Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses
Vibrio cholerae is a common waterborne pathogen that can cause pandemic cholera in humans. The bacterium with heavy metal-tolerant phenotypes is frequently isolated from aquatic products, however, its tolerance mechanisms remain unclear. In this study, we investigated for the first time the response...
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Frontiers Media S.A.
2023-10-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1294177/full |
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| author | Beiyu Zhang Beiyu Zhang Jingjing Xu Jingjing Xu Meng Sun Meng Sun Pan Yu Pan Yu Yuming Ma Yuming Ma Lu Xie Lanming Chen Lanming Chen |
| author_facet | Beiyu Zhang Beiyu Zhang Jingjing Xu Jingjing Xu Meng Sun Meng Sun Pan Yu Pan Yu Yuming Ma Yuming Ma Lu Xie Lanming Chen Lanming Chen |
| author_sort | Beiyu Zhang |
| collection | DOAJ |
| description | Vibrio cholerae is a common waterborne pathogen that can cause pandemic cholera in humans. The bacterium with heavy metal-tolerant phenotypes is frequently isolated from aquatic products, however, its tolerance mechanisms remain unclear. In this study, we investigated for the first time the response of such V. cholerae isolates (n = 3) toward the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses by comparative secretomic and proteomic analyses. The results showed that sublethal concentrations of the Pb2+ (200 μg/mL), Cd2+ (12.5 μg/mL), and Zn2+ (50 μg/mL) stresses for 2 h significantly decreased the bacterial cell membrane fluidity, but increased cell surface hydrophobicity and inner membrane permeability, whereas the Ni2+ (50 μg/mL) stress increased cell membrane fluidity (p < 0.05). The comparative secretomic and proteomic analysis revealed differentially expressed extracellular and intracellular proteins involved in common metabolic pathways in the V. cholerae isolates to reduce cytotoxicity of the heavy metal stresses, such as biosorption, transportation and effluxing, extracellular sequestration, and intracellular antioxidative defense. Meanwhile, different defensive strategies were also found in the V. cholerae isolates to cope with different heavy metal damage. Remarkably, a number of putative virulence and resistance-associated proteins were produced and/or secreted by the V. cholerae isolates under the heavy metal stresses, suggesting an increased health risk in the aquatic products. |
| first_indexed | 2024-03-11T15:38:20Z |
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| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-11T15:38:20Z |
| publishDate | 2023-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-a36fa90cb61f46bfac9f18f413155e642023-10-26T13:33:40ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-10-011410.3389/fmicb.2023.12941771294177Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stressesBeiyu Zhang0Beiyu Zhang1Jingjing Xu2Jingjing Xu3Meng Sun4Meng Sun5Pan Yu6Pan Yu7Yuming Ma8Yuming Ma9Lu Xie10Lanming Chen11Lanming Chen12Key Laboratory of Quality and Safety Risk Assessment for Aquatic Products on Storage and Preservation (Shanghai), Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Shanghai, ChinaCollege of Food Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Quality and Safety Risk Assessment for Aquatic Products on Storage and Preservation (Shanghai), Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Shanghai, ChinaCollege of Food Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Quality and Safety Risk Assessment for Aquatic Products on Storage and Preservation (Shanghai), Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Shanghai, ChinaCollege of Food Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Quality and Safety Risk Assessment for Aquatic Products on Storage and Preservation (Shanghai), Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Shanghai, ChinaCollege of Food Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Quality and Safety Risk Assessment for Aquatic Products on Storage and Preservation (Shanghai), Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Shanghai, ChinaCollege of Food Science and Technology, Shanghai Ocean University, Shanghai, ChinaShanghai-MOST Key Laboratory of Health and Disease Genomics (Chinese National Human Genome Center at Shanghai), Institute of Genome and Bioinformatics, Shanghai Institute for Biomedical and Pharmaceutical Technologies, Shanghai, ChinaKey Laboratory of Quality and Safety Risk Assessment for Aquatic Products on Storage and Preservation (Shanghai), Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Shanghai, ChinaCollege of Food Science and Technology, Shanghai Ocean University, Shanghai, ChinaVibrio cholerae is a common waterborne pathogen that can cause pandemic cholera in humans. The bacterium with heavy metal-tolerant phenotypes is frequently isolated from aquatic products, however, its tolerance mechanisms remain unclear. In this study, we investigated for the first time the response of such V. cholerae isolates (n = 3) toward the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses by comparative secretomic and proteomic analyses. The results showed that sublethal concentrations of the Pb2+ (200 μg/mL), Cd2+ (12.5 μg/mL), and Zn2+ (50 μg/mL) stresses for 2 h significantly decreased the bacterial cell membrane fluidity, but increased cell surface hydrophobicity and inner membrane permeability, whereas the Ni2+ (50 μg/mL) stress increased cell membrane fluidity (p < 0.05). The comparative secretomic and proteomic analysis revealed differentially expressed extracellular and intracellular proteins involved in common metabolic pathways in the V. cholerae isolates to reduce cytotoxicity of the heavy metal stresses, such as biosorption, transportation and effluxing, extracellular sequestration, and intracellular antioxidative defense. Meanwhile, different defensive strategies were also found in the V. cholerae isolates to cope with different heavy metal damage. Remarkably, a number of putative virulence and resistance-associated proteins were produced and/or secreted by the V. cholerae isolates under the heavy metal stresses, suggesting an increased health risk in the aquatic products.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1294177/fullVibrio choleraeheavy metalsecretomeproteometolerance mechanismfood safety |
| spellingShingle | Beiyu Zhang Beiyu Zhang Jingjing Xu Jingjing Xu Meng Sun Meng Sun Pan Yu Pan Yu Yuming Ma Yuming Ma Lu Xie Lanming Chen Lanming Chen Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses Frontiers in Microbiology Vibrio cholerae heavy metal secretome proteome tolerance mechanism food safety |
| title | Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses |
| title_full | Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses |
| title_fullStr | Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses |
| title_full_unstemmed | Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses |
| title_short | Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses |
| title_sort | comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by vibrio cholerae against the heavy metal cd2 ni2 pb2 and zn2 stresses |
| topic | Vibrio cholerae heavy metal secretome proteome tolerance mechanism food safety |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1294177/full |
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