Ultrastructural Complexity in Unconventional Cells

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Single-celled organisms have dominated the planet for over 3 billion years, yet their traits are the least understood of all extant organisms. Of the three major lineages of microbial life, single-celled eukaryotes are the most complex. Unlike bacteria and archaea, eukaryotic cells have nuclei, endomembrane systems, endosymbiotically acquired organelles and elaborate cytoskeletons supporting a vast array of specialized cell extensions and behaviors. Our research program is designed to explore unconventional eukaryotes in order to help unravel the composition, interrelationships and innovative cellular traits in lineages that span the tree of life. The research aims to accelerate the discovery of novel single-celled eukaryotes and reconstruct complex ultrastructural systems using comparative molecular methods and high-resolution microscopy. A central goal in biology is to understand the function of complex structures and how they arose from simpler precursors. This is especially challenging in the field of comparative cell biology because these studies require sophisticated technologies, spatial reasoning at a fine scale and detailed terminology associated with unfamiliar organisms. Morphological complexity is normally associated with multicellularity, as seen in the camera-type eyes found in several groups of animals. However, some single-celled eukaryotes have also acquired extremely complex traits by arranging standard subcellular components in extraordinary ways. Dinoflagellates, for instance, represent a major lineage of eukaryotes with an unusually high level of cellular diversity. Our lab has shown that some dinoflagellates have an eye-like "ocelloid" consisting of subcellular analogues to a cornea, lens, iris and retina. These same species also have intricate harpoon-like "nematocysts", some of which use a single pressurized capsule for propulsion, while others uniquely launch 11 to 15 projectiles from an arrangement similar to a Gatling gun. Comparative studies of traits like these offer idiosyncratic systems for tracing novel cases of convergence and the intermediate stages that gave rise to highly integrated structures. Research on the unity and diversity of complex ultrastuctural traits is exploratory and progresses in four principal phases: (1) collection of uncultivated organisms from diverse environments; (2) single-cell preparation and characterization using high-resolution microscopy (CLSM, FIB-SEM, TEM); (3) single-cell isolation for transcriptomics and genomics; (4) computational analyses associated with digital image processing and bioinformatics. Outcomes of this research accelerate the discovery of new traits in eukaryotic cells from diverse environments and identify novel ways in which single-celled organisms have solved basic problems, such as locomotion, feeding, defense and photoreception.