Endosymbiosis and genome evolution in eukaryotic microbes

我们正处于一场科学革命之中，这场革命建立在我们对DNA的理解之上，DNA是生命的遗传分子。使用分子生物学的工具，我们正在以十年前无法想象的方式探索我们周围的世界。真正取得显著进展的一个领域是我们对微生物生物圈的理解。数以千计物种的基因组(基因蓝图)已经被破译，不仅是实验室培养的生物，还有直接从它们的自然栖息地提取的微生物：人类的肠道、海洋、土壤，甚至我们呼吸的空气。对这些丰富的遗传数据的比较分析表明，水平基因转移--跨越物种边界的遗传物质交换--是一种强大的进化力量。越来越多的人支持这样一种观点，即当考虑到微生物时，达尔文的“生命之树”实际上是一张生命之网--一个复杂的网络，基因在30亿多年的时间里在不同的生命形式之间垂直和水平地流动。阿奇博尔德实验室研究共生在复杂生命形式进化中的作用。内共生的过程，即一个细胞占据另一个细胞的内部，不仅涉及基因的“混合和匹配”，也涉及整个生物体的“混合和匹配”。在像我们自己这样的复杂细胞中产生能量的线粒体，本质上是驯化的细菌：它们是通过内共生从自由生活的细菌细胞进化而来的。叶绿体是植物和藻类的聚光室，也是内生共生生物的来源。在这个提案中，我们将应用分子和基于计算机的研究方法来研究单细胞藻类中的DNA。其目标是详细了解内共生的模式和过程，以及它在复杂的光合作用真核生物起源中的作用。我们研究的特定微生物在细胞上相当于俄罗斯的筑巢玩偶：它们是细胞反复内共生的结果，在这些细胞中，细胞驻留在其他细胞中，而其他细胞本身又嵌套在更大的细胞中。这些一系列的内生共生事件已经产生了一些地球上最丰富和最重要的生态初级生产者，包括硅藻(海洋的“明珠”)、巨型海藻和甲藻，它们引起了“赤潮”，也是珊瑚礁的重要组成部分。尽管它具有明显的生物学意义，但人们对次级内共生的机制细节知之甚少。我们将分析某些藻类的基因组，以深入了解(I)在不同物种中，基因如何以及如何频繁地从一个亚细胞室移动到另一个亚细胞室，以及(Ii)这些古老进化的嵌合体细胞在多大程度上是生物化学的产物。除了生命本身的起源之外，线粒体和质体的内生共生起源可以说是地球历史上最重要的事件。然而，直到最近，共生还被斥为进化上的怪异现象。现实情况是，光合作用的海洋微生物承担了地球上一半的初级生产，并形成了海洋食物网的基础。对于我们来说，了解这些有机体来自哪里；它们如何相互作用；以及它们可能如何适应人类引发的环境变化，这一点很重要。

We are in the midst of a scientific revolution built on our understanding of DNA, the hereditary molecule of life. Using the tools of molecular biology, we are exploring the world around us in ways unimaginable just a decade ago. One area in which truly remarkable advances have taken place is our understanding of the microbial biosphere. The genomes (genetic ‘blueprints’) of thousands of species have been decoded, not only organisms cultured in the lab but microbes taken directly from their natural habitats: the human gut, the oceans, soil, even the air we breathe. Comparative analyses of this wealth of genetic data have revealed that horizontal gene transfer—the exchange of genetic material across species boundaries—is a potent evolutionary force. There is increasing support for the notion that when microbes are considered, Darwin’s ‘tree of life’ is in fact a web of life—a complex net through which genes have flowed both vertically and horizontally between diverse life forms for more than three billion years. The Archibald Laboratory studies the role of symbiosis in the evolution of complex life forms. The process of endosymbiosis, in which one cell takes up residence inside another, involves the ‘mixing and matching’ not just of genes but entire organisms. The mitochondria that produce energy inside complex cells such as our own are, in essence, domesticated bacteria: they descend from free-living bacterial cells by endosymbiosis. Plastids (chloroplasts), the light gathering compartments of plants and algae, are also of endosymbiotic origin. In this proposal we will apply molecular and computer-based research approaches to the study of DNA in single-celled algae. The goal is to develop a detailed understanding of the pattern and process of endosymbiosis and its role in the origin of complex photosynthetic eukaryotes. The particular microbes we study are the cellular equivalent of ‘Russian nesting dolls’: they evolved as a result of repeated rounds of endosymbiosis in which cells come to reside within other cells, which are themselves nested within larger cells. These serial endosymbiosis events have generated some of the most abundant and ecologically important primary producers on Earth, including diatoms (the ‘jewels’ of the ocean), giant kelp, and dinoflagellate algae, which cause ‘red tides’ and are also essential components of coral reefs. Despite its obvious biological significance, relatively little is known about the mechanistic details of secondary endosymbiosis. We will analyze the genomes of certain algal groups to gain insight into (i) how and how often genes move from one sub-cellular compartment to another in different species and (ii) the extent to which these anciently-evolved chimaeric cells are the product of ‘mix and match’ biochemistry.Next to the origin of life itself, the endosymbiotic origins of mitochondria and plastids were arguably the most important events in the history of our planet. Yet until quite recently symbiosis was dismissed as an evolutionary oddity. The reality is that photosynthetic marine microbes carry out half of the primary production on Earth and form the foundation of oceanic food webs. It is important for us to understand where these organisms came from; how they interact with one another; and how they are likely to adapt to human-induced environmental change.