Endosymbiosis and genome evolution in eukaryotic microbes

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.