The engine room of life

How one road trip turned a 20-year-old theory of photosynthesis on its head.

Road trips can lead to the most extraordinary adventures. That’s why there is a whole genre of movies devoted to them.

Unlike in the movies, a road trip that Professor Elmars Krausz, PhD student Joe Hughes and Post-Doctoral Fellow Barry Prince took back from Melbourne one very hot day three years ago was not meant to be a journey of discovery.

The team from the Research School of Chemistry were simply travelling back to Canberra from a conference. But the road trip turned out to be the beginning of a huge journey of discovery for Krausz and his team. It marked a turning point in how we understand oxygenic photosynthesis – the engine room of life – and turned a 20-year theory on its head. It was during that road trip, tossing ideas around the car, that the group concocted a new theory about the strange results they were getting from their experiments with spinach in the Laser and Optical Spectroscopy Laboratory.

Using high-resolution lasers, they discovered the rate at which energy is fed into photosynthetic reaction centres is very strongly controlled by biological speed humps - a great surprise and opposite to what had been understood. Photosystem II also absorbed energy at far longer wavelengths than previously thought.

“It [oxygenic photosynthesis] makes the air we breathe and the food we eat, yet we really don’t know how it works,” Krausz says.“We discovered that the special reaction centres that power oxygen production have been misunderstood for decades.’’

This discovery and subsequent results have fuelled a slowly but steadily growing amount of international attention on the team’s work, and brought international visitors to ANU. In July, Krausz will present the team’s work at the prestigious Photosynthesis Gordon Conference in New Hampshire, an invitation-only opportunity for people working on frontier research to present their ideas.

“All life on the planet is sustained by photosynthesis, with a few minor exceptions,” says Krausz. “Photosynthesis is what allows life to happen. [With the sun] we essentially have a nuclear reactor working 93 million miles away that has been working for billions of years with no need for refueling or dealing with radioactive waste disposal problems.”

To understand what it is that Krausz and his team are looking at, you have to travel back to what he calls the “greatest ever ecological disaster to happen to our planet.”

“Before oxygenic photosynthesis, we had sulphur bacteria – they were the ones who got their energy from H2S (hydrogen sulphide). H2O (water) is related to H2S, but H2S is much easier to extract the electrons out of,” says Krausz.” But the problem with H2S, besides the smell, is that there isn’t enough of it around to allow much to happen.

“One organism somehow evolved a trick so as to be able to get the electrons out of water, putting it in the box seat [in evolutionary terms] because (a) there was heaps of water around and (b) the oxygen that was the byproduct of this process was utterly toxic to almost everything else. Not only did it have an infinite supply of a fuel to work with, it killed everything else. The oxygen also changed the atmosphere and surface geology of the entire planet.

“The most severe ecological disaster that ever happened to the planet was [the development of] oxygen-evolving organisms. Oxygen in the atmosphere weathered the rocks, increasing the amount of available iron [that is needed in every organism]. Oxygen also led to the formation of the ozone layer. The ozone layer, by protecting the surface of the planet from extreme ultraviolet radiation, allowed life to come out of the water. These little water munching things were responsible for some of the most dramatic, sustained and profound changes that ever occurred in our biosphere,” explains Krausz.

All atmospheric oxygen is of biological origin. The main culprit, however, is not plants but humble cyanobacteria. These single-cell organisms, which were present on Earth more than 3.5 billion years ago and pre-date plants, were initially responsible for all oxygen production and are still responsible for more than 60 per cent of current oxygen production.

Species of cyanobacteria present in the ocean, Synechococcus and Prochlorococcus, are not only some of the smallest photosynthetic organisms known – they are also, by far, the most abundant species on the planet. Their small size made them difficult to detect even with powerful microscopes. Nonetheless they constitute most of the biomass on the planet. Prochlorococcus was only discovered in 1985.

