New Insights on the Diurnal Mechanism of Calcification in the Stony Coral, Stylophora pistillata

Maayan Neder,Raoul Saar,Gilad Antler,Assaf Malik,Tali Mass

doi:10.3389/fmars.2021.745171

Abstract

Scleractinian corals are evolutionary-successful calcifying marine organisms, which utilize an endo-symbiotic relationship with photosynthetic dinoflagellate algae that supply energy products to their coral hosts. This energy further supports a higher calcification rate during the day in a process known as light enhanced calcification. Although this process has been studied for decades, the mechanisms behind it are still unknown. However, photosynthesis and respiration also cause daily fluctuations in oxygen and pH levels, resulting in the coral facing highly variable conditions. Here we correlated gene expression patterns with the physiological differences along the diel cycle to provide new insights on the daily dynamic processes, including circadian rhythm, calcification, symbiosis, cellular arrangement, metabolism, and energy budget. During daytime, when solar radiation levels are highest, we observed increased calcification rate combined with an extensive up-regulation of genes associated with reactive oxygen species, redox, metabolism, ion transporters, skeletal organic matrix, and mineral formation. During the night, we observed a vast shift toward up-regulation of genes associated with cilia movement, tissue development, cellular movement, antioxidants, protein synthesis, and skeletal organic matrix formation. Our results suggest that light enhanced calcification is related to several processes that occur across the diel cycle; during nighttime, tissue might elevate away from the skeleton, extending the calcifying space area to enable the formation of a new organic framework template. During daytime, the combination of synthesis of acid-rich proteins and a greater flux of ions to the sites of calcification facilitate the conditions for extensive mineral growth.

Highlights

Coral reefs are among the most diverse and productive ecosystems in the ocean and provide substantial economic and cultural resources (Spalding et al, 2001)
We performed Gene Ontology (GO) functional-enrichment based on kyoto encyclopedia of genes and genomes (KEGG) pathway database (Kanehisa et al, 2004) and S. pistillata Trinotate annotations to identify functional terms associated with diel cycle (Figure 2 and Supplementary Table 1)
Host Genes Associated With Photosynthesis-Dependent Oxidative Stress We found that biological processes (BP) like “antioxidant activity” terms are over-represented during the night (Figure 2H), whereas “redox” related terms were overrepresented at all time points (Figures 2A,G)

Summary

Introduction

Coral reefs are among the most diverse and productive ecosystems in the ocean and provide substantial economic and cultural resources (Spalding et al, 2001). Stony corals that form the reefs evolved during the Cambrian period (503 Ma) (McFadden et al, 2021) and are one of the first known metazoans to precipitate a calcium carbonate exoskeleton in a biologically mediated process (Knoll, 2003). This process leads to the production of approximately 4 kg calcium carbonate per square meter per year in the oceans (Smith and Kinsey, 1976). Oxygen levels have important implications on corals’ energy budget as they determine whether aerobic versus anaerobic metabolic pathways are used, which, in turn, has implications for the efficiency of the energy production (Nelson and Altieri, 2019)

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