Under pressure: How comb jellies have adapted to life on the ocean floor

The bottom of the ocean is not hospitable. There is no light; the temperature is freezing; and the pressure of all the water above will literally crush you. The animals that live at these depths have developed biophysical adaptations that allow them to survive in these harsh conditions. What are these adaptations and how have they developed?

Itay Budin, assistant professor of chemistry and biochemistry at the University of California San Diego, worked with researchers from across the country to study the cell membranes of ctenophores (“comb jellies”) and found that they had unique lipid structures that allowed them to shrink under intense pressure to live. Their work appears in Science.

Adapting to the environment

First of all, although comb jellies look like jellyfish, they are not closely related. Comb jellies belong to the phylum Ctenophora (pronounced tee-no-for-a). They are predators that can grow to the size of a volleyball and live in oceans all over the world and at various depths, from the surface to the deep sea.

Cell membranes have thin layers of lipids and proteins that must maintain certain properties for cells to function properly. While it has been known for decades that some organisms have adapted their lipids to maintain fluidity in extreme cold – called homeoviscous adaptation – it was not known how organisms living in the deep sea adapted to extreme pressure, or whether the pressure adaptation was the major change. The same as the cold adaptation.

Budin had studied the homeoviscous adaptation in E. coli bacteria, but when Steven Haddock, senior scientist at the Monterey Bay Aquarium Research Institute (MBARI), asked whether ctenophores had the same homeoviscous adaptation to compensate for extreme pressure, Budin was intrigued.

Complex organisms have different types of lipids. People have thousands of them: the heart has different ones from the lungs, which are different from those in the skin, and so on. They also have different shapes; some are cylindrical and some are shaped like cones.

To answer whether ctenophores adapted to cold and pressure through the same mechanism, the team needed to control for the temperature variable. Jacob Winnikoff, the study’s lead author who worked at both MBARI and UC San Diego, analyzed ctenophores collected from the Northern Hemisphere, including those living on the ocean floor in California (cold, high pressure) and those from the surface of the Arctic Ocean (cold, no high pressure).

“It turns out that comb jellies have evolved unique lipid structures to compensate for intense pressure. These structures are different from those that compensate for intense cold,” Budin said. “So much so that the pressure holds their cell membranes together.”

The researchers call this adaptation “homeocurvature” because the curvature-forming shape of the lipids has adapted to the comb jellyfish’s unique habitat. In the deep sea, the cone-shaped lipids have evolved into exaggerated cone shapes. The pressure of the ocean counteracts the exaggeration so that the lipid form is normal, but only at this extreme pressure. When deep sea comb jellyfish are brought to the surface, the exaggerated cone shape returns, the membranes split and the animals disintegrate.

The molecules with an exaggerated cone shape are a type of phospholipids called plasmalogens. Plasmalogens are abundant in the human brain and their declining abundance is often associated with declining brain function and even neurodegenerative diseases such as Alzheimer’s disease. This makes them very interesting for scientists and medical researchers.

“One of the reasons we chose to study ctenophores is because their lipid metabolism is similar to that of humans,” Budin said. “And while I wasn’t surprised to find plasmalogens, I was shocked to see that they make up as much as three-quarters of the lipid count of a deep-sea ctenophore.”

To further test this discovery, the team went back to E. coli and performed two experiments in high-pressure chambers: one with unmodified bacteria and a second with bacteria that had been bioengineered to synthesize plasmalogens. While the unmodified E. coli died, the E. coli strain with plasmalogens thrived.

These experiments were conducted over the course of several years and with collaborators from multiple institutions and disciplines. At UC San Diego, in addition to Budin, whose group conducted the biophysics and microbiology experiments, the lab of Distinguished Professor of Chemistry and Biochemistry Edward Dennis conducted lipid analysis using mass spectrometry. Marine biologists at MBARI collected comb jellies to study, while physicists at the University of Delaware performed computer simulations to validate membrane behavior at different pressures.

Budin, who is interested in studying how cells regulate lipid production, hopes this discovery will lead to further research into the role plasmalogens play in brain health and disease.

“I think the research shows that plasmalogens have really unique biophysical properties,” he said. “So now the question is, how are those properties important to the function of our own cells? I think that’s an important message.”