Abstract
Disruption of neuronal function is likely to influence limits to thermal tolerance. We hypothesized that with acute warming the structure and function of neuronal membranes in the Antarctic notothenioid fish Chaenocephalus aceratus are more vulnerable to perturbation than membranes in the more thermotolerant notothenioid Notothenia coriiceps. Fluidity was quantified in synaptic membranes, mitochondrial membranes, and myelin from brains of both species of Antarctic fishes. Polar lipid compositions and cholesterol contents were analyzed in myelin; cholesterol was measured in synaptic membranes. Thermal profiles were determined for activities of two membrane-associated proteins, acetylcholinesterase (AChE) and Na+/K+-ATPase (NKA), from brains of animals maintained at ambient temperature or exposed to their critical thermal maxima (CTMAX). Synaptic membranes of C. aceratus were consistently more fluid than those of N. coriiceps (P < 0.0001). Although the fluidities of both myelin and mitochondrial membranes were similar among species, sensitivity of myelin fluidity to in vitro warming was greater in N. coriiceps than in C. aceratus (P < 0.001), which can be explained by lower cholesterol contents in myelin of N. coriiceps (P < 0.05). Activities of both enzymes, AChE and NKA, declined upon CTMAX exposure in C. aceratus, but not in N. coriiceps. We suggest that hyper-fluidization of synaptic membranes with warming in C. aceratus may explain the greater stenothermy in this species, and that thermal limits in notothenioids are more likely to be influenced by perturbations in synaptic membranes than in other membranes of the nervous system.
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Data Availability
The datasets generated during and/or analyzed during the current study will be made available in Dryad Digital Repository upon acceptance for publication.
Abbreviations
- AChE:
-
Acetylcholine esterase
- ANCOVA:
-
Analysis of covariance
- ANOVA:
-
Analysis of variance
- CNPase:
-
Cyclic nucleotide phosphodiesterase
- CTMAX :
-
Critical thermal maximum
- DPH:
-
1,6-diphenyl-1,3,5-hexatriene
- ePC:
-
Plasmalogen PC
- LDH:
-
Lactate dehydrogenase
- NKA:
-
Sodium-potassium ATPase
- PC:
-
Phosphatidylcholine
- PE:
-
Phosphatidylethanolamine
- PI:
-
Phosphatidylinositol
- PK:
-
Pyruvate kinase
- PS:
-
Phosphatidylserine
- SDH:
-
Succinate dehydrogenase
- UI:
-
Unsaturation index
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Acknowledgements
Field work for this study represented a collaborative effort between ourselves and Dr. Stuart Egginton, Dr. Anthony Farrell, Dr. Michael Friedlander, Dr. Iskander Ismailov, Dr. Theresa Grove, Elizabeth Evans, and Jordan Scharping. Michael Ortego carried out assays for determining apparent Km. Our thanks to Dr. Bruce Carlson for help with statistical analyses and to Dr. Steve McCormick for advice on NKA assays. We owe our thanks for logistic support to the staff at Palmer Station, and the masters and crew of the ARSV Laurence M. Gould. The lipid analyses described in this work were performed at the Kansas Lipidomics Research Center Analytical Laboratory. Instrument acquisition and lipidomics method development was supported by National Science Foundation (EPS 0236913, MCB 1413036, DBI 0521587, DBI1228622), Kansas Technology Enterprise Corporation, K-IDeA Networks of Biomedical Research Excellence (INBRE) of National Institute of Health (P20GM103418), and Kansas State University.
Funding
Financial support for this research was provided by the US National Science Foundation [Grant no. PLR 1341602].
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Biederman, A.M., Kuhn, D.E., O’Brien, K.M. et al. Physical, chemical, and functional properties of neuronal membranes vary between species of Antarctic notothenioids differing in thermal tolerance. J Comp Physiol B 189, 213–222 (2019). https://doi.org/10.1007/s00360-019-01207-x
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DOI: https://doi.org/10.1007/s00360-019-01207-x