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06-08-2023

Octopuses adapt to seasonal temperatures by rewiring their brains

In the grand tapestry of life, the octopus, with its eight twisting arms and sharp intellect, stands out as one of the most fascinating creatures of the deep. But beneath its pulsating colors and inscrutable gaze lies a unique biological strategy for adapting to its ever-changing environment.

Unlike many organisms, octopuses don’t thermoregulate. This means their well-developed brains are exposed to and potentially threatened by fluctuations in temperature. Yet, these adaptable cephalopods have evolved an intriguing way to shield their neural networks from seasonal temperature shifts: RNA editing.

The role of RNA in this incredible feat

RNA, the messenger molecule bridging DNA and proteins, is subject to an exceptional degree of editing in the two-spot octopus, according to a new study published in the journal Cell. This rewiring of genetic information, the researchers believe, could be a widespread strategy among octopuses and squid to defend their brains from environmental hazards.

“We generally think that our genetic information is fixed, but the environment can influence how you encode proteins, and in cephalopods this happens on a massive scale,” says senior author Joshua Rosenthal of the Marine Biological Laboratory of Woods Hole, Massachusetts.

In comparison to DNA mutations that drive evolution over generations, RNA editing offers a nimble, temporary way for individual organisms to adjust to their surroundings. It’s a process known to occur across all life forms, but RNA recoding – a subtype of editing that alters the resulting protein structure – is far more prevalent among the soft-bodied cephalopods like octopuses and squid.

“RNA recoding gives organisms the option to express a diverse quiver of proteins when and where they choose,” Rosenthal explains. “In cephalopods, most of the recoding is for proteins that are really important for nervous system function, so the natural question is, are they using this to acclimate to changes in their physical environment?”

How the study was conducted

Keen to unravel this mystery, the research team embarked on an exploration of whether octopuses utilize RNA editing to counter temperature shifts, and if so, whether this editing affects their brain proteins.

California two-spot octopuses, small, yellowish-brown species with two luminous blue eyespots beneath their real eyes, were the subjects of their inquiry. Native to the coastlines of California and Mexico, these octopuses, with their already sequenced genomes, presented a unique opportunity for the researchers to study RNA editing in relation to temperature variation.

The scientists acclimated wild-caught adult octopuses to either warm (22ºC) or cold (13ºC) waters in tanks at the Marine Biological Laboratory. After several weeks, they scrutinized the RNA transcripts from both sets of octopuses, searching for signs of RNA editing among more than 60,000 previously identified editing sites.

What the research team discovered

“Temperature-sensitive editing occurred at about one third of our sites – over 20,000 individual places – so this is not something that happens here or there; this is a global phenomenon,” says co-senior author Eli Eisenberg of Tel-Aviv University, who managed the computational aspects of the study. “But that being said, it does not happen equally: proteins that are edited tend to be neural proteins, and almost all sites that are temperature sensitive are more highly edited in the cold.”

Delving further into their findings, the team noted that certain types of neural proteins, particularly those linked with cell membranes and calcium-binding proteins, were more likely to be sensitive to temperature.

The researchers then turned their attention to the speed at which these changes occur. By adjusting the temperature in tanks housing juvenile octopuses – from 14°C to 24°C and vice versa at hourly 0.5°C increments – they measured the extent of RNA editing at several time points. They found the process happens astonishingly quickly.

“We had no real idea how quickly this can occur: whether it takes weeks or hours,” says first author Matthew Birk, who led the project as a postdoctoral fellow at the Marine Biological Laboratory and is now an assistant professor at Saint Francis University. “We could see significant changes in less than a day, and within 4 days, they were at the new steady-state levels that you find them in after a month.”

Going a step further yielded even more surprises

Taking the study a step further, the team collaborated with Kristen Verhey at the University of Michigan and Roger Sutton at Texas Tech to understand how RNA recoding impacts protein structure function. 

They zeroed in on kinesin and synaptotagmin, two proteins vital for nervous system function, and compared the edited and unedited versions. In both instances, they observed that recoding introduced structural changes in the proteins, altering their function.

The researchers also confirmed that temperature-sensitive RNA editing happens in the wild in response to seasonal temperature fluctuations. Wild octopuses, captured in winter versus summer, displayed similar patterns of temperature-sensitive RNA editing as those noted in the laboratory setting. 

This pattern extended beyond the California two-spot octopuses to the closely related Verrill’s two-spot octopus, bolstering the researchers’ suspicions that temperature-sensitive RNA editing might be common among other octopuses and squid.

Nevertheless, mysteries still abound. It remains unclear how octopuses regulate RNA editing and why editing is more prevalent in response to cold temperatures.

In future research, the scientists aim to uncover whether octopuses and other cephalopods utilize RNA recoding to adapt to other environmental variables, such as low oxygen availability or varied social environments. It seems that the octopus, with its flexible RNA and remarkable ability to adapt, still has plenty of secrets to share.

More about Octopuses

Octopuses are a type of mollusk belonging to the class Cephalopoda, which also includes squid, cuttlefish, and nautiluses. Here’s a rundown of some key facts and characteristics about these fascinating creatures:

Physical Features

Octopuses are renowned for their bulbous heads, large eyes, and eight arms adorned with suction cups. These arms are incredibly dexterous and strong. They use them to explore their environment, manipulate objects, capture prey, and for defense. Despite their solid appearance, octopuses are boneless and can squeeze through incredibly small spaces.

Intelligence

Octopuses are among the most intelligent invertebrates. They demonstrate complex behaviors, such as using tools, solving puzzles, and escaping from enclosures. Some species have been observed to use rocks and shells to construct “forts” or defensive perimeters around their lairs.

Camouflage and Defense

Octopuses are masters of disguise. They can change the color and texture of their skin to blend in with their environment in a matter of seconds, making them virtually invisible to predators. If threatened, they can also release a cloud of black ink to confuse predators and facilitate their escape.

Diet and Hunting

Octopuses are primarily carnivorous, feeding on crabs, shrimps, lobsters, fish, and other small sea creatures. Some larger species, such as the giant Pacific octopus, have been known to prey on sharks and seabirds. They typically use their strong arms and suction cups to capture prey, and their sharp beak to break open shells.

Reproduction and Life Cycle

Octopuses have a relatively short lifespan, with most species living for only a few years. After mating, the female lays thousands to hundreds of thousands of eggs, which she obsessively guards and cares for. Once the eggs hatch, both parents usually die soon after. This is called semelparity or “big bang” reproduction.

Species Diversity

There are approximately 300 known species of octopus, ranging from the small and relatively common common octopus (Octopus vulgaris) to the giant Pacific octopus (Enteroctopus dofleini), which is the largest known octopus species. The latter can reach an arm span of up to 30 feet and weigh more than 600 pounds.

Habitat

Octopuses are found in every ocean of the world, from the warm waters of the tropics to the cold seafloor. They inhabit a range of depths, from shallow coastal waters to abyssal depths.

Conservation

While some octopus species are common and not currently at risk, others are less well-known and could be threatened by factors such as habitat destruction, pollution, and climate change. Overfishing is also a concern for some species, as octopuses are caught for food in many parts of the world.

Scientific Research

Octopuses are of great interest to scientists due to their unique biology and behavior. Their ability to regenerate lost arms, their complex nervous system, their sophisticated camouflage abilities, and their unique methods of manipulating RNA are just a few of the areas that researchers are studying.

In short, octopuses are complex, intelligent, and highly adaptable creatures with a wide range of fascinating behaviors and abilities.

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