Discovery of Hyperactive Antifreeze Protein from Phylogenetically Distant Beetles Questions Its Evolutionary Origin
Beetle hyperactive antifreeze protein (AFP) has a unique ability to maintain a supercooling state of its body fluids, however, less is known about its origination. Here, we found that a popular stag beetle <i>Dorcus hopei binodulosus</i> (<i>Dhb</i>) synthesizes at least 6 is...
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| Format: | Article |
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MDPI AG
2021-03-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/22/7/3637 |
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| author | Tatsuya Arai Akari Yamauchi Ai Miura Hidemasa Kondo Yoshiyuki Nishimiya Yuji C. Sasaki Sakae Tsuda |
| author_facet | Tatsuya Arai Akari Yamauchi Ai Miura Hidemasa Kondo Yoshiyuki Nishimiya Yuji C. Sasaki Sakae Tsuda |
| author_sort | Tatsuya Arai |
| collection | DOAJ |
| description | Beetle hyperactive antifreeze protein (AFP) has a unique ability to maintain a supercooling state of its body fluids, however, less is known about its origination. Here, we found that a popular stag beetle <i>Dorcus hopei binodulosus</i> (<i>Dhb</i>) synthesizes at least 6 isoforms of hyperactive AFP (<i>Dhb</i>AFP). Cold-acclimated <i>Dhb</i> larvae tolerated −5 °C chilled storage for 24 h and fully recovered after warming, suggesting that <i>Dhb</i>AFP facilitates overwintering of this beetle. A <i>Dhb</i>AFP isoform (~10 kDa) appeared to consist of 6−8 tandem repeats of a 12-residue consensus sequence (TCTxSxNCxxAx), which exhibited 3 °C of high freezing point depression and the ability of binding to an entire surface of a single ice crystal. Significantly, these properties as well as DNA sequences including the untranslated region, signal peptide region, and an AFP-encoding region of <i>Dhb</i> are highly similar to those identified for a known hyperactive AFP (<i>Tm</i>AFP) from the beetle <i>Tenebrio molitor</i> (<i>Tm</i>). Progenitor of <i>Dhb</i> and <i>Tm</i> was branched off approximately 300 million years ago, so no known evolution mechanism hardly explains the retainment of the DNA sequence for such a long divergence period. Existence of unrevealed gene transfer mechanism will be hypothesized between these two phylogenetically distant beetles to acquire this type of hyperactive AFP. |
| first_indexed | 2024-03-10T12:44:53Z |
| format | Article |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T12:44:53Z |
| publishDate | 2021-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-c51837991198423aa24747c3e11dd4402023-11-21T13:36:01ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-03-01227363710.3390/ijms22073637Discovery of Hyperactive Antifreeze Protein from Phylogenetically Distant Beetles Questions Its Evolutionary OriginTatsuya Arai0Akari Yamauchi1Ai Miura2Hidemasa Kondo3Yoshiyuki Nishimiya4Yuji C. Sasaki5Sakae Tsuda6Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Sapporo 062-8517, JapanGraduate School of Life Sciences, Hokkaido University, Sapporo 060-0810, JapanBioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Sapporo 062-8517, JapanBioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Sapporo 062-8517, JapanBioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Sapporo 062-8517, JapanGraduate School of Frontier Sciences, The University of Tokyo, Kashiwa 277-8561, JapanBioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Sapporo 062-8517, JapanBeetle hyperactive antifreeze protein (AFP) has a unique ability to maintain a supercooling state of its body fluids, however, less is known about its origination. Here, we found that a popular stag beetle <i>Dorcus hopei binodulosus</i> (<i>Dhb</i>) synthesizes at least 6 isoforms of hyperactive AFP (<i>Dhb</i>AFP). Cold-acclimated <i>Dhb</i> larvae tolerated −5 °C chilled storage for 24 h and fully recovered after warming, suggesting that <i>Dhb</i>AFP facilitates overwintering of this beetle. A <i>Dhb</i>AFP isoform (~10 kDa) appeared to consist of 6−8 tandem repeats of a 12-residue consensus sequence (TCTxSxNCxxAx), which exhibited 3 °C of high freezing point depression and the ability of binding to an entire surface of a single ice crystal. Significantly, these properties as well as DNA sequences including the untranslated region, signal peptide region, and an AFP-encoding region of <i>Dhb</i> are highly similar to those identified for a known hyperactive AFP (<i>Tm</i>AFP) from the beetle <i>Tenebrio molitor</i> (<i>Tm</i>). Progenitor of <i>Dhb</i> and <i>Tm</i> was branched off approximately 300 million years ago, so no known evolution mechanism hardly explains the retainment of the DNA sequence for such a long divergence period. Existence of unrevealed gene transfer mechanism will be hypothesized between these two phylogenetically distant beetles to acquire this type of hyperactive AFP.https://www.mdpi.com/1422-0067/22/7/3637antifreeze protein (AFP)thermal hysteresis (TH)stag beetleice bindingfreeze avoidancesupercooling |
| spellingShingle | Tatsuya Arai Akari Yamauchi Ai Miura Hidemasa Kondo Yoshiyuki Nishimiya Yuji C. Sasaki Sakae Tsuda Discovery of Hyperactive Antifreeze Protein from Phylogenetically Distant Beetles Questions Its Evolutionary Origin International Journal of Molecular Sciences antifreeze protein (AFP) thermal hysteresis (TH) stag beetle ice binding freeze avoidance supercooling |
| title | Discovery of Hyperactive Antifreeze Protein from Phylogenetically Distant Beetles Questions Its Evolutionary Origin |
| title_full | Discovery of Hyperactive Antifreeze Protein from Phylogenetically Distant Beetles Questions Its Evolutionary Origin |
| title_fullStr | Discovery of Hyperactive Antifreeze Protein from Phylogenetically Distant Beetles Questions Its Evolutionary Origin |
| title_full_unstemmed | Discovery of Hyperactive Antifreeze Protein from Phylogenetically Distant Beetles Questions Its Evolutionary Origin |
| title_short | Discovery of Hyperactive Antifreeze Protein from Phylogenetically Distant Beetles Questions Its Evolutionary Origin |
| title_sort | discovery of hyperactive antifreeze protein from phylogenetically distant beetles questions its evolutionary origin |
| topic | antifreeze protein (AFP) thermal hysteresis (TH) stag beetle ice binding freeze avoidance supercooling |
| url | https://www.mdpi.com/1422-0067/22/7/3637 |
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