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Evidence for non-colligative function of small cryoprotectants in a freeze-tolerant insect.
Proc Biol Sci. 2019 03 27; 286(1899):20190050.PB

Abstract

Freeze tolerance, the ability to survive internal ice formation, facilitates survival of some insects in cold habitats. Low-molecular-weight cryoprotectants such as sugars, polyols and amino acids are hypothesized to facilitate freeze tolerance, but their in vivo function is poorly understood. Here, we use a combination of metabolomics and manipulative experiments in vivo and ex vivo to examine the function of multiple cryoprotectants in the spring field cricket Gryllus veletis. Cold-acclimated G. veletis are freeze-tolerant and accumulate myo-inositol, proline and trehalose in their haemolymph and fat body. Injecting freeze-tolerant crickets with proline and trehalose increases survival of freezing to lower temperatures or for longer times. Similarly, exogenous myo-inositol and trehalose increase ex vivo freezing survival of fat body cells from freeze-tolerant crickets. No cryoprotectant (alone or in combination) is sufficient to confer freeze tolerance on non-acclimated, freeze-intolerant G. veletis. Given that each cryoprotectant differentially impacts survival in the frozen state, we conclude that small cryoprotectants are not interchangeable and likely function non-colligatively in insect freeze tolerance. Our study is the first to experimentally demonstrate the importance of non-colligative cryoprotectant function for insect freeze tolerance both in vivo and ex vivo, with implications for choosing new molecules for cryopreservation.

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Authors+Show Affiliations

Toxopeus J
1 Department of Biology, University of Western Ontario , 1151 Richmond Street North, London, Ontario , Canada N6A 5B7.
Koštál V
2 Institute of Entomology, Biology Centre, Czech Academy of Sciences , Branišovská 1160/31, České Budějovice 37005 , Czech Republic.
Sinclair BJ
1 Department of Biology, University of Western Ontario , 1151 Richmond Street North, London, Ontario , Canada N6A 5B7.

MeSH

AcclimatizationAnimalsCold TemperatureCryoprotective AgentsFat BodyFreezingGryllidaeHemolymphLongevityMaleMetabolomicsNymphProlineTrehalose

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

30890098

Citation

Toxopeus, Jantina, et al. "Evidence for Non-colligative Function of Small Cryoprotectants in a Freeze-tolerant Insect." Proceedings. Biological Sciences, vol. 286, no. 1899, 2019, p. 20190050.
Toxopeus J, Koštál V, Sinclair BJ. Evidence for non-colligative function of small cryoprotectants in a freeze-tolerant insect. Proc Biol Sci. 2019;286(1899):20190050.
Toxopeus, J., Koštál, V., & Sinclair, B. J. (2019). Evidence for non-colligative function of small cryoprotectants in a freeze-tolerant insect. Proceedings. Biological Sciences, 286(1899), 20190050. https://doi.org/10.1098/rspb.2019.0050
Toxopeus J, Koštál V, Sinclair BJ. Evidence for Non-colligative Function of Small Cryoprotectants in a Freeze-tolerant Insect. Proc Biol Sci. 2019 03 27;286(1899):20190050. PubMed PMID: 30890098.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Evidence for non-colligative function of small cryoprotectants in a freeze-tolerant insect. AU - Toxopeus,Jantina, AU - Koštál,Vladimír, AU - Sinclair,Brent J, PY - 2019/3/21/entrez PY - 2019/3/21/pubmed PY - 2020/3/5/medline KW - Gryllus veletis KW - acclimation KW - cold tolerance KW - cryopreservation KW - cryoprotectants KW - freeze tolerance SP - 20190050 EP - 20190050 JF - Proceedings. Biological sciences JO - Proc Biol Sci VL - 286 IS - 1899 N2 - Freeze tolerance, the ability to survive internal ice formation, facilitates survival of some insects in cold habitats. Low-molecular-weight cryoprotectants such as sugars, polyols and amino acids are hypothesized to facilitate freeze tolerance, but their in vivo function is poorly understood. Here, we use a combination of metabolomics and manipulative experiments in vivo and ex vivo to examine the function of multiple cryoprotectants in the spring field cricket Gryllus veletis. Cold-acclimated G. veletis are freeze-tolerant and accumulate myo-inositol, proline and trehalose in their haemolymph and fat body. Injecting freeze-tolerant crickets with proline and trehalose increases survival of freezing to lower temperatures or for longer times. Similarly, exogenous myo-inositol and trehalose increase ex vivo freezing survival of fat body cells from freeze-tolerant crickets. No cryoprotectant (alone or in combination) is sufficient to confer freeze tolerance on non-acclimated, freeze-intolerant G. veletis. Given that each cryoprotectant differentially impacts survival in the frozen state, we conclude that small cryoprotectants are not interchangeable and likely function non-colligatively in insect freeze tolerance. Our study is the first to experimentally demonstrate the importance of non-colligative cryoprotectant function for insect freeze tolerance both in vivo and ex vivo, with implications for choosing new molecules for cryopreservation. SN - 1471-2954 UR - https://www.unboundmedicine.com/medline/citation/30890098/Evidence_for_non_colligative_function_of_small_cryoprotectants_in_a_freeze_tolerant_insect_ DB - PRIME DP - Unbound Medicine ER -