How cyanobacteria developed photosynthetic membranes over the course of evolution

New study provides first  insights into how thylakoid membranes - the internal compartments where oxygen-producing photosynthesis takes place - emerged during evolution. By comparing the genomes of cyanobacteria with and without thylakoids, the researchers have identified proteins that may have contributed to their formation. 

A tree leaf can be pictured as a small town powered by solar energy. Each cell in this leaf contains a power station - the chloroplast - whose thylakoids act as solar panels. These specialised internal membranes (thylakoids) carry out the photosynthetic reactions that produce oxygen, in plants and algae as well as in cyanobacteria, whose chloroplasts are their distant descendants. The emergence of thylakoids is regarded as a significant milestone in the history of life. By improving the efficiency of oxygenic photosynthesis, these structures may have contributed to the Great Oxygenation Event, which occurred around 2.4 billion years ago - a period during which oxygen began to accumulate sustainably in the Earth’s atmosphere.

However, how these membranes first arose remains poorly understood. “The process is complex,” explains Louise Hambücken, a researcher at the Laboratory of Eukaryotic Phylogenomics at the University of Liège, “it involves both the formation of the membrane itself and the tightly coordinated assembly of the associated proteins . And we still know very little about how these mechanisms emerged in the earliest cyanobacteria.” The scarcity of fossils from this period further complicates our understanding of this part of our history.To tackle this, the ULiège team – which is studying the origin and evolution of photosynthesis in these basal cyanobacteria – has focused on a group of modern cyanobacteria, the Gloeobacterales, which are considered to be close to the ancestral state. “The Gloeobacterales lack thylakoids and carry out photosynthesis at the plasma membrane surrounding the cell,” the young researcher adds. This led the team at the University of Liège to conduct a large-scale comparative bioinformatics analysis. “By comparing a wide variety of cyanobacterial genomes, both with and without thylakoids, we identified proteins potentially involved in the formation of these membranes.” This is the first study to investigate the evolutionary processes underlying thylakoid formation through such an approach.

The comparison also focused on photosystem II, revealing which stages of its assembly were already present, absent or different in the Gloeobacterales. Photosystem II is a large complex of proteins and pigments embedded in the photosynthetic membrane, which is the thylakoid membranes in most cyanobacteria and the plasma membrane in Gloeobacterales. It is one of the two ‘photosystems’ (hence its name, Photosystem II) that carry out the light-dependent reactions of photosynthesis. Its distinctive feature is that it uses light energy to extract electrons from water. This reaction releases oxygen and protons, enabling photosynthetic organisms to convert the Sun’s energy into chemical energy. On an evolutionary scale, this process has contributed to the gradual accumulation of oxygen in the Earth’s atmosphere.

“These findings are part of fundamental research and have no direct application at this stage,” concludes Dr Luc Cornet, a researcher at the Laboratory of Eukaryotic Phylogenomics (ULiège). “However, they provide an initial basis for gradually reconstructing the evolutionary history of thylakoids and for better understanding how oxygenic photosynthesis has been optimised over time.” In the longer term, a better understanding of how specialised biological membranes are organised and modified could also open up new avenues in biotechnology and synthetic biology, centred on energy conversion within the cell. The study sheds new light on how cyanobacteria gradually relocated their photosynthetic machinery from the cell membrane to dedicated internal structures that act as miniature solar power stations: the thylakoids.