Australasian Science Magazine

A Chroococcidiopsis colony containing both normal and “far-red” photosynthetic cells. Credit: Dennis Nürnberg

By Elmars Krausz

The discovery of a new form of photosynthesis extends the limits where life can survive on Earth, and might provide a first step to terraforming Mars.

Earth is blessed with an abundant supply of liquid water, and is continuously bathed in light from the Sun. Nature has taken advantage of these conditions to evolve more than a trillion life forms.

Life needs chemical energy to drive its machinery along. Essentially, it requires an oxidisable chemical as a source of electrons. Early life forms exploited a number of processes, but in the end the “voltage” of these sources of electrons and the availability of the relevant chemicals were limited. So nature took another tack.

Each quantum of visible light coming from the Sun has an “energy” of more than 1 V – enough to do a lot of chemistry. Each colour of light has a different “voltage”. For example, a single silicon solar cell on your roof produces up to 0.8 V by absorbing near-infrared light, while plants use chlorophyll molecules to absorb red light, which has more energy and can generate a maximum of 1.8 V.

By inventing photosynthesis, nature provided a “voltage kick” to photo­active molecules in the photosynthetic apparatus (e.g. chlorophyll), enabling them to extract electrons from a far wider range of molecules. Some of the early photosynthetic organisms extracted electrons from hydrogen sulphide (H2S).

A monumental breakthrough occurred when photosynthetic bacteria found a way of splitting water, which is a far more abundant source of electrons than hydrogen sulphide. However, stripping electrons from water requires a minimum voltage of 1.2 V, whereas H2S needs just 0.14 V. It’s important that there is a photochemical “safety margin” to stop oxidation from running backwards or generating unwanted side-products.

The incredible feat of being able to oxidise water, in what is the most energetic process in all of biology, with high efficiency and in a process close to the limits of possibility, has completely transformed the planet. Oxygenic photosynthesis has allowed complex life forms to evolve and proliferate. The process has not only provided us with the food we eat and the oxygen we breathe, but has transformed the planet into the beautiful orb we inhabit.

A cross-section of beach rock from Heron Island showing chlorophyll-f-containing Chroococcidiopsis growing deep into the rock, several millimetres below the surface. Credit: Dennis Nürnberg

Life in Extreme Environments

A recent genetic analysis (https://goo.gl/JkyCtX) has highlighted the amazing diversity of bacteria and archaea present in the tree of life. These single-celled organisms were the first (and remain the best) chemists on the planet. They perform difficult and absolutely critical chemical transformations, such as the fixation of atmospheric nitrogen and carbon dioxide as well as splitting water into oxygen and hydrogen.

Many of these skills have been passed on to plants; chloroplasts in plant cells are basically stripped-down versions of cyanobacteria. In fact, the catalyst that splits water is the same in all plants and cyanobacteria. After billions of years of evolution, nature has only found one way to split water. The ability to fix nitrogen remains unique to bacteria; plants haven’t been able to do it.

Among the trillion life forms on the planet are the extremophiles. These survive under extreme conditions of heat or cold, extreme acidity or alkalinity, ionising radiation, high pressure, high salinity or low/high light. Extremophiles are dominantly single-celled bacteria and archaea, and examples cluster at the base of many branches of the tree of life.

Studies of these outliers can be particularly important. Their robustness enable stable, highly purified enzymes to be isolated and crystallised. These purified samples are invaluable for detailed studies of fundamental processes occurring in each enzyme.

Extremophiles we have studied include the bacterium Thermosynechococcus vulcanus, which can survive a scalding temperature of 70°C, and the red alga Cyanidioschyzon merolae, which grows happily in hot, strong acid. The genus

Chroococcidiopsis thermalis is famous for surviving when exposed to the desiccation and radiation experienced on the outside of the International Space Station. Fundamental processes, such as the mechanism of water splitting, are often the same in both extremophiles and “normal” plant and cyanobacterial systems, but there can also be remarkable and important differences.

Lissoclinum patella shields the cyanobacteria Acaryochloris marina growing beneath it from all but far-red light. Courtesy: National Science Foundation

Splitting Water with Far-Red Light

An extraordinary extremophile, Acaryochloris marina, was discovered by Japanese researchers in 1993 on the remote island of Palau in the Western Pacific (https://goo.gl/gmuXqB). It was found growing on the underside of the sea squirt Lissoclinum patella while being strongly shaded by a layer of “normal” cyanobacteria. As a consequence, this strange cyanobacterium sees little light. Indeed the light it does receive is so far into the red part of the visible spectrum that it’s not usually able to drive oxygenic photosynthesis.

