Biology subjects

Burnetti, A. J.

Publications and source records attributed to Burnetti, A. J..

4 recordsLinked to original sources

bioRxiv2023

Examining the role of oxygen-binding proteins on the early evolution of multicellularity

Oxygen availability is a key factor in the evolution of multicellularity, as larger and more sophisticated organisms often require mechanisms allowing efficient oxygen delivery to their tissues. One such mechanism is the presence of oxygen-binding proteins, such as globins and hemerythrins, which arose in the ancestor of bilaterian animals. Despite their importance, the precise mechanisms by which oxygen-binding proteins influenced the early stages of multicellular evolution under varying environmental oxygen levels are not yet clear. We addressed this knowledge gap by heterologously expressing the oxygen binding proteins myoglobin and myohemerythrin in snowflake yeast, a model system of simple, undifferentiated multicellularity. These proteins increased the depth and rate of oxygen diffusion, increasing the fitness of snowflake yeast growing aerobically. Experiments show that, paradoxically, oxygen-binding proteins confer a greater fitness benefit for larger organisms under high, not low, O2 conditions. We show via biophysical modeling that this is because facilitated diffusion is more efficient when oxygen is abundant, transporting a greater quantity of O2 which can be used for metabolism. By alleviating anatomical diffusion limitations to oxygen consumption, the evolution of O2-binding proteins in the oxygen-rich Neoproterozoic may have been a key breakthrough enabling the evolution of increasingly large, complex multicellular metazoan lineages.

evolutionary biology↗

bioRxiv2023

Entanglement in living systems

Many organisms exhibit branching morphologies that twist around each other and become entangled. Entanglement occurs when different objects interlock with each other, creating complex and often irreversible configurations. This physical phenomenon is well-studied in non-living materials, such as granular matter, polymers, and wires, where it has been shown that entanglement is highly sensitive to the geometry of the component parts. However, entanglement is not yet well understood in living systems, despite its presence in many organisms. In fact, recent work has shown that entanglement can evolve rapidly, and play a crucial role in the evolution of tough, macroscopic multicellular groups. Here, through a combination of experiments, simulations, and numerical analyses, we show that growth generically facilitates entanglement for a broad range of geometries. We find that experimentally grown entangled branches can be difficult or even impossible to disassemble through translation and rotation of rigid components, suggesting that there are many configurations of branches that growth can access that agitation cannot. We use simulations to show that branching trees readily grow into entangled configurations. In contrast to non-growing entangled materials, these trees entangle for a broad range of branch geometries. We thus propose that entanglement via growth is largely insensitive to the geometry of branched-trees, but instead will depend sensitively on time scales, ultimately achieving an entangled state once sufficient growth has occurred. We test this hypothesis in experiments with snowflake yeast, a model system of undifferentiated, branched multicellularity, showing that lengthening the time of growth leads to entanglement, and that entanglement via growth can occur for a wide range of geometries. Taken together, our work demonstrates that entanglement is more readily achieved in living systems than in their non-living counterparts, providing a widely-accessible and powerful mechanism for the evolution of novel biological material properties.

biophysics↗

bioRxiv2023

Proteostatic tuning underpins the evolution of novel multicellular traits

The evolution of multicellularity paved the way for the origin of complex life on Earth, but little is known about the mechanistic basis of early multicellular evolution. Here, we examine the molecular basis of multicellular adaptation in the Multicellularity Long Term Evolution Experiment (MuLTEE). We demonstrate that cellular elongation, a key adaptation underpinning increased biophysical toughness and organismal size, is convergently driven by downregulation of the chaperone Hsp90. Mechanistically, Hsp90-mediated morphogenesis operates by destabilizing the cyclin-dependent kinase Cdc28, resulting in delayed mitosis and prolonged polarized growth. Reinstatement of Hsp90 or Cdc28 expression resulted in shortened cells that formed smaller groups with reduced multicellular fitness. Together, our results show how ancient protein folding systems can be tuned to drive rapid evolution at a new level of biological individuality by revealing novel developmental phenotypes. TeaserDownregulation of Hsp90 decouples cell cycle progression and growth to drive the evolution of macroscopic multicellularity.

evolutionary biology↗

bioRxiv2022

Using light for energy: examining the evolution of phototrophic metabolism via synthetic construction

The origin of phototrophy was pivotal in increasing the size and scale of the biosphere, as it allowed organisms to utilize light-driven energy transport to drive biological processes. Retinalophototrophy, one of two independently evolved phototrophic pathways, consists of a simple system of microbial rhodopsins which have spread broadly through the tree of life via horizontal gene transfer. Here, we sought to determine whether Saccharomyces cerevisiae, a heterotrophic fungus with no known evolutionary history of phototrophy, can function as a facultative artificial phototroph after acquiring a single rhodopsin gene. We transformed S. cerevisiae into a facultative phototroph by inserting a rhodopsin protein from Ustilago maydis into the yeast vacuole, allowing light to pump protons into the vacuolar compartment, a function typically driven by consuming ATP. We show that yeast with rhodopsins gain a selective advantage when grown under green light, growing more rapidly than their non-phototrophic ancestor or rhodopsin-bearing yeast cultured in the dark. These results underscore the remarkable ease with which rhodopsins may be horizontally transferred even in eukaryotes, providing novel biological function without first requiring evolutionary optimization.

cell biology↗