Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles.
Oxygenic photosynthesis evolved at least 2.4 Ga; all oxygenic organisms use the ribulose bisphosphate carboxylase-oxygenase (Rubisco)-photosynthetic carbon reduction cycle (PCRC) rather than one of the five other known pathways of autotrophic CO(2) assimilation. The high CO(2) and (initially) O(2)-free conditions permitted the use of a Rubisco with a high maximum specific reaction rate. As CO(2) decreased and O(2) increased, Rubisco oxygenase activity increased and 2-phosphoglycolate was produced, with the evolution of pathways recycling this inhibitory product to sugar phosphates. Changed atmospheric composition also selected for Rubiscos with higher CO(2) affinity and CO(2)/O(2) selectivity correlated with decreased CO(2)-saturated catalytic capacity and/or for CO(2)-concentrating mechanisms (CCMs). These changes increase the energy, nitrogen, phosphorus, iron, zinc and manganese cost of producing and operating Rubisco-PCRC, while biosphere oxygenation decreased the availability of nitrogen, phosphorus and iron. The majority of algae today have CCMs; the timing of their origins is unclear. If CCMs evolved in a low-CO(2) episode followed by one or more lengthy high-CO(2) episodes, CCM retention could involve a combination of environmental factors known to favour CCM retention in extant organisms that also occur in a warmer high-CO(2) ocean. More investigations, including studies of genetic adaptation, are needed.
Division of Plant Sciences, The James Hutton Institute, University of Dundee at TJHI, Invergowrie, Dundee DD2 5DA, UK. j.a.raven@dundee.ac.uk
John A
JA
Raven
Mario
M
Giordano
John
J
Beardall
Stephen C
SC
Maberly
D001272:Atmosphere / Q000737:chemistry*; D052818:Autotrophic Processes; D005075:Biological Evolution; D002244:Carbon / Q000737:chemistry*; D057486:Carbon Cycle; D002245:Carbon Dioxide / Q000737:chemistry*; D000458:Cyanobacteria / Q000737:chemistry / Q000201:enzymology*; D004058:Diffusion; D004789:Enzyme Activation; D006016:Glycolates / Q000737:chemistry; D009584:Nitrogen / Q000737:chemistry; D010084:Oxidation-Reduction; D010105:Oxygenases / Q000737:chemistry; D010788:Photosynthesis; D012273:Ribulose-Bisphosphate Carboxylase / Q000737:chemistry*
D006016:Glycolates; D002245:Carbon Dioxide; D002244:Carbon; D010105:Oxygenases; D012273:Ribulose-Bisphosphate Carboxylase; C013193:phosphoglycolate; D009584:Nitrogen