Normal organisms use only one type of chlorophyll, chlorophyll-a, to generate the voltage needed to split water. Acaryochloris marina, however, is dominated by chlorophyll-d, which absorbs energy in the far-red, as well as a small amount of chlorophyll-a.

In 2010, an Australian and international team investigated cyanobacterial mats growing a few millimetres below the surface of stromatolites in Shark Bay, Western Australia. When extracting pigments from the mat they uncovered an entirely new chlorophyll they named chlorophyll-f (https://goo.gl/7yXKye). This molecule, which differs only subtly from other chlorophylls, also absorbs far-red light at a wavelength even longer than chlorophyll-d.

Chlorophyll-f has since been found in a wide range of organisms. The critical question was: what is it doing? The consensus view was that it only assisted in harvesting far-red light, which then fed “normal” chlorophyll-a photosynthesis by simply using heat to make up for its voltage deficit.

This question has been answered with our wide-ranging study of Chroococcidiopsis thermalis, which has now been published in Science (https://goo.gl/66MXAS). When grown in normal light, the photosystems in Chroococcidiopsis are entirely normal, using only chlorophyll-a. However, when grown in far-red light its photosystems are still dominated by chlorophyll-a but it introduces a few chlorophyll-f pigments and one chlorophyll-d. We were able to show that the far-red chlorophylls generated the voltage required to perform oxygenic photosynthesis and thus perform a critical function. This defines a new type of photosynthesis.

What Are the Limits?

It was long thought that in order to split water, you needed red light at a wavelength of ~680 nm. This defined the “red-limit” of photosynthesis. Our new work shows that a wavelength of 730 nm can do the job for Chroococcidiopsis. This far-red light option corresponds to having 0.11 V less excess voltage available to split water, and thus reduces the safety margin.

Can we go further and use even longer wavelength far-red light, and thus do with even less voltage? This would enable photosynthesis to access a wider section of the Sun’s light spectrum, making it more adaptable and more efficient.

A clue to the possibility of further extending the red limit comes when observing Chroococcidiopsis grown under far-red light. In this scenario the organism becomes sensitive to white light. Operating on 0.11 V less may compromise the photo-protection mechanisms of Chroococcidiopsis grown in far-red light. Splitting water and making oxygen leads to the possibility of extremely damaging by-products and back-reactions. By-products include peroxides, superoxides, singlet oxygen and other reactive oxygen species.

In normal photosynthesis, some of the higher voltage available from chlorophyll-a is used to protect against such processes. It now seems that the far-red light-driven process we have uncovered in Chroococcidiopsis may indeed be the ultimate red limit of photosynthesis.

Could We Terraform Mars?

There has been long and intense interest as to whether life exists or could even survive on other planets. Life, as we know it, requires the presence of liquid water. Simpler life forms that preceded photosynthetic organisms could perhaps occupy niches on other planets, but oxygenic photosynthesis on a massive scale would be needed for life to proliferate and for Mars to provide an atmosphere in which we could breathe.

Chroococcidiopsis could perhaps survive on Mars. Indeed, our studies highlight its ability to grow using the far-red light that may filter through rocks on the Martian surface. By growing under rocks, protection from lethal ultraviolet and other forms of cosmic radiation would be provided.

Armed with a deeper knowledge of fundamental photosynthetic processes, we could look to engineer extremophiles optimised for the environment in each microclimate on Mars. It would certainly help if Mars could be made somewhat warmer so that more liquid water might become available on the surface. This water could perhaps be sourced from something like the large lake of cold and salty liquid water recently discovered 1.5 km below the Martian south pole (https://goo.gl/NfgzLP).

Using climate modelling to determine a strategy for geo­­engineering the surface temperature of Mars could be a goal. However, determining whether the transformation of Mars could be performed on a useful timescale remains to be seen.

Our work on a new type of photosynthesis discovered in Chroococcidiopsis has shown that this organism has uniquely different fluorescence signatures to those seen in normal photosynthetic organisms. Normal photosystem fluorescence, measured from satellites, is routinely used to provide a detailed map of global photosynthetic activity. Our new fluorescence signature may therefore help us look for a far-red photo­synthetic process on other worlds.

However, the first priority is to treasure and care for the beautiful planet we inhabit.