A coastal coccolithophore maintains pH homeostasis and switches carbon sources in response to ocean acidification

Abstract

Ocean acidification will potentially inhibit calcification by marine organisms; however, the response of the most prolific ocean calcifiers, coccolithophores, to this perturbation remains under characterized. Here we report novel chemical constraints on the response of the widespread coccolithophore species Ochrosphaera neapolitana (O. neapolitana) to changing-CO2 conditions. We cultured this algae under three pCO2-controlled seawater pH conditions (8.05, 8.22, and 8.33). Boron isotopes within the algae’s extracellular calcite plates show that this species maintains a constant pH at the calcification site, regardless of CO2-induced changes in pH of the surrounding seawater. Carbon and oxygen isotopes in the algae’s calcite plates and carbon isotopes in the algae’s organic matter suggest that O. neapolitana utilize carbon from a single internal dissolved inorganic carbon (DIC) pool for both calcification and photosynthesis, and that a greater proportion of dissolved CO2 relative to HCO3− enters the internal DIC pool under acidified conditions. These two observations may explain how O. neapolitana continues calcifying and photosynthesizing at a constant rate under different atmospheric-pCO2 conditions.

Oxygen isotope composition of waters recorded in carbonates in strong clumped and oxygen isotopic disequilibrium

“…We thus suggest that inside coccolithosomes, coccolith precursors precipitate in equilibrium with the body water for oxygen isotopes but that the body water has a different δ 18 O value than the seawater, which explains the observed δ 18 O apparent fractionation while the 47 composition reflects culture temperature (Katz et al, 2017). It has already been highlighted through geochemical analysis of coccoliths that coccolithosome water has altered pH (Liu et al, 2018) and ion concentrations (Hermoso et al, 2017) in comparison to seawater. We hypothesize that the internal δ 18 O water would thus be another parameter controlled by the coccolithophore algae.…”

“…However, this requires that solid carbonate and water reached isotopic equilibrium, which is often hard to prove. Conversely, carbonate precipitation in isotopic disequilibrium is commonly encountered Loyd et al, 2016). Out of equilibrium, δ 18 O and 47 values are particularly known to occur in biogenic carbonates (Thiagarajan et al, 2011;Bajnai et al, 2018) -the most abundant carbonates in the sedimentary record.…”

“…Even though the identification of these vital effects does not prevent δ 18 O and 47 tools from being pow-Published by Copernicus Publications on behalf of the European Geosciences Union. 1732 C. Thaler et al: δ 18 O signature of waters recorded in disequilibrium carbonates erful paleothermometers as empirical calibrations taking vital effects into account allow temperature reconstructions, it has become crucial to determine if the δ 18 O and 47 disequilibria observed in carbonates as diverse as those found in coral reefs (Saenger et al, 2012), brachiopods (Bajnai et al, 2018), microbialites and methane seep carbonates (Loyd et al, 2016) along with speleothems could be explained by oxygen isotope disequilibria occurring in dissolved inorganic carbon (DIC) involved in carbonate precipitation. In this case, δ 18 O and 47 disequilibria in biogenic carbonates would record information, however unavailable yet, on the physiological characteristics of carbonate-forming organisms.…”

Ocean acidification induces subtle shifts in gene expression and DNA methylation in mantle tissue of the Eastern oyster (Crassostrea virginica)

“…Observed non-negative effects may be the result of individual resilience or the capacity of certain species to acclimatize to OA. One way this may occur is via the maintenance of pH homeostasis at the site of calcification despite an increasingly acidic environment, which is a polyphyletic response to ocean acidification (Liu et al, 2018) that has been observed in scleractinian corals (Al-Horani et al, 2002;Ries, 2011;Venn et al, 2011;McCulloch et al, 2012;Holcomb et al, 2014) , foraminifera (Rink et al, 1998;Köhler-Rink and Kühl, 2000;de Nooijer et al, 2008de Nooijer et al, , 2009 , calcareous green algae (De Beer and Larkum, 2001) , coralline red algae (Donald et al, 2017;Anagnostou et al, 2019;Liu et al, 2020) , coccolithophores (Liu et al 2018), and bivalves (Ramesh et al, 2017;Cameron et al, 2019) . In bivalves, calcification occurs within the extrapallial fluid (EPF) located between the shell and mantle epithelium, the composition of which is regulated via the active exchange of ions and other constituents through the mantle epithelium (Crenshaw and Neff, 1969;Crenshaw, 1972) .…”

Author reply to Reviewer comments

“…Early work on ocean acidification suggested the ballast effect is at risk from ocean acidification weakening phytoplankton calcification rates (Riebesell et al, 2000); however, these concerns have since been reduced by studies demon-strating net increases in calcification and primary production with increasing pCO 2 (Iglesias-Rodriguez et al, 2008), adaptability of phytoplankton calcifiers to acidified conditions (Lohbeck et al, 2012;Liu et al, 2018), adaptability of primary producer assemblages to acidification (Hoppe et al, 2018), and field evidence of historical increases in calcification over the past 200 years (Iglesias-Rodriguez et al, 2008). Looking into the geological record, coccolithophores were more robust (Bolton et al, 2016) and more ubiquitous in warmer, more acidic oceans of the past (Hannisdal et al, 2012).…”