COMMENTARY

Coral calcification feels the acid

Alexander C. Gagnon1 Earth Sciences Division and Molecular Foundry, Lawrence Berkeley National Laboratory, Berkeley, CA 94720; and School of Oceanography, University of Washington, Seattle, WA 98195

s the world’s largest reservoir tion, showing the utility of calcifying fluid of exchangeable carbon on mil- pH data (10, 11). A lennial timescales, the oceans Although the boron isotope results play a dominant role in global provide a rich picture of calcifying fluid change. Indeed, the oceans currently act pH, a number of questions remain re- as a major sink for anthropogenic carbon garding the interpretation of these data. (1), partially moderating increases in at- Specifically, it is unknown whether boron fl mospheric CO2 at the expense of a more isotopes indeed probe calcifying uid pH acidic ocean. One of the great challenges or whether physiological effects related for the next century is understanding to coprecipitation, ion transport, or other how this shift in seawater chemistry will processes act to distort the pH signal. affect marine systems. Serving as a vivid Furthermore, there are questions re- microcosm for the ocean as whole, coral garding which fractionation factor should reefs display the beauty, diversity, and be used to generate pH estimates from complexity of the ocean, while also ex- Fig. 1. Coral calcifying fluid pH decreases with boron data. Depending on the choice of hibiting the ocean’s sensitivity to envi- ocean acidification, as shown by Venn et al. (3) this factor, calcifying fluid pH is either ronmental perturbations. Built from from direct pH measurements in the tropical coral offset from seawater, as plotted in Fig. 1, a framework of CaCO skeletons, coral S. pistillata (blue boxes), and as inferred from or, with the use of an alternative frac- 3 previous boron isotope measurements (6–10). Bo- reefs are particularly sensitive to ocean tionation factor, no pH difference is fi fi ron isotope data from S. pistillata (yellow boxes) fl acidi cation because acidi ed seawater and other tropical species (yellow diamonds) found between the calcifying uid and tends to slow skeletal growth (2). Despite roughly agree with direct measurements, whereas seawater. Direct measurements of cal- the threat posed by ocean acidification to deep-sea coral (orange circles) are characterized by cifying fluid pH could help resolve these reef health, the detailed mechanisms re- higher calcifying fluid pH values and lower sensi- issues, validating the boron isotope pale- sponsible for this sensitivity are still poorly tivity to seawater pH. Compared with seawater oproxy while also establishing the role of understood. In PNAS, Venn et al. (3) (dashed line), tropical coral calcifying fluid pH is calcifying fluid pH in coral’s response to more offset under more acidified conditions. Calci- ocean acidification. address a key component of this problem, fl fying uid pH calculated from boron isotope data Early and groundbreaking attempts to providing a detailed view of the chemical- using an δ11B of total boron of 39.16 ‰, a fraction- scale changes that link coral skeletal directly measure calcifying fluid pH in ation of 1.0272, and with pKB set by temperature growth and ocean acidification. and salinity. Total pH scale is used throughout. coral relied on microelectrodes (12), but Seawater is primarily buffered by dis- extensive use of this technique has been solved inorganic carbon thorough the limited by the complexity of the method. − reduces the potential for skeletal growth, equilibria among dissolved CO2, HCO3 , As an alternative approach to micro- 2− whereas, conversely, organisms can en- and CO3 , intimately linking the acid– electrodes, confocal microscopy combined base chemistry of the ocean with carbon courage growth through pH elevation. with fluorescent probes can directly char- dynamics. Ocean acidification is a direct The balance between these two forces acterize the calcifying fluid in coral. This result of this intimate connection; subject modulates skeletal growth. Furthermore, technique relies on a unique coral culture to mass balance and charge balance con- this balance is expressed in the pH of method (13) whereby a thin sheet of straints, adding more carbon to seawater the calcifying fluid. Thus, it is vitally im- skeleton is grown across glass slides, sim- shifts the buffer state of the ocean toward portant to measure how calcifying fluid plifying skeletal geometry and allowing lower pH. At a smaller scale, many marine pH is affected by ocean acidification and optical access to the site of calcification. fi calcifiers appear to exploit the connection to understand what mechanisms regulate This approach was rst used with bulky fl between pH and inorganic carbon. Skeletal this response. uorescent dyes to demonstrate direct growth in coral occurs in an extracellular transport between seawater and the site Most current estimates of calcifying fi region termed the calcifying space, which fluid pH rely on an indirect geochemical of calci cation (14, 15). Exploiting this seawater pathway, Venn et al. (16) loaded allows coral to control local chemistry technique, the boron isotope pH proxy (5). the calcifying fluid of cultured coral with (4). By increasing the pH of the calcifying Boron isotope measurements from the fl a