Francisco Javier López Gordillo

Aquatic photoautotrophs experience strong physicochemical constraints on inorganic carbon acquisition due to low CO2 and O2 diffusion in water producing a strong reduction in the gas conductance. These limitations have driven the widespread evolution of CO2-concentrating mechanisms (CCMs), which enhance CO2 availability around Rubisco and mitigate its catalytic inefficiencies. A compilation of the Rubisco kinetics and apparent photosynthetic CO2 affinities (1/Km CO2) for a wide range of taxa shows that, despite the structural diversity of CCMs, there is an evolutive convergence among cyanobacteria, diatoms, haptophytes, and some rhodophytes and chlorophytes with similarly high 1/Km CO2, therefore operating almost CO2-saturated photosynthesis under ambient conditions. Notably, none of the compiled species achieves CO2 saturation solely through Rubisco kinetics, underscoring the central role of CCMs in aquatic carbon fixation. CCM effectiveness (the ratio between Rubisco CO2 semi-saturation constant under 21% O2 and apparent photosynthetic semi-saturation constant for CO2, Kcair/Km CO2) varies widely across the compiled species but is consistently higher in organisms possessing Rubisco-containing microcompartments, although pyrenoids are not strictly required for concentrating CO2 around Rubisco above ambient levels. Furthermore, an inverse relationship between Rubisco carboxylation efficiency and 1/Km CO2 supports a divergent CCM-Rubisco coevolutionary trajectory compared with terrestrial plants, likely influenced by intracellular photosynthetic O2 accumulation under submerged conditions. The present review synthesizes current knowledge on CCM diversity and its regulation under future global change scenarios but also reanalyzes CCM effectiveness and its co-evolution with Rubisco kinetic traits across aquatic oxygenic phototrophs, highlighting major knowledge gaps to be filled by future research.

The coccolithophoreEmiliania huxleyishows a variety of responses to ocean acidification (OA) and to high-CO₂concentrations, but there is still controversy on differentiating between these two factors when using different strains and culture methods. A heavily calcified type A strain isolated from the Norwegian Sea was selected and batch cultured in order to understand whether acclimation to OA was mediated mainly by CO₂or H⁺, and how it impacted cell growth performance, calcification, and physiological stress management.Emiliania huxleyiresponded differently to each acidification method. CO₂-enriched aeration (1200 µatm, pH 7.62) induced a negative effect on the cells when compared to acidification caused by decreasing pH alone (pH 7.60). The growth rates of the coccolithophore were more negatively affected by high pCO₂than by low pH without CO₂enrichment with respect to the control (400 µatm, pH 8.1). High CO₂also affected cell viability and promoted the accumulation of reactive oxygen species (ROS), which was not observed under low pH. This suggests a possible metabolic imbalance induced by high CO₂alone. In contrast, the affinity for carbon uptake was negatively affected by both low pH and high CO₂. Photochemistry was only marginally affected by either acidification method when analysed by PAM fluorometry. The POC and PIC cellular quotas and the PIC:POC ratio shifted along the different phases of the cultures; consequently, calcification did not follow the same pattern observed in cell stress and growth performance. Specifically, acidification by HCl addition caused a higher proportion of severely deformed coccoliths, than CO₂enrichment. These results highlight the capacity of CO₂rather than acidification itself to generate metabolic stress, not reducing calcification.

Continuous winter darkness at a latitude of 79°N was simulated in cultures of four species of Arctic seaweeds at 3 and 8°C. The laminarians Saccharina latissima and Alaria esculenta, and the rhodophytes Phycodrys rubens and Ptilota gunneri were monitored for 4 months in total darkness and after 1 week following light return in early spring, under controlled laboratory conditions. Biomass loss during darkness was enhanced by the high temperature in all species. At 8°C, the two laminarians were unable to resume growth upon re-illumination. Alaria esculenta showed new blade production by the end of the dark period, but only at 3°C. In all species, the photosynthetic ability was sustained, not suspended, during the whole dark period. P. rubens exhibited lower photosynthetic potential at 8°C than at 3°C during the darkness period, but it was able to recover its O₂ evolving potential upon re-illumination, as P. gunneri and S. latissima did, but the latter only at 3°C. The reactivation of photosynthesis seemed to involve photosystem II over photosystem I, as 7 d of photoperiod after the prolonged darkness was not enough to fully recover the PAM-related photosynthetic parameters. Only small changes were recorded in the internal chemical composition (total C, total N, carbohydrates, proteins, and lipids), but species-specific differences were observed. Unlike subarctic areas with an operating photoperiod along the year, a warmer polar night might pose a limit to the ability of multi-year seaweeds to occupy the new ice-free illuminated areas of the Arctic coasts, so that newcomers will potentially be restricted to the spring-summer season.

