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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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Autores principales: Hara, Yuichiro, Shibahara, Reira, Kondo, Koyuki, Abe, Wataru, Kunieda, Takekazu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8277472/
https://www.ncbi.nlm.nih.gov/pubmed/34255978
http://dx.doi.org/10.1098/rsob.200413
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author Hara, Yuichiro
Shibahara, Reira
Kondo, Koyuki
Abe, Wataru
Kunieda, Takekazu
author_facet Hara, Yuichiro
Shibahara, Reira
Kondo, Koyuki
Abe, Wataru
Kunieda, Takekazu
author_sort Hara, Yuichiro
collection PubMed
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.
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spelling pubmed-82774722021-07-22 Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer Hara, Yuichiro Shibahara, Reira Kondo, Koyuki Abe, Wataru Kunieda, Takekazu Open Biol Research 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. The Royal Society 2021-07-14 /pmc/articles/PMC8277472/ /pubmed/34255978 http://dx.doi.org/10.1098/rsob.200413 Text en © 2021 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Research
Hara, Yuichiro
Shibahara, Reira
Kondo, Koyuki
Abe, Wataru
Kunieda, Takekazu
Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal 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 Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8277472/
https://www.ncbi.nlm.nih.gov/pubmed/34255978
http://dx.doi.org/10.1098/rsob.200413
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