Abstract
In poikilotherms, temperature changes challenge the integration of physiological function. Within the complex nervous systems of the behaviorally sophisticated coleoid cephalopods, these problems are substantial. 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 structures 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.
| Original language | English |
|---|---|
| Pages (from-to) | 2544-2555.e13 |
| Journal | Cell |
| Volume | 186 |
| Issue number | 12 |
| DOIs | |
| State | Published - 8 Jun 2023 |
Bibliographical note
Publisher Copyright:© 2023 Elsevier Inc.
Funding
Octopus bimaculatus individuals sampled on Santa Catalina Island were collected under CA Department of Fish and Wildlife scientific collecting permit SC-191820001. M.A.B. was supported by an NSF Postdoctoral Research Fellowship in Biology (DBI-1907197). K.J.V. was supported by NIH R35GM131744. E.E. was supported by NSF-BSF BSF 2020759, BSF 2017262, and BSF 2013094. J.J.C.R. was supported by NSF-BSF 2110074, NSF 2220587, BSF 2017262, BSF 2013094, and NSF 1827509. All octopus drawings in figures were created by Roger Hall. We thank the MBL's cephalopods program for their support in this study. Conceptualization, M.A.B. E.E. and J.J.C.R.; methodology, M.A.B. J.D.H. and J.J.C.R.; investigation, M.A.B. M.J.D. S.M. Y.Y. and J.J.C.R.; data curation, M.A.B. and R.B.S.; formal analysis, M.A.B. N.L.-B. I.T. R.B.S. and E.E.; funding acquisition, M.A.B. K.J.V. E.E. and J.J.C.R.; software, M.A.B.; validation, M.A.B. and J.J.C.R.; visualization, M.A.B. and R.B.S.; writing, M.A.B. K.J.V. R.B.S. E.E. and J.J.C.R.; project administration, K.J.V. R.B.S. and J.J.C.R.; supervision, R.B.S. E.E. and J.J.C.R.; resources, J.J.C.R. The authors declare no competing interests. One or more of the authors of this paper received support from a program designed to increase minority representation in their field of research. Octopus bimaculatus individuals sampled on Santa Catalina Island were collected under CA Department of Fish and Wildlife scientific collecting permit SC-191820001. M.A.B. was supported by an NSF Postdoctoral Research Fellowship in Biology ( DBI-1907197 ). K.J.V. was supported by NIH R35GM131744 . E.E. was supported by NSF-BSF BSF 2020759 , BSF 2017262 , and BSF 2013094 . J.J.C.R. was supported by NSF-BSF 2110074 , NSF 2220587 , BSF 2017262 , BSF 2013094 , and NSF 1827509 . All octopus drawings in figures were created by Roger Hall. We thank the MBL’s cephalopods program for their support in this study.
| Funders | Funder number |
|---|---|
| NSF-BSF | 2110074, BSF 2017262, 2220587, 1827509, BSF 2013094, BSF 2020759 |
| National Science Foundation | DBI-1907197 |
| National Institutes of Health | R35GM131744 |
| California Department of Fish and Wildlife | SC-191820001 |
Keywords
- ADAR
- RNA editing
- RNA modifications
- acclimation
- cephalopod
- epitranscriptome
- kinesin
- neural plasticity
- synaptotagmin
- temperature