The Origin and Role of Organic Matrix in Coral Calcification: Insights From Comparing Coral Skeleton and Abiogenic Aragonite

Abstract

Understanding the mechanisms of coral calcification is critical for accurately projecting coral reef futures under ocean acidification and warming. Recent suggestions that calcification is primarily controlled by organic molecules and the biological activity of the coral polyp imply that ocean acidification may not affect skeletal accretion. The basis for these suggestions relies heavily on correlating the presence of organic matter with the orientation and disorder of aragonite crystals in the skeleton, carrying the assumption that organic matter observed in the skeleton was produced by the polyp to control calcification. Here we use Raman spectroscopy to test whether there are differences in organic matter content between coral skeleton and abiogenic aragonites precipitated from seawater, both before and after thermal annealing (heating). We measured the background fluorescence and intensity of C-H bonding signals in the Raman spectra, which are commonly attributed to coral polyp-derived skeletal organic matrix (SOM) and have been used to map its distribution. Surprisingly, we found no differences in either fluorescence or C-H bonding between abiogenic aragonite and coral skeleton. Annealing reduced the molecular disorder in coral skeleton, potentially due to removal of organic matter, but the same effect was also observed in the abiogenic aragonites. The presence of organic molecules in the abiogenic aragonites is further supported by measurements of N content and δ 15 N. Together, our data suggest that some of what has been interpreted in previous studies as polyp-derived SOM may actually be seawater-sourced organic matter or some other signal not unique to biogenic aragonite. Finally, we create a high-resolution Raman map of a Pocillopora skeleton to demonstrate how patterns of fluorescence and elevated calcifying fluid aragonite saturation state ( Ar ) along centers of calcification are consistent with both biological and physico-chemical controls. Our aim is to advance discussion on biological mediation of calcification and the implications for coral resilience in a high-CO 2 world.

Investigating marine bio‐calcification mechanisms in a changing ocean with in vivo and high‐resolution ex vivo Raman spectroscopy

“…The ~10-20 μm wide oscillations of Ω Ar in the S. pistillata specimen (Figure 3b) may reflect daily bands. Additionally, we observed elevated Ω Ar at the centers of calcification (COCs; the yellow band indicating high Ω Ar in the center of the skeletal spine in Figure 3d), consistent with previous Raman analyses of P. damicornis (DeCarlo, Ren, & Farfan, 2018) and Porites lutea (Wall & Nehrke, 2012). The deep-sea cup coral, D. dianthus, showed complex patterns of Ω Ar , with a central axis of centers of calcification in addition to fine-scale Ω Ar banding throughout the skeleton (Figure 3e).…”

“…Raman spectroscopy has recently been applied to quantify the response of corals, coralline algae, and fish otoliths to simulated ocean acidification (Coll-Lladó, Giebichenstein, Webb, Bridges, & de la serrana, 2018;Comeau et al, 2018;Cornwall et al, 2018;DeCarlo et al, 2017;DeCarlo, Ren et al, 2018;Foster & Clode, 2016;Kamenos et al, 2013;Kamenos, Perna, Gambi, Micheli, & Kroeker, 2016). While these studies have revealed changes in both the mineralogy and disorder of calcified structures under ocean acidification, they have so far conducted Raman spectroscopy analyses of powders or made spot measurements on intact samples.…”

“…Organic matrices may also play an important role in calcification for some taxa, and Raman spectroscopy has been used to characterize their distribution in shells and skeletons (DeCarlo, Ren et al, 2018;Von Euw et al, 2017;Jolivet, Bardeau, Fablet, Paulet, & Pontual, 2013;Nehrke et al, 2011). Furthermore, studies of simulated ocean acidification and warming can quantify changes in calcifying fluid Ω Ar of corals, and mineralogy of coralline algae and foraminifera, without sacrificing experimental replicates (Box 1).…”

Regulation of ion transport and energy metabolism enables certain coral genotypes to maintain calcification under experimental ocean acidification

“…They are sensitive to internal pH (reviewed by Busa, 1986), with increased pH leading to depolymerization (Regula, Pfeiffer, & Berlin, 1981). The upregulation of microtubule associated GO terms in Colony 4 may point to the role that the organic matrix has in facilitating carbonate precipitation (DeCarlo, Ren, & Farfan, 2018). Coupled with the upregulation of proton transport and energy metabolism, these gene ontology terms probably explain the capacity for the genotype represented by Colony 4 to withstand ocean acidification for weeks.…”

Mineralogy of Deep-Sea Coral Aragonites as a Function of Aragonite Saturation State

“…This argument is based primarily on the idea that coral aragonite is formed via an amorphous calcium carbonate (ACC) precursor phase (Mass et al, 2017;Von Euw et al, 2017) that is predominantly driven by proteins such as coral acid-rich proteins (CARPs) (Mass et al, 2013) or a skeletal organic matrix that can precipitate aragonite regardless of surrounding seawater aragonite saturation states. Yet, the notion that calcification is entirely controlled by organic matrices regardless of seawater chemistry is not supported by observations that abiogenic aragonites precipitated from seawater contain similar amounts of organics as coral skeletons (DeCarlo et al, 2018), and it is inconsistent with many coral culturing experiments (Chan and Connolly, 2013).…”