Unity and Diversity of Ultrastructural Systems in Single Celled Eukaryotes

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For over 3 billion years, microbes have dominate the planet in terms of abundance and diversity, yet the fundamental and innovative properties of microbes are the least understood of all organisms. Of the three major lineages of microbial life (Eukarya, Bacteria and Archaea), single-celled eukaryotes are by far the most complex, having nuclei, endomembrane systems, symbiotically acquired organelles and elaborate cytoskeletons supporting a vast array of cell extensions and behaviors. Despite being composed of only a single cell, each microbial eukaryote is essentially a universe in and of itself, and advances in our understanding of these organisms have overturned long-held views about the diversity of cells. Accordingly, the proposed research program is designed to explore this foreign world in order to help unravel the total composition, interrelationships and history of life. The research aims to discover and characterize novel ultrastructural systems in single-celled eukaryotes and make contributions to an all-species Encyclopedia of Life, consisting of digital images and DNA sequences. Individual projects will span a broad sampling of eukaryotic diversity in order to resolve large-scale patterns of ultrastructural trait evolution (e.g., convergence). The research program will continue to study, in parallel, four major groups of single-celled eukaryotes that encompass what are arguably the three most dissimilar modes of eukaryotic life on the planet: predation, photoautotrophy, and parasitism. The independent but corresponding patterns of morphological change in marine predatory flagellates, such as euglenids, dinoflagellates and cryomonads, represent an ideal comparative system for investigating the constraints and reoccurring innovations in cell evolution. All three groups have diversified within the spaces between grains of sand and have independently acquired sophisticated feeding apparatuses, modes of gliding locomotion, symbiotic associations with bacteria, and photosynthetic organelles. The proposed research program will also address a fourth group of eukaryotes that provides compelling insights into one of the most enigmatic evolutionary transformations in the history of life: the origin of obligate intracellular parasites from free-living, photoautotrophic ancestors. Apicomplexans are closely related to free-living dinoflagellates, and despite being infamous as pathogens of humans and livestock (e.g., Plasmodium), most of apicomplexan diversity is thriving in the world’s oceans. The origin and diversification of apicomplexans will be addressed by exploring the comparative ultrastructure and molecular phylogeny of marine gregarines, which are large and dynamic single-celled parasites that infect marine invertebrate hosts. Research on the diversity of single-celled eukaryotes is, in essence, exploratory and progresses in five phases: (1) discovery, isolation and cultivation of the organisms from nature (e.g., Bamfield Marine Sciences Centre and other regions of the Pacific Ocean); (2) identification and ultrastructural characterization of the organisms using light, fluorescence confocal and electron microscopy; (3) molecular characterization of the organisms; (4) computational analyses associated with image processing, next-generation sequencing and molecular phylogenetics; and (5) evolutionary synthesis using comparative methods. The proposed research program will accelerate the discovery of new lineages of eukaryotic cells from diverse environments, expand and refine the overall phylogenetic framework for understanding eukaryotic diversity, and identify unconventional ways in which these organisms have solved basic biological problems (e.g., cell locomotion, feeding, and photoreception).