Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification

Ocean acidification (OA) has posed formidable threats to marine calcifiers. In response to elevated CO2 levels, marine calcifiers have developed multiple strategies to survive, such as taking advantage of apoptosis, but its regulation mechanism remains largely unknown. Here, we used the Pacific oyst...

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Main Authors: Xiudan Wang, Changmei Li, Zhihao Jia, Tongxiao Xu, Yilin Wang, Mingzhu Sun, Shuhui Han, Xia Wang, Limei Qiu
Format: Article
Language:English
Published: Elsevier 2021-07-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651321003468
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author Xiudan Wang
Changmei Li
Zhihao Jia
Tongxiao Xu
Yilin Wang
Mingzhu Sun
Shuhui Han
Xia Wang
Limei Qiu
author_facet Xiudan Wang
Changmei Li
Zhihao Jia
Tongxiao Xu
Yilin Wang
Mingzhu Sun
Shuhui Han
Xia Wang
Limei Qiu
author_sort Xiudan Wang
collection DOAJ
description Ocean acidification (OA) has posed formidable threats to marine calcifiers. In response to elevated CO2 levels, marine calcifiers have developed multiple strategies to survive, such as taking advantage of apoptosis, but its regulation mechanism remains largely unknown. Here, we used the Pacific oyster Crassostrea gigas as model to understand the apoptotic responses and regulation mechanism at short- (7 d) to long-term (56 d) CO2 exposure (pH = 7.50). The apoptosis of hemocytes was significantly induced after short-term treatment (7–21 d) but was suppressed under long-term CO2 exposure (42–56 d). Similarly, caspase-3 and caspase-9 were also increased post short-term exposure and fell back to normal levels after long-term exposure. These data together indicated diverse regulation mechanisms of apoptosis through different exposure periods. Through analysis of the B-cell lymphoma 2 (Bcl-2) family mitochondrial apoptosis regulators, we showed that only CgBcl-XL’s expression kept at high levels after 42- and 56-day CO2 exposure. CgBcl-XL shared sequence, and structural similarity with its mammalian counterpart, and knockdown of CgBcl-XL in hemocytes via RNA interference promoted apoptosis. The protein level of CgBcl-XL was significantly increased after long-term CO2 exposure (28–56 d), and its distribution in hemocytes became more concentrated and dense. Therefore, CgBcl-XL serves as an essential anti-apoptotic protein for tipping the balance of cell apoptosis, which may play a key role in survival under long-term CO2 exposure. These results reveal a potential adaptation strategy of oysters towards OA and the variable environment changes through the modulation of apoptosis.
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spelling doaj.art-0da7568f83ac4b94932ae272df3fa0d02022-12-21T22:30:17ZengElsevierEcotoxicology and Environmental Safety0147-65132021-07-01217112235Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidificationXiudan Wang0Changmei Li1Zhihao Jia2Tongxiao Xu3Yilin Wang4Mingzhu Sun5Shuhui Han6Xia Wang7Limei Qiu8Shandong Provincial Key Laboratory of Biochemical Engineering, College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao 266042, ChinaShandong Provincial Key Laboratory of Biochemical Engineering, College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao 266042, ChinaCambridge-Suda Genomic Resource Center, Soochow University, Suzhou 215123, ChinaShandong Provincial Key Laboratory of Biochemical Engineering, College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao 266042, ChinaShandong Provincial Key Laboratory of Biochemical Engineering, College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao 266042, ChinaShandong Provincial Key Laboratory of Biochemical Engineering, College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao 266042, ChinaShandong Provincial Key Laboratory of Biochemical Engineering, College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao 266042, ChinaShandong Provincial Key Laboratory of Biochemical Engineering, College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao 266042, China; Correspondence to: Qingdao University of Science and Technology, 42 Zhengzhou Street, Qingdao 266042, China.CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China; Correspondence to: Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Street, Qingdao 266003, China.Ocean acidification (OA) has posed formidable threats to marine calcifiers. In response to elevated CO2 levels, marine calcifiers have developed multiple strategies to survive, such as taking advantage of apoptosis, but its regulation mechanism remains largely unknown. Here, we used the Pacific oyster Crassostrea gigas as model to understand the apoptotic responses and regulation mechanism at short- (7 d) to long-term (56 d) CO2 exposure (pH = 7.50). The apoptosis of hemocytes was significantly induced after short-term treatment (7–21 d) but was suppressed under long-term CO2 exposure (42–56 d). Similarly, caspase-3 and caspase-9 were also increased post short-term exposure and fell back to normal levels after long-term exposure. These data together indicated diverse regulation mechanisms of apoptosis through different exposure periods. Through analysis of the B-cell lymphoma 2 (Bcl-2) family mitochondrial apoptosis regulators, we showed that only CgBcl-XL’s expression kept at high levels after 42- and 56-day CO2 exposure. CgBcl-XL shared sequence, and structural similarity with its mammalian counterpart, and knockdown of CgBcl-XL in hemocytes via RNA interference promoted apoptosis. The protein level of CgBcl-XL was significantly increased after long-term CO2 exposure (28–56 d), and its distribution in hemocytes became more concentrated and dense. Therefore, CgBcl-XL serves as an essential anti-apoptotic protein for tipping the balance of cell apoptosis, which may play a key role in survival under long-term CO2 exposure. These results reveal a potential adaptation strategy of oysters towards OA and the variable environment changes through the modulation of apoptosis.http://www.sciencedirect.com/science/article/pii/S0147651321003468Ocean acidificationCrassostrea gigasApoptosisCgBcl-XL
spellingShingle Xiudan Wang
Changmei Li
Zhihao Jia
Tongxiao Xu
Yilin Wang
Mingzhu Sun
Shuhui Han
Xia Wang
Limei Qiu
Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification
Ecotoxicology and Environmental Safety
Ocean acidification
Crassostrea gigas
Apoptosis
CgBcl-XL
title Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification
title_full Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification
title_fullStr Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification
title_full_unstemmed Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification
title_short Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification
title_sort regulation of apoptosis by pacific oyster crassostrea gigas reveals acclimation strategy to co2 driven acidification
topic Ocean acidification
Crassostrea gigas
Apoptosis
CgBcl-XL
url http://www.sciencedirect.com/science/article/pii/S0147651321003468
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