Virulence of Vibrio alginolyticus Accentuates Apoptosis and Immune Rigor in the Oyster Crassostrea hongkongensis
Vibrio species are ubiquitously distributed in marine environments, with important implications for emerging infectious diseases. However, relatively little is known about defensive strategies deployed by hosts against Vibrio pathogens of distinct virulence traits. Being an ecologically relevant hos...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-09-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.746017/full |
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| author | Fan Mao Fan Mao Kunna Liu Kunna Liu Kunna Liu Nai-Kei Wong Nai-Kei Wong Xiangyu Zhang Xiangyu Zhang Xiangyu Zhang Wenjie Yi Wenjie Yi Wenjie Yi Zhiming Xiang Zhiming Xiang Shu Xiao Shu Xiao Ziniu Yu Ziniu Yu Yang Zhang Yang Zhang |
| author_facet | Fan Mao Fan Mao Kunna Liu Kunna Liu Kunna Liu Nai-Kei Wong Nai-Kei Wong Xiangyu Zhang Xiangyu Zhang Xiangyu Zhang Wenjie Yi Wenjie Yi Wenjie Yi Zhiming Xiang Zhiming Xiang Shu Xiao Shu Xiao Ziniu Yu Ziniu Yu Yang Zhang Yang Zhang |
| author_sort | Fan Mao |
| collection | DOAJ |
| description | Vibrio species are ubiquitously distributed in marine environments, with important implications for emerging infectious diseases. However, relatively little is known about defensive strategies deployed by hosts against Vibrio pathogens of distinct virulence traits. Being an ecologically relevant host, the oyster Crassostrea hongkongensis can serve as an excellent model for elucidating mechanisms underlying host-Vibrio interactions. We generated a Vibrio alginolyticus mutant strain (V. alginolyticus△vscC) with attenuated virulence by knocking out the vscC encoding gene, a core component of type III secretion system (T3SS), which led to starkly reduced apoptotic rates in hemocyte hosts compared to the V. alginolyticusWT control. In comparative proteomics, it was revealed that distinct immune responses arose upon encounter with V. alginolyticus strains of different virulence. Quite strikingly, the peroxisomal and apoptotic pathways are activated by V. alginolyticusWT infection, whereas phagocytosis and cell adhesion were enhanced in V. alginolyticus△vscC infection. Results for functional studies further show that V. alginolyticusWT strain stimulated respiratory bursts to produce excess superoxide (O2•−) and hydrogen peroxide (H2O2) in oysters, which induced apoptosis regulated by p53 target protein (p53tp). Simultaneously, a drop in sGC content balanced off cGMP accumulation in hemocytes and repressed the occurrence of apoptosis to a certain extent during V. alginolyticus△vscC infection. We have thus provided the first direct evidence for a mechanistic link between virulence of Vibrio spp. and its immunomodulation effects on apoptosis in the oyster. Collectively, we conclude that adaptive responses in host defenses are partially determined by pathogen virulence, in order to safeguard efficiency and timeliness in bacterial clearance. |
| first_indexed | 2024-12-17T20:05:30Z |
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| id | doaj.art-9a33b90b5d2a4d9ab3423db99d66a310 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-17T20:05:30Z |
| publishDate | 2021-09-01 |
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| series | Frontiers in Immunology |
| spelling | doaj.art-9a33b90b5d2a4d9ab3423db99d66a3102022-12-21T21:34:20ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-09-011210.3389/fimmu.2021.746017746017Virulence of Vibrio alginolyticus Accentuates Apoptosis and Immune Rigor in the Oyster Crassostrea hongkongensisFan Mao0Fan Mao1Kunna Liu2Kunna Liu3Kunna Liu4Nai-Kei Wong5Nai-Kei Wong6Xiangyu Zhang7Xiangyu Zhang8Xiangyu Zhang9Wenjie Yi10Wenjie Yi11Wenjie Yi12Zhiming Xiang13Zhiming Xiang14Shu Xiao15Shu Xiao16Ziniu Yu17Ziniu Yu18Yang Zhang19Yang Zhang20Chinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, ChinaChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, ChinaCollege of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, ChinaChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaDepartment