Biophysical models for studying patterns of RuBisCO small subunit evolution.

Abstract

For much of Earth's history, key enzymes have dominated the conversion of energy into the production of biomass. This history extends hundreds of millions of years into the past, but the available record provides few direct indicators of the emergence and evolution of enzymes that shaped our planet. A good example is Ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO), which is responsible for the fixation of CO2 in conjunction with oxygenic photosynthesis and is estimated to be the most abundant enzyme on Earth. RuBisCO form-I is the only form composed of a large and small subunit. The biochemical role that the small subunit plays is unclear, and the circumstances of its coevolution with the large subunit or with drastic changes to the Earth's surface environment such as the concentrations of CO2 and O2 gases are also unknown. Here, we explore how the small subunit-mediated RuBisCO form-I transition by generating a phylogenetic tree of proteins, reconstructing its ancestral sequences, and analyzing the structure as well as function of the ancestral large-small subunit RuBisCO complexes. From ancient and extant structures, we identify the general attributes that define the interaction between the two RuBisCO subunits and inspect how these interactions have evolved with reference to the ancestral large subunit RuBisCO forms and the partition and diffusion of CO2 and O2 at different relative concentrations of the two gasses. Our results are consistent with the possibility that the small subunit was an evolutionary response to the global rise of atmospheric O2 over 2 billion years ago, and that it impacted large subunit CO2 diffusion. Our research highlights how a protein subunit that emerged billions of years ago in response to a change in the planet's atmosphere impacts the function of an essential protein complex.