pubmed.ncbi.nlm.nih.gov

Coral calcification in a changing World and the interactive dynamics of pH and DIC upregulation - PubMed

️Sun Jan 01 2017

Coral calcification in a changing World and the interactive dynamics of pH and DIC upregulation

Malcolm T McCulloch et al. Nat Commun. 2017.

Abstract

Coral calcification is dependent on the mutualistic partnership between endosymbiotic zooxanthellae and the coral host. Here, using newly developed geochemical proxies (δ¹¹B and B/Ca), we show that Porites corals from natural reef environments exhibit a close (r² ∼0.9) antithetic relationship between dissolved inorganic carbon (DIC) and pH of the corals' calcifying fluid (cf). The highest DIC_cf (∼ × 3.2 seawater) is found during summer, consistent with thermal/light enhancement of metabolically (zooxanthellae) derived carbon, while the highest pH_cf (∼8.5) occurs in winter during periods of low DIC_cf (∼ × 2 seawater). These opposing changes in DIC_cf and pH_cf are shown to maintain oversaturated but stable levels of carbonate saturation (Ω_cf ∼ × 5 seawater), the key parameter controlling coral calcification. These findings are in marked contrast to artificial experiments and show that pH_cf upregulation occurs largely independent of changes in seawater carbonate chemistry, and hence ocean acidification, but is highly vulnerable to thermally induced stress from global warming.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing financial interests.

Figures

**Figure 1. Mechanisms involved in coral calcification.**
Calcification occurs within the subcalicoblastic space from an initial seawater-derived fluid with additional metabolic sourced supply of DIC. Elevation of calcifying fluid pH_cf occurs via removal of protons from the calcification site by Ca²⁺-ATPase exchangers. The carbonic anhydrases (CA) catalyse the forward reactions converting CO₂ into HCO₃⁻ ions. Transfer of DIC into the subcalicoblastic space may occur via diffusion of CO₂ and/or by HCO₃⁻ pumping via bicarbonate anion transporters (BAT). The link between the activity of zooxanthellae located in the oral coral endoderm tissue to the generation of metabolic DIC within the aboral endoderm and calicoblastic cells (orange) and transport to the calcifying fluid remains uncertain (Figure modified from McCulloch *et al*.31).

**Figure 2. Seasonal time series of coral calcifying fluid pH_cf and DIC_cf.**
(a) *Porites* spp. coral calcifying fluid pH_cf derived from δ¹¹B systematics (see ‘Methods’ section and Supplementary Data) for colonies D-2 and D-3 from Davies Reef (18.8° S) in the Great Barrier Reef, Queensland. Shading denotes the summer period when pH_cf and seawater pH_sw values are at a minimum. Dashed line shows pH*_cf expected from artificial experimental calibrations (pH*_cf=0.32 pH_sw+5.2) with an order of magnitude lower seasonal range than measured pH_cf values. (b) Same as previous for *Porites* colonies from Coral Bay (CB-1 and CB-2) in the Ningaloo Reef of Western Australia (23.2° S) showing seasonal fluctuations in pH_cf and seawater pH_sw. The blue shading denotes the anomalously cool summer temperatures in 2010. (c) Enrichments in calcifying fluid DIC_cf (left axis; coloured circles) derived from combined B/Ca and δ¹¹B systematics together with synchronous seasonal variations in reef-water temperatures (right axis; black line) for *Porites* colonies from Davies Reef (GBR). The strong temperature/light control on DIC_cf is consistent with enhanced metabolic activity of zooxanthellae symbionts in summer. (d) Same as previous but for *Porites* from Coral Bay (Ningaloo Reef, Western Australia).

**Figure 3. Covariation between calcifying fluid parameters Ω_cf versus seasonal temperature and pH_cf versus DIC_cf.**
(a) Covariation of calcifying fluid saturation state (Ω_cf) with reef-water temperature showing a five- to sixfold elevation in Ω_cf relative to reef-waters for *Porites* corals from Davies Reef (D-2 and D-3) in the Great Barrier Reef and from Coral Bay (CB-1 and CB-2) in the Ningaloo Reef. Note the very narrow range (±5 to ±10%) of high Ω_cf values for each colony. (b) Subparallel arrays of inversely correlated (r²=0.88–0.94) calcifying fluid pH_cf and DIC_cf/DIC_sw values reflecting specific bio-environmental controls at the colony level on metabolic DIC_cf/DIC_sw. Seasonal variations in metabolic supplied DIC_cf are offset by opposing changes in pH_cf that act to moderate the overall variations in Ω_cf, the ultimate controller of skeletal growth rates.

**Figure 4. Seasonal time series of calcifying fluid pH_cf and Ω_cf together with calculated calcification rates G.**
(a) Calcifying fluid pH_cf and Ω_cf values for *Porites* coral (D-2) from Davies Reef (GBR), where Ω_cf=[Ca²⁺]_cf [CO₃²⁻]_cf/K_arag. Dashed line shows the Ω*_cf calculated using fixed experimental pH*_cf values (see Fig. 2a,b). (b) Same as previous for Coral Bay (Ningaloo Reef, Western Australia) *Porites* (CB-2). (c) Calcification rates calculated using the inorganic rate equation G=k(Ω−1)ⁿ, where k and n are the temperature-dependent constant and order of the reaction, respectively. Because of opposing changes in pH_cf relative to DIC_cf (Fig. 1), Ω_cf and hence coral growth rates are strongly modulated reducing seasonal variations by twofold compared to those estimated from fixed condition experiments (G*). (d) Same as previous for *Porites* from Coral Bay (Ningaloo Reef, Western Australia).