of Pharmacology, Shantou University Medical College, Shantou, ChinaChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, ChinaCollege of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, ChinaChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, ChinaCollege of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, ChinaChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, ChinaChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, ChinaChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, ChinaChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, ChinaVibrio species are ubiquitously distributed in marine environments, with important implications for emerging infectious diseases. However, relatively little is known about defensive strategies deployed by hosts against Vibrio pathogens of distinct virulence traits. Being an ecologically relevant host, the oyster Crassostrea hongkongensis can serve as an excellent model for elucidating mechanisms underlying host-Vibrio interactions. We generated a Vibrio alginolyticus mutant strain (V. alginolyticus△vscC) with attenuated virulence by knocking out the vscC encoding gene, a core component of type III secretion system (T3SS), which led to starkly reduced apoptotic rates in hemocyte hosts compared to the V. alginolyticusWT control. In comparative proteomics, it was revealed that distinct immune responses arose upon encounter with V. alginolyticus strains of different virulence. Quite strikingly, the peroxisomal and apoptotic pathways are activated by V. alginolyticusWT infection, whereas phagocytosis and cell adhesion were enhanced in V. alginolyticus△vscC infection. Results for functional studies further show that V. alginolyticusWT strain stimulated respiratory bursts to produce excess superoxide (O2•−) and hydrogen peroxide (H2O2) in oysters, which induced apoptosis regulated by p53 target protein (p53tp). Simultaneously, a drop in sGC content balanced off cGMP accumulation in hemocytes and repressed the occurrence of apoptosis to a certain extent during V. alginolyticus△vscC infection. We have thus provided the first direct evidence for a mechanistic link between virulence of Vibrio spp. and its immunomodulation effects on apoptosis in the oyster. Collectively, we conclude that adaptive responses in host defenses are partially determined by pathogen virulence, in order to safeguard efficiency and timeliness in bacterial clearance.https://www.frontiersin.org/articles/10.3389/fimmu.2021.746017/fullVibrio alginolyticusoystervirulencehost-pathogen interactionsproteomics |
| spellingShingle | Fan Mao Fan Mao Kunna Liu Kunna Liu Kunna Liu Nai-Kei Wong Nai-Kei Wong Xiangyu Zhang Xiangyu Zhang Xiangyu Zhang Wenjie Yi Wenjie Yi Wenjie Yi Zhiming Xiang Zhiming Xiang Shu Xiao Shu Xiao Ziniu Yu Ziniu Yu Yang Zhang Yang Zhang Virulence of Vibrio alginolyticus Accentuates Apoptosis and Immune Rigor in the Oyster Crassostrea hongkongensis Frontiers in Immunology Vibrio alginolyticus oyster virulence host-pathogen interactions proteomics |
| title | Virulence of Vibrio alginolyticus Accentuates Apoptosis and Immune Rigor in the Oyster Crassostrea hongkongensis |
| title_full | Virulence of Vibrio alginolyticus Accentuates Apoptosis and Immune Rigor in the Oyster Crassostrea hongkongensis |
| title_fullStr | Virulence of Vibrio alginolyticus Accentuates Apoptosis and Immune Rigor in the Oyster Crassostrea hongkongensis |
| title_full_unstemmed | Virulence of Vibrio alginolyticus Accentuates Apoptosis and Immune Rigor in the Oyster Crassostrea hongkongensis |
| title_short | Virulence of Vibrio alginolyticus Accentuates Apoptosis and Immune Rigor in the Oyster Crassostrea hongkongensis |
| title_sort | virulence of vibrio alginolyticus accentuates apoptosis and immune rigor in the oyster crassostrea hongkongensis |
| topic | Vibrio alginolyticus oyster virulence host-pathogen interactions proteomics |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.746017/full |
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