Ocean acidification and warming are affecting polar regions with particular intensity. Rocky shores of the Antarctic Peninsula are dominated by canopy-forming Desmarestiales. This study investigates the physiological and transcriptomic responses of the endemic macroalga Desmarestia anceps to a combination of different levels of temperature (2 and 7 °C), dissolved CO₂ (380 and 1000 ppm), and irradiance (65 and 145 µmol photons m⁻² s⁻¹). Growth and photosynthesis increased at high CO₂ conditions, and strongly decreased at 2 °C plus high irradiance, in comparison to the other treatments. Photoinhibition at 2 °C plus high irradiance was evidenced by the photochemical performance and intensive release of dissolved organic carbon. The highest number of differentially regulated transcripts was observed in thalli exposed to 2 °C plus high irradiance. Algal ¹³C isotopic discrimination values suggested an absence of down-regulation of carbon-concentrating mechanisms at high CO₂. CO₂ enrichment induced few transcriptomic changes. There was high and constitutive gene expression of many photochemical and inorganic carbon utilization components, which might be related to the strong adaptation of D. anceps to the Antarctic environment. These results suggest that increased temperature and CO₂ will allow D. anceps to maintain its productivity while tolerating higher irradiances than at present conditions.

Previous research suggested that the polar and temperate populations of the kelp Saccharina latissima represent different ecotypes. The ecotypic differentiation might also be reflected in their biochemical composition (BC) under changing temperatures and pCO₂. Accordingly, it was tested if the BC of Arctic (Spitsbergen) and temperate S. latissima (Helgoland) is different and if they are differently affected by changes in temperature and pCO₂. Thalli from Helgoland grown at 17 °C and 10 °C and from Spitsbergen at 10 °C and 4 °C were all tested at either 380, 800, or 1,500 µatm pCO₂, and total C-, total N-, protein, soluble carbohydrate, and lipid content, as well as C/N-ratio were measured. At 10 °C, the Arctic population had a higher content of total C, soluble carbohydrates, and lipids, whereas the N- and protein content was lower. At the lower tested temperature, the Arctic ecotype had particularly higher contents of lipids, while content of soluble carbohydrates increased in the Helgoland population only. In Helgoland-thalli, elevated pCO₂ caused a higher content of soluble carbohydrates at 17 °C but lowered the content of N and lipids and increased the C/N-ratio at 10 °C. Elevated pCO₂ alone did not affect the BC of the Spitsbergen population. Conclusively, the Arctic ecotype was more resilient to increased pCO₂ than the temperate one, and both ecotypes differed in their response pattern to temperature. This differential pattern is discussed in the context of the adaptation of the Arctic ecotype to low temperature and the polar night.

The effects of increased CO₂ and irradiance on the physiological performance of the chlorophyte Dunaliella tertiolecta were studied at different PAR and UVR (UVA + UVB) irradiances, simulating the solar radiation at different depths, at present (390 ppmv, LC) and predicted CO₂ levels for the year 2100 (1000 ppmv, HC). Elevated CO₂ resulted in higher optimum and effective quantum yields (F_v/F_m and ϕ_PSII, respectively), electron transport rates (ETR) and specific growth rates (μ). Cell stress was alleviated in HC with respect to LC as evidenced by a decrease in reactive oxygen species (ROS) accumulation. DNA damage showed a 42-fold increase in cyclobutane-pyrimidine dimer (CPD) formation under the highest irradiance (1100 μmol quanta m⁻² s⁻¹) in LC with respect to the lowest irradiance (200 μmol quanta m⁻² s⁻¹). Photolyase (CII-PCD-PL) gene expression was upregulated under HC resulting in a drastic decrease in CPD accumulation to only 25% with respect to LC. Proliferating cell nuclear antigen (PCNA) accumulation was always higher in HC and the accumulation pattern indicated its involvement in repair or growth depending on the irradiance dose. The repressor of silencing (ROS1) was only marginally involved in the response, suggesting that photoreactivation was the most relevant mechanism to overcome UVR damage. Our results demonstrate that future scenarios of global change result in alleviation of irradiance stress by CO₂-induced photoprotection in D. tertiolecta.