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

地球上的大部分生命依靠氧气进行有氧呼吸。事实上，人们认为哺乳动物的生殖系统不能在比现在低得多的氧气浓度下运作。因此，了解氧气是如何产生、维持和消耗的是至关重要的。氧的循环只是众多“氧化还原耦合”生物地球化学循环中的一个，其中大部分转化是由生物学进行的。例如，我们的原始地球完全缺乏游离氧，直到20多亿年前光合作用的进化将其从水中解放出来。直到今天，氧气浓度的上升对复杂生命形式的进化至关重要。然而，这种增长远不是线性的。的确，在地球历史的大部分时间里，氧浓度一直保持在不到今天的1%的水平，地球化学指标表明，大约6亿年前，大气中的氧浓度出现了巨大而迅速的波动。重要的是，我们要确定哪些事件催化了这些波动，以预测未来的宜居性。在地质时间尺度上，氧浓度受三个因素控制：1)生物圈初级生产量；2)光合作用到有氧呼吸的全球平衡；3)富碳有机质埋入海洋沉积物的速率。目前大约25%的初级生产是由一组微生物——海洋蓝藻进行的。这个群体代表了地球上数量最多的光合生物。它们大约在6.5亿年前进化，略早于氧浓度的快速上升，这表明它们独特的生理机能可能推动了这种上升。然而，我们不知道这个群体是如何在海洋环境中变得如此丰富的。我们最近发现了一种独特的基因变化，它控制着光合作用的一个重要方面。这种基因变化涉及被称为羧基体的细胞机制，它允许碳固定有效地发挥作用。这组蓝藻从远亲细菌中获得羧基体，并随后传递给所有后代。在这里，我们提出这种独特的遗传变化允许光合作用在营养有限的情况下更好地进行。我们称之为少营养假说。如果这种基因变化能让这些生物适应少营养，这将促进它们迅速扩张到广阔的新元古代海洋中，否则那里就没有初级生产者。其结果将是行星初级生产力的大幅增加和大气中氧气的增加。通过结合跨学科的方法，我们将检验这个令人兴奋的假设。我们将结合羧基体基因的“遗传移植”和细胞模型来了解它们对细胞生理学的潜在影响。我们将利用田间工作，对羧酶体类型的营养状况选择进行实验研究。然后，我们将把这些数据与蓝藻的进化情景整合到新元古代海洋的地球化学模型中，以了解这种机制是否能合理地解释支持复杂生命的氧气的增加。我们的发现将对我们理解地球上生命的可居住性以及地球以外复杂生命的存在具有重要意义。

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.