Temperature-dependent RNA editing in octopus extensively recodes the neural proteome

In poikilotherms, temperature changes challenge the integration of physiological function. Within the com-plex nervous systems of the behaviorally sophisticated coleoid cephalopods, these problems are substan-tial. RNA editing by adenosine deamination is a well-positioned mechanism for environmental acclimation. We report that the neural proteome of Octopus bimaculoides undergoes massive reconfigurations via RNA editing following a temperature challenge. Over 13,000 codons are affected, and many alter proteins that are vital for neural processes. For two highly temperature-sensitive examples, recoding tunes protein function. For synaptotagmin, a key component of Ca2+-dependent neurotransmitter release, crystal struc-tures and supporting experiments show that editing alters Ca2+ binding. For kinesin-1, a motor protein driving axonal transport, editing regulates transport velocity down microtubules. Seasonal sampling of wild-caught specimens indicates that temperature-dependent editing occurs in the field as well. These data show that A-to-I editing tunes neurophysiological function in response to temperature in octopus and most likely other coleoids.

Automated summary

Temperature changes pose a challenge to the physiological function integration in poikilotherms. Among the behaviorally sophisticated coleoid cephalopods, the complex nervous systems face substantial problems in this aspect. RNA editing through adenosine deamination is a mechanism well-suited for environmental acclimation. This study reveals that Octopus bimaculoides' neural proteome undergoes significant reconfigurations via RNA editing in response to temperature changes, affecting over 13,000 codons and altering vital proteins.