A new conceptual model of coral biomineralisation: hypoxia as the physiological driver of skeletal extension

Abstract

That corals skeletons are built of aragonite crystals with taxonomy-linked ultrastructure has been well understood since the 19th century. Yet, the way by which corals control this crystallization process remains an unsolved question. Here, I outline a new conceptual model of coral biomineralisation that endeavours to relate known skeletal features with homeostatic functions beyond traditional growth (structural) determinants. In particular, I propose that the dominant physiological driver of skeletal extension is night-time hypoxia, which is exacerbated by the respiratory oxygen demands of the coral's algal symbionts (= zooxanthellae). The model thus provides a new narrative to explain the high growth rate of symbiotic corals, by equating skeletal deposition with the "work-rate" of the coral host needed to maintain a stable and beneficial symbiosis. In this way, coral skeletons are interpreted as a continuous (long-run) recording unit of the stability and functioning of the coral–algae endosymbiosis. After providing supportive evidence for the model across multiple scales of observation, I use coral core data from the Great Barrier Reef (Australia) to highlight the disturbed nature of the symbiosis in recent decades, but suggest that its onset is consistent with a trajectory that has been followed since at least the start of the 1900s. In concluding, I outline how the proposed capacity of cnidarians (which includes modern reef corals) to overcome the metabolic limitation of hypoxia via skeletogenesis also provides a new hypothesis to explain the sudden appearance in the fossil record of calcified skeletons at the Precambrian–Cambrian transition – and the ensuing rapid appearance of most major animal phyla

Effects of elevated pCO2 and feeding on net calcification and energy budget of the Mediterranean cold-water coral Madrepora oculata

“…Earlier measurements of RQ in zooxanthellate corals ranged between 0.7 and 1.0 (Gattuso and Jaubert, 1990), which is also the range of values for aerobic metabolism. The high values found in the present study might consequently be due to anaerobic glycolysis driving calcification as suggested by Wooldridge (2013), via the glyoxylate cycle, which was shown to be present in cnidarians (Kondrashov et al, 2006). As RQ is calculated as the number of moles of CO 2 released per mole of O 2 consumed, the lack of O 2 consumption during anaerobic conditions could lead to RQ values higher than 1.…”

Corals sustain growth but not skeletal density across the Florida Keys Reef Tract despite ongoing warming

“…At moderate temperatures, coral growth accelerates with increasing temperature (Lough & Barnes, ); however, once a thermal optimum is reached, calcification declines with further warming (Castillo, Ries, Bruno, & Westfield, ; Jokiel & Coles, ). Recent theory supports the existence of such an optimum based on physiological factors known to regulate biomineralization (Wooldridge, ). Moreover, a comprehensive record of Porites growth rates from the Great Barrier Reef reflects this pattern temporally, with an extended period of increasing calcification until 1990 followed by a drastic decline throughout the modern era of climate warming (De'ath et al, ).…”

Immunolocalization of skeletal matrix proteins in tissue and mineral of the coral Stylophora pistillata

“…3 A and B) (15). Each layer is ∼2 to 5 μm thick, which likely represents a single day's growth (22,51). The thickening of the septa is ensured by superimposition of growth layers that surround the EMZ (14, 15, 52).…”

“…Recently, it was suggested that each couplet of organic-seed (e.g., negative etching) and fiber interaction represents a single 24-h period (22). However, despite numerous biochemical and structural studies, the precise localization of distinct SOM proteins and how these proteins interact with the mineral remains poorly understood.…”