The genomic basis for colonizing the freezing Southern Ocean revealed by Antarctic toothfish and Patagonian robalo genomes

Liangbiao Chen, Ying Lu, Wenhao Li, Yandong Ren, Mengchao Yu, Shouwen Jiang, Yanxia Fu, Jian Wang, Sihua Peng, Kevin T. Bilyk, Katherine R. Murphy, Xuan Zhuang, Mathias Hune, Wanying Zhai, Wen Wang, Qianghua Xu, Chi Hing Christina Cheng

Research output: Contribution to journalArticle

Abstract

BACKGROUND: The Southern Ocean is the coldest ocean on Earth but a hot spot of evolution. The bottom-dwelling Eocene ancestor of Antarctic notothenioid fishes survived polar marine glaciation and underwent adaptive radiation, forming >120 species that fill all water column niches today. Genome-wide changes enabling physiological adaptations and the rapid expansion of the Antarctic notothenioids remain poorly understood. RESULTS: We sequenced and compared 2 notothenioid genomes-the cold-adapted and neutrally buoyant Antarctic toothfish Dissostichus mawsoni and the basal Patagonian robalo Eleginops maclovinus, representing the temperate ancestor. We detected >200 protein gene families that had expanded and thousands of genes that had evolved faster in the toothfish, with diverse cold-relevant functions including stress response, lipid metabolism, protein homeostasis, and freeze resistance. Besides antifreeze glycoprotein, an eggshell protein had functionally diversified to aid in cellular freezing resistance. Genomic and transcriptomic comparisons revealed proliferation of selcys-transfer RNA genes and broad transcriptional upregulation across anti-oxidative selenoproteins, signifying their prominent role in mitigating oxidative stress in the oxygen-rich Southern Ocean. We found expansion of transposable elements, temporally correlated to Antarctic notothenioid diversification. Additionally, the toothfish exhibited remarkable shifts in genetic programs towards enhanced fat cell differentiation and lipid storage, and promotion of chondrogenesis while inhibiting osteogenesis in bone development, collectively contributing to the achievement of neutral buoyancy and pelagicism. CONCLUSIONS: Our study revealed a comprehensive landscape of evolutionary changes essential for Antarctic notothenioid cold adaptation and ecological expansion. The 2 genomes are valuable resources for further exploration of mechanisms underlying the spectacular notothenioid radiation in the coldest marine environment.

Original languageEnglish (US)
JournalGigaScience
Volume8
Issue number4
DOIs
StatePublished - Apr 1 2019

Fingerprint

Freezing
Oceans and Seas
Genes
Genome
Proteins
Antifreeze Proteins
Selenoproteins
Radiation
Physiological Adaptation
Chondrogenesis
DNA Transposable Elements
Bone Development
Glycoproteins
Transfer RNA
Oxidative stress
Lipid Metabolism
Adipocytes
Osteogenesis
Cell Differentiation
Oils and fats

Keywords

  • Antarctic notothenioids
  • adaptive radiation
  • climate change
  • genome
  • oxidative stress

ASJC Scopus subject areas

  • Computer Science Applications
  • Health Informatics

Cite this

The genomic basis for colonizing the freezing Southern Ocean revealed by Antarctic toothfish and Patagonian robalo genomes. / Chen, Liangbiao; Lu, Ying; Li, Wenhao; Ren, Yandong; Yu, Mengchao; Jiang, Shouwen; Fu, Yanxia; Wang, Jian; Peng, Sihua; Bilyk, Kevin T.; Murphy, Katherine R.; Zhuang, Xuan; Hune, Mathias; Zhai, Wanying; Wang, Wen; Xu, Qianghua; Cheng, Chi Hing Christina.

In: GigaScience, Vol. 8, No. 4, 01.04.2019.

Research output: Contribution to journalArticle

Chen, L, Lu, Y, Li, W, Ren, Y, Yu, M, Jiang, S, Fu, Y, Wang, J, Peng, S, Bilyk, KT, Murphy, KR, Zhuang, X, Hune, M, Zhai, W, Wang, W, Xu, Q & Cheng, CHC 2019, 'The genomic basis for colonizing the freezing Southern Ocean revealed by Antarctic toothfish and Patagonian robalo genomes', GigaScience, vol. 8, no. 4. https://doi.org/10.1093/gigascience/giz016
Chen, Liangbiao ; Lu, Ying ; Li, Wenhao ; Ren, Yandong ; Yu, Mengchao ; Jiang, Shouwen ; Fu, Yanxia ; Wang, Jian ; Peng, Sihua ; Bilyk, Kevin T. ; Murphy, Katherine R. ; Zhuang, Xuan ; Hune, Mathias ; Zhai, Wanying ; Wang, Wen ; Xu, Qianghua ; Cheng, Chi Hing Christina. / The genomic basis for colonizing the freezing Southern Ocean revealed by Antarctic toothfish and Patagonian robalo genomes. In: GigaScience. 2019 ; Vol. 8, No. 4.
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AU - Chen, Liangbiao

AU - Lu, Ying

AU - Li, Wenhao

AU - Ren, Yandong

AU - Yu, Mengchao

AU - Jiang, Shouwen

AU - Fu, Yanxia

AU - Wang, Jian

AU - Peng, Sihua

AU - Bilyk, Kevin T.

