Rubisco kinetic adaptations to extreme environments.

Photosynthetic and chemosynthetic extremophiles have evolved adaptations to thrive in challenging environments by finely adjusting their metabolic pathways through evolutionary processes. A prime adaptation target to allow autotrophy in extreme conditions is the enzyme Rubisco, which plays a central role in the conversion of inorganic to organic carbon. Here, we present an extensive compilation of Rubisco kinetic traits from a wide range of species of bacteria, archaea, algae, and plants, sorted by phylogenetic group, Rubisco type, and extremophile type.

The diversity and coevolution of Rubisco and CO concentrating mechanisms in marine macrophytes.

The kinetic properties of Rubisco, the most important carbon-fixing enzyme, have been assessed in a small fraction of the estimated existing biodiversity of photosynthetic organisms. Until recently, one of the most significant gaps of knowledge in Rubisco kinetics was marine macrophytes, an ecologically relevant group including brown (Ochrophyta), red (Rhodophyta) and green (Chlorophyta) macroalgae and seagrasses (Streptophyta). These organisms express various Rubisco types and predominantly possess CO -concentrating mechanisms (CCMs), which facilitate the use of bicarbonate for photosynthesis.

Singular adaptations in the carbon assimilation mechanism of the polyextremophile cyanobacterium Chroococcidiopsis thermalis.

Cyanobacteria largely contribute to the biogeochemical carbon cycle fixing ~ 25% of the inorganic carbon on Earth. However, the carbon acquisition and assimilation mechanisms in Cyanobacteria are still underexplored regardless of being of great importance for shedding light on the origins of autotropism on Earth and providing new bioengineering tools for crop yield improvement. Here, we fully characterized these mechanisms from the polyextremophile cyanobacterium Chroococcidiopsis thermalis KOMAREK 1964/111 in comparison with the model cyanobacterial strain, Synechococcus sp.

Carbon assimilation in upper subtidal macroalgae is determined by an inverse correlation between Rubisco carboxylation efficiency and CO concentrating mechanism effectiveness.

Seaweeds have a wide ecophysiological and phylogenetic diversity with species expressing different Rubisco forms that frequently coexist with biophysical CO concentrating mechanisms (CCMs), an adaptation that overcomes the low CO availability and gas diffusion in seawater. Here, we assess the possible coevolution between the Rubisco catalysis and the type and effectiveness of CCMs present in six upper subtidal macroalgal species belonging to three phylogenetic groups of seaweeds. A wide diversity in the Rubisco kinetic traits was found across the analyzed species, although the specificity factor was the only parameter explained by the expressed Rubisco form.

The trajectory in catalytic evolution of Rubisco in Posidonia seagrass species differs from terrestrial plants.

The CO2-fixing enzyme Ribulose bisphosphate carboxylase-oxygenase (Rubisco) links the inorganic and organic phases of the global carbon cycle. In aquatic systems, the catalytic adaptation of algae Rubiscos has been more expansive and followed an evolutionary pathway that appears distinct to terrestrial plant Rubisco. Here, we extend this survey to differing seagrass species of the genus Posidonia to reveal how their disjunctive geographical distribution and diverged phylogeny, along with their CO2 concentrating mechanisms (CCMs) effectiveness, have impacted their Rubisco kinetic properties.

Correlative adaptation between Rubisco and CO-concentrating mechanisms in seagrasses.

Submerged angiosperms sustain some of the most productive and diverse ecosystems worldwide. However, their carbon acquisition and assimilation mechanisms remain poorly explored, missing an important step in the evolution of photosynthesis during the colonization of aquatic environments by angiosperms. Here we reveal a convergent kinetic adaptation of Rubisco in phylogenetically distant seagrass species that share catalytic efficiencies and CO and O affinities up to three times lower than those observed in phylogenetically closer angiosperms from terrestrial, freshwater and brackish-water habitats.

High-CO Levels Rather than Acidification Restrict Emiliania huxleyi Growth and Performance.

The coccolithophore Emiliania huxleyi shows a variety of responses to ocean acidification (OA) and to high-CO concentrations, 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 CO or H, and how it impacted cell growth performance, calcification, and physiological stress management. Emiliania huxleyi responded differently to each acidification method.

Anatomical and biochemical evolutionary ancient traits of Araucaria araucana (Molina) K. Koch and their effects on carbon assimilation.

The study of ancient species provides valuable information concerning the evolution of specific adaptations to past and current environmental conditions. Araucaria araucana (Molina) K. Koch belongs to one of the oldest families of conifers in the world, but despite this, there are few studies focused on its physiology and responses to changes in environmental conditions.

