An invisible force begins life

Scientists study how frictional forces drive evolution in marine organisms.

When a potter works on a spinning wheel, the friction between their hands and the soft clay helps them shape it into all kinds of shapes and creations. In a fascinating parallel, marine oocytes (immature egg cells) exploit friction within different compartments within themselves to undergo developmental changes after conception. A study conducted by Heisenberg's group at the Institute of Science and Technology in Austria (ISTA), published in Nature physicsnow describes how this works.

Sea squirts attached to coral reefs. The marine organism is an excellent model for studying vertebrate developmental processes.

Diverse marine life: the world of sea squirts

The sea is full of wonderful life forms. From algae and colorful fish to sea snails and sea squirts, a completely different world reveals itself underwater. Sea squirts, or bowls in particular, are very unusual: after the freely moving larval stage, the larva settles and attaches to hard surfaces such as rocks or coral, developing tubes (siphons), which are their distinguishing feature. Although they look like rubber blobs as adults, they are the closest invertebrate relatives to humans. Especially in their larval stages, sea squirts are surprisingly similar to us.

Therefore, ascetes are often used as model organisms to study early embryonic development Vertebrates To which humans belong. “While ascidians exhibit basic developmental and morphological features of vertebrates, they also have the cellular and genomic simplicity typical of vertebrates.” Invertebrates“The ascidian larva in particular is an ideal model for understanding early vertebrate development,” explains Carl Philipp Heisenberg, a professor at the Institute of Science and Technology Austria (ISTA).

The researchers labeled the actin protein in the actomyosin cortex (left, green staining) and myoplasm (right, blue staining) to visualize their movement after the egg is fertilized. When the actomyosin shell in the lower region of the egg moves, it mechanically interacts with the myoplasm, causing it to buckle. The buckles eventually dissolve into the contraction pole. Credit: © Caballero-Mancebo et al./Nature Physics

His research group's most recent work, published in Nature physics, now provides new insights into its development. The results indicate that when ascetic eggs are fertilized, frictional forces play a crucial role in remodeling and reorganizing their interiors, heralding the next steps in their developmental cascade.

Deciphering egg metamorphosis

Ovules are female germ cells involved in reproduction. After successful fertilization by male sperm, animal eggs typically undergo cytoplasmic reorganization, changing their cellular contents and components. This process lays a blueprint for the fetus's later development. For example, in the case of ascetes, this modification leads to the formation of a bell-like protuberance – a small protuberance or nasal shape – known as the contraction pole (CP), where essential substances that facilitate fetal maturation accumulate. But the underlying mechanism driving this process is unknown.

Formation of a contraction pole. Microscopic time-lapse of cell shape changes in xenografted oocytes after fertilization: from unfertilized egg to contraction pole initiation to contraction pole formation to contraction pole reabsorption. Credit: ©Caballero-Mancebo et al./Nature Physics

A group of scientists from ISTA, Paris City University, CNRS, King's College London and the Sorbonne set out to unravel this mystery. For this endeavour, the Heisenberg Group imported adult ascidians from the Roscoff Marine Terminal in France. Almost all sea squirts are hermaphrodites, as they produce both male and female germ cells. “In the laboratory, we keep them in saltwater tanks in a Classify“A convenient way to obtain eggs and sperm to study their early embryonic development,” says Silvia Caballero Mancebo, first author of this study and a former doctoral student in Heisenberg's lab.

Formation of a contraction pole. Microscopic time-lapse of cell shape changes in ascetic oocytes after fertilization: from an unfertilized egg (first image from left) to contraction pole initiation (second and third images from left) and contraction pole formation (fourth image from left). Credit: © Caballero-Mancebo et al./Nature physics

The scientists analyzed the fertilized ascetic eggs microscopically and realized that they were following highly reproducible changes in cell shape that lead to the formation of the contractile pole. The researchers' first investigation focused on the actomyosin (cell) cortex, a dynamic structure found beneath the cell membrane in animal cells. It consists of actin filaments and motor proteins, and generally acts as a motor for shape changes in cells.

“We discovered that when cells are fertilized, increased tension in the actomyosin cortex causes them to contract, triggering their movement (flow), leading to the initial changes in cell shape,” Caballero-Mancebo continues. However, actomyosin flow ceased during contraction pole expansion, suggesting that there are additional players responsible for protrusion.

Silvia Caballero Mancebo. The ISTA graduate finds great pleasure in solving nature's mysteries and turning them into novels. Image credit: © Nadine Boncioni/ISTA

Frictional forces affect cell remodeling

The scientists took a closer look at other cellular components that may play a role in contraction pole expansion. In doing so, they encountered the myoplasm, a layer made up of organelles and intracellular molecules (related forms of which are found in many vertebrate and invertebrate eggs), centered in the lower region of the ascetic egg cell. “This specific layer behaves like a solid, stretchable material, it changes shape with the egg during fertilization,” explains Caballero-Mancebo.

Carl Philipp Heisenberg at the Institute of Science and Technology in Austria (ISTA). The research group of cell biologists at ISTA studies sea squirts and zebrafish and tries to understand how disorganized groups of cells transform into elaborate shapes as they develop. Image credit: © Nadine Boncioni/ISTA

During the flow of the actomyosin shell, the myoplasm folds and forms numerous buckles due to the frictional forces existing between the two components. As actomyosin movement stops, frictional forces also disappear. “This arrest eventually leads to expansion of the contraction pole as multiple myoplasmic buckles dissolve into a well-defined bell-shaped protrusion,” adds Caballero-Mancebo.

The study provides new insight into how mechanical forces determine cell and organism shape. It shows that frictional forces have a pivotal role in the formation and formation of a developing organism. However, scientists are only just beginning to understand the specific role of friction in embryonic development. “The myoplasm is also interesting, because it is involved in other embryonic processes in ascetes as well,” Heisenberg adds. “Exploring its unusual physical properties and understanding how it plays a role in the formation of sea squirts will be very interesting.”

Reference: “Frictional forces determine cytoplasmic reorganization and shape changes of oocytes upon fertilization” by Sylvia Caballero-Mancebo, Rushikesh Shinde, Madison Bolger-Munroe, Matilda Perozzo, Gregory Zipp, Irene Stikari, David LaBrosse-Arias, Vanessa Zaiden, Jack Mirren, Andrew Callan Jones, Rafael Voitoris and Carl Philipp Heisenberg, January 9, 2024, Nature physics.
doi: 10.1038/s41567-023-02302-1