Biology subjects

Day, T. C.

Publications and source records attributed to Day, T. C..

7 recordsLinked to original sources

bioRxiv2025

Multicellular group formation as a resource competition strategy for marine bacteria

Multicellularity can enhance bacterial resilience and robustness in nature. Traits like access to otherwise inaccessible substrates, increased stress tolerance and predation resistance provide ecological advantages that may scaffold the evolution of multicellular complexity. While multicellularity arises in many ecological contexts, we lack general principles to predict which environments favor these traits. Here, we ask how the physical size of multicellular groups affects their ability to compete for resources, focusing on marine bacteria that degrade organic matter. These bacteria compete for resources ranging from nanoscale dissolved organic matter to millimeter-scale particles. Using a theory of size-dependent fluid encounters, we identify a regime where resource encounters depend on group size. Experiments with the group-forming marine bacteria Vibrio splendidus 12B01 support the prediction that larger groups encounter resources more frequently. However, analysis of per-capita resource allocation reveals a trade-off: group size is inversely related to both the mean and variance of per-capita encounters. Cells in groups obtain fewer resources per cell than single cells, but experience more consistent encounters, sheltering them from large fluctuations in resource acquisition. Stochastic simulations support this tradeoff and predict a broad range of conditions in which consistency enables multicellular groups to out-compete or coexist with single cells. Our findings suggest that group formation is a potentially widespread but overlooked strategy for resource competition in marine heterotrophic bacteria, shaped by biophysical constraints on resource encounters. Significance StatementMulticellular groups are thought to arise in ecological settings where group-level traits confer a fitness advantage. However, linking these evolutionary drivers to specific ecological mechanisms remains a major challenge in understanding the origins of multicellular life. In this study, we draw inspiration from the microscale ecology of marine bacteria that play a key role in the oceans carbon cycle. These bacteria often rely on high local population densities to secrete enough extracellular enzymes to degrade organic matter and access nutrients. By combining experimental measurements with a mathematical theory of encounters and stochastic simulations of competition dynamics, we show that multicellular bacterial groups often out-compete single cells. Our results suggest that the advantage of multicellular groups stems from a tradeoff between the consistency and quantity of resource encounters, arising from purely physical processes. The physics of encounters offers a generic framework that can be leveraged to understand ecological scaffolds of multicellularity.

microbiology↗

bioRxiv2025

Emergence of coordinated cell division during the evolution of multicellularity

Upon making the transition from unicellularity to multicellularity, many previously optimized cellular traits experience the renewed scrutiny of natural selection due to their novel effects on emergent multicellular phenotypes. Yet we lack a comprehensive understanding of how and why specific cellular traits influence multicellular phenotypes and fitness. The snowflake yeast model system provides a tractable entry point for such investigations. The effects of several cell-level traits (cellular aspect ratio, cell volume, bud neck strength) on multicellular cluster size have been characterized, but we found that these properties were insufficient to explain the difference in cluster size between the two strains that serve as the ancestors of the ongoing Multicellularity Long-Term Evolution Experiment (MuLTEE). Using time-lapse microscopy and single cell tracking, we identified the timing of cell division as a cellular trait that strongly influences multicellular morphology and size in snowflake yeast. The "petite" ancestor divides asynchronously, with a 25% longer first division, while the "grande" ancestor divided synchronously. Using network theoretical and biophysical models, we showed that strains exhibiting a first division delay generate more highly-branched network topologies, accelerating the accumulation of crowding-induced mechanical stress, resulting in clusters that fracture at smaller sizes. Conversely, synchronously dividing strains produce more symmetric, larger clusters. Synchronous cell division can provide benefits through both faster growth and larger size, suggesting multiple potential selective pathways for its evolution. Furthermore, we explore how accelerated first division can produce even larger groups and how another unexpected mechanism for modifying cluster size, apoptosis rate, may interfere with these effects. Our results identify cell division timing as a previously underappreciated axis of phenotypic variation that strongly influences multicellular morphology. This suggests that temporal regulation of cell division represents an evolutionarily accessible mechanism for early control of morphogenesis in nascent multicellular organisms with permanent intercellular bonds.

evolutionary biology↗

bioRxiv2024

Whole-genome duplication in the Multicellularity Long Term Evolution Experiment

Whole-genome duplication (WGD) is widespread across eukaryotes and can promote adaptive evolution1-4. However, given the instability of newly-formed polyploid genomes5-7, understanding how WGDs arise in a population, persist, and underpin adaptations remains a challenge. Using our ongoing Multicellularity Long Term Evolution Experiment (MuLTEE)8, we show that diploid snowflake yeast (Saccharomyces cerevisiae) under selection for larger multicellular size rapidly undergo spontaneous WGD. From its origin within the first 50 days of the experiment, tetraploids persist for the next 950 days (nearly 5,000 generations, the current leading edge of our experiment) in ten replicate populations, despite being genomically unstable. Using synthetic reconstruction, biophysical modeling, and counter-selection experiments, we found that tetraploidy evolved because it confers immediate fitness benefits in this environment, by producing larger, longer cells that yield larger clusters. The same selective benefit also maintained tetraploidy over long evolutionary timescales, inhibiting the reversion to diploidy that is typically seen in laboratory evolution experiments. Once established, tetraploidy facilitated novel genetic routes for adaptation, playing a key role in the evolution of macroscopic multicellular size via the origin of evolutionarily conserved aneuploidy. These results provide unique empirical insights into the evolutionary dynamics and impacts of WGD, showing how it can initially arise due to its immediate adaptive benefits, be maintained by selection, and fuel long-term innovations by creating additional dimensions of heritable genetic variation.

