Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer
Trehalose is a versatile non-reducing sugar. In some animal groups possessing its intrinsic production machinery, it is used as a potent protectant against environmental stresses, as well as blood sugar. However, the trehalose biosynthesis genes remain unidentified in the large majority of metazoan...
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| Format: | Article |
| Language: | English |
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The Royal Society
2021-07-01
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| Series: | Open Biology |
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| Online Access: | https://royalsocietypublishing.org/doi/10.1098/rsob.200413 |
| _version_ | 1811185769006497792 |
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| author | Yuichiro Hara Reira Shibahara Koyuki Kondo Wataru Abe Takekazu Kunieda |
| author_facet | Yuichiro Hara Reira Shibahara Koyuki Kondo Wataru Abe Takekazu Kunieda |
| author_sort | Yuichiro Hara |
| collection | DOAJ |
| description | Trehalose is a versatile non-reducing sugar. In some animal groups possessing its intrinsic production machinery, it is used as a potent protectant against environmental stresses, as well as blood sugar. However, the trehalose biosynthesis genes remain unidentified in the large majority of metazoan phyla, including vertebrates. To uncover the evolutionary history of trehalose production machinery in metazoans, we scrutinized the available genome resources and identified bifunctional trehalose-6-phosphate synthase-trehalose-6-phosphate phosphatase (TPS–TPP) genes in various taxa. The scan included our newly sequenced genome assembly of a desiccation-tolerant tardigrade Paramacrobiotus sp. TYO, revealing that this species retains TPS–TPP genes activated upon desiccation. Phylogenetic analyses identified a monophyletic group of the many of the metazoan TPS–TPP genes, namely ‘pan-metazoan’ genes, that were acquired in the early ancestors of metazoans. Furthermore, coordination of our results with the previous horizontal gene transfer studies illuminated that the two tardigrade lineages, nematodes and bdelloid rotifers, all of which include desiccation-tolerant species, independently acquired the TPS–TPP homologues via horizontal transfer accompanied with loss of the ‘pan-metazoan’ genes. Our results indicate that the parallel evolution of trehalose synthesis via recurrent loss and horizontal transfer of the biosynthesis genes resulted in the acquisition and/or augmentation of anhydrobiotic lives in animals. |
| first_indexed | 2024-04-11T13:34:52Z |
| format | Article |
| id | doaj.art-e9da4dcb719940c182a8e61adee9de24 |
| institution | Directory Open Access Journal |
| issn | 2046-2441 |
| language | English |
| last_indexed | 2024-04-11T13:34:52Z |
| publishDate | 2021-07-01 |
| publisher | The Royal Society |
| record_format | Article |
| series | Open Biology |
| spelling | doaj.art-e9da4dcb719940c182a8e61adee9de242022-12-22T04:21:36ZengThe Royal SocietyOpen Biology2046-24412021-07-0111710.1098/rsob.200413Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transferYuichiro Hara0Reira Shibahara1Koyuki Kondo2Wataru Abe3Takekazu Kunieda4Research Center for Genome and Medical Sciences, Tokyo Metropolitan Institute of Medical Science, Tokyo, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biology, Dokkyo Medical University, Tochigi, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanTrehalose is a versatile non-reducing sugar. In some animal groups possessing its intrinsic production machinery, it is used as a potent protectant against environmental stresses, as well as blood sugar. However, the trehalose biosynthesis genes remain unidentified in the large majority of metazoan phyla, including vertebrates. To uncover the evolutionary history of trehalose production machinery in metazoans, we scrutinized the available genome resources and identified bifunctional trehalose-6-phosphate synthase-trehalose-6-phosphate phosphatase (TPS–TPP) genes in various taxa. The scan included our newly sequenced genome assembly of a desiccation-tolerant tardigrade Paramacrobiotus sp. TYO, revealing that this species retains TPS–TPP genes activated upon desiccation. Phylogenetic analyses identified a monophyletic group of the many of the metazoan TPS–TPP genes, namely ‘pan-metazoan’ genes, that were acquired in the early ancestors of metazoans. Furthermore, coordination of our results with the previous horizontal gene transfer studies illuminated that the two tardigrade lineages, nematodes and bdelloid rotifers, all of which include desiccation-tolerant species, independently acquired the TPS–TPP homologues via horizontal transfer accompanied with loss of the ‘pan-metazoan’ genes. Our results indicate that the parallel evolution of trehalose synthesis via recurrent loss and horizontal transfer of the biosynthesis genes resulted in the acquisition and/or augmentation of anhydrobiotic lives in animals.https://royalsocietypublishing.org/doi/10.1098/rsob.200413anhydrobiosisTPS–TPPparallel evolutiontrehalosetardigradehorizontal gene transfer |
| spellingShingle | Yuichiro Hara Reira Shibahara Koyuki Kondo Wataru Abe Takekazu Kunieda Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer Open Biology anhydrobiosis TPS–TPP parallel evolution trehalose tardigrade horizontal gene transfer |
| title | Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer |
| title_full | Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer |
| title_fullStr | Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer |
| title_full_unstemmed | Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer |
| title_short | Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer |
| title_sort | parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer |
| topic | anhydrobiosis TPS–TPP parallel evolution trehalose tardigrade horizontal gene transfer |
| url | https://royalsocietypublishing.org/doi/10.1098/rsob.200413 |
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