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Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature

Wen, Xin and Wang, Sen and Duman, John G. and Arifin, Josh Fnu and Juwita, Vonny and Goddard, William A., III and Rios, Alejandra and Liu, Fan and Kim, Soo-Kyung and Abrol, Ravinder and DeVries, Arthur L. and Henling, Lawrence M. (2016) Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature. Proceedings of the National Academy of Sciences of the United States of America, 113 (24). pp. 6683-6688. ISSN 0027-8424. PMCID PMC4914155. http://resolver.caltech.edu/CaltechAUTHORS:20160526-095348614

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Abstract

The remarkable adaptive strategies of insects to extreme environments are linked to the biochemical compounds in their body fluids. Trehalose, a versatile sugar molecule, can accumulate to high levels in freeze-tolerant and freeze-avoiding insects, functioning as a cryoprotectant and a supercooling agent. Antifreeze proteins (AFPs), known to protect organisms from freezing by lowering the freezing temperature and deferring the growth of ice, are present at high levels in some freeze-avoiding insects in winter, and yet, paradoxically are found in some freeze-tolerant insects. Here, we report a previously unidentified role for AFPs in effectively inhibiting trehalose precipitation in the hemolymph (or blood) of overwintering beetle larvae. We determine the trehalose level (29.6 ± 0.6 mg/mL) in the larval hemolymph of a beetle, Dendroides canadensis, and demonstrate that the hemolymph AFPs are crucial for inhibiting trehalose crystallization, whereas the presence of trehalose also enhances the antifreeze activity of AFPs. To dissect the molecular mechanism, we examine the molecular recognition between AFP and trehalose crystal interfaces using molecular dynamics simulations. The theory corroborates the experiments and shows preferential strong binding of the AFP to the fast growing surfaces of the sugar crystal. This newly uncovered role for AFPs may help explain the long-speculated role of AFPs in freeze-tolerant species. We propose that the presence of high levels of molecules important for survival but prone to precipitation in poikilotherms (their body temperature can vary considerably) needs a companion mechanism to prevent the precipitation and here present, to our knowledge, the first example. Such a combination of trehalose and AFPs also provides a novel approach for cold protection and for trehalose crystallization inhibition in industrial applications.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1601519113 DOIArticle
http://www.pnas.org/content/113/24/6683.abstractPublisherArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1601519113/-/DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4914155/PubMed CentralArticle
ORCID:
AuthorORCID
Goddard, William A., III0000-0003-0097-5716
Abrol, Ravinder0000-0001-7333-6793
Additional Information:© 2016 National Academy of Sciences. Edited by David L. Denlinger, Ohio State University, Columbus, OH, and approved April 28, 2016 (received for review January 30, 2016). Published online before print May 25, 2016. This work was supported by National Institutes of Health Grant GM086249 (to X.W.). The Bruker KAPPA APEXII X-ray diffractometer was purchased via a National Science Foundation (NSF) Chemistry Research Instrumentation and Facilities: Departmental Multi-user Instrumentation (CRIF:MU) award to the California Institute of Technology (Caltech) (CHE-0639094). W.A.G. thanks NSF (EFRI-1332411) for support of Caltech theory efforts in this project. A.R. thanks Caltech Minority Undergraduate Research Fellowships funded by the Howard Hughes Medical Institute. The LC-MS was supported by National Center for Research Resources Grant S10-RR025631 to the University of California, Los Angeles, where Dr. Greg Khitrov provided assistance. Author contributions: X.W. and S.W. designed research; X.W. and S.W. initiated research; X.W. oversaw research; X.W., S.W., J.G.D., J.F.A., V.J., W.A.G., A.R., F.L., S.-K.K., R.A., A.L.D., and L.M.H. performed research; X.W., S.W., and W.A.G. analyzed data; and X.W., S.W., J.G.D., W.A.G., A.L.D., and L.M.H. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. Data deposition: The structures have been deposited at the Cambridge Crystallographic Data Centre, www.ccdc.cam.ac.uk/structures (CSD reference nos. 1053435 and 1053434). This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1601519113/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NIHGM086249
NSFCHE-0639094
NSFEFRI-1332411
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
National Center for Research ResourcesS10-RR025631
Subject Keywords:insects; environmental stress; trehalose; crystallization; antifreeze protein
PubMed Central ID:PMC4914155
Record Number:CaltechAUTHORS:20160526-095348614
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160526-095348614
Official Citation:Xin Wen, Sen Wang, John G. Duman, Josh Fnu Arifin, Vonny Juwita, William A. Goddard III, Alejandra Rios, Fan Liu, Soo-Kyung Kim, Ravinder Abrol, Arthur L. DeVries, and Lawrence M. Henling Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature PNAS 2016 113 (24) 6683-6688; published ahead of print May 25, 2016, doi:10.1073/pnas.1601519113
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:67381
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:26 May 2016 17:17
Last Modified:18 Jul 2017 20:47

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