Nonphytotoxic and pH-responsive ZnO-ZIF‑8 loaded with honokiol as a "nanoweapon" effectively controls the soil-borne bacterial pathogen Ralstonia solanacearum

Xunliang Huang; Yue Xing; Hao Jiang; Ya Pu; Song Yang; Zhensheng Kang; Lin Cai

doi:10.1016/j.jhazmat.2024.134502

Nonphytotoxic and pH-responsive ZnO-ZIF‑8 loaded with honokiol as a "nanoweapon" effectively controls the soil-borne bacterial pathogen Ralstonia solanacearum

J Hazard Mater. 2024 May 3:472:134502. doi: 10.1016/j.jhazmat.2024.134502. Online ahead of print.

Authors

Xunliang Huang¹, Yue Xing², Hao Jiang², Ya Pu³, Song Yang², Zhensheng Kang⁴, Lin Cai⁵

Affiliations

¹ National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China; College of Tobacco Science of Guizhou University, Guizhou Key Laboratory for Tobacco Quality, Guiyang 550025, China.
² National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China.
³ College of Tobacco Science of Guizhou University, Guizhou Key Laboratory for Tobacco Quality, Guiyang 550025, China.
⁴ State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, China. Electronic address: kangzs@nwsuaf.edu.cn.
⁵ National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China; College of Tobacco Science of Guizhou University, Guizhou Key Laboratory for Tobacco Quality, Guiyang 550025, China; State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, China. Electronic address: lincai@gzu.edu.cn.

PMID: 38743980
DOI: 10.1016/j.jhazmat.2024.134502

Abstract

The development of intelligently released and environmentally safe nanocarriers not only aligns with the sustainable agricultural strategy but also offers a potential solution for controlling severe soil-borne bacterial diseases. Herein, the core-shell structured nanocarrier loaded with honokiol bactericide (honokiol@ZnO-ZIF-8) was synthesized via a one-pot method for the targeted control of Ralstonia solanacearum, the causative agent of tobacco bacterial wilt disease. Results indicated that honokiol@ZnO-ZIF-8 nanoparticles induced bacterial cell membrane and DNA damage through the production of excessive reactive oxygen species (ROS), thereby reducing bacterial cell viability and ultimately leading to bacterial death. Additionally, the dissociation mechanism of the nanocarriers was elucidated for the first time through thermodynamic computational simulation. The nanocarriers dissociate primarily due to H⁺ attacking the N atom on imidazole, causing the rupture of the Zn-N bond under acidic conditions and at room temperature. Furthermore, honokiol@ZnO-ZIF-8 exhibited potent inhibitory effects against other prominent Solanaceae pathogenic bacteria (Pseudomonas syringae pv. tabaci), demonstrating its broad-spectrum antibacterial activity. Biosafety assessment results indicated that honokiol@ZnO-ZIF-8 exhibited non-phytotoxicity towards tobacco and tomato plants, with its predominant accumulation in the roots and no translocation to aboveground tissues within a short period. This study provides potential application value for the intelligent release of green pesticides. ENVIRONMENT IMPLICATION: The indiscriminate use of agrochemicals poses a significant threat to environmental, ecological security, and sustainable development. Slow-release pesticides offer a green and durable strategy for crop disease control. In this study, we developed a non-phytotoxic and pH-responsive honokiol@ZnO-ZIF-8 nano-bactericide based on the pathogenesis of Ralstonia solanacearum. Thermodynamic simulation revealed the dissociation mechanism of ZIF-8, with different acidity controlling the dissociation rate. This provides a theoretical basis for on-demand pesticide release while reducing residue in the. Our findings provide strong evidence for effective soil-borne bacterial disease control and on-demand pesticide release.

Keywords: Antibacterial mechanism; Nanopesticides; Natural product; Ralstonia solanacearum; Smart release mechanism.