Crassulacean acid metabolism in the context of other carbon-concentrating mechanisms in freshwater plants: a review

Inorganic carbon can be in short-supply in freshwater relative to that needed by freshwater plants for photosynthesis because of a large external transport limitation coupled with frequent depleted concentrations of CO2 and elevated concentrations of O2. Freshwater plants have evolved a host of avoidance, exploitation and amelioration strategies to cope with the low and variable supply of inorganic carbon in water. Avoidance strategies rely on the spatial variation in CO2 concentrations within and among lakes. Exploitation strategies involve anatomical and morphological features that take advantage of sources of CO2 outside of the water column such as the atmosphere or sediment. Amelioration strategies involve carbon concentrating mechanisms (CCM) based on uptake of bicarbonate, which is widespread, C4-fixation which is infrequent and Crassulacean Acid Metabolism (CAM) which is of intermediate frequency. CAM enables aquatic plants to take up inorganic carbon in the night. Furthermore, daytime inorganic carbon uptake is generally not inhibited and therefore CAM is considered to be a carbon conserving mechanism. CAM in aquatic plants is a plastic mechanism regulated by environmental variables and is generally down-regulated when inorganic carbon does not limit photosynthesis. CAM is regulated in the long term (acclimation during growth), but is also affected by environmental conditions in the short term (response on a daily basis). In aquatic plants CAM appears to be an ecologically important mechanism for increasing inorganic carbon uptake, since the in situ contribution from CAM to the C-budget generally is high (18-55%)

Biochemical and biophysical CO2 concentrating mechanisms in two species of freshwater macrophyte within the genus Ottelia (Hydrocharitaceae)

Two freshwater macrophytes, Ottelia alismoides and Ottelia acuminata, were grown at low (mean 5 µmol L-1) and high (mean 400 µmol L-1) CO2 concentrations under natural conditions. The ratio of PEPC to RubisCO was 1.8 in O. acuminata in both treatments. In O. alismoides, this ratio was 2.8 and 5.9 when grown at high and low CO2, respectively, as a result of a 2-fold increase of PEPC activity. The activity of PPDK was similar to and changed in-line with PEPC (1.9-fold change). The activity of the decarboxylating NADP-malic enzyme (ME) was very low in both species while NAD-ME activity was high and increased with PEPC activity in O. alismoides. These results suggest that O. alismoides might perform a type of C4 metabolism with NAD-ME decarboxylation, despite lacking Kranz anatomy. The C4-activity was still present at high CO2 suggesting that it could be constitutive. O. alismoides at low CO2 showed diel acidity variation of up to 34 μequiv g-1 FW indicating it may also operate a form of Crassulacean Acid Metabolism (CAM). pH-drift experiments showed that both species were able to use bicarbonate. In O. acuminata, the kinetics of carbon uptake were altered by CO2 growth conditions, unlike in O. alismoides. Thus the two species appear to regulate their carbon concentrating mechanisms differently in response to changing CO2. The Hydrocharitaceae have many species with evidence for C4, CAM, or a metabolism involving organic acids, and are worthy of further study

Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change

Carbon dioxide concentrating mechanisms (also known as inorganic carbon concentrating mechanisms; both abbreviated as CCMs) presumably evolved under conditions of low CO2 availability. However, the timing of their origin is unclear since there are no sound estimates from molecular clocks, and even if there were, there are no proxies for the functioning of CCMs. Accordingly, we cannot use previous episodes of high CO2 (e.g. the Palaeocene-Eocene Thermal Maximum) to indicate how organisms with CCMs responded. Present and predicted environmental change in terms of increased CO2 and temperature are leading to increased CO2 and HCO3- and decreased CO32- and pH in surface seawater, as well as decreasing the depth of the upper mixed layer and increasing the degree of isolation of this layer with respect to nutrient flux from deeper waters. The outcome of these forcing factors is to increase the availability of inorganic carbon, photosynthetic active radiation (PAR) and ultraviolet B radiation (UVB) to aquatic photolithotrophs and to decrease the supply of the nutrients (combined) nitrogen and phosphorus and of any non-aeolian iron. The influence of these variations on CCM expression has been examined to varying degrees as acclimation by extant organisms. Increased PAR increases CCM expression in terms of CO2 affinity, while increased UVB has a range of effects in the organisms examined; little relevant information is available on increased temperature. Decreased combined nitrogen supply generally increases CO2 affinity, decreased iron availability increases CO2 affinity, and decreased phosphorus supply has varying effects on the organisms examined. There are few data sets showing interactions among the observed changes, and even less information on genetic (adaptation) changes in response to the forcing factors. In freshwaters, changes in phytoplankton species composition may alter with environmental change with consequences for frequency of species with or without CCMs. The information available permits less predictive power as to the effect of the forcing factors on CCM expression than for their overall effects on growth. CCMs are currently not part of models as to how global environmental change has altered, and is likely to further alter, algal and aquatic plant primary productivity

Trade-offs and synergies in the structural and functional characteristics of leaves photosynthesizing in aquatic environments

Aquatic plants, comprising different divisions of embryophytes, derive from terrestrial ancestors. They have evolved to live in water, both fresh and salty, an environment that presents unique challenges and opportunities for photosynthesis and growth. These include, compared to air, a low water stress, a greater density, and attenuation of light, and a more variable supply of inorganic carbon, both in concentration and chemical species, but overall a lower carbon availability, and the opportunity to take up nutrients from the water. The leaves of many aquatic plants are linear, dissected, whorled, or cylindrical with a large volume of air spaces. They tend to have a high specific leaf area, thin cuticles, and usually lack functional stomata. Exploiting the availability of chemicals in their environment, freshwater macrophytes may incorporate silica in their cell wall, while seagrasses contain sulphated polysaccharides, similar to those of marine macroalgae; both groups have low lignin content. This altered cell wall composition produces plants that are more flexible and therefore more resistant to hydraulic forces (mechanical stress arising from water movement). Aquatic plants may have enhanced light harvesting complexes conferring shade adaptation, but also have mechanisms to cope with high light. Aquatic plants have evolved numerous strategies to overcome potential carbon-limitation in water. These include growing in micro-environments where CO2 is high, producing leaves and roots that exploit CO2 from the air or sediment and operating concentrating mechanisms that increase CO2 (CCM) around the primary carboxylating enzyme, ribulose-1,5-bisphosphate carboxylase-oxygenase. These comprise C4 metabolism, crassulacean acid metabolism, and the ability to exploit the often high concentrations of HCO3−, and ~50% of freshwater macrophytes and ~85% of seagrasses have one or more CCM. Many of these adaptations involve trade-offs between conflictin constraints and opportunities while others represent ‘synergies’ that help to maximize the productivity of this important group of plants