Tiny crustacean could hold key to understanding embryogenesis

Parhyale hawaiensis, a tiny crustacean, has gained attention due to its remarkable attributes. Referred to as a “living Swiss army knife,” this species possesses numerous distinct appendages, each characterized by its size and shape, and each serving a specific function. These fascinating creatures, coupled with their easily observable growth conditions, make them an ideal model organism for developmental studies.

Researchers Dillon Cislo, Mark Bowick, and Sebastian Streichan from UC Santa Barbara have highlighted the significance of Parhyale hawaiensis embryos in understanding tissue morphogenesis. Tissue morphogenesis aims to elucidate the process by which a mass of embryonic cells transforms into the intricate body parts of an adult organism. Unlike organisms that undergo metamorphosis, Parhyale hawaiensis is a “direct developer,” constructing its adult form in a miniature version.

Transitioning from randomly arranged cells to the intricately articulated appendages of the adult structure is a remarkable phenomenon. Cislo, a postdoctoral researcher at Rockefeller University, conducted this research during his time as a graduate student at UCSB. He collaborated with theoretical physicists Bowick, Boris Schraiman, and Streichan, who specializes in the physics of living matter.

Traditionally, studying embryogenesis involved fixing multiple embryos of a model organism, such as fruit flies, at different developmental stages to analyze the sequence of events leading to body development. However, understanding how young cells establish their positions and arrangements has been a challenging aspect to observe.

This area of investigation lies at the intersection of biology and active matter physics. The collective behavior of systems comprising multiple independent “agents” that locally consume energy falls under the domain of active matter physics. Active matter encompasses various examples, including starling murmurations, bacterial colonies, crowds, and even non-biological scenarios like swarms of robots.

Understanding how Parhyale hawaiensis and its cells work together during embryonic development is a topic of great interest in biology and active matter physics. The unique attributes of this tiny crustacean provide valuable insights into the complex processes underlying tissue morphogenesis.

Order from disorder

During the embryonic development of Parhyale hawaiensis, the cells face the challenge of organizing themselves despite the lack of a strict relationship between the division axes of parent and daughter cells. This complexity arises because tissues rely on the organization and orientation of their constituent cells for their structures and functions.

To investigate how P. hawaiensis cells overcome this potential disorder during proliferation, the researchers monitored the development of an embryo three days after fertilization. Initially, the embryo appeared as a thin layer of cells on top of a spherical yolk. To facilitate observation, the researchers computationally flattened the curved cell arrangement while preserving its three-dimensional geometry. This enabled them to track the cells’ division and movement in the first dynamic analysis of this stage of P. hawaiensis’ early development.

After twelve hours, the population of cells had more than doubled and organized themselves into a grid, with each row corresponding to a segment of the adult body. Subsequently, waves of cell division occurred within the monolayer of cells, starting from the midline and propagating laterally along the head-to-tail axis of the future organism.

The cell divisions were not random. Instead of simply increasing in number without order, the cells would divide, and some daughter cells would reorient themselves by up to 90 degrees before undergoing further division to maintain alignment with the head-to-tail axis.

As the cells followed this division choreography, new rows of cells were inserted between existing rows, pushing the adjacent rows apart. This process is energetically demanding and would typically require extremely high temperatures in non-living physical systems such as metals and crystals. However, Parhyale hawaiensis accomplishes this reorganization at room temperature. The researchers speculate that there may be a biological signal guiding the general axis of cell division, although it remains undiscovered.

Despite the fragility and energy requirements involved, the fourfold orientation observed during the early stages of the crustacean’s development is crucial. Proper body function relies on the coordinated orientation of the animal’s limbs. Just like our hands or legs, the limbs of Parhyale hawaiensis have specific orientations. Any misalignment or rotation of these limbs would significantly impede normal daily activities.

Shaking things up

A crucial aspect to consider is that the organization observed in Parhyale hawaiensis exists in a unique state that lies between a fluid and a solid. According to Bowick, from a physics perspective, this phase resembles that of a superfluid.

Despite the gridlike organization and order generated by the cells, the potential for disorder resulting from the fluidic state and cell divisions is essential for the necessary flexibility in a biological system. As the cells divide, they exert forces on each other, contributing to fluctuations and variations in the system.

The researchers discovered that the cells, equipped with their individual motors and internal “clocks” for autonomous division, introduce a certain amount of “noise” or fluctuations during the early cell proliferation stage and subsequent tissue elongation stage.

Although this noise may initially seem counterproductive to the formation of a complex organism with multiple appendages, the researchers argue that it is actually crucial for a robust developmental process. The fourfold orientation of the system allows it to occupy a “Goldilocks zone” between order and disorder, enabling it to accommodate minor discrepancies in the process while still building the desired structure.

Through simulations, the researchers demonstrated that despite variations in timing, division concentration, or the presence of cells that didn’t reorient themselves, the system could still reach the same end result.

The study reveals that biology does not require tight control to achieve the desired outcome, a finding made possible through dynamic analysis. The shaking up of the system caused by cell divisions allows it to settle into a subtle ordered state, illustrating the importance of controlled disorder in biological development.

This research provides a rare glimpse into a lesser-explored aspect of developmental biology, one that operates based on geometric organizational principles and the unique fourfold orientation observed in Parhyale hawaiensis.

Unlike other animals where embryonic cells rely on chemical signals for orientation, in P. hawaiensis, the grid patterning is a mechanical event that spans two regions. This allows both regions, one close to the head and one farther away, to agree on the positions of their cells. The grid also determines the locations and orientations of the cells that will develop into limbs even before their formation.

According to Streichan, this work highlights how biology leverages physics for its purposes. The findings also hold potential implications for materials science, suggesting that driving material systems out of equilibrium, inspired by biological mechanisms, could lead to the creation of remarkable structures.

Source: University of California – Santa Barbara

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