Effects of Caulerpa taxifolia on Physiological Processes and Gene Expression of Acropora hyacinthus during Thermal Stress

SIMPLE SUMMARY: This study explored the crucial issue of how the physiology and molecular response of the hermatypic coral Acropora hyacinthus was affected by the foliaceous macroalgae Caulerpa taxifolia at various temperatures. Therefore, the different ways including indirect and direct coculturing with seaweed were set up at an ambient temperature (27 °C) and at a +3 °C increase. Firstly, the results demonstrated that macroalgae could prominently trigger a drop in the density of zooxanthellae at various temperatures, which has been associated with the biological processes of vesicle transport, autophagy, and apoptosis regulated by the Rab5, ATG5, and Casp7 transcription factors. Secondly, oxidative stress (CAT, SODC, HPS family) and microbial immune response (IFI47, TRAF family) biological processes were violently aggravated by heat stress, resulting in cell apoptosis, at which point Caulerpa taxifolia alleviated the pressure influences. ABSTRACT: An increasing ecological phase shift from coral-dominated reefs to macroalgae-dominated reefs as a result of anthropogenic impacts, such as eutrophication, sedimentation, and overfishing, has been observed in many reef systems around the world. Ocean warming is a universal threat to both corals and macroalgae, which may alter the outcome of competition between them. Therefore, in order to explore the effects of indirect and direct exposure to macroalgae on the physiological, biochemical, and genetic expression of corals at elevated temperature, the coral Acropora hyacinthus and highly invasive green algae Caulerpa taxifolia were chosen. Physiologically, the results exhibited that, between the control and direct contact treatments, the density and chlorophyll a content of zooxanthella decreased by 53.1% and 71.2%, respectively, when the coral indirectly contacted with the algae at an ambient temperature (27 °C). Moreover, the enzyme activities of superoxide dismutase (SOD) and catalase (CAT) in coral tissue were enhanced by interacting with algae. After an increase of 3 °C, the density and chlorophyll a content of the zooxanthella reduced by 84.4% and 93.8%, respectively, whereas the enzyme activities of SOD and CAT increased 2.3- and 3.1-fold. However, only the zooxanthellae density and pigment content decreased when Caulerpa taxifolia was co-cultured with Acropora hyacinthus at 30 °C. Molecularly, different from the control group, the differentially expressed genes (DEGs) such as Rab family, ATG family, and Casp7 genes were significantly enriched in the endocytosis, autophagy, and apoptosis pathways, regardless of whether Acropora hyacinthus was directly or indirectly exposed to Caulerpa taxifolia at 27 °C. Under thermal stress without algae interaction, the DEGs were significantly enriched in the microbial immune signal transduction pathways, such as the Toll-like receptor signaling pathway and TNF signaling pathway, while multiple cellular immunity (IFI47, TRAF family) and oxidative stress (CAT, SODC, HSP70) genes were upregulated. Inversely, compared with corals without interaction with algae at 30 °C, the DEGs of the corals that interacted with Caulerpa taxifolia at 30 °C were remarkably enriched in apoptosis and the NOD-like receptor signaling pathway, including the transcription factors such as the Casp family and TRAF family. In conclusion, the density and chlorophyll a content of zooxanthella maintained a fading tendency induced by the macroalgae at ambient temperatures. The oxidative stress and immune response levels of the coral was elevated at 30 °C, but the macroalgae alleviated the negative effects triggered by thermal stress.