“Our focus has been on that bit of the photosynthetic apparatus that splits the water to produce oxygen. Most organisms don’t make hydrogen gas, although there are some that do, and the hydrogen part of water in most systems ends up as bio-energetic protons. If we can find out how this is done, not only do we have the potential of improving agriculture and aquiculture (most of the biomass on the planet is in the ocean, not on the land), but we also have the potential to produce sustainable energy by mimicking the processes in nature.

“What we are looking at is how this process works with the clear vision to provide a sustainable energy source for human societies and not rely on the accumulated photosynthetic product of billions of years [such as coal and oil].

“An urgent problem that impacts on everyone on the planet is carbon dioxide production. What we need is an energy producing process that is at least carbon dioxide neutral. If it absorbs carbon dioxide all the better!”

Krausz says there is potential in hydrogen production by cyanobacteria. “This is a clearly attractive prospect because you’re absorbing CO2 using sunlight and making hydrogen in a concerted process. This is what we’re hoping to develop – a truly sustainable molecular energy technology capable of serving the needs of all.”

Like the production of oxygen by Cyanobacteria, the path that led Krausz and his team to challenging a scientific orthodoxy was an evolutionary one.

“Paul Smith here at ANU was making this really good preparation of spinach, which just consisted of the active part of Photosystem II. Associate Professor Ron Pace, who was Paul’s supervisor, said ‘Why don’t you have a look at this [the spinach preparation].’”

“Ron arranged for a biochemistry PhD student from Sweden, Sindra Peterson, to come to ANU to help study the preparation. The team started looking at the preparation with their lab instruments, and noticed what Krausz calls “a really nice spectrum,” with features they couldn’t find in the literature.

“We started to study it a bit and we found a few effects that hadn’t been reported. We put out a little spiel, and people said ‘Oh, that’s all really been done, and it’s not interesting. What you have to study are highly refined particles.’ And we said ‘OK, all right, but somehow it doesn’t seem to add up.’ We persisted with studying these Photosystem II preparations and we became quite sure it was like a flimsy Lego construction – as soon as you took out one bit, the whole thing fell apart and wasn’t really a thing anymore. Certainly not representative of the full assembly, the real thing that produced oxygen.”

The team persisted and began to shine laser beams on the spinach preparations at low temperatures. “We found a phenomenal effect,” says Krausz. As part of this laser excitation experiment, we discovered that the whole dynamics of the Photosystem II core was really very different to what people were saying.

“We got into it to see how low you can go. We kept reducing the energy at which we were exciting the preparation with the laser and we found that we could really even go further. This has really opened up an entirely new area [for us].”
Interest and acceptance for the ANU findings is growing, but Krausz says he doesn’t feel his team is on a one-way ticket to science superstardom just yet.

“You can’t really know in science, because serendipity is a component, and of course your hard work and energy, but the most fantastic things can come to nothing and the smallest things can grow to great things.

“I was invited to conference last October in Amsterdam, where everyone was talking about what was going on at ANU. They had to believe the results but they couldn’t really cope with what it meant, and they were kind of hoping that it didn’t matter, and that they were still right.”

The team believes that while they may be on the pointy end of research, rather than the applied end, their work has great potential for practical outcomes, and the practical solutions to energy production it may have mean it is worth supporting to reduce the fossil fuel use that contributes to climate change. In effect, the road trip is still just beginning.

“We really want to combine with other people in Australia and worldwide to build a substantial effort in Molecular Energy Technologies. The approach can be built upon an intimate knowledge of natural systems, and applying it to chemical aspects of artificial photosynthesis. It can be done. We really can bring all those things together but it needs a recognition by society, industry and government of the fundamental priority to this nation and the entire planet of a sustainable and renewable energy supply,” says Krausz.

“In the short term we can try and bury the carbon dioxide we generate; we can build nuclear reactors; we can look to greater energy efficiencies. These approaches may buy some time. The truth is we need to do all these things. We have to try everything and we need to do it now.”

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ANU Reporter
Autumn 2006