Archaean green-light environments drove the evolution of cyanobacteria’s light-harvesting system

Abstract

Cyanobacteria induced the great oxidation event around 2.4 billion years ago, probably triggering the rise in aerobic biodiversity. While chlorophylls are universal pigments used by all phototrophic organisms, cyanobacteria use additional pigments called phycobilins for their light-harvesting antennas—phycobilisomes—to absorb light energy at complementary wavelengths to chlorophylls. Nonetheless, an enigma persists: why did cyanobacteria need phycobilisomes? Here, we demonstrate through numerical simulations that the underwater light spectrum during the Archaean era was probably predominantly green owing to oxidized Fe(III) precipitation. The green-light environments, probably shaped by photosynthetic organisms, may have directed their own photosynthetic evolution. Genetic engineering of extant cyanobacteria, simulating past natural selection, suggests that cyanobacteria that acquired a green-specialized phycobilin called phycoerythrobilin could have flourished under green-light environments. Phylogenetic analyses indicate that the common ancestor of modern cyanobacteria embraced all key components of phycobilisomes to establish an intricate energy transfer mechanism towards chlorophylls using green light and thus gained strong selective advantage under green-light conditions. Our findings highlight the co-evolutionary relationship between oxygenic phototrophs and light environments that defined the aquatic landscape of the Archaean Earth and envision the green colour as a sign of the distinct evolutionary stage of inhabited planets. Cyanobacteria use both chlorophylls and phycobilins to absorb light energy, and authors here use cultivation experiments, numerical simulations and protein phylogenetics to argue that cyanobacteria evolved in a green-light environment during the Archaean era in which green-specialized phycobilins would have been selectively advantageous.