**Figure 5. Experimentally determined B/Ca partition coefficient as a function of hydrogen ion concentration.**
Measured B/Ca partition coefficient (K_D) as defined by equation (4) from the data of Holcomb *et al*. The line represents a best-fit exponential curve to the data with K_D^B/Ca=K_D,0 exp([H⁺]_T), where K_D,0=2.97±0.17 × 10⁻³ (±95% CI), =0.0202±0.042, r²=0.64 and n=63. The range for pH_cf of upregulating calcifiers (that is, *Porites* spp.) is between ∼8 and ∼9 (shaded); equivalent to [H⁺]_T of between 1 and 10 nmol kg⁻¹ giving a range in K_D^B/Ca (× 10⁻³) of 2.6–2.8, and therefore relatively in-sensitive to changes in coral pH_cf. Importantly, our experimentally determined K_D^B/Ca value is an order of magnitude higher than the previous estimate by Allison *et al*., (open diamond) and consistent with the substitution of B(OH)₄⁻ with CO₃²⁻.

formula image — **Figure 5. Experimentally determined B/Ca partition coefficient as a function of hydrogen ion concentration.**
Measured B/Ca partition coefficient (K_D) as defined by equation (4) from the data of Holcomb *et al*. The line represents a best-fit exponential curve to the data with K_D^B/Ca=K_D,0 exp([H⁺]_T), where K_D,0=2.97±0.17 × 10⁻³ (±95% CI), =0.0202±0.042, r²=0.64 and n=63. The range for pH_cf of upregulating calcifiers (that is, *Porites* spp.) is between ∼8 and ∼9 (shaded); equivalent to [H⁺]_T of between 1 and 10 nmol kg⁻¹ giving a range in K_D^B/Ca (× 10⁻³) of 2.6–2.8, and therefore relatively in-sensitive to changes in coral pH_cf. Importantly, our experimentally determined K_D^B/Ca value is an order of magnitude higher than the previous estimate by Allison *et al*., (open diamond) and consistent with the substitution of B(OH)₄⁻ with CO₃²⁻.

Cited by

Using B isotopes and B/Ca in corals from low saturation springs to constrain calcification mechanisms.
Wall M, Fietzke J, Crook ED, Paytan A. Wall M, et al. Nat Commun. 2019 Aug 8;10(1):3580. doi: 10.1038/s41467-019-11519-9. Nat Commun. 2019. PMID: 31395889 Free PMC article.
Thermal stress reduces pocilloporid coral resilience to ocean acidification by impairing control over calcifying fluid chemistry.
Guillermic M, Cameron LP, De Corte I, Misra S, Bijma J, de Beer D, Reymond CE, Westphal H, Ries JB, Eagle RA. Guillermic M, et al. Sci Adv. 2021 Jan 8;7(2):eaba9958. doi: 10.1126/sciadv.aba9958. Print 2021 Jan. Sci Adv. 2021. PMID: 33523983 Free PMC article.
The Evolution of Calcification in Reef-Building Corals.
Wang X, Zoccola D, Liew YJ, Tambutte E, Cui G, Allemand D, Tambutte S, Aranda M. Wang X, et al. Mol Biol Evol. 2021 Aug 23;38(9):3543-3555. doi: 10.1093/molbev/msab103. Mol Biol Evol. 2021. PMID: 33871620 Free PMC article.
Ion transporter gene expression is linked to the thermal sensitivity of calcification in the reef coral Stylophora pistillata.
Bernardet C, Tambutté E, Techer N, Tambutté S, Venn AA. Bernardet C, et al. Sci Rep. 2019 Dec 10;9(1):18676. doi: 10.1038/s41598-019-54814-7. Sci Rep. 2019. PMID: 31822787 Free PMC article.
Surface ocean pH variations since 1689 CE and recent ocean acidification in the tropical South Pacific.
Wu HC, Dissard D, Douville E, Blamart D, Bordier L, Tribollet A, Le Cornec F, Pons-Branchu E, Dapoigny A, Lazareth CE. Wu HC, et al. Nat Commun. 2018 Jun 29;9(1):2543. doi: 10.1038/s41467-018-04922-1. Nat Commun. 2018. PMID: 29959313 Free PMC article.

References

1. Darwin C. The Voyage of the Beagle: Journal of Researches into the Natural History and Geology of the Countries Visited During the Voyage of HMS Beagle Round the World Modern Library (2010).
1. Hughes T. P. et al.. Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933 (2003). - PubMed
1. Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar. Freshw. Res. 50, 839–866 (1999).
1. Ciais P. et al.. in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Stocker, T. F. et al..) 465–570 (Cambridge University Press, 2014).
1. Furla P., Galgani I., Durand I. & Allemand D. Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J. Exp. Biol. 203, 3445–3457 (2000). - PubMed

Coral calcification in a changing World and the interactive dynamics of pH and DIC upregulation - PubMed