CERBERUS Cataclastic hydrogen and oxidant production in the deep biosphere: uncovering the ancient role of microbial antioxidant enzymes

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CERBERUS - SummaryIt has been estimated that there is more microbial life under our feet in deep rocks and sediments than there is on the surface or our planet - yet there are still large gaps in our understanding of how this life survives in the absence of light and photosynthesis. There is now strong evidence that hydrogen gas, produced by water reacting with rocks, is an important source of energy (or food) for subsurface microbes - and that the use of this hydrogen dates back to the very first life that arose on Earth. A very substantial source of subsurface hydrogen is generated from the grinding of rocks along geological faults, with freshly fractured rock surfaces 'splitting' water to form hydrogen gas, alongside an equal amount of oxygen equivalent (oxidants) such as the highly oxidizing and toxic chemical hydrogen peroxide, used in bleaching.While previous studies have measured the amount of hydrogen produced during geological faulting, CERBERUS focuses on the other side of the equation - what happens to the oxidants? Through initial experiments we show that these oxidants are likely only being released from minerals at very hot temperatures where only the most heat-loving microorganisms, known as hyperthermophiles, can live and thrive, at temperatures close to or over the boiling point of water. From studies back-tracing particular genes common to all life to a Last Universal Common Ancestor (LUCA) we know that such heat-living microorganisms were likely to have been the first life to arise on Earth, and that they used hydrogen. However, the gene back-tracing has also suggested that LUCA contained abundant mechanisms for dealing with oxygen and hydrogen peroxide, while some of the most deeply rooted braches of the 'universal tree of life' contain oxygen utilizing microorganisms. To date, the most widely accepted reason for these oxygen-utilizing genes is that they result from later genetic 'contamination' of all life after the oxygen-producing photosynthesis evolved on our planet, many hundreds of millions of years after life first started. In CERBERUS, we suggest an alternative. That life first arose in hot, subsurface fractures where there was not only hydrogen present, but also hydrogen peroxide produced from water splitting on fractured rock surfaces. We further suggest that these microorganisms evolved key enzymes to combat these oxidants, including those that could convert the more toxic hydrogen peroxide to less toxic oxygen - and in doing so generate usable energy to power life and drive further evolution.CERBERUS will carry out new experiments, measuring how both hydrogen and oxidants are produced in fractured rock-water reactions up to and beyond the known limit of current life (122 deg C). To some experiments we will add pure strains of hyperthermophilic microorganisms, to see how they can alter the products of the reactions, and to see if they can grow from the hydrogen, hydrogen peroxide and oxygen produced during the reactions. Results from CERBERUS should shine a light on how life can survive in the Earth's deep, hot subsurface - and give insight into how early life took hold on our planet.