Luc Cornet
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 provided a major advantage, as it increased photosynthetic efficiency. However, how this significant transition occurred remains an understudied question. The biogenesis of modern thylakoid membranes relies on a highly synchronized process involving numerous assembly factors and showing important differences between the two photosystems. Together, these features suggest 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 further addresses the paradox of cyanobacterial diversification in an euxinic environment, toxic to photosystem II.
https://www.nature.com/articles/s42003-025-09100-w

Cyanobacteria are the only prokaryotes that perform oxygenic photosynthesis by utilizing two photosystems in their electron transport chain (ETC), with photosystem II (PSII) splitting water molecules. In most cyanobacteria, this process occurs within the membranes of specialized compartments called the thylakoids. The process by which the ETC is integrated into the thylakoids has been studied for certain subunits and involves the coordination of numerous assembly factors, of which only a fraction has been identified so far. In Gloeobacterales, the most basal group of extant cyanobacteria, these photosystems and the ETC are instead integral to the plasma membrane. While recent studies suggest an appearance of oxygenic photosynthesis well before the Great Oxidation Event (GOE), the structural advantages of thylakoids hint to a key role in GOE, though their origin remains unclear. The aim of this project is to test the hypothesis that the emergence of thylakoids is related to anoxygenic photosynthesis and alternative electron flows, conferring an advantage in the photic zone of Proterozoic oceans, where oxic and sulfidic-rich conditions coexisted. In this project, metabolic modelling by flux balance analysis will be used to test hypothetical evolutionary stages of thylakoids in simulated conditions.

Louise Hambücken, Denis Baurain, Luc Cornet
Thylakoid membranes (TM) in cyanobacteria and chloroplasts host the light-dependent reactions of oxygenic photosynthesis which involve a linear electron transfer (LET) chain composed of multi- subunit complexes, including notably Photosystem II (PSII). Gloeobacterales, the earliest-diverging cyanobacterial lineage, lack TM and perform photosynthesis within specialized regions of the cytoplasmic membrane (CM), thereby representing an ancestral state with respect to other cyanobacteria, all equipped with TM and known as Phycobacteria. The emergence of TM, which increased the membrane surface available for oxygenic photosynthesis, was a key innovation that likely contributed to the Great Oxidation Event. This evolutionary transition involved the formation of a distinct membrane compartment, followed by the relocation of LET components from the CM to TM. Here, we present a phylogenomic analysis identifying three candidate proteins associated with membrane trafficking that may contribute to TM biogenesis, including the SPFH family member Slr1106, which we show was acquired via lateral gene transfer. Moreover, evolutionary analysis of 36 PSII assembly factors indicates key modifications in late-stage PSII assembly, notably in manganese homeostasis, and highlights structural changes in the early-acting YidC translocase that may have facilitated the relocation of LET components from the CM to TM. Altogether, our phylogenetic and functional prediction analyses of proteins involved in membrane dynamics and PSII assembly factors bring new insights into the molecular innovations that led to the emergence of TM.
https://doi.org/10.1101/2025.11.06.686923

Louise Hambücken, Edi Sudianto, Jimmy H. Saw, Denis Baurain, Luc Cornet
Oxygenic photosynthesis, which converts solar energy into carbohydrates via a linear electron transport chain and two photosystems (PSII and PSI), first appeared in cyanobacteria approximately 3.3 Ga and drove the Great Oxidation Event around 2.4 Ga. During this period, euxinic conditions—characterized by sulfidic, anoxic oceans—posed a metabolic challenge to cyanobacteria, as sulfide inhibits PSII, the reaction center responsible for water splitting. Here, we report the presence of an early-diverging form of the sulfide quinone reductase (SQR) enzyme in Antarctic representatives of Gloeobacterales, the earliest-branching cyanobacterial lineage lacking thylakoids. Phylogenetic analyses reveal that these SQR sequences are the earliest-diverging cyanobacterial SQR known to date, predating the multiple lateral gene transfer events previously observed in the phylum. Additional searches in metagenomic datasets indicate that such sequences are restricted to cold environments. Our findings unveil possible adaptive strategies of early cyanobacteria to cope with sulfidic stress and point to Antarctic lakes as preserved natural laboratories for investigating cyanobacterial diversification and the evolution of oxygenic photosynthesis under euxinic conditions.
https://doi.org/10.1101/2025.10.24.684318

Edi Sudianto, Denis Baurain, Luc Cornet
Gloeobacterales has long been considered a “living fossil” cyanobacterial order, owing to its lack of thylakoid membranes and basal phylogenetic position. However, our study reveals that Gloeobacterales actively integrate horizontally transferred genes into their core metabolism. In Gloeobacteraceae—one of the two families within the order—these genes encode a complete ribose ATP synthase binding cassette (ABC) importer and downstream enzymes, enabling the heterotrophic uptake of external ribose and its assimilation into central carbon metabolism, along with photosynthesis, indicative of photomixotrophy. Beyond ribose utilization, their central carbon metabolism exhibits a mosaic architecture shaped by the integration of foreign genes into the Calvin-Benson-Bassham cycle, the pentose phosphate pathway, and the Embden-Meyerhof-Parnas pathway. Uniquely, these genes appear to have been acquired through multiple independent transfer events, as reflected by their dispersed genomic locations and diverse bacterial donors, including other cyanobacteria and Pseudomonadota. These findings contradict the long-standing view of Gloeobacterales as metabolically primitive relics. Instead, Gloeobacterales is likely a dynamic lineage that continues to adapt and evolve through metabolic innovation and the assimilation of foreign genes into its genomes.
https://doi.org/10.1101/2025.11.10.686926