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Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea

Hadal environments (depths below 6,000 m) are characterized by extremely high hydrostatic pressures, low temperatures, a scarce food supply, and little light. The evolutionary adaptations that allow vertebrates to survive in this extreme environment are poorly understood. Here, we constructed a high...

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Autores principales: Mu, Yinnan, Bian, Chao, Liu, Ruoyu, Wang, Yuguang, Shao, Guangming, Li, Jia, Qiu, Ying, He, Tianliang, Li, Wanru, Ao, Jingqun, Shi, Qiong, Chen, Xinhua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8118300/
https://www.ncbi.nlm.nih.gov/pubmed/33983934
http://dx.doi.org/10.1371/journal.pgen.1009530
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author Mu, Yinnan
Bian, Chao
Liu, Ruoyu
Wang, Yuguang
Shao, Guangming
Li, Jia
Qiu, Ying
He, Tianliang
Li, Wanru
Ao, Jingqun
Shi, Qiong
Chen, Xinhua
author_facet Mu, Yinnan
Bian, Chao
Liu, Ruoyu
Wang, Yuguang
Shao, Guangming
Li, Jia
Qiu, Ying
He, Tianliang
Li, Wanru
Ao, Jingqun
Shi, Qiong
Chen, Xinhua
author_sort Mu, Yinnan
collection PubMed
description Hadal environments (depths below 6,000 m) are characterized by extremely high hydrostatic pressures, low temperatures, a scarce food supply, and little light. The evolutionary adaptations that allow vertebrates to survive in this extreme environment are poorly understood. Here, we constructed a high-quality reference genome for Yap hadal snailfish (YHS), which was captured at a depth of ~7,000 m in the Yap Trench. The final YHS genome assembly was 731.75 Mb, with a contig N50 of 0.75 Mb and a scaffold N50 of 1.26 Mb. We predicted 24,329 protein-coding genes in the YHS genome, and 24,265 of these genes were successfully functionally annotated. Phylogenetic analyses suggested that YHS diverged from a Mariana Trench snailfish approximately 0.92 million years ago. Many genes associated with DNA repair show evidence of positive selection and have expanded copy numbers in the YHS genome, possibly helping to maintain the integrity of DNA under increased hydrostatic pressure. The levels of trimethylamine N-oxide (TMAO), a potent protein stabilizer, are much higher in the muscles of YHS than in those of shallow-water fish. This difference is perhaps due to the five copies of the TMAO-generating enzyme flavin-containing monooxygenase-3 gene (fmo3) in the YHS genome and the abundance of trimethylamine (TMA)-generating bacteria in the YHS gut. Thus, the high TMAO content might help YHS adapt to high hydrostatic pressure by improving protein stability. Additionally, the evolutionary features of the YHS genes encoding sensory-related proteins are consistent with the scarce food supply and darkness in the hadal environments. These results clarify the molecular mechanisms underlying the adaptation of hadal organisms to the deep-sea environment and provide valuable genomic resources for in-depth investigations of hadal biology.
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spelling pubmed-81183002021-05-24 Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea Mu, Yinnan Bian, Chao Liu, Ruoyu Wang, Yuguang Shao, Guangming Li, Jia Qiu, Ying He, Tianliang Li, Wanru Ao, Jingqun Shi, Qiong Chen, Xinhua PLoS Genet Research Article Hadal environments (depths below 6,000 m) are characterized by extremely high hydrostatic pressures, low temperatures, a scarce food supply, and little light. The evolutionary adaptations that allow vertebrates to survive in this extreme environment are poorly understood. Here, we constructed a high-quality reference genome for Yap hadal snailfish (YHS), which was captured at a depth of ~7,000 m in the Yap Trench. The final YHS genome assembly was 731.75 Mb, with a contig N50 of 0.75 Mb and a scaffold N50 of 1.26 Mb. We predicted 24,329 protein-coding genes in the YHS genome, and 24,265 of these genes were successfully functionally annotated. Phylogenetic analyses suggested that YHS diverged from a Mariana Trench snailfish approximately 0.92 million years ago. Many genes associated with DNA repair show evidence of positive selection and have expanded copy numbers in the YHS genome, possibly helping to maintain the integrity of DNA under increased hydrostatic pressure. The levels of trimethylamine N-oxide (TMAO), a potent protein stabilizer, are much higher in the muscles of YHS than in those of shallow-water fish. This difference is perhaps due to the five copies of the TMAO-generating enzyme flavin-containing monooxygenase-3 gene (fmo3) in the YHS genome and the abundance of trimethylamine (TMA)-generating bacteria in the YHS gut. Thus, the high TMAO content might help YHS adapt to high hydrostatic pressure by improving protein stability. Additionally, the evolutionary features of the YHS genes encoding sensory-related proteins are consistent with the scarce food supply and darkness in the hadal environments. These results clarify the molecular mechanisms underlying the adaptation of hadal organisms to the deep-sea environment and provide valuable genomic resources for in-depth investigations of hadal biology. Public Library of Science 2021-05-13 /pmc/articles/PMC8118300/ /pubmed/33983934 http://dx.doi.org/10.1371/journal.pgen.1009530 Text en © 2021 Mu et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Mu, Yinnan
Bian, Chao
Liu, Ruoyu
Wang, Yuguang
Shao, Guangming
Li, Jia
Qiu, Ying
He, Tianliang
Li, Wanru
Ao, Jingqun
Shi, Qiong
Chen, Xinhua
Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea
title Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea
title_full Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea
title_fullStr Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea
title_full_unstemmed Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea
title_short Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea
title_sort whole genome sequencing of a snailfish from the yap trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8118300/
https://www.ncbi.nlm.nih.gov/pubmed/33983934
http://dx.doi.org/10.1371/journal.pgen.1009530
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