Improving photosynthesis through the enhancement of Rubisco carboxylation capacity.

Rising human population, along with the reduction in arable land and the impacts of global change, sets out the need for continuously improving agricultural resource use efficiency and crop yield (CY). Bioengineering approaches for photosynthesis optimization have largely demonstrated the potential for enhancing CY. This review is focused on the improvement of Rubisco functioning, which catalyzes the rate-limiting step of CO2 fixation required for plant growth, but also catalyzes the ribulose-bisphosphate oxygenation initiating the carbon and energy wasteful photorespiration pathway.

Analyzing the causes of method-to-method variability among Rubisco kinetic traits: from the first to the current measurements.

Due to the importance of Rubisco in the biosphere, its kinetic parameters have been measured by different methodologies in a large number of studies over the last 60 years. These parameters are essential to characterize the natural diversity in the catalytic properties of the enzyme and they are also required for photosynthesis and cross-scale crop modeling. The present compilation of Rubisco kinetic parameters in model species revealed a wide intraspecific laboratory-to-laboratory variability, which was partially solved by making corrections to account for differences in the assay buffer composition and in the acidity constant of dissolved CO2, as well as for differences in the CO2 and O2 solubilities.

How do vascular plants perform photosynthesis in extreme environments? An integrative ecophysiological and biochemical story.

In this work, we review the physiological and molecular mechanisms that allow vascular plants to perform photosynthesis in extreme environments, such as deserts, polar and alpine ecosystems. Specifically, we discuss the morpho/anatomical, photochemical and metabolic adaptive processes that enable a positive carbon balance in photosynthetic tissues under extreme temperatures and/or severe water-limiting conditions in C species. Nevertheless, only a few studies have described the in situ functioning of photoprotection in plants from extreme environments, given the intrinsic difficulties of fieldwork in remote places.

Evolutionary trends in RuBisCO kinetics and their co-evolution with CO concentrating mechanisms.

RuBisCO-catalyzed CO fixation is the main source of organic carbon in the biosphere. This enzyme is present in all domains of life in different forms (III, II, and I) and its origin goes back to 3500 Mya, when the atmosphere was anoxygenic. However, the RuBisCO active site also catalyzes oxygenation of ribulose 1,5-bisphosphate, therefore, the development of oxygenic photosynthesis and the subsequent oxygen-rich atmosphere promoted the appearance of CO concentrating mechanisms (CCMs) and/or the evolution of a more CO -specific RuBisCO enzyme.

Potential improvement of photosynthetic CO assimilation in crops by exploiting the natural variation in the temperature response of Rubisco catalytic traits.

The enhancement of the photosynthetic capacity of crops by the expression of more efficient Rubisco versions has been a main target in the field of plant photosynthesis improvement. However, such an increase in the photosynthetic efficiency will depend on the environmental conditions and on the responsiveness of Rubisco to temperature and CO availability. After an exhaustive compilation and standardization of the data published so far, a large natural variability in the thermal responses of Rubisco kinetic parameters in higher plant species was revealed.

Rubisco carboxylation kinetics and inorganic carbon utilization in polar versus cold-temperate seaweeds.

Despite the high productivity and ecological importance of seaweeds in polar coastal regions, little is known about their carbon utilization mechanisms, especially the kinetics of the CO2-fixing enzyme Rubisco. We analyzed Rubisco carboxylation kinetics at 4 °C and 25 °C in 12 diverse polar seaweed species (including cold-temperate populations of the same species) and the relationship with their ability to use bicarbonate, by using 13C isotope discrimination and pH drift experiments. We observed a large variation in Rubisco carboxylation kinetics among the selected species, although no correlation was found between either the Michaelis-Menten constant for CO2 (Kc) or Rubisco content per total soluble protein ([Rubisco]/[TSP]) and the ability to use bicarbonate for non-green seaweeds.

Increased temperature and CO2 alleviate photoinhibition in Desmarestia anceps: from transcriptomics to carbon utilization.

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).

Increased pCO and temperature reveal ecotypic differences in growth and photosynthetic performance of temperate and Arctic populations of Saccharina latissima.

The Arctic population of the kelp Saccharina latissima differs from the Helgoland population in its sensitivity to changing temperature and CO levels. The Arctic population does more likely benefit from the upcoming environmental scenario than its Atlantic counterpart. The previous research demonstrated that warming and ocean acidification (OA) affect the biochemical composition of Arctic (Spitsbergen; SP) and cold-temperate (Helgoland; HL) Saccharina latissima differently, suggesting ecotypic differentiation.

Biochemical composition of temperate and Arctic populations of Saccharina latissima after exposure to increased pCO2 and temperature reveals ecotypic variation.

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.