Impact of seawater acidification on pH at the tissue–skeleton interface and calcification in reef corals

Abstract

Insight into the response of reef corals and other major marine calcifiers to ocean acidification is limited by a lack of knowledge about how seawater pH and carbonate chemistry impact the physiological processes that drive biomineralization. Ocean acidification is proposed to reduce calcification rates in corals by causing declines in internal pH at the calcifying tissue-skeleton interface where biomineralization takes place. Here, we performed an in vivo study on how partial-pressure CO 2 -driven seawater acidification impacts intracellular pH in coral calcifying cells and extracellular pH in the fluid at the tissue-skeleton interface [subcalicoblastic medium (SCM)] in the coral Stylophora pistillata. We also measured calcification in corals grown under the same conditions of seawater acidification by measuring lateral growth of colonies and growth of aragonite crystals under the calcifying tissue. Our findings confirm that seawater acidification decreases pH of the SCM, but this decrease is gradual relative to the surrounding seawater, leading to an increasing pH gradient between the SCM and seawater. Reductions in calcification rate, both at the level of crystals and whole colonies, were only observed in our lowest pH treatment when pH was significantly depressed in the calcifying cells in addition to the SCM. Overall, our findings suggest that reef corals may mitigate the effects of seawater acidification by regulating pH in the SCM, but they also highlight the role of calcifying cell pH homeostasis in determining the response of reef corals to changes in external seawater pH and carbonate chemistry.he impacts of ocean acidification on marine calcifying organisms are predicted to be varied and in many cases deleterious (1-3). Though several studies on marine calcifiers have investigated how rates of calcification respond to ocean acidification scenarios (4), comparatively few studies tackle how ocean acidification impacts the physiological mechanisms that drive calcification itself. A mechanistic understanding of calcification responses to shifts in external seawater pH and carbonate chemistry is critical to predicting how corals and other major marine calcifiers respond and potentially acclimate to ocean acidification (5).The calcium carbonate (aragonite) skeletons of scleractinian corals make up a large component of shallow and deepwater reefs at both tropical and temperate latitudes. Corals form their skeletons by producing aragonite crystals in a fluid-filled medium called the subcalicoblastic medium (SCM) underlying the calcifying tissue [calicoblastic epithelium (CE)] (Fig. S1). The calicoblastic epithelium promotes calcification by exerting biological control over the SCM in a number of ways (reviewed in refs. 6 and 7). One important process is that the CE elevates pH in the SCM (pH SCM ) relative to the exterior seawater pH (8), possibly by the removal of protons via a by a Ca 2+ ATPase (9-12). This increase in pH SCM favors the conversion of bicarbonate to carbonate, elevating the saturation state ...

Corals concentrate dissolved inorganic carbon to facilitate calcification

“…Skeletal d 11 B ECF pH estimates ( Fig. 1; Table 1) confirm that corals actively increase the pH of the ECF above that of seawater 12,16 . The ECF composition reflects the balance of DIC inputs and outputs, namely, seawater diffusion, molecular CO 2 invasion, proton extrusion and calcification (Fig.…”

“…Corals were analysed in duplicate (indicated by 1 or 2 annotation). Analyses (7)(8)(9)(10)(11)(12)(13)(14)(15)(16) were collected on each sample (Table 1) with the exceptions of RR 3.7 mM 2 and RR 5.3 mM 1 where only 2 and 1, respectively, credible d 11 B analysis (exhibiting the 42 Ca spike throughout the analysis) were obtained. Errors are calculated as for the field corals and horizontal lines denote seawater concentrations calculated from observations of pH and TA in the culture seawater 22 .…”

Breakdown of coral colonial form under reduced pH conditions is initiated in polyps and mediated through apoptosis

“…Similar indications originate from multiple laboratory experiments under high-CO 2 conditions, with a wide variety of calcifying marine species, including corals, that exhibit reduced calcification and growth rates (17,24). Under these conditions, corals must invest more energy to maintain homeostasis (25) and to continue depositing skeleton (26). Therefore, the occurrence of increased apoptosis resulting in tissue loss of the coenosarc in pH-stressed corals could be a mechanism whereby colonial corals rid themselves of energetically costly processes (e.g., calcification) and tissues.…”

Biomineralization in perforate foraminifera

“…Compared to foraminifera, biomineralization in corals (Al-Horani et al, 2003;Sinclair and Risk, 2006;Venn et al, 2013), coccolithophores (Marsh, 2003;Taylor et al, 2011;Ziveri et al, 2012;Bach et al, 2013), gastropods (e.g. Nehrke and Nouet, 2011) and bivalves (Nudelman et al, 2006;Nehrke et al, 2012;Shi et al, 2013) are understood in greater detail.…”