Is cold the new hot? Elevated ubiquitin-conjugated protein levels in tissues of Antarctic fish as evidence for cold-denaturation of proteins in vivo

Abstract

Levels of ubiquitin (Ub)-conjugated proteins, as an index of misfolded or damaged proteins, were measured in notothenioid fishes, with both Antarctic (Trematomus bernacchii, T. pennellii, Pagothenia borchgrevinki) and non-Antarctic (Notothenia angustata, Bovichtus variegatus) distributions, as well as non-notothenioid fish from the Antarctic (Lycodichthys dearborni, Family Zoarcidae) and New Zealand (Bellapiscis medius, Family Tripterygiidae), in an effort to better understand the effect that inhabiting a sub-zero environment has on maintaining the integrity of the cellular protein pool. Overall, levels of Ub-conjugated proteins in cold-adapted Antarctic fishes were significantly higher than New Zealand fishes in gill, liver, heart and spleen tissues suggesting that life at sub-zero temperatures impacts protein homeostasis. The highest tissue levels of ubiquitinated proteins were found in the spleen of all fish. Ub conjugate levels in the New Zealand N. angustata, more closely resembled levels measured in other Antarctic fishes than levels measured in other New Zealand species, likely reflecting their recent shared ancestry with Antarctic notothenioids.

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Acknowledgements

We are indebted to many individuals who assisted us during the course of this project. In particular, we thank the field team members of Bravo 134 (Dr. B. Buckley, T. Crombie, J. Dutton, C. Osovitz and M. Zippay) for logistical support in obtaining Antarctic specimens. We further thank the United States Antarctic Program and Raytheon Polar Services Corporation for logistical and field support at McMurdo Station, Antarctica. We thank the University of Otago (Dunedin, New Zealand) for access to research facilities at Portobello Marine Laboratory (PML). In particular, we gratefully acknowledge the staff of PML, especially Bev Dickson (Lab Manager), Karen Bonney and Rene van Baalen for assistance in the collection of N. angustata and logistical support at PML. Finally, we thank Dr. Nann Fangue and Julia Uberuaga for their help in the collection of B. variegatus. This research was supported by National Science Foundation grant ANT-0440799 to G.E.H. and by a Natural Sciences and Engineering Research Council of Canada Postdoctoral Fellowship to A.E.T. This research was conducted in accordance with U.S. Federal animal welfare laws via approval and oversight by the University of California, Santa Barbara Institutional Animal Care and Use Committee (IACUC) (Protocol No. 634). Specimens were collected in compliance with the U.S. regulations governing collection of Antarctic organisms, the Antarctic Conservation Act of 1978 (Public Law 95-541) and the Antarctic Marine Living Resources Convention Act of 1984 (Public Law 98-623) and complied with the current laws of New Zealand.

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Correspondence to Gretchen E. Hofmann.

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Communicated by H.V. Carey.

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Todgham, A.E., Hoaglund, E.A. & Hofmann, G.E. Is cold the new hot? Elevated ubiquitin-conjugated protein levels in tissues of Antarctic fish as evidence for cold-denaturation of proteins in vivo. J Comp Physiol B 177, 857–866 (2007). https://doi.org/10.1007/s00360-007-0183-2

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Keywords

  • Antarctic fish
  • Protein denaturation
  • Ubiquitin
  • Cold adaptation
  • Notothenioid