evolutionary biology↗

bioRxiv2023

The biophysical basis of bacterial colony growth

Bacteria often attach to surfaces and grow densely-packed communities called biofilms. As biofilms grow, they expand across the surface, increasing their surface area and access to nutrients. Thus, the overall growth rate of a biofilm is directly dependent on its "range expansion" rate. One factor that limits the range expansion rate is vertical growth; at the biofilm edge there is a direct trade-off between horizontal and vertical growth--the more a biofilm grows up, the less it can grow out. Thus, the balance of horizontal and vertical growth impacts the range expansion rate and, crucially, the overall biofilm growth rate. However, the biophysical connection between horizontal and vertical growth remains poorly understood, due in large part to difficulty in resolving biofilm shape with sufficient spatial and temporal resolution from small length scales to macroscopic sizes. Here, we experimentally show that the horizontal expansion rate of bacterial colonies is controlled by the contact angle at the biofilm edge. Using white light interferometry, we measure the three-dimensional surface morphology of growing colonies, and find that small colonies are surprisingly well-described as spherical caps. At later times, nutrient diffusion and uptake prevent the tall colony center from growing exponentially. However, the colony edge always has a region short enough to grow exponentially; the size and shape of this region, characterized by its contact angle, along with cellular doubling time, determines the range expansion rate. We found that the geometry of the exponentially growing biofilm edge is well-described as a spherical-cap-napkin-ring, i.e., a spherical cap with a cylindrical hole in its center (where the biofilm is too tall to grow exponentially). We derive an exact expression for the spherical-cap-napkin-ring-based range expansion rate; further, to first order, the expansion rate only depends on the colony contact angle, the thickness of the exponentially growing region, and the cellular doubling time. We experimentally validate both of these expressions. In line with our theoretical predictions, we find that biofilms with long cellular doubling times and small contact angles do in fact grow faster than biofilms with short cellular doubling times and large contact angles. Accordingly, sensitivity analysis shows that biofilm growth rates are more sensitive to their contact angles than to their cellular growth rates. Thus, to understand the fitness of a growing biofilm, one must account for its shape, not just its cellular doubling time.

biophysics↗

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↗

bioRxiv2021

De novo evolution of macroscopic multicellularity

While early multicellular lineages necessarily started out as relatively simple groups of cells, little is known about how they became Darwinian entities capable of open-ended multicellular adaptation1,2. To explore this, we initiated the Multicellularity Long Term Evolution Experiment (MuLTEE), selecting for larger group size in the snowflake yeast (Saccharomyces cerevisiae) model system. Given the historical importance of oxygen limitation3, our ongoing experiment consists of three metabolic treatments4: anaerobic, obligately aerobic, and mixotrophic yeast. After 600 rounds of selection, snowflake yeast in the anaerobic treatment evolved to be macroscopic, becoming ~2{middle dot}104 times larger (~mm scale) and ~104-fold more biophysically tough, while retaining a clonal multicellular life cycle. They accomplished this through sustained biophysical adaptation, evolving increasingly elongate cells that initially reduced the strain of cellular packing, then facilitated branch entanglements that enabled groups of cells to stay together even after many cellular bonds fracture. In contrast, snowflake yeast competing for low oxygen remained microscopic, evolving to be just ~6-fold larger, underscoring the critical role of oxygen levels in the evolution of multicellular size. Taken together, this work provides unique insight into an ongoing evolutionary transition in individuality, showing how simple groups of cells overcome fundamental biophysical limitations via gradual, yet sustained, multicellular adaptation.

evolutionary biology↗

bioRxiv2021

Cellular organization in lab-evolved and extant multicellular species obeys a maximum entropy law

The prevalence of multicellular organisms is due in part to their ability to form complex structures. How cells pack in these structures is a fundamental biophysical issue, underlying their functional properties. However, much remains unknown about how cell packing geometries arise, and how they are affected by random noise during growth - especially absent developmental programs. Here, we quantify the statistics of cellular neighborhoods of two different multicellular eukaryotes: lab-evolved "snowflake" yeast and the green alga Volvox carteri. We find that despite large differences in cellular organization, the free space associated with individual cells in both organisms closely fits a modified gamma distribution, consistent with maximum entropy predictions originally developed for granular materials. This entropic cellular packing ensures a degree of predictability despite noise, facilitating parent-offspring fidelity even in the absence of developmental regulation. Together with simulations of diverse growth morphologies, these results suggest that gamma-distributed cell neighborhood sizes are a general feature of multicellularity, arising from conserved statistics of cellular packing.

biophysics↗