Antifreeze protein-induced superheating of ice inside Antarc

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TitleAntifreeze protein-induced superheating of ice inside Antarctic notothenioid fishes inhibits melting during summer warmingAbstractAntifreeze proteins (AFPs) of polar marine teleost fishes are widely recognized as an evolutionary innovation of vast adaptive value in that, by adsorbing to and inhibiting the growth of internalized environmental ice crystals, they prevent death by inoculative freezing. Paradoxically, systemic accumulation of AFP-stabilized ice could also be lethal. Whether or how fishes eliminate internal ice is unknown. To investigate if ice inside high-latitude Antarctic notothenioid fishes could melt seasonally, we measured its melting point and obtained a decadal temperature record from a shallow benthic fish habitat in McMurdo Sound, Antarctica. We found that AFP-stabilized ice resists melting at temperatures above the expected equilibrium freezing/melting point (eqFMP), both in vitro and in vivo. Superheated ice was directly observed in notothenioid serum samples and in solutions of purified AFPs, and ice was found to persist inside live fishes at temperatures more than 1 ^circC above their eqFMP for at least 24 h, and at a lower temperature for at least several days. Field experiments confirmed that superheated ice occurs naturally inside wild fishes. Over the long-Term record (1999-2012), seawater temperature surpassed the fish eqFMP in most summers, but never exceeded the highest temperature at which ice persisted inside experimental fishes. Thus, because of the effects of AFP-induced melting inhibition, summer warming may not reliably eliminate internal ice. Our results expose a potentially antagonistic pleiotropic effect of AFPs: beneficial freezing avoidance is accompanied by melting inhibition that may contribute to lifelong accumulation of detrimental internal ice crystals.AcknowledgementsWe thank the staff at McMurdo Station and Scott Base; E. DeVries, B. Evans, L. Fields, K. Hoefling, B. Hunt, L. Hunt, K. Meister, K. Murphy, B. Palmintier, R. Robbins, S. Rupp, and R. Tien for assistance in the field; members of the J. W. Thornton laboratory for their support; A. Rempel for helpful discussion; and C. Brooks for providing a conductivity, temperature, and depth cast from the research vessel Nathaniel B. Palmer. This work was supported by US National Science Foundation Awards OPP 0231006 (to A.L.D. and C.-H.C.C.) and ANT 1142158 (to C.-H.C.C. and A.L.D.) and a National Science Foundation Graduate Research fellowship (to P.A.C.).

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1st AuthorCziko, P.AuthorCziko, P.DeVries, A.Evans, C.Christina Cheng, C.-H.Year2014JournalProceedings of the National Academy of Sciences of the United States of AmericaVolume111Number40Pages14583-14588DOI10.1073/pnas.1410256111URLhttps://www.scopus.com/inward/recor.....302a5b6feccf8ee07dd620544Keywordsantifreeze proteiniceantifreeze proteinfish proteinice, animal experimentAntarcticaantartic notothenioid fishaquatic environmentArticlecontrolled studycrystalenvironmental temperatureexperimental fishfield experimentfishfreezingice coverin vitro studymelting pointnonhumanpleiotropypriority journalsea icesummerteleostwarmingadaptationanimalcrystallizationecosystemfishmetabolismphysiological processphysiologyseasontemperature, Adaptation, PhysiologicalAnimalsAntarctic RegionsAntifreeze ProteinsCrystallizationEcosystemFish ProteinsFishesFreezingIcePhysiological PhenomenaSeasonsTemperature, rank5

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TypeArticleCitationCziko, P., DeVries, A., Evans, C. and Christina Cheng, C.-H. (2014). Antifreeze protein-induced superheating of ice inside Antarctic notothenioid fishes inhibits melting during summer warming. Proceedings of the National Academy of Sciences of the United States of America, 111(40): 14583-14588 IdentifierCziko2014Relevancerank5