Scaffolding proteins guide the evolution of algal light harvesting antennas

Photosynthetic organisms have developed diverse antennas composed of chromophorylated proteins to increase photon capture. Cryptophyte algae acquired their photosynthetic organelles (plastids) from a red alga by secondary endosymbiosis. Cryptophytes lost the primary red algal antenna, the red algal phycobilisome, replacing it with a unique antenna composed of alpha beta protomers, where the beta subunit originates from the red algal phycobilisome. The origin of the cryptophyte antenna, particularly the unique alpha subunit, is unknown. Here we show that the cryptophyte antenna evolved from a complex between a red algal scaffolding protein and phycoerythrin beta. Published cryo-EM maps for two red algal phycobilisomes contain clusters of unmodelled density homologous to the cryptophyte-alpha beta protomer. We modelled these densities, identifying a new family of scaffolding proteins related to red algal phycobilisome linker proteins that possess multiple copies of a cryptophyte-alpha-like domain. These domains bind to, and stabilise, a conserved hydrophobic surface on phycoerythrin beta, which is the same binding site for its primary partner in the red algal phycobilisome, phycoerythrin alpha. We propose that after endosymbiosis these scaffolding proteins outcompeted the primary binding partner of phycoerythrin beta, resulting in the demise of the red algal phycobilisome and emergence of the cryptophyte antenna. Cryptophytes acquired plastids from red algae but replaced the light-harvesting phycobilisome with a unique cryptophyte antenna. Here via analysis of phycobilisome cryo-EM structures, Rathbone et al. propose that the alpha subunit of the cryptophyte antenna originated from phycobilisome linker proteins

Automated summary

Cryptophyte algae developed a unique antenna structure through evolution from a complex between a red algal scaffolding protein and phycoerythrin beta. The interaction of these scaffolding proteins with phycoerythrin beta led to the demise of the red algal phycobilisome and the emergence of the cryptophyte antenna. Through analysis of phycobilisome cryo-EM structures, a new family of scaffolding proteins related to red algal phycobilisome linker proteins was identified, shedding light on the origin of the cryptophyte antenna.