Octopuses rewire their brains to adapt to seasonal temperature shifts


Date:
June 8, 2023
Source:
Cell Press
Summary:
Octopuses don't thermoregulate, so their powerful brains are
exposed to - - and potentially threatened by -- changes in
temperature. Researchers report that two-spot octopuses adapt to
seasonal temperature shifts by producing different neural proteins
under warm versus cool conditions.

The octopuses achieve this by editing their RNA, the messenger
molecule between DNA and proteins. This rewiring likely protects
their brains, and the researchers suspect that this unusual strategy
is used widely amongst octopuses and squid.


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FULL STORY ========================================================================== Octopuses don't thermoregulate, so their powerful brains are exposed to
-- and potentially threatened by -- changes in temperature. Researchers
report June 8 in the journal Cell that two-spot octopuses adapt to
seasonal temperature shifts by producing different neural proteins under
warm versus cool conditions. The octopuses achieve this by editing their
RNA, the messenger molecule between DNA and proteins. This rewiring
likely protects their brains, and the researchers suspect that this
unusual strategy is used widely amongst octopuses and squid.

"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.

Compared to DNA mutations, which allow organisms to adapt over the
course of generations, RNA editing offers a temporary and flexible way
for individuals to adapt to environmental changes. RNA editing occurs
across the tree of life, but RNA recoding -- when the editing changes
the subsequent protein structure -- is much rarer, except in soft-bodied cephalopods like octopuses and squid. Humans have millions of editing
sites but editing affects the protein products in only ~3% of their
genes, whereas coleoid or "smart" cephalopods recode the majority of
their neural proteins.

"RNA recoding gives organisms the option to express a diverse quiver of proteins when and where they choose," says Rosenthal. "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?" To address
this question, the research team explored whether octopuses undergo RNA
editing in response to shifts in temperature and whether this editing
impacts the function of their brain proteins. In the wild, octopuses
are exposed to changes in temperature that can occur both rapidly,
for example, when they dive to colder depths or there is upwelling,
and slowly, when the seasons change.

The team focused on California two-spot octopuses (Octopus bimaculoides)
- - small, yellowish-brown octopuses who sport two iridescent blue
false eyes under their real eyes. These octopuses live off the coast of California and Mexico, and their genome has already been sequenced.

To investigate whether RNA editing is associated with temperature
variation, the researchers acclimated wild-caught adult octopuses to
warm (22-oC) or cold (13-oC) waters in tanks at the Marine Biological Laboratory. After several weeks, they compared the RNA transcripts for
the cold- and warm-acclimated octopuses to the genome to look for signs
of RNA editing at over 60,000 previously identified editing sites.

"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 handled 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." They also
noticed that certain types of neural proteins were more likely to be
sensitive to temperature, for example, proteins that are associated
with cell membranes (which are themselves very temperature-sensitive)
and calcium-binding proteins.

Next, the team explored how quickly these changes occurred. Working with thumbnail-sized juvenile octopuses this time, the researchers gradually
heated or cooled tanks -- from 14DEGC to 24DEGC or vice versa at 0.5DEGC
hourly increments -- over the course of about 20 hours and measured the
extent of RNA editing at several time points: before the temperature
change, immediately after the temperature change was complete, and up
to 4 days later. They were surprised by how rapidly RNA editing occurred.

"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." Next,
in collaboration with Kristen Verhey at University of Michigan and Roger
Sutton at Texas Tech, the team explored whether this recoding impacted
protein structure function. They focused on kinesin and synaptotagmin,
two proteins that are critical for nervous system function, and compared
the edited and unedited versions of each protein. In both cases, they
found evidence that the recoding produced structural changes in the
proteins that would impact their function.

They also showed that temperature-sensitive RNA editing occurs in
wild octopuses in response to seasonal temperature fluctuations. Wild
octopuses captured in winter versus summer displayed similar patterns of temperature- sensitive RNA editing to those observed in the lab. This
was true not only for California two spot octopuses but also for the
closely related Verrill's two- spot octopus (Octopus bimaculatus), and
the researchers suspect that temperature-sensitive RNA editing occurs
widely among other octopuses and squid.

Open questions remain about how the octopuses are regulating this RNA
editing, and it's unclear why editing occurs more frequently in response
to cold temperatures.

Next, the researchers want to explore whether octopuses and other
cephalopods use RNA recoding to adapt to other environmental variables,
such as low oxygen availability or varied social environments.

This research was supported by the National Science Foundation, the
National Institutes of Health, and the United States-Israel Binational
Science Foundation.

* RELATED_TOPICS
o Plants_&_Animals
# Biology # Cell_Biology # Molecular_Biology #
Biochemistry_Research
o Earth_&_Climate
# Environmental_Awareness # Climate # Environmental_Issues
# Global_Warming
* RELATED_TERMS
o Octopus o Intelligence_of_squid_and_octopuses o RNA o DNA
o Heat_shock_protein o Gene o Season o Protein

========================================================================== Story Source: Materials provided by Cell_Press. Note: Content may be
edited for style and length.


========================================================================== Journal Reference:
1. Matthew A. Birk, Noa Liscovitch-Brauer, Matthew J. Dominguez, Sean
McNeme, Yang Yue, J. Damon Hoff, Itamar Twersky, Kristen J. Verhey,
R.

Bryan Sutton, Eli Eisenberg, Joshua
J.C. Rosenthal. Temperature-dependent RNA editing in octopus
extensively recodes the neural proteome. Cell, 2023; 186 (12):
2544 DOI: 10.1016/j.cell.2023.05.004 ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2023/06/230608120915.htm

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