Sea anemones begin life as slightly egg-shaped, free-swimming larvae and metamorphose into elongated, tube-shaped adults that cling to rock and have tentacles around their mouths. This involves drastic behavioral and life-form changes, as well as extensive tissue changes. Although embryonic development has received much research attention in the past and the behavior of early embryos has been studied, it is not clear to what extent an embryo’s physical activity influences its own body shape change.
Historically, scientists seeking to map the links between dynamic behavior and the body changes occurring during metamorphosis have been hampered by the lack of live imaging strategies that capture the dynamics of this life-history transition. Researchers from the European Molecular Biology Laboratory (EMBL) have now overcome this obstacle by applying their expertise in live imaging, computational methodology, biophysics and genetics. You managed to turn Live 2D and 3D imaging into quantitative traits to follow the changes in the bodies of developing starlet sea anemones (Nematostella). The results were published in the journal Current Biology.
The experts established a method of high-throughput live imaging using a specially adapted microscope and observed the changes that occur during the transition from larvae to polyps in 707 anemones. This happened over about seven days, and the researchers recorded the changes at 5-minute intervals. They found that the circularity of the larvae decreased dramatically during the transition, mainly due to a 3- to 4-fold increase in the length of the polyp body as it became more tubular and developed oral tentacles.
During this time, the sea anemones behaved like hydraulic pumps, taking in water and regulating body pressure through muscle activity. Researchers performed specific patterns of gymnastic movements that applied pressure to specific tissues, thereby sculpting the body’s shape as it lengthened. Too much or too little muscle activity, or a drastic change in the organization of their muscles, could cause the sea anemone to deviate from its normal shape.
“Humans use a skeleton of muscles and bones to move. In contrast, sea anemones use a hydroskeleton made up of muscles and a water-filled cavity,” said Aissam Ikmi, EMBL group leader. The same hydraulic muscles that help developing sea anemones move also appear to influence their development. Using an image analysis pipeline to measure body column length, diameter, estimated volume and mobility in large datasets, the scientists found this Nematostella Larvae naturally divide into two groups: slow-developing and fast-developing larvae. To the team’s surprise, the more active the larvae are, the longer it takes for them to develop.
“Our work shows how developing sea anemones essentially ‘train’ to build their morphology, but it appears that they cannot use their hydroskeleton to move and develop simultaneously,” Ikmi said.
The developing anemones use this hydraulic system to remodel their tissues during this time. Through the use of peristaltic waves, squeezing, and longitudinal contractions, they stimulate tissue proliferation at some sites and cell death at others, thereby altering the organization of their body tissues.
“There were many challenges with this research,” explained first author and former EMBL predoctoral fellow Anniek Stokkermans, now a postdoc at the Hubrecht Institute in the Netherlands. “This animal is very active. Most microscopes can’t record fast enough to keep up with the animal’s movements, resulting in blurry images, especially if you want to view it in 3D. Also, the animal is quite dense, so most microscopes can’t even see halfway through the animal.”
To see both deeper and faster, Ling Wang, an applications engineer in the Prevedel group at EMBL, built a microscope to capture live, developing sea anemone larvae in 3D during their natural behavior.
“For this project, Ling specially adapted one of our core technologies, Optical Coherence Microscopy, or OCM. The main advantage of OCM is that the animals can move freely under the microscope and still provide a clear, detailed view inside and in 3D,” said Robert Prevedel, group leader at EMBL. “It was an exciting project that shows the many different interfaces between EMBL groups and disciplines.”
Using this specialized tool, researchers were able to quantify volumetric changes in tissue and body cavity. “To grow larger, sea anemones inflate themselves like a balloon by absorbing water from the environment,” explains Stokkermans. “Then, by contracting different types of muscles, they can regulate their short-term shape, much like squeezing an inflated balloon on one side and watching it expand on the other. We believe that this pressure-driven local expansion helps to stretch the tissue, slowly increasing the length of the animal. In this way, labor can have both short-term and long-term effects.”
In order to better understand the hydraulics and their function, the researchers worked together with experts from various disciplines. Prachiti Moghe, an EMBL predoctoral researcher in the Hiiragi group, measured changes in pressure that drive body deformations. In addition, Harvard University mathematician L. Mahadevan and engineer Aditi Chakrabarti presented a mathematical model to quantify the role of hydraulic pressure in controlling shape changes at the system level. They also constructed reinforced balloons with ribbons and ribbons that mimic the different shapes and sizes found in both normal and muscle-damaged animals.
“Given the ubiquity of hydrostatic skeletons in the animal kingdom, particularly in marine invertebrates, our study suggests that active muscle hydraulics play a broad role in the design principle of soft-bodied animals,” Ikmi said. “In many engineered systems, hydraulics is defined by the ability to harness pressure and flow into mechanical work, with far-reaching ramifications in spacetime. As animal multicellularity evolved in an aquatic environment, we propose that early animals likely exploited the same physics, with hydraulics influencing both developmental and behavioral decisions.”
“We still have a lot of questions about these new findings,” Stokkermans said. “Why are there different activity levels? How exactly do cells sense pressure and translate it into a developmental outcome? In addition, since tube-like structures form the basis of many of our organs, the mechanisms underlying them need to be studied Nematostella will also help gain a better understanding of how hydraulics play a role in organ development and function.”
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Through Alison Bosman, Earth.com Staff writer
