On the Non-Oxygenic Origins of Thylakoids

Abstract

Thylakoid membranes are the site of oxygenic photosynthesis, one of the most important biochemical processes on earth. The ancestral state of these membranes is represented today in Gloeobacterales, where they are lacking and photosynthesis instead takes place in the cytoplasmic membrane. The evolutionary transition from this ancestral state to the modern thylakoid membranes was a major advantage, as it increased surface area devoted to the photosystems and thus photosynthetic efficiency. However, how this transition occurred remains a significant and surprisingly understudied biological question. With a highly synchronized process involving numerous assembly factors, the biogenesis of thylakoid membranes suggests the existence of intermediate evolutionary states during the emergence of this compartment. Here, I propose a non-oxygenic origin of thylakoid membranes, where these intermediate states were initially dedicated to alternative electron flows. This hypothesis addresses the paradox of cyanobacterial diversification in an euxinic environment, which is toxic to photosystem II.