Unique high-temperature tolerance mechanisms of zoochlorellae Symbiochlorum hainanensis derived from scleractinian coral Porites lutea

Abstract

ABSTRACT Global warming is a key issue that causes coral bleaching mainly because of the thermosensitivity of zooxanthellae. Compared with the well-studied zooxanthellae Symbiodiniaceae in coral holobionts, we rarely know about other coral symbiotic algae, let alone their thermal tolerance. In this study, a zoochlorellae, Symbiochlorum hainanensis, isolated from the coral Porites lutea, was proven to have a threshold temperature of 38°C. Meanwhile, unique high-temperature tolerance mechanisms were suggested by integrated transcriptomics and real-time quantitative PCR, physiological and biochemical analyses, and electron microscopy observation. Under heat stress, S. hainanensis shared some similar response strategies with zooxanthellae Effrenium sp., such as increased ascorbate peroxidase, glutathione peroxidase, superoxide dismutase activities and chlorophyll a, thiamine, and thiamine phosphate contents. In particular, more chloroplast internal layered structure, increased CAT activity, enhanced selenate reduction, and thylakoid assembly pathways were highlighted for S. hainanensis ’s high-temperature tolerance. Notably, it is the first time to reveal a whole selenate reduction pathway from SeO 4 2− to Se 2− and its contribution to the high-temperature tolerance of S. hainanensis . These unique mechanisms, including antioxidation and maintaining photosynthesis homeostasis, efficiently ensure the high-temperature tolerance of S. hainanensis than Effrenium sp. Compared with the thermosensitivity of coral symbiotic zooxanthellae Symbiodiniaceae, this study provides novel insights into the high-temperature tolerance mechanisms of coral symbiotic zoochlorellae S. hainanensis , which will contribute to corals’ survival in the warming oceans caused by global climate change. IMPORTANCE The increasing ocean temperature above 31°C–32°C might trigger a breakdown of the coral-Symbiodiniaceae symbioses or coral bleaching because of the thermosensitivity of Symbiodiniaceae; therefore, the exploration of alternative coral symbiotic algae with high-temperature tolerance is important for the corals’ protection under warming oceans. This study proves that zoochlorellae Symbiochlorum hainanensis can tolerate 38°C, which is the highest temperature tolerance known for coral symbiotic algae to date, with unique high-temperature tolerance mechanisms. Particularly, for the first time, an internal selenium antioxidant mechanism of coral symbiotic S. hainanensis to high temperature was suggested.