Photosynthesis and light-dependent proton pumps increase boundary layer pH in tropical macroalgae: a proposed mechanism to sustain calcification under ocean acidification

Highlights

• Tropical calcifying macroalgae raise boundary layer pH due to photosynthesis

• Different mechanisms of inorganic carbon uptake control pH increase

• Proton pumps in light without photosynthesis appear important calcification

• Photosynthesis-driven pH increase allows calcification with ocean acidification

Abstract

Ocean acidification (OA) projections predict ocean pH to decline between 0.2 and 0.4 by 2100 with potential negative consequences for marine calcifiers without acclimation or adaption strategies to accomodate greater [H+] in seawater. Biotic control of calcified reef macroalgae thalli surface diffusive boundary layer (DBL) chemistry may overcome low pH in seawater as one strategy to accommodate OA conditions. To investigate this strategy, we examined surface DBL O2 and pH dynamics in five calcifying macroalgae (Halimeda, Udotea, Jania, Neogoniolithon, crustose coralline algae [CCA]) from the Florida Reef Tract under ambient (8.1) and low (7.65) pH using microsensors (100 μm) at the thalli surface in a flow-through flume. The role of photosynthesis and photosystem II (PSII)-independent proton pumps in controlling DBL pH were examined. Four of the five macroalgae exhibited a strong positive linear relationship between O2 production and increasing pH in the first 15–30 s of irradiance. Once a quasi-steady-state O2 concentration was reached (300 s), all species had DBL pH that were higher (0.02–0.32) than bulk seawater. The DBL pH increase was greatest at low pH and dependent on PSII. Some evidence was found for a light-dependent, but PSII-independent, proton pump. High DBL Δ pH upon illumination was likely in response to carbon concentrating mechanisms (CCMs) for photosynthesis. CCMs may be a HCO3−–H+ symport, OH– antiport or other DIC transport system, accompanied by proton efflux. HCO3– dehydration by external carbonic anhydrase (CAext) also produces OH– that can neutralize H+ in the DBL. CO2 or HCO3– uptake for photosynthesis may also engage H+/OH– fluxes as part of intracellular acid-base regulation changing DBL pH. A higher Δ pH within the DBL at low pH could be accounted for by greater CO2 diffusion and/or lower efficiencies in exporting cellular H+ across a lower concentration gradient, and/or a more efficient removal of H+ by CAext-driven dehydration of HCO3−. In the dark, Δ pH was less than in the light as these dynamics were primarily due to photosynthesis. We present a conceptual model of inorganic carbon uptake and ion transport pathways, as well as other processes associated with photosynthesis that drive DBL Δ pH and sustain tropical macroalgal calcification in the light under OA. In the dark, unless PSII-independent proton pumps are present, which do not appear to be ubiquitous amongst species, acidification processes likely dominate, resulting in CaCO3 net dissolution, particularly under OA conditions.

McNicholl C., Koch M. S. & Hofmann L. C., 2019. Photosynthesis and light-dependent proton pumps increase boundary layer pH in tropical macroalgae: a proposed mechanism to sustain calcification under ocean acidification. Journal of Experimental Marine Biology and Ecology 521: 151208. doi: 10.1016/j.jembe.2019.151208. Article (subscription required).

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