Photosynthesis was acquired by eukaryotes some 2 billion years ago through the merger of two cells, one inside another, a process called endosymbiosis. Similar to the origin of mitochondria, this process resulted in new cellular organelles that in this case are called the plastids. There exists different kinds of plastids, perhaps the best known are the chloroplasts. From the origin of plastids by endosymbiosis between early eukaryotes and cyanobacteria evolved the first eukaryotic algae, giving rise to land plants but also triggering the evolution of most photosynthetic eukaryotes by subsequent endosymbioses between these first algae and other eukaryotes. Thus, the origin of plastids profoundly changed the course of eukaryotic life by being the launching point that shaped the biological diversity of most primary producers, and allowing life as we know it to evolve. Despite this importance, our understanding of how plastids originated remains largely uncertain. The current paradigm describes this transformative event as a single primary endosymbiosis, but we argue in PlastidOrigin that critical data is lacking, notably from the vast hidden environmental diversity of microbes, to adequately test this hypothesis. In this project, we propose to gain insight into the origin of plastids by addressing four main questions: 1) What is the currently hidden diversity of high-ranked microbial taxa, similar to better known ‘kingdoms’ of life such as animals or plants, related to known photosynthetic lineages? 2) What can we find out about these cells, for example do they have plastids? 3) Are some lineages genetically predisposed to establish plastids from the acquisition of foreign genes by lateral gene transfers? 4) What was the composition, size, and origin of the ancestral primary plastid proteomes? To answer these questions, we will link environmental sequencing (notably using long-read sequencing), single-cell transcriptomics, and genomics to cell structure and behavior of novel key lineages related to known algae, and produce crucially missing plastid proteomes to allow comprehensive comparative proteomic analysis. This project will not only have immediate implications on our understanding of the origin of plastids and more generally the fundamental process of endosymbiosis, but the approaches developed will be a test bed for future global studies aimed at understanding the evolution and ecology of the microbial majority of complex life.