pH-sensitive fluorescent indicator, dem- uid in this space, coral shift dissolved skeletons of cultured tropical coral (6–8) inorganic carbon from predominantly onstrating that they could directly probe − − suggest that calcifying fluid pH is elevated HCO toward higher [CO 2 ]. This local pH. 3 3 with respect to seawater, but that this pH biological manipulation favors skeletal Following up on their earlier work, systematically decreases with seawater pH fi growth, as the thermodynamic driving Venn et al. (3) have now de nitively fl fl force for CaCO mineralization, the satu- (Fig. 1). Thus, calcifying uid pH is im- shown that calcifying uid pH decreases 3 fi fi ration state (Ω), depends in large part on pacted by ocean acidi cation. Further- with ocean acidi cation (Fig. 1) through 2− more, different species of coral seem to direct measurements in the cultured [CO3 ]. Thus, pH is a useful indicator for elevate calcifying fluid pH by different the energetics of CaCO3 biomineraliza- tion, with higher pH roughly indicating amounts (Fig. 1). In particular, deep-sea more favorable growth conditions, even coral show higher calcifying fluid pH val- Author contributions: A.C.G. wrote the paper. though several additional parameters ues and lower pH sensitivity than tropical The author declares no conflict of interest. ultimately control the Ω of a solution. species (9, 10). These results could explain See companion article on page 1634. Following this schema, ocean acidification divergent sensitivities to ocean acidifica- 1E-mail: [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1221308110 PNAS | January 29, 2013 | vol. 110 | no. 5 | 1567–1568 Downloaded by guest on September 29, 2021 tropical coral Stylophora pistillata. Com- why does seawater chemistry impact cal- like decrease in calcification rate is in- pared with boron isotope data from the cifying fluid pH at all? This question is consistent with constant alkalinity pumping. same species, directly measured pH ex- at the heart of the ocean acidification Furthermore, a constant alkalinity-pumping hibits a somewhat steeper sensitivity to problem and is also key for understanding model cannot explain compositional pat- acidification, but this slope is reasonably what sets the sensitivity of the boron terns found in coral cultured at higher similar to boron-isotope–derived slopes isotope proxy. than ambient pH (20). In these nonacidified from other tropical coral. Although only conditions, coral may regulate alkalinity one species of coral has been measured pumping to reach a target calcifying fluid fl Venn et al. have now by the uorescence method thus far, pH. This alternative hypothesis predicts the rough agreement between the two definitively shown that that calcifying fluid pH should remain techniques is exciting: direct pH mea- relatively constant at higher than ambient surements appear to affirm that boron fl fl calcifying uid pH seawater pH values, a pattern that may isotopes measure calcifying uid pH in be followed in deep-sea coral (Fig. 1) and coral. If this interpretation is correct, the decreases with ocean that is a clear target for future experiments boron isotope proxy must respond to pH in tropical coral. Alternatively, McCulloch indirectly: the signal is first filtered through acidification. et al. (10) propose that calcifying fluid the physiology of biomineralization. pH and skeletal growth rates are ulti- Clearly, further experiments across a range of different coral will be necessary to con- Local pH elevation is thought to be mately limited by the energy required to firm this picture—but the path forward controlled through alkalinity pumping, maintain a particular pH gradient. Indeed, is promising. as supported by geochemical arguments the metabolic cost of pH regulation and the At a more fundamental level, we need (17) and by the presence of a biological effect of this process on an organism-scale to understand why calcifying fluid varies pump in coral that is capable of exchang- energy balance is likely to play a major role + 2+ fi with external pH and what modulates this ing 2H for Ca across cell membranes in modulating the impact of ocean acidi - fi sensitivity. One key observation, first noted (18). If the rate of this alkalinity pumping cation on marine calci ers. Probing the by using boron isotopes (10, 11) and now is insensitive to seawater pH, calcification mechanism of coral biomineralization is confirmed through direct measurements rates and calcifying fluid pH would de- clearly an area of intensely active research, (3), is that the pH offset between calcifying crease with ocean acidification. This but, by using the technique demonstrated fluid and seawater increases with acidifi- model can explain compositional patterns by Venn et al. (3), as well as a growing cation; coral build a stronger pH gradient and growth rate sensitivity in some culture set of biological and geochemical tools, at lower pH. Given that coral actively alter experiments (19). However, Venn et al. we are finally poised to understand at calcifying fluid pH, with an even stronger (3) use their pH results together with a chemical scale how and why coral calci- biological effect under harsher conditions, growth rate data to show that a threshold- fication feels ocean acidification.

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