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   PID: hpt/lnx 1.9.0-cur 2019-01-08   
   TID: hpt/lnx 1.9.0-cur 2019-01-08   
    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   
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   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   
      
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   Story Source: Materials provided by Cell_Press. Note: Content may be   
   edited for style and length.   
      
      
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   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   
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   Link to news story:   
   https://www.sciencedaily.com/releases/2023/06/230608120915.htm   
      
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