Abstract
ABSTRACT Inorganic carbon availability can limit primary productivity and control species composition of freshwater phytoplankton. This is despite the presence of CO2-concentrating mechanisms (CCMs) in some species that maximize inorganic carbon uptake. We investigated the effects of inorganic carbon on the seasonal distribution, growth rates and photosynthesis of a freshwater diatom, Asterionella formosa, and the nature of its CCM using genomics. In a productive lake, the frequency of A. formosa declined with CO2 concentration below air-equilibrium. In contrast, CO2 concentrations at 2.5-times air-equilibrium did not increase growth rate, cell C-quota or the ability to remove inorganic carbon. A pH-drift experiment strongly suggested that HCO3 − as well as CO2 could be used. Calculations combining hourly inorganic carbon concentrations in a lake with known CO2 and HCO3 − uptake kinetics suggested that rates of photosynthesis of A. formosa would be approximately carbon saturated and largely dependent on CO2 uptake when CO2 was at or above air-equilibrium. However, during summer carbon depletion, HCO3 − would be the major form of carbon taken up and carbon saturation will fall to around 30%. Genes encoding proteins involved in CCMs were identified in the nuclear genome of A. formosa. We found carbonic anhydrases from subclasses α, β, γ and θ, as well as solute carriers from families 4 and 26 involved in HCO3 − transport, but no periplasmic carbonic anhydrase. A model of the components of the CCM and their location in A. formosa showed that they are more similar to Phaeodactylum tricornutum than to Thalassiosira pseudonana, two marine diatoms.
Highlights
Photosynthesis in water can rely on CO2 and HCO3- as exogenous sources of inorganic carbon
The seasonal distribution of A. formosa in relation to CO2 concentration Over 32 years, CO2 concentration in Esthwaite Water varied by 61,000-fold, between 2.7 ·103 and 166 μmol l-1, with the very low CO2 minima occurring in summer (Fig. 1)
Anabaena species were present at all concentrations of CO2 and were most prevalent when CO2 was low (Fig. 3), while A. formosa was absent, or present less than 15% of the dates when CO2 concentration was less than 0.3 μmol l-1
Summary
Photosynthesis in water can rely on CO2 and HCO3- as exogenous sources of inorganic carbon. The primary carboxylation enzyme in the Calvin–Benson–Bassham cycle, ribulose1,5-bisphosphate carboxylase/oxygenase (RubisCO), fixes CO2 with a relatively low affinity and performs an oxygenation reaction when concentrations of CO2 at its active site are low. This can leads to photorespiration (Bowes & Ogren 1972) and reduced productivity. Marine diatom RubisCO proteins have a Michaelis–Menten constant between 23 and 68 μmol l-1 (Young et al 2016) Assuming that these values apply to freshwater diatoms, the airequilibrium concentration of CO2 in fresh water at an atmospheric CO2 partial pressures of 400 ppm varies between 25 μmol l-1 at 5°C and 14 μmol l-1 at 25°C. In productive lakes, the concentration of CO2 can fall several orders of magnitude below air-equilibrium (Talling 1976; Maberly 1996) potentially limiting photosynthesis even further
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