New Publication on Morphological Entanglement in Living Systems

We have a new paper in Physical Review X on Morphological Entanglement in Living Systems, first-authored by Dr. Thomas Day and in collaboration with friends in the Ratcliff Lab at Georgia Tech.

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 nonliving 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 nongrowing 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, depends sensitively on timescales, 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 nonliving counterparts, providing a widely accessible and powerful mechanism for the evolution of novel biological material properties.

Farewell to Dr. Thomas Day

The most recently graduated member of the Yunker Lab, Thomas studied how physics constrains the evolution of early multicellular organisms. He defended his thesis in February 2023. It was titled Biophysical Constraints of Multicellularity: Building a Darwinian Material.

“Speedy” Tom Day grew up in the small town of Haddam, Connecticut, and ran Cross Country and Track & Field at Lafayette College while pursuing his undergraduate degree. At Georgia Tech, he kindled a new love for long bike rides. Among other activities, he also enjoys playing and listening to live music; this has led to an emergence of an N+1 problem, regarding how many instruments he owns vs. how many he needs.

Tom left Georgia Tech to start a postdoc with Julia Schwartzman at USC. He was a core part of our lab’s social and scientific lives, and we will miss him greatly. We are excited to see what Tom will do in the future!

New article on the vertical growth of biofilms

We have a new paper on the vertical growth of biofilms.

The primary mode for microbial life on Earth is the biofilm, in which microbes attach to a surface and then reproduce, forming crowded, growing communities. As these colonies develop, they expand horizontally and vertically. While horizontal growth across the surface is well studied, much less is known about the vertical growth of biofilms. This knowledge gap persists despite the importance of vertical growth for determining access to nutrients and oxygen—as well as the fact that vertical growth dynamics represent a fundamental aspect of biofilm physiology.

The lack of clarity about vertical growth dynamics is due in part to the experimental difficulty in measuring the height of a biofilm with sufficient precision over many different time scales in a non-destructive manner. Common techniques for characterizing the height and topographies of colonies lack the requisite resolution (e.g., confocal microscopy), are too slow and potentially destructive (e.g., atomic force microscopy), or do not allow time lapse measurements (e.g., scanning electron microscopy). Thus, we lack an empirical picture of how vertical growth dynamics proceed over short and long time scales. We overcome these barriers using white-light interferometry, which enables us to continuously measure the topography of developing biofilms with nanometer resolution out-of-plane. With this technique, we measured the topographies of a diverse cohort of microbes, including: prokaryotes and eukaryotes, gram positive and gram negative bacteria, anaerobic and aerobic species, different cell sizes and shapes, and differences in extracellular matrix production. Thanks to their unprecedented high spatial and temporal resolution, these measurements enabled us to determine how, exactly, vertical growth proceeds.

New paper on maximum entropy cell packing

We have a new paper from grad student Tom Day, and in collaboration with Prof. Will Ratcliff (GT) and Prof. Ray Goldstein (Cambridge).

The success of multicellular organisms is due in part to their ability to assemble cells into complex, functional arrangements. However, self-assembly is subject to random noise that affects the final emergent structure. As the physiology of multicellular organisms can depend sensitively on structural details—in particular, the geometry of cellular packing—these fluctuations can directly impact fitness. Further, while extant multicellular organisms possess developmental mechanisms that can suppress or make use of random noise, nascent multicellular organisms do not possess such developmental programs, yet must generate repeatable multicellular structures to be successful. Understanding the origin and evolution of multicellularity thus requires understanding the impact of random noise on multicellular self-assembly.

Addressing this topic is particularly challenging as multicellularity has evolved independently over 25 times, and each separate lineage has evolved different rules for assembly. There are thus few, if any, general principles uniting multicellular organisms with different growth morphologies. For example, organisms that grow with persistent mother-daughter bonds (like plants or fungi) `freeze’ structural randomness in place; in contrast, organisms with ‘sticky’ cell-cell adhesion (like animals) can rearrange, so their final structure will be impacted by noise in reproduction and intercellular interactions. But this comparison only scratches the surface of the diversity of multicellular structures (e.g., from biofilms to trees to whales), which vary in dimensionality, topology, evolutionary history, and more. It thus would appear that random noise manifests uniquely in different kinds of multicellular organisms, without uniting rules.

