Biochemical Response to Freezing in the Siberian Salamander <i>Salamandrella keyserlingii</i>
The Siberian salamander <i>Salamandrella keyserlingii</i> Dybowski, 1870 is a unique amphibian that is capable to survive long-term freezing at −55 °C. Nothing is known on the biochemical basis of this remarkable freezing tolerance, except for the fact that it uses glycerol as a low mole...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2021-11-01
|
| Series: | Biology |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2079-7737/10/11/1172 |
| _version_ | 1797511142016286720 |
|---|---|
| author | Sergei V. Shekhovtsov Nina A. Bulakhova Yuri P. Tsentalovich Ekaterina A. Zelentsova Ekaterina N. Meshcheryakova Tatiana V. Poluboyarova Daniil I. Berman |
| author_facet | Sergei V. Shekhovtsov Nina A. Bulakhova Yuri P. Tsentalovich Ekaterina A. Zelentsova Ekaterina N. Meshcheryakova Tatiana V. Poluboyarova Daniil I. Berman |
| author_sort | Sergei V. Shekhovtsov |
| collection | DOAJ |
| description | The Siberian salamander <i>Salamandrella keyserlingii</i> Dybowski, 1870 is a unique amphibian that is capable to survive long-term freezing at −55 °C. Nothing is known on the biochemical basis of this remarkable freezing tolerance, except for the fact that it uses glycerol as a low molecular weight cryoprotectant. We used <sup>1</sup>H-NMR analysis to study quantitative changes of multiple metabolites in liver and hindlimb muscle of <i>S. keyserlingii</i> in response to freezing. For the majority of molecules we observed significant changes in concentrations. Glycerol content in frozen organs was as high as 2% w/w, which confirms its role as a cryoprotectant. No other putative cryoprotectants were detected. Freezing resulted in ischemia manifested as increased concentrations of glycolysis products: lactate and alanine. Unexpectedly, we detected no increase in concentrations of succinate, which accumulates under ischemia in various tetrapods. Freezing proved to be a dramatic stress with reduced adenosine phosphate pool and high levels of nucleotide degradation products (hypoxanthine, β-alanine, and β-aminoisobutyrate). There was also significant increase in the concentrations of choline and glycerophosphocholine, which may be interpreted as the degradation of biomembranes. Thus, we found that freezing results not only in macroscopical damage due to ice formation, but also to degradation of DNA and biomembranes. |
| first_indexed | 2024-03-10T05:42:12Z |
| format | Article |
| id | doaj.art-67a18d285c854eb493c248aee98cf437 |
| institution | Directory Open Access Journal |
| issn | 2079-7737 |
| language | English |
| last_indexed | 2024-03-10T05:42:12Z |
| publishDate | 2021-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Biology |
| spelling | doaj.art-67a18d285c854eb493c248aee98cf4372023-11-22T22:28:24ZengMDPI AGBiology2079-77372021-11-011011117210.3390/biology10111172Biochemical Response to Freezing in the Siberian Salamander <i>Salamandrella keyserlingii</i>Sergei V. Shekhovtsov0Nina A. Bulakhova1Yuri P. Tsentalovich2Ekaterina A. Zelentsova3Ekaterina N. Meshcheryakova4Tatiana V. Poluboyarova5Daniil I. Berman6Institute of the Biological Problems of the North FEB RAS, 685000 Magadan, RussiaInstitute of the Biological Problems of the North FEB RAS, 685000 Magadan, RussiaInternational Tomography Center SB RAS, 630090 Novosibirsk, RussiaInternational Tomography Center SB RAS, 630090 Novosibirsk, RussiaInstitute of the Biological Problems of the North FEB RAS, 685000 Magadan, RussiaInstitute of Cytology and Genetics SB RAS, 630090 Novosibirsk, RussiaInstitute of the Biological Problems of the North FEB RAS, 685000 Magadan, RussiaThe Siberian salamander <i>Salamandrella keyserlingii</i> Dybowski, 1870 is a unique amphibian that is capable to survive long-term freezing at −55 °C. Nothing is known on the biochemical basis of this remarkable freezing tolerance, except for the fact that it uses glycerol as a low molecular weight cryoprotectant. We used <sup>1</sup>H-NMR analysis to study quantitative changes of multiple metabolites in liver and hindlimb muscle of <i>S. keyserlingii</i> in response to freezing. For the majority of molecules we observed significant changes in concentrations. Glycerol content in frozen organs was as high as 2% w/w, which confirms its role as a cryoprotectant. No other putative cryoprotectants were detected. Freezing resulted in ischemia manifested as increased concentrations of glycolysis products: lactate and alanine. Unexpectedly, we detected no increase in concentrations of succinate, which accumulates under ischemia in various tetrapods. Freezing proved to be a dramatic stress with reduced adenosine phosphate pool and high levels of nucleotide degradation products (hypoxanthine, β-alanine, and β-aminoisobutyrate). There was also significant increase in the concentrations of choline and glycerophosphocholine, which may be interpreted as the degradation of biomembranes. Thus, we found that freezing results not only in macroscopical damage due to ice formation, but also to degradation of DNA and biomembranes.https://www.mdpi.com/2079-7737/10/11/1172freeze tolerancefreezingcryoprotectantsglycolysisSiberian salamander<i>Salamandrella keyserlingii</i> |
| spellingShingle | Sergei V. Shekhovtsov Nina A. Bulakhova Yuri P. Tsentalovich Ekaterina A. Zelentsova Ekaterina N. Meshcheryakova Tatiana V. Poluboyarova Daniil I. Berman Biochemical Response to Freezing in the Siberian Salamander <i>Salamandrella keyserlingii</i> Biology freeze tolerance freezing cryoprotectants glycolysis Siberian salamander <i>Salamandrella keyserlingii</i> |
| title | Biochemical Response to Freezing in the Siberian Salamander <i>Salamandrella keyserlingii</i> |
| title_full | Biochemical Response to Freezing in the Siberian Salamander <i>Salamandrella keyserlingii</i> |
| title_fullStr | Biochemical Response to Freezing in the Siberian Salamander <i>Salamandrella keyserlingii</i> |
| title_full_unstemmed | Biochemical Response to Freezing in the Siberian Salamander <i>Salamandrella keyserlingii</i> |
| title_short | Biochemical Response to Freezing in the Siberian Salamander <i>Salamandrella keyserlingii</i> |
| title_sort | biochemical response to freezing in the siberian salamander i salamandrella keyserlingii i |
| topic | freeze tolerance freezing cryoprotectants glycolysis Siberian salamander <i>Salamandrella keyserlingii</i> |
| url | https://www.mdpi.com/2079-7737/10/11/1172 |
| work_keys_str_mv | AT sergeivshekhovtsov biochemicalresponsetofreezinginthesiberiansalamanderisalamandrellakeyserlingiii AT ninaabulakhova biochemicalresponsetofreezinginthesiberiansalamanderisalamandrellakeyserlingiii AT yuriptsentalovich biochemicalresponsetofreezinginthesiberiansalamanderisalamandrellakeyserlingiii AT ekaterinaazelentsova biochemicalresponsetofreezinginthesiberiansalamanderisalamandrellakeyserlingiii AT ekaterinanmeshcheryakova biochemicalresponsetofreezinginthesiberiansalamanderisalamandrellakeyserlingiii AT tatianavpoluboyarova biochemicalresponsetofreezinginthesiberiansalamanderisalamandrellakeyserlingiii AT daniiliberman biochemicalresponsetofreezinginthesiberiansalamanderisalamandrellakeyserlingiii |