturally occurring pre-adaptations. It also provides a perspective on the massive occurrence of symbiont-bearing foraminifera in the early Cenozoic hothouse climate.