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Biology subjects

Larson, B. T.

Publications and source records attributed to Larson, B. T..

5 recordsLinked to original sources

Regulated development of cannibalistic supergiant cells

Virtually all paradigms in developmental biology apply to differentiating cells and tissues within multicellular animals and plants. However, unicellular eukaryotes, which must simultaneously perform all roles necessary for organismal function, also form complex and specialized structures, using processes that take place exclusively within the confines of a single cell. Here, we describe a ciliate (Euplotes gigatrox sp. nov.) undergoing drastic morphological transformations within a genetically uniform population, the most spectacular being the appearance of "supergiants" that increase in size, change shape, and modify their locomotion and feeding behaviour to cannibalize clonal relatives. We explore supergiant formation from the perspective of life cycle, ecological strategy, and gene expression, demonstrating that supergiants are distinct, regulated, transcriptionally unique stages. These reversibly differentiated cells require both external and internal triggers to develop and have evolved regulatory loops to ensure coupling between environmental and physiological conditions. This system provides a blueprint for approaching both cell differentiation and functional ecology in unicellular organisms, which might open new avenues for the generalization and contextualization of known morphogenetic mechanisms, as well as the discovery of new ones.

cell biology↗

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Multicellularity evolved multiple times independently during eukaryotic diversification1-4. Two distinct mechanisms underpin multicellularity5: clonality (serial cell division without sister-cell separation) and aggregation (whereby independent cells assemble into a multicellular entity). Clonal and aggregative multicellularity are traditionally considered mutually exclusive1,6-9, with rare exceptions10, and evolutionary hypotheses have addressed why multicellularity might diverge toward one or the other extreme3,4. Both animals and their sister group, the choanoflagellates, are currently only known to acquire multicellularity clonally4,11-13. Here, we show that the choanoflagellate Choanoeca flexa14 forms motile and contractile cell monolayers (or "sheets") through multiple mechanisms: C. flexa sheets can form purely clonally, purely aggregatively, or by a combination of both processes. We characterise the life history of C. flexa in its natural environment - ephemeral splash pools on the island of Curacao - and show that C. flexa undergoes reversible transitions between unicellularity and multicellularity during cycles of evaporation and refilling. Different splash pools house genetically distinct strains of C. flexa, between which aggregation is constrained by kin recognition15-18. We show that clonal-aggregative multicellularity serves as a versatile strategy for the robust re-establishment of multicellularity in this variable and fast-fluctuating environment. Our findings challenge former generalisations about choanoflagellates and expand the option space of choanozoan multicellularity.

evolutionary biology↗

A unicellular walker embodies a finite state machine

Cells are complex biochemical systems whose behavior emerges from interactions among myriad molecular components. Computation is often invoked as a general framework for navigating this cellular complexity. However, it is unclear how cells might embody computational processes such that theories of computation, including finite state machine models, could be productively applied. Here, we demonstrate finite state machine-like processing embodied in cells using the walking behavior of Euplotes eurystomus, a ciliate that walks across surfaces using fourteen motile appendages (cirri). We found that cellular walking entails regulated transitions between a discrete set of gait states. The set of observed transitions decomposes into a small group of high-probability, temporally irreversible transitions and a large group of low-probability time-symmetric transitions, thus revealing stereotypy in sequential patterns of state transitions. Simulations and experiments suggest that the sequential logic of the gait is functionally important. Taken together, these findings implicate a finite state machine-like process. Cirri are connected by microtubule bundles (fibers), and we found that the dynamics of cirri involved in different state transitions are associated with the structure of the fiber system. Perturbative experiments revealed that the fibers mediate gait coordination, suggesting a mechanical basis of gait control.

cell biology↗

A hydraulic instability drives the cell death decision in the nematode germline

Oocytes are large and resourceful. During oogenesis some germ cells grow, typically at the expense of others that undergo apoptosis. How germ cells are selected to live or die out of a homogeneous population remains unclear. Here we show that this cell fate decision in C. elegans is mechanical and related to tissue hydraulics. Germ cells become inflated when the pressure inside them is lower than in the common cytoplasmic pool. This condition triggers a hydraulic instability which amplifies volume differences and causes some germ cells to grow and others to shrink. Shrinking germ cells are extruded and die, as we demonstrate by reducing germ cell volumes via thermoviscous pumping. Together, this reveals a robust mechanism of mechanochemical cell fate decision making in the germline.

developmental biology↗

Biophysical principles of choanoflagellate self-organization

Inspired by the patterns of multicellularity in choanoflagellates, the closest living relatives of animals, we quantify the biophysical processes underlying the morphogenesis of rosette colonies in the choanoflagellate Salpingoeca rosetta. We find that rosettes reproducibly transition from an early stage of 2D growth to a later stage of 3D growth, despite the underlying stochasticity of the cell lineages. We postulate that the extracellular matrix (ECM) exerts a physical constraint on the packing of proliferating cells, thereby sculpting rosette morphogenesis. Our perturbative experiments coupled with biophysical simulations demonstrates the fundamental importance of a basally-secreted ECM for rosette morphogenesis. In addition, this yields a morphospace for the shapes of these multicellular colonies, consistent with observations of a range of choanoflagellates. Overall, our biophysical perspective on rosette development complements previous genetic perspectives and thus helps illuminate the interplay between cell biology and physics in regulating morphogenesis.\n\nSignificance statementComparisons among animals and their closest living relatives, the choanoflagellates, have begun to shed light on the origin of animal multicellularity and development. Here we complement previous genetic perspectives on this process by focusing on the biophysical principles underlying colony morphology and morphogenesis. Our study reveals the crucial role of the extracellular matrix in shaping the colonies and leads to a phase diagram that delineates the range of morphologies as a function of the biophysical mechanisms at play.

biophysics↗