Transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stress

High temperature and hypoxia greatly threaten marine life and aquaculture. Scallops, a diverse and ecologically important group of high economic value, mostly thrive in fluctuating environments, and are vulnerable to environmental stress. In the present study, the molecular response mechanism of sca...

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Main Authors: Junxia Mao, Xiaofang Huang, Hongyan Sun, Xin Jin, Wenjuan Guan, Jiahui Xie, Yiying Wang, Xubo Wang, Donghong Yin, Zhenlin Hao, Ying Tian, Jian Song, Jun Ding, Yaqing Chang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2022.971796/full
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author Junxia Mao
Xiaofang Huang
Hongyan Sun
Xin Jin
Wenjuan Guan
Jiahui Xie
Yiying Wang
Xubo Wang
Donghong Yin
Zhenlin Hao
Ying Tian
Jian Song
Jun Ding
Yaqing Chang
author_facet Junxia Mao
Xiaofang Huang
Hongyan Sun
Xin Jin
Wenjuan Guan
Jiahui Xie
Yiying Wang
Xubo Wang
Donghong Yin
Zhenlin Hao
Ying Tian
Jian Song
Jun Ding
Yaqing Chang
author_sort Junxia Mao
collection DOAJ
description High temperature and hypoxia greatly threaten marine life and aquaculture. Scallops, a diverse and ecologically important group of high economic value, mostly thrive in fluctuating environments, and are vulnerable to environmental stress. In the present study, the molecular response mechanism of scallops to a combination of environmental stressors was investigated via transcriptome analysis of the gill tissues in three scallop species, the Yesso scallop (Patinopecten yessoensis), Zhikong scallop (Chlamys farreri) and bay scallop (Argopecten irradians) that were exposed to transient heat, hypoxia and a combination thereof. The Yesso scallop had the most differentially expressed genes (DEGs) compared with the other two scallop species, indicating the highest sensitivity of the Yesso scallop to environmental stress. With increased temperature and decreased dissolved oxygen, the number of DEGs was greatly increased in the three scallop species, indicative of the enhancement in gene expression regulation in scallops in response to severe environmental changes. Heat and hypoxia had a synergistic effect on scallops. GO and KEGG enrichment analysis of DEGs under different stressors revealed overlapping molecular mechanisms of response in scallops following exposure to heat and hypoxia. Several immune and apoptosis-related pathways were highly enriched in the upregulated DEGs of the three scallops, suggesting that immune system activation and apoptosis promotion occurred in scallops in response to environmental stress. Heat shock proteins (HSPs) were significantly upregulated under heat and hypoxia, which likely assisted in correct protein folding to facilitate the adaption of the scallops to the altered environment. Additionally, the HIF-1 signaling pathway—the key pathway associated with hypoxia response—was triggered by extremely acute environmental changes. Comparative transcriptome analysis revealed 239 positively selected genes among the different scallops, including those involved in immune system and environmental adaptation, suggesting a long-term mechanism of environmental adaptation. The present study provides new insights into the molecular response mechanism in scallops to multiple environmental stressors and improves our understanding of the adaptive mechanisms of marine organisms under changing global climate conditions.
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spelling doaj.art-3f1638d302d34565948a568ce96ef25b2022-12-22T01:44:26ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-09-01910.3389/fmars.2022.971796971796Transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stressJunxia MaoXiaofang HuangHongyan SunXin JinWenjuan GuanJiahui XieYiying WangXubo WangDonghong YinZhenlin HaoYing TianJian SongJun DingYaqing ChangHigh temperature and hypoxia greatly threaten marine life and aquaculture. Scallops, a diverse and ecologically important group of high economic value, mostly thrive in fluctuating environments, and are vulnerable to environmental stress. In the present study, the molecular response mechanism of scallops to a combination of environmental stressors was investigated via transcriptome analysis of the gill tissues in three scallop species, the Yesso scallop (Patinopecten yessoensis), Zhikong scallop (Chlamys farreri) and bay scallop (Argopecten irradians) that were exposed to transient heat, hypoxia and a combination thereof. The Yesso scallop had the most differentially expressed genes (DEGs) compared with the other two scallop species, indicating the highest sensitivity of the Yesso scallop to environmental stress. With increased temperature and decreased dissolved oxygen, the number of DEGs was greatly increased in the three scallop species, indicative of the enhancement in gene expression regulation in scallops in response to severe environmental changes. Heat and hypoxia had a synergistic effect on scallops. GO and KEGG enrichment analysis of DEGs under different stressors revealed overlapping molecular mechanisms of response in scallops following exposure to heat and hypoxia. Several immune and apoptosis-related pathways were highly enriched in the upregulated DEGs of the three scallops, suggesting that immune system activation and apoptosis promotion occurred in scallops in response to environmental stress. Heat shock proteins (HSPs) were significantly upregulated under heat and hypoxia, which likely assisted in correct protein folding to facilitate the adaption of the scallops to the altered environment. Additionally, the HIF-1 signaling pathway—the key pathway associated with hypoxia response—was triggered by extremely acute environmental changes. Comparative transcriptome analysis revealed 239 positively selected genes among the different scallops, including those involved in immune system and environmental adaptation, suggesting a long-term mechanism of environmental adaptation. The present study provides new insights into the molecular response mechanism in scallops to multiple environmental stressors and improves our understanding of the adaptive mechanisms of marine organisms under changing global climate conditions.https://www.frontiersin.org/articles/10.3389/fmars.2022.971796/fullscallopsheathypoxiatranscriptomeresponse mechanism
spellingShingle Junxia Mao
Xiaofang Huang
Hongyan Sun
Xin Jin
Wenjuan Guan
Jiahui Xie
Yiying Wang
Xubo Wang
Donghong Yin
Zhenlin Hao
Ying Tian
Jian Song
Jun Ding
Yaqing Chang
Transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stress
Frontiers in Marine Science
scallops
heat
hypoxia
transcriptome
response mechanism
title Transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stress
title_full Transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stress
title_fullStr Transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stress
title_full_unstemmed Transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stress
title_short Transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stress
title_sort transcriptome analysis provides insight into adaptive mechanisms of scallops under environmental stress
topic scallops
heat
hypoxia
transcriptome
response mechanism
url https://www.frontiersin.org/articles/10.3389/fmars.2022.971796/full
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