Octopuses edit RNA to adapt to the cold: masters of adaptation

Woods Hole, Mass. — Each cell comes with a limited set of instructions encoded in its DNA. However, life is unpredictable and animals need flexibility to adapt when conditions change. New research led by Joshua Rosenthal of the Marine Biological Laboratory (MBL) and Eli Eisenberg at Tel Aviv University shows that octopuses and their close relatives adapt elegantly to environmental challenges by interfering with RNA, a messenger molecule that gives DNA direction.

In a new study appearing June 8 in the journal Cell, Rosenthal and his colleagues documented enormous increases in RNA processing when octopuses, squid and fish called coleoid cephalopods acclimated to cold water. After cooling the octopi’s tanks, the team saw increased protein-modifying activity at more than 13,000 RNA sites in the animals’ nervous systems. In two of these cases, they studied how changing one letter of the code of an RNA molecule changes the function of proteins produced by neurons.

By editing RNA, cephalopods seem to have found a unique way to change their physiology, says MBL senior scientist Rosenthal.

“We are used to thinking that all living things are pre-programmed from birth with a certain set of instructions,” he says. “The idea that the environment can influence genetic information, as we have shown in cephalopods, is a new concept.”

The mystery of massive RNA editing in cephalopods

The cell’s molecular machinery transcribes the instructions encoded in DNA into RNA, some of which make proteins. The researchers discovered that cells have the ability to replace one member of the four-letter genetic code — a molecule that replaces adenosine — with inosine, which acts like one of the original four, guanosine. Although the same process occurs in humans and most other animals, it rarely affects the RNA required for protein production.

In 2015, Rosenthal and colleagues showed that squid use protein-modifying RNA editing (called A-to-I) on a massive scale, and later did the same in octopuses.

“The big question for us is, ‘What are they using it for?'” says Rosenthal.

Because the processing only temporarily changes the RNA, the researchers suspected that these animals were using it to adapt to their environment. For the current study, they focused on the effects of one such factor, temperature, on the nervous system. Temperature is important because it controls the activity of enzymes, which in turn drive chemical reactions important to all physiological processes.

Like other cephalopods, the California two-spotted octopus (Octopus bimaculoides) they studied cannot generate its own body heat to combat the temperature drops that accompany tides, changes in water depth and the seasons.

After acclimating the octopuses to temperatures at the warm end (22 degrees C/72 degrees F) and the cold end (about 13 degrees C/55 degrees F) of their natural range, the researchers studied their RNA. Within its molecular code, they monitored activity at sites where they knew processing would occur. In octopuses in cold tanks, they found a significant increase in 13,285 sites where a single letter change changes the protein. For those in warm tanks, they found rises in 550 such locations.

Subsequent experiments suggested that RNA editing may help animals adapt to gradual changes, but not to the rapid changes associated with traveling from warm surface water to cooler depths, for example.

To confirm the laboratory work, Matthew Birk, now an assistant professor at the University of St. Francis in Pennsylvania, recorded the temperature near the octopus nests in winter and late summer, and then collected the animals.

With the help of colleagues from the University of Michigan and Texas Tech University, the team investigated how RNA editing changed the function of two proteins important for nerve function in octopuses. The primary protein kinesin-1 transports cargo along the long branches of neurons. By editing the RNA, they found that it changes the speed at which the molecule moves. Similarly, it changes the responsiveness of a protein called synaptotagmin, which provides communication between neurons.

Is there a secret to the complexity of cephalopods?

Cephalopods use this type of genetic engineering to adapt to change in many ways other than adapting to cold water, Rosenthal suspects. “I think this is the tip of the iceberg,” he says of the findings.

This may, in part, explain how these organisms achieve complex behaviors. For example, octopuses can solve mechanical puzzles and mimic colors and textures to camouflage themselves. Such abilities require nervous systems composed of a complex array of proteins.

“What mechanisms do they use to create this complexity?” “I think RNA editing is one of them,” says Rosenthal.

Written by Wynn Parry

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