Upper ocean oxygenation, evolution of RuBisCO and the Phanerozoic succession of phytoplankton

Abstract

Evidence is compiled to demonstrate a redox scale within Earth's photosynthesisers that correlates the specificity of their RuBisCO with organismal metabolic tolerance to anoxia, and ecological selection by dissolved O2/CO2 and nutrients. The Form 1B RuBisCO found in the chlorophyte green algae, has a poor selectivity between the two dissolved substrates, O2 and CO2, at the active site. This enzyme appears adapted to lower O2/CO2 ratios, or more “anoxic” conditions and therefore requires additional energetic or nutrient investment in a carbon concentrating mechanism (CCM) to boost the intracellular CO2/O2 ratio and maintain competitive carboxylation rates under increasingly high O2/CO2 conditions in the environment. By contrast the coccolithophores and diatoms evolved containing the more selective Rhodophyte Form 1D RuBisCO, better adapted to a higher O2/CO2 ratio, or more oxic conditions. This Form 1D RuBisCO requires lesser energetic or nutrient investment in a CCM to attain high carboxylation rates under environmentally high O2/CO2 ratios. Such a physiological relationship may underpin the succession of phytoplankton in the Phanerozoic oceans: the coccolithophores and diatoms took over the oceanic realm from the incumbent cyanobacteria and green algae when the upper ocean became persistently oxygenated, alkaline and more oligotrophic. The facultatively anaerobic green algae, able to tolerate the anoxic conditions of the water column and a periodically inundated soil, were better poised to adapt to the fluctuating anoxia associated with periods of submergence and emergence and transition onto the land. The induction of a CCM may exert a natural limit to the improvement of RuBisCO efficiency over Earth history. Rubisco specificity appears to adapt on the timescale of ∼100 Myrs. So persistent elevation of CO2/O2 ratios in the intracellular environment around the enzyme, may induce a relaxation in RuBisCO selectivity for CO2 relative to O2. The most efficient RuBisCO for net carboxylation is likely to be found in CCM-lacking algae that have been exposed to hyperoxic conditions for at least 100 Myrs, such as intertidal brown seaweeds.