Interplay among environmental factors, development of CO2 concentrating mechanisms and phylogenetic constraints shaping Rubisco evolution across aquatic photosynthetic organisms

Abstract

Rubisco is the main CO2-fixing enzyme in the biosphere and sustains the vast majority of food chains on Earth. Although Rubisco catalysis is currently an area of active study, there is still a strong debate about the main drivers shaping Rubisco evolution. Thus, an integrative and complete meta-analysis of study-to-study normalized Rubisco kinetic data becomes an essential requisite to succeed in providing new relevant information on Rubisco phylogenetic evolution and environmental adaptation. The aim of this study was to undertake an exhaustive compilation of all the data published so far on the in vitro Rubisco catalytic parameters of autotrophic organisms containing Rubisco, from bacteria to vascular plants. Rubisco evolution was re-evaluated in the context of its environmental drivers and the effectiveness of CO2 concentrating mechanisms (CCMs). The phylogenetic signal in Rubisco catalysis was also analyzed by evaluating the dependence of variation in kinetic traits on the phylogenetic tree constructed from the Rubisco large subunit sequence. Our results showed that phylogenetic constraints in Rubisco adaptation mostly determine the specificity factor values of current species. However, the adaptation of the Rubisco affinity for CO2 and carboxylation efficiency has been more influenced by the environmental conditions than by phylogenetic constraints, either provoking an evolution of a more CO2-affine and efficient Rubisco enzyme under limiting intracellular CO2 conditions, or a relaxation of CO2 affinity and efficiency when co-evolved with CCMs. Importantly, this analysis questions the canonical trade-off between Rubisco kinetic traits previously described for Spermatophyta and recognizes a larger plasticity of Rubisco kinetics than previously thought. This information will be especially useful for understanding the effects in the productivity and ecological success of the different aquatic organisms in future scenarios of Global Change.