Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses

Beiyu Zhang; Jingjing Xu; Meng Sun; Pan Yu; Yuming Ma; Lu Xie; Lanming Chen

doi:10.3389/fmicb.2023.1294177

Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd²⁺, Ni²⁺, Pb²⁺, and Zn²⁺) stresses

Front Microbiol. 2023 Oct 26:14:1294177. doi: 10.3389/fmicb.2023.1294177. eCollection 2023.

Authors

Beiyu Zhang^{1

2}, Jingjing Xu^{1

2}, Meng Sun^{1

2}, Pan Yu^{1

2}, Yuming Ma^{1

2}, Lu Xie³, Lanming Chen^{1

2}

Affiliations

¹ Key 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, China.
² College of Food Science and Technology, Shanghai Ocean University, Shanghai, China.
³ Shanghai-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, China.

Abstract

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.

Keywords: Vibrio cholerae; food safety; heavy metal; proteome; secretome; tolerance mechanism.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was financially supported by the Science and Technology Commission of Shanghai Municipality, grant number 17050502200, and the National Natural Science Foundation of China, grant number 31671946.