December 2015, Amsterdam

Conceptual model of stony coral calcification under ocean acidification

The image below gives an overview of calcification processes that hypothetically occur in stony corals at decreasing seawater pH. Thick lines indicate stronger fluxes than thin lines.

Why?

Calcium carbonate (CaCO₃) deposits constitute the structural backbone of coral reefs. As three-dimensional framework, reef deposits are home to a great diversity of fish, crustaceans, worms, mollusks, echinoderms, tunicates, sponges and cnidarians. However, at the moment, ocean acidification threatens CaCO₃ deposits at the reef, as CaCO₃ dissolves at low pH.

Stony corals are the principal producers of CaCO₃ deposits of coral reefs. In stony corals, calcium deposits are located below 2 or 4 layers of coral tissue (1 layer epidermis, at most sites 2 layers gastrodermis, and 1 layer calicodermis). For this reason, corals can exert some control over the pH at the site of their CaCO₃ deposits. Since this control has not fully been characterized, the precise impact of ocean acidification on stony coral calcification is unknown.

What do you see?

This conceptual model distinguishes three scenarios:

1. At ambient seawater pH (pH = 8), metabolic carbon dioxide (CO₂), seawater bicarbonate (HCO₃^-) and seawater carbonate (CO₃^2-) are used to produce CaCO₃. Metabolic CO₂ is transferred along the diffusion gradient (that is, along decreasing acidity) from the calicodermis to the calcification site. Enzymes called Ca²⁺ ATPases remove protons that enter the calcification site with seawater influx, and protons that are produced by the calcification reactions. While transcellular seawater proton input is depicted here, it may also occur paracellularly.
2. In an acidified seawater scenario (pH = 7.5), 1) more protons enter the calcification site with seawater influx; 2) proton efflux is hampered by a decreased diffusion gradient over the coral-seawater interface; and 3) the availability of CO₃^2- ions decreases, resulting in an increased production of protons by calcification. Plasma membrane Ca²⁺ ATPases are enhanced to promote proton efflux, yet pH at the calcification site decreases proportionally to the decrease in seawater pH. The influx of metabolic CO₂ from the calicodermis decreases. An increased proportion of organic matrix supports and strengthens the skeleton at lower pH. Coral metabolism is enhanced to meet increased energetic demands.
3. When the decrease in external pH exceeds the coral its pH tolerance (roughly pH≤7), the intracellular pH of the calicodermis cannot be maintained. This likely collapses cellular homeostasis and may suppress coral metabolism, disrupting the biological control over calcification and/or reducing the acquisition of metabolic energy and CO₂ for biocalcification.

In other words, corals are hypothesized to compensate for the adverse effects of ocean acidification until a certain tipping point (roughly, seawater pH≤7) where cells become too acidic to function properly. Corals could compensate for decreasing seawater pH, for instance, by pumping protons away from the CaCO₃ skeleton. Or by producing organic matrix constituents that support the CaCO₃ skeleton. If so, corals need to invest more energy to maintain and keep producing CaCO₃ deposits in acidifying waters.

Holobiont interactions

Corals do not calcify in solitude; they are accompanied by a great diversity of symbiotic microbes, ranging from zooxanthellae to protists, fungi, archaea and bacteria. Together, the coral host and all its symbionts are called the coral holobiont. Some microbes inhabiting corals are agents of coral disease. Others are beneficial to coral health. Using the conceptual model as a starting point, we identified three possible ways in which symbionts could contribute to coral calcification. These are:

1. The supply of reactants to the calcification site, including organic matrix constituents and CaCO₃ reactants.
2. Removal of inhibitory compounds from the calcification site, such as protons, CO₂ and inhibitory phosphates.
3. Supply of energy to the coral, by providing oxygen or photoassimilates.

Given these possibilities for coral symbionts to help corals calcify, could changes in coral symbiont composition - in favour of symbionts that contribute to coral calficiation - help corals to sustain calcification in acidifying oceans? This question relates to the so-called hologenome theory of evolution. It is discussed in my literature review.

Related content

Support for the conceptual model on coral calcification, examples of potential symbiotic interactions with coral calcification and the likeliness of hologenome driven evolution of coral calcification are discussed in my literature review.