The Origins and Evolution of an Early Microbial Rhodopsin Protein

Abstract

The advent of cellular organisms took place sometime between the start of prebiotic chemosynthesis on Earth and the evolution of the last universal common ancestor. Cellularity is now a fundamental organizational principle shared by all life on Earth and represents a key transition in evolutionary history. The emergence of cellular organization necessitated organisms to evolve a means to permit and regulate the exchange of material between the intracellular compartment and the extracellular environment. This capability implies both the ability to embed proteins into their membranes and to translocate molecules across their membranes. Other factors integral to the progression of early cellular life were the maintenance of transmembrane potential and chemiosmotic coupling for generating and conserving energy, and pigments to absorb light energy for photosynthetic and phototrophic metabolisms. Microbial rhodopsins, a superfamily of photoactive membrane proteins, have been suggested to be the simplest and possibly most ancient form of a phototrophic metabolism, likely providing a mechanism for microbial energy capture in Earth’s early shallow marine ecosystems. The retinal-based photosystem (rhodopsin) is composed of one retinal chromophore and one opsin protein. In this system, light absorption directly drives a conformational change in the protein via the isomerization of the retinal moiety to carry out biological functions such as ion pumping and ATP synthesis. Here, computational approaches were used to investigate the evolutionary history of rhodopsin proteins, combining phylogenic reconstruction and ancestral sequence inferences. Additionally, protein structure modeling and biophysical predictions were used to reveal ancestral rhodopsin functionality. Together, these results may shed light on the evolution of pigment-based metabolisms and prove beneficial for understanding the characteristics of early cellular membranes.