Photosynthesis and light-dependent proton pumps increase boundary layer pH in tropical macroalgae: A proposed mechanism to sustain calcification under 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 O 2 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 O 2 production and increasing pH in the first 15-30 s of irradiance. Once a quasi-steady-state O 2 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 HCO 3 −-H + symport, OHantiport or other DIC transport system, accompanied by proton efflux. HCO 3 dehydration by external carbonic anhydrase (CA ext) also produces OHthat can neutralize H + in the DBL. CO 2 or HCO 3 uptake for photosynthesis may also engage H + /OHfluxes 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 CO 2 diffusion and/ or lower efficiencies in exporting cellular H + across a lower concentration gradient, and/or a more efficient removal of H + by CA ext-driven dehydration of HCO 3 −. 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 CaCO 3 net dissolution, particularly under OA conditions. nate (CO 3 2−) by~50-60% (Fabry et al., 2008; Koch et al., 2013). The decline in CO 3 2lowers the saturation state (Ω) of carbonate minerals of calcite and aragonite (~60%). The high concentration of Ca 2+ in

Rhodolith Physiology Across the Atlantic: Towards a Better Mechanistic Understanding of Intra- and Interspecific Differences

“…Also, comparisons among different species, from the same habitat, suggest a variability in the strength of the coupling between photosynthesis and calcification (Vaśquez-Elizondo and Enrıquez, 2016;Qui-Minet et al, 2021). The direct relationship between these processes was demonstrated early on (Digby, 1977;Pentecost, 1978;Borowitzka, 1981;Borowitzka, 1987) and is supported by recent studies (e.g., Martin et al, 2013;Vaśquez-Elizondo and Enrıquez, 2016;Sordo et al, 2019), which showed a decline in calcification upon inhibition of photosynthesis (Hofmann et al, 2016;McNicholl et al, 2019). This link has been related to an elevation of the pH at the calcification site due to photosynthetic activity.…”

“…It has been suggested that calcification is a biologically induced, rather than a controlled process, associated with cell wall organic-matrixinduced mineralization (Nash et al, 2019). However, mechanistic studies and derived models suggest that coralline algae exert some control over the calcification process, by promoting favorable conditions for CaCO 3 precipitation through photosynthesis and active dissolved inorganic carbon (DIC) and ion transport pathways (Comeau et al, 2013;Koch et al, 2013;Hofmann et al, 2016;Cornwall et al, 2017;McNicholl et al, 2019). Recent studies showed that the extent of photosynthesis-promoted increase of pH in the DBL (pH DBL ) is species-specific and influenced by external seawater pH, but also by species' morphology, due to its strong influence on DBL thickness (Cornwall et al, 2017;Schubert et al, 2021a).…”

When descriptive ecology meets physiology: a study in a South Atlantic rhodolith bed

“…Although calcification is correlated to photosynthesis, there are also metabolically controlled photosynthesis-independent ion pumps and channels with the efflux of Ca 2+ and H + outside the cells in the dark and influx under light (Hofmann et al ., 2016). The proton pumps in light are important to pH regulation at the thalli surface and calcification under ocean acidification (McNicholl et al ., 2019).…”

Approaches and involved principles to control pH/pCO2 stability in algal cultures

“…Higher levels of algal biomass can result in self-shading, therefore, leading to reduced levels of photosynthetically active radiation (PAR) and/ or altered exposures of changed light spectrum to the cells due to differences in primary and secondary absorption (re-absorbtion of the attenuated light by other cells). On the other hand, water motion dynamics in aerated, mixed or shaken cultures can affect the thickness of diffusion boundary layers (DBL) surrounding cells or individuals; therefore, different levels of water motion or current can result in different levels of pH, pCO 2 , and pO 2 near the cell or thallus surface compared to the bulk medium (Hurd 2015;McNicholl et al 2019). Consequently, inadequate mixing can lead to significant localized variations in all physical and chemical parameters during cultures of algae (Borowitzka 2016).…”