In this paper, we show that random fluctuations in cell packing geometry follow a universal distribution, predictable from the maximum entropy principle. We experimentally observe this distribution in both snowflake yeast, a lab-created multicellular organism and the green alga Volvox carteri, which first evolved multicellularity in the Triassic. Maximum entropy cell packing statistics therefore unite organisms with and without canalized multicellular development, and organisms with markedly different growth morphologies. With these experimental observations and additional computational simulations, we show that maximum entropy packing is a fundamental property of multicellular groups, independent of growth morphology. 

Using snowflake yeast, we also show that maximum entropy cell packing plays a central role in the transition to multicellularity. The multicellular life cycle in this model system (growth of the group followed by fracture into multiple groups) arises directly from the maximum entropy distribution of free space within multicellular clusters. In fact, we show that the distribution of size across the population is completely predictable from maximum entropy considerations. Variation in the statistics of cellular packing therefore underlies the emergence of repeatable multicellular traits, such as group size at fracture, demonstrating how randomness can underlie the emergence of heritable multicellular traits prior to the evolution of multicellular development.

In a related vein, a theoretical analysis of V. carteri shows that the effects of fluctuations in intercellular space on the motility of green algae is small. These results show that the effects of random cell packing can be beneficial, detrimental, or neutral in character.

In summary, we show that the maximum entropy principle guides the organization of cellular space in organisms that are profoundly different: varying in their developmental regulation, and generating multicellular structures with different growth morphologies and dimensionalities. These fluctuations in multicellular packing appear as unavoidable as thermal fluctuations are to equilibrium phenomena, suggesting that maximum entropy packing statistics may represent a general principle, uniting all multicellular organisms.

Dead cell debris stops microbial warfare

We published a new paper (link) showing that the material properties of dead cells impacts microbial social interactions.

How do antagonistic bacteria coexist in crowded biofilms? Most contact killing studies focus on cellular and sub-cellular events over short time scales, showing that the abundance of ‘target’ cells (i.e., cells that are susceptible to attack) can rapidly decrease. These observations reinforce the idea that contact killing is a highly potent antagonistic strategy. Thus, for killer and target cells to coexist, the current assumption is that target cells must possess strain-specific, genetically controlled defense mechanisms. However, we found that physical consequences of cell death prevent further lethal attacks from occurring. Dead cell debris accumulates at the interfaces between killer and target cells, contact a physical barrier. The barrier separates killer and target cells, preventing contact and thus preventing contact killing. Our results indicate that while very effective at reducing the population of competing cells on first contact, contact killing can actually help antagonistic bacteria coexist.

New rules for the evolution of specialization

We have a new paper in eLife (link) in which we show that specialization may evolve more readily than previously thought.

The single most important benefit of multicellularity is the fact that organisms can evolve specialized cell types (i.e., being a brain or skin cell), but we know little about how specialization first evolved. It has long been assumed that specialization will evolve only if there is an accelerating, or convex, return on investment; for example, if twice the investment in a given task produces four times the yield. We have been studying the role of group structure in the evolution of specialization, using a minimal individual-based model. Surprisingly, we found that for a broad class of sparsely connected structures, specialization evolves even with saturating, or concave, returns on investment. Sparsely connected groups are able to connect many complementary specialists, which increases the benefit of specialization, without also connecting many like-specialists, which decreases the value of specialization. Our results remove a significant barrier to the evolution of specialization – the existence of accelerating returns on investment – and thus suggest that the evolution of specialization is even more favorable than previously thought

New paper on the cyberphysical risks of hacked cars

What do hacked connected cars have in common with biophysics and soft matter? Active and emergent phenomena! In a collaboration with Jesse Silverberg of Multiscale Systems, Inc., we find that the consequences of a large scale hack of connected cars could be dire – but are predicted through an extension of percolation theory! Paper here, and summary in Physics here.