Squids, octopuses and cuttlefish are undeniable masters of deception and camouflage. Its extraordinary ability to change color, texture and shape is unmatched even by modern technology.
Researchers at UC Santa Barbara professor Daniel Morse's lab have long been interested in the optical properties of color-changing animals that are particularly intrigued by the opalescent coastal squid. Also known as California market squid, these animals have evolved their ability to finely and continuously adjust their color and brightness to a level unmatched by other creatures. This allows them to communicate and hide in plain sight on the bright ocean.
In previous work, researchers have found that specialized proteins, called reflectins, control reflective pigment cells – iridocytes – which in turn contribute to altering the creature's visibility and overall appearance. But it was still a mystery how the reflections really worked.
"We now wanted to understand how this remarkable molecular machine works," said Morse, distinguished professor emeritus of the Department of Molecular, Cellular and Developmental Biology and lead author of an article appearing in Journal of Biological Chemistry. Understanding this mechanism, he said, would provide information on tunable control of emerging properties, which could open the door to the next generation of bioinspired synthetic materials.
Like most cephalopods, the opalescent squid on the coast practice their witchcraft through what may be the most sophisticated skin found anywhere in nature. Small muscles manipulate the texture of the skin, while iridescent pigments and cells affect its appearance. A group of cells controls your color by expanding and contracting cells in your skin that contain pigment sacs.
Behind these pigment cells is a layer of iridescent cells – those iridocytes – that reflect light and contribute to the color of animals throughout the visible spectrum. Squids also have leukophores, which control the reflectance of white light. Together, these layers of light-reflecting pigment-containing cells give squids the ability to control the brightness, color and tone of their skin in an extraordinarily wide palette.
Unlike the color of the pigments, the highly dynamic tones of the opalescent coastal squid result from altered iridocyte structure. Light bounces between nanometer-sized features the same size as wavelengths in the visible part of the spectrum, producing color. As these structures change their dimensions, colors change. Reflectin proteins are behind the ability of these shapes to change shape, and the researchers' task was to find out how they do the work.
Thanks to a combination of genetic engineering and biophysical analysis, scientists have found the answer, and it turned out to be a much more elegant and powerful mechanism than previously thought.
"The results were very surprising," said first author Robert Levenson, a postdoctoral researcher in Morse's lab. The group hoped to find one or two spots on the protein that controlled its activity, he said. "Instead, our evidence has shown that the capabilities of the reflectins that control their signal detection and resulting assembly are scattered throughout the protein chain."
An osmotic engine
Reflectin, which is contained in closely packed membrane layers in iridocytes, looks a bit like a string of beads on a string, the researchers found. Usually, the links between the beads are strongly positively charged, so they repel each other, straightening the proteins like raw spaghetti.
Morse and his team found that nerve signals to reflective cells trigger the addition of phosphate groups to links. These negatively charged phosphate groups neutralize link repulsion, allowing proteins to fold. The team was especially excited to find that this fold exposed sticky new surfaces on the beadlike parts of the reflectin, allowing them to group together. Up to four phosphates can bind to each reflectin protein, providing the squid with a precisely tunable process: The more phosphates are added, the more proteins fold, progressively exposing more emerging hydrophobic surfaces and larger clusters.
As these clusters grow, many small and single proteins in solution become fewer larger groups of multiple proteins. This alters fluid pressure within the membrane cells, expelling water – a type of "osmotic motor" that responds to the slightest changes in the charge generated by neurons, to which fragments of thousands of leukophores and iridocytes are connected. The resulting dehydration reduces the thickness and spacing of the membrane cells, which shift the wavelength of the reflected light progressively from red to yellow, then to green and finally blue. The more concentrated solution also has a higher refractive index, which increases the brightness of the cells.
"We had no idea that the mechanism we would discover was so extraordinarily complex, yet contained and so elegantly integrated into a multifunctional molecule – block copolymeric reflection – with opposing domains so delicately balanced that they act like a metastable machine, continually detecting and responding to neuronal signaling by precisely adjusting the osmotic pressure of an intracellular nanostructure to precisely adjust the color and brightness of the reflected light, "said Morse.
In addition, the researchers found, the entire process is reversible and cyclable, allowing the squid to continually adjust the optical properties required by its situation.
New design principles
Researchers have successfully manipulated the reflex in previous experiments, but this study marks the first demonstration of the underlying mechanism. Now it could provide new ideas for scientists and engineers who design materials with adjustable properties. "Our findings reveal a fundamental link between the properties of biomolecular materials produced in living systems and the highly engineered synthetic polymers that are now being developed at the frontiers of industry and technology," said Morse.
"As reflectin works to control osmotic pressure, I can visualize applications for new energy storage and conversion media, pharmaceutical and industrial applications involving viscosity and other liquid properties and medical applications," he added.
Notably, some of the processes at work in these reflected proteins are shared by the proteins that cluster pathologically in Alzheimer's disease and other degenerative conditions, Morse noted. He plans to investigate why this mechanism is reversible, cyclable, harmless, and useful for reflectin, but irreversible and pathological to other proteins. Perhaps well-structured differences in their sequences may explain the disparity and even point to new avenues for disease prevention and treatment.
Marine biologists clarify how specialized squid skin cells are able to control animal coloration
Robert Levenson et al. Calibration between trigger and color: neutralization of a genetically coded coulombic switch and dynamic stop precisely adjust the reflection set, Journal of Biological Chemistry (2019). DOI: 10.1074 / jbc.RA119.010339
A wonderful molecular machine (2019, November 15)
consulted November 15, 2019
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