Blog - Tiny but mighty: Algae hold the secret to turbo-charging photosynthesis in plants.

(Author: Nicky Atkinson, Editor: Helen Feord)

Photosynthesis is one of the most amazing biological processes that happens on our planet. Not to mention crucial. All around us, photosynthetic organisms are using this unique process to actually fix carbon from the air and incorporate it into living things, giving rise to nearly all the biomass on earth as well as providing us with food and balancing atmospheric carbon dioxide (CO₂) levels. To put this into perspective, ten times more CO₂ is fixed by plants each year than is released by burning fossil fuels. No wonder the earth looks green from space.

But despite appearing pretty successful, most land plants that you see around you, including crops such as rice, wheat and soybean (known as C3 plants), have a major flaw when it comes to photosynthesis. The problem is with an important and ancient enzyme, called Rubisco, which carries out carbon fixation during photosynthesis. Rubisco has been around for over 3 billion years, even before the earth had high levels of oxygen. It is a very slow enzyme and has a poor specificity for CO₂ over oxygen in our current atmosphere. In C3 plants this means that for every two molecules of carbon that it fixes during photosynthesis, it also fixes around one oxygen molecule, leading to a wasteful side reaction. To compensate, C3 plants spend an immense amount of resources into producing excess Rubisco, up to 40% of their protein production in some cases. This means that Rubisco is the most abundant protein on earth. But is there a less wasteful solution?

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Meanwhile in the oceans, a tiny but mighty set of photosynthetic organisms, single-celled algae, have found an inventive way to solve the Rubisco problem. CO₂ is much scarcer in water than air, meaning that algal Rubisco has an even tougher time discriminating against oxygen. But despite this difficulty, and their small size, single-celled photosynthetic organisms account for up to half of carbon fixation globally.

So what solution have algae come up with to become so successful? The key is a CO₂-concentrating mechanism (CCM). Aquatic green algae such as Chlamydomonas reinhardtii have a specialised structure in their chloroplasts called a pyrenoid, where Rubisco is brought together into a liquid-like condensate and provided with a high concentration of CO₂ by molecular pumps. This allows Rubisco to operate like a turbo-charged engine at maximum speed and almost eliminates any wasteful fixation of oxygen.

If only C3 plants could acquire this ingenious trick. With a CCM, modellers suggest that photosynthetic efficiency could be increased by up to 60%, which would likely be translated straight into productivity, giving a huge boost to crop yields. Given that population growth is rapidly outstripping the rate at which crop yields are increasing, the world is heading for devastating food shortages by 2050. So a productivity increase of 60% in any crop plant is not to be sniffed at. In fact, this is one of the highest yielding strategies for enhancing plant photosynthesis. Researchers at Princeton and the University of Edinburgh are trying to do exactly that. By taking CCM components from Chlamydomonas reinhartii and transferring them to the model land plant Arabidopsis, they hope to establish a working CCM in a C3 plant for the first time in history.

In the last month, the labs of Martin Jonikas (Princeton) and Alistair McCormick (UoE) have made two huge steps forward in this project. Not only have they established the mechanism by which Rubisco is held together into the ball-like pyrenoid in algae, they have engineered a proto-pyrenoid in a plant cell, consisting of an algal-style Rubisco held together by its linker protein EPYC1.

So what’s the secret to green algae’s elusive pyrenoid structure? In the pyrenoid, Rubisco needs to be packed together tightly into a matrix so that it can be bathed in a high concentration of CO₂. But it also must be accessible to various accessory proteins which ensure its smooth running. The secret is a flexible linker protein called EPYC1, which acts like molecular glue for Rubisco. Martin Jonikas and colleagues have established that EPYC1 has 5 Rubisco-binding sites along its length, allowing it to bind together different Rubisco molecules in the pyrenoid matrix. When this happens, phase separation is induced. This is like the effect of mixing oil with water – droplets appear that keep the two liquids apart – and is a mechanism used frequently by cells to separate different compartments. What’s even more interesting is that each individual interaction between EPYC1 and Rubisco is quite weak, meaning contacts can exchange rapidly and allowing the two proteins to flow past each other, whilst remaining in a densely packed matrix.

Our work solves the longstanding mystery of how Rubisco is held together in the pyrenoid matrix

Martin Jonikas

Whilst the stateside team is uncovering the secret to algae’s success, the UK team is going a step further – building a working pyrenoid in a higher plant cell from scratch! Because C3 plants do not actively concentrate CO₂, they are therefore prime targets for giving photosynthesis a helping hand. The McCormick lab here in the Institute of Molecular Plant Sciences at the University of Edinburgh, used the friendly and amenable lab favourite, Arabidopsis, as a platform for engineering a new type of pyrenoid. First, they introduced a hybrid plant-algal Rubisco that has the ability to bind to EPYC1, through genetic engineering. Then they added the molecular glue, EPYC1, with a signal attached to send it to the chloroplast. Sure enough, EPYC1 was able to bring the Rubisco together into a dense matrix, just like in algae, giving rise to a phase-separated condensate (like the oil droplet!) inside each plant chloroplast, which the team has named the proto-pyrenoid. The next step will be to add the CO₂ pumping mechanism that will feed the aggregated Rubisco with a high concentration of CO₂, allowing plant Rubisco to reach its full potential and speeding up photosynthesis!

This achievement is a major step forward in improving photosynthetic efficiency in higher plants using a strategy that researchers believe will have a dramatic effect on boosting crop productivity. Crop plants with this mechanism in place could also have improved water use efficiency, giving them an advantage when it comes to the fluctuating conditions caused by climate change. And they may just help us feed the world a little more effectively!

Related Links

Condensation of Rubisco into a proto-pyrenoid in higher plant chloroplasts

The structural basis of Rubisco phase separation in the pyrenoid