AU - Murphy, Katherine R.

AU - Zhuang, Xuan

AU - Hune, Mathias

AU - Zhai, Wanying

AU - Wang, Wen

AU - Xu, Qianghua

AU - Cheng, Chi Hing Christina

PY - 2019/4/1

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N2 - BACKGROUND: The Southern Ocean is the coldest ocean on Earth but a hot spot of evolution. The bottom-dwelling Eocene ancestor of Antarctic notothenioid fishes survived polar marine glaciation and underwent adaptive radiation, forming >120 species that fill all water column niches today. Genome-wide changes enabling physiological adaptations and the rapid expansion of the Antarctic notothenioids remain poorly understood. RESULTS: We sequenced and compared 2 notothenioid genomes-the cold-adapted and neutrally buoyant Antarctic toothfish Dissostichus mawsoni and the basal Patagonian robalo Eleginops maclovinus, representing the temperate ancestor. We detected >200 protein gene families that had expanded and thousands of genes that had evolved faster in the toothfish, with diverse cold-relevant functions including stress response, lipid metabolism, protein homeostasis, and freeze resistance. Besides antifreeze glycoprotein, an eggshell protein had functionally diversified to aid in cellular freezing resistance. Genomic and transcriptomic comparisons revealed proliferation of selcys-transfer RNA genes and broad transcriptional upregulation across anti-oxidative selenoproteins, signifying their prominent role in mitigating oxidative stress in the oxygen-rich Southern Ocean. We found expansion of transposable elements, temporally correlated to Antarctic notothenioid diversification. Additionally, the toothfish exhibited remarkable shifts in genetic programs towards enhanced fat cell differentiation and lipid storage, and promotion of chondrogenesis while inhibiting osteogenesis in bone development, collectively contributing to the achievement of neutral buoyancy and pelagicism. CONCLUSIONS: Our study revealed a comprehensive landscape of evolutionary changes essential for Antarctic notothenioid cold adaptation and ecological expansion. The 2 genomes are valuable resources for further exploration of mechanisms underlying the spectacular notothenioid radiation in the coldest marine environment.

AB - BACKGROUND: The Southern Ocean is the coldest ocean on Earth but a hot spot of evolution. The bottom-dwelling Eocene ancestor of Antarctic notothenioid fishes survived polar marine glaciation and underwent adaptive radiation, forming >120 species that fill all water column niches today. Genome-wide changes enabling physiological adaptations and the rapid expansion of the Antarctic notothenioids remain poorly understood. RESULTS: We sequenced and compared 2 notothenioid genomes-the cold-adapted and neutrally buoyant Antarctic toothfish Dissostichus mawsoni and the basal Patagonian robalo Eleginops maclovinus, representing the temperate ancestor. We detected >200 protein gene families that had expanded and thousands of genes that had evolved faster in the toothfish, with diverse cold-relevant functions including stress response, lipid metabolism, protein homeostasis, and freeze resistance. Besides antifreeze glycoprotein, an eggshell protein had functionally diversified to aid in cellular freezing resistance. Genomic and transcriptomic comparisons revealed proliferation of selcys-transfer RNA genes and broad transcriptional upregulation across anti-oxidative selenoproteins, signifying their prominent role in mitigating oxidative stress in the oxygen-rich Southern Ocean. We found expansion of transposable elements, temporally correlated to Antarctic notothenioid diversification. Additionally, the toothfish exhibited remarkable shifts in genetic programs towards enhanced fat cell differentiation and lipid storage, and promotion of chondrogenesis while inhibiting osteogenesis in bone development, collectively contributing to the achievement of neutral buoyancy and pelagicism. CONCLUSIONS: Our study revealed a comprehensive landscape of evolutionary changes essential for Antarctic notothenioid cold adaptation and ecological expansion. The 2 genomes are valuable resources for further exploration of mechanisms underlying the spectacular notothenioid radiation in the coldest marine environment.

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KW - adaptive radiation

KW - climate change

KW - genome

KW - oxidative stress

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