Core protein synthesis adaptations drive biological novelty in octopus

Much of biology focuses on how differences in the genetic code give rise to new functions, but far less attention is given to adaptations in other components of the central dogma. Octopuses exhibit complex nervous systems and sophisticated behaviors that rival vertebrates, but via an entirely distinct evolutionary history. How did octopuses distinctly evolve such novel traits? Here, we serendipitously discover that octopus ribosomes contain a structural adaptation in the catalytic ribosomal RNA (rRNA) domain, a conserved center for protein synthesis across all life1. This rRNA modification is unique among all animals and mediates enhanced accuracy of protein synthesis, decreases protein misfolding and aggregation, and supports translation during adaptive RNA editing when occupying new environments. Thus, the octopus uses modifications in the core protein synthesis machinery to drive biological novelty, a strategy which could support the evolution of unique organismal traits across life. Overall design: To characterise gene expression differences in cephalopods, we performed RNA-Seq on arm and brain tissues derived from Octopus bimaculoides and Euprymna berryi. Additionally, to quantify RNA editing, we performed RNA seq from octopus and squid tissues that were subjected to a cold acclimation protocol (6 degrees C decline in ambient temperature over 2 weeks).