Horizontal gene transfer of cyanobacterial carbon fixing machinery: Implications for the rise of modern atmospheric oxygen

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Much of life on Earth relies on oxygen for aerobic respiration. Indeed, it is thought that mammalian reproductive systems cannot operate at oxygen concentrations much lower than today's 21%. It is therefore vitally important that we understand how oxygen is generated, maintained and consumed. The cycling of oxygen is just one of numerous 'redox-coupled' biogeochemical cycles, whereby the majority of transformations are carried out by biology. For instance, our primordial Earth completely lacked free oxygen, until the evolution of photosynthesis freed it from water more than two billion years ago. The subsequent rise of oxygen concentrations until today has been crucial for the evolution of complex life forms. Yet, this rise has been far from linear. Indeed, for most of Earth's history, oxygen concentration remained at less than one percent of today's value, with geochemical proxies suggesting large and rapid fluctuations in atmospheric oxygen roughly 600 million years ago. It is important that we establish what events catalyse these swings, to predict future habitability. Over geological timescales, oxygen concentration is controlled by three factors: 1) The amount of primary production of the biosphere, 2) The global balance of photosynthesis to aerobic respiration and 3) The rate of burial of carbon-rich organic matter into mostly marine sediments. Roughly 25% of present primary production is carried out by one group of microorganisms, marine cyanobacteria. This group represent the most numerically abundant photosynthetic organisms on Earth. They evolved roughly 650 million years ago, narrowly pre-dating a rapid rise in oxygen concentration, suggesting their distinct physiology could have driven this rise. However, we have no understanding of how this group became so abundant in the marine environment. We recently identified a genetic change that is unique to this group that controls an important aspect of photosynthesis. This genetic change involves cellular machinery, called the carboxysome, which allows carbon fixation to function efficiently. This group of cyanobacteria acquired their carboxysome from distantly related bacteria and it has subsequently been passed to all descendants. Here, we propose that this unique genetic change allows photosynthesis to better operate when nutrients are limiting. We call this the oligotrophy hypothesis. If this genetic change would have allowed these organisms to adapt to oligotrophy, this would have promoted their rapid expansion into the vast Neoproterozoic oceans, which were otherwise devoid of primary producers. The result would have been a large increase in planetary primary productivity and increase in atmospheric oxygen. By combining interdisciplinary approaches, we will test this exciting hypothesis . We will combine 'genetic transplants' of carboxysome genes and cellular modelling to understand their underlying effect on cell physiology. We will use field work to experimentally test selection of trophic status on carboxysome type. We will then integrate this data with evolutionary scenarios of cyanobacteria into geochemical models of the Neoproterozoic oceans to understand if this mechanism could plausibly explain the rise in oxygen supporting complex life. Our findings will have important implications for our understanding of the habitability of life on Earth and the existence of complex life beyond our planet.