The synergistic effect of biosynthesized CuONPs and phage (ϕPB2) as a novel approach for controlling Ralstonia solanacearum

IF 5.2 2区 农林科学 Q1 AGRICULTURE, MULTIDISCIPLINARY
Hongbao Zhang, Liuti Cai, Kai Yuan, Zhongwei Liu, Maoyang Ran, Siang Chen, Wu Cai, Cheng Rao, Lin Cai, Dong Zhou
{"title":"The synergistic effect of biosynthesized CuONPs and phage (ϕPB2) as a novel approach for controlling Ralstonia solanacearum","authors":"Hongbao Zhang,&nbsp;Liuti Cai,&nbsp;Kai Yuan,&nbsp;Zhongwei Liu,&nbsp;Maoyang Ran,&nbsp;Siang Chen,&nbsp;Wu Cai,&nbsp;Cheng Rao,&nbsp;Lin Cai,&nbsp;Dong Zhou","doi":"10.1186/s40538-024-00630-9","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><p>As a vital soil-borne pathogenic bacterium, <i>Ralstonia solanacearum</i> can cause wilt disease in multiple <i>Solanaceae</i> plants. Several phages, such as ϕPB2, could infect <i>R</i>. <i>solanacearum</i> acting as a potential biological control agent in soil. In addition, some nanoparticles, especially copper preparation, also showed high toxicity on <i>R. solanacearum</i> with low toxicity on plant. However, whether they can be administered in combination and how effective they are in inhibiting the plant disease caused by <i>R</i>. <i>solanacearum</i> is known very little.</p><h3>Results</h3><p>In this work, the characterization of CuONPs using scanning electron microscope, transmission electron microscope, X-ray photoelectron spectroscopy, Fourier transform infrared spectroscopy, and X-ray diffraction ascertained the presence of CuONPs which were nanometer particle of 83 nm. Then it was found that combined application of CuONPs with phage (ϕPB2) was superior to that of ϕPB2 or CuONPs alone in controlling tobacco bacterial wilt, with the CuONPs (250 mg/mL) and phage (10<sup>6</sup> PFU/mL) ratio being the best, at 79.1%. The combination of CuONPs and ϕPB2 also showed no obvious toxicity on tobacco growth than control like single application of CuONPs or ϕPB2. Furthermore, the transcriptome changes of <i>R</i>. <i>solanacearum</i> analysis indicated that the combination application and single allocation of CuONPs could inhibit “biofilm formation”, molecular function, biological processes, cellular components, metabolic process, and so on. In addition, the combination application showed higher inhibition of motility and biofilm, and better enhancement of cell membrane permeability, protein leakage, MDA concentration, and enzyme activity of their respiratory chain dehydrogenase than single application of CuONPs or phage (ϕPB2). Transcriptomes analysis also supported that the addition of ϕPB2 enhanced the toxicity of CuONPs by influencing the ABC transporters and quorum sensing, metabolic processes, and cellular biosynthetic processes of <i>R. solanacearum</i>.</p><h3>Conclusion</h3><p>In total, our work not only proposed a novel way to increase the bactericidal effect of nanomaterials by adding phage, but also discovered the influence, synergistic effects, and mechanisms, which is useful to design novel way to combat phytopathogenic bacteria in the complicated environment.</p><h3>Graphical abstract</h3>\n<div><figure><div><div><picture><source><img></source></picture></div></div></figure></div></div>","PeriodicalId":512,"journal":{"name":"Chemical and Biological Technologies in Agriculture","volume":"11 1","pages":""},"PeriodicalIF":5.2000,"publicationDate":"2024-08-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://chembioagro.springeropen.com/counter/pdf/10.1186/s40538-024-00630-9","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Chemical and Biological Technologies in Agriculture","FirstCategoryId":"97","ListUrlMain":"https://link.springer.com/article/10.1186/s40538-024-00630-9","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"AGRICULTURE, MULTIDISCIPLINARY","Score":null,"Total":0}
引用次数: 0

Abstract

Background

As a vital soil-borne pathogenic bacterium, Ralstonia solanacearum can cause wilt disease in multiple Solanaceae plants. Several phages, such as ϕPB2, could infect R. solanacearum acting as a potential biological control agent in soil. In addition, some nanoparticles, especially copper preparation, also showed high toxicity on R. solanacearum with low toxicity on plant. However, whether they can be administered in combination and how effective they are in inhibiting the plant disease caused by R. solanacearum is known very little.

Results

In this work, the characterization of CuONPs using scanning electron microscope, transmission electron microscope, X-ray photoelectron spectroscopy, Fourier transform infrared spectroscopy, and X-ray diffraction ascertained the presence of CuONPs which were nanometer particle of 83 nm. Then it was found that combined application of CuONPs with phage (ϕPB2) was superior to that of ϕPB2 or CuONPs alone in controlling tobacco bacterial wilt, with the CuONPs (250 mg/mL) and phage (106 PFU/mL) ratio being the best, at 79.1%. The combination of CuONPs and ϕPB2 also showed no obvious toxicity on tobacco growth than control like single application of CuONPs or ϕPB2. Furthermore, the transcriptome changes of R. solanacearum analysis indicated that the combination application and single allocation of CuONPs could inhibit “biofilm formation”, molecular function, biological processes, cellular components, metabolic process, and so on. In addition, the combination application showed higher inhibition of motility and biofilm, and better enhancement of cell membrane permeability, protein leakage, MDA concentration, and enzyme activity of their respiratory chain dehydrogenase than single application of CuONPs or phage (ϕPB2). Transcriptomes analysis also supported that the addition of ϕPB2 enhanced the toxicity of CuONPs by influencing the ABC transporters and quorum sensing, metabolic processes, and cellular biosynthetic processes of R. solanacearum.

Conclusion

In total, our work not only proposed a novel way to increase the bactericidal effect of nanomaterials by adding phage, but also discovered the influence, synergistic effects, and mechanisms, which is useful to design novel way to combat phytopathogenic bacteria in the complicated environment.

Graphical abstract

生物合成的 CuONPs 和噬菌体(ϕPB2)的协同作用是控制茄腐镰刀菌的一种新方法
Ralstonia solanacearum 是一种重要的土传病原菌,可导致多种茄科植物发生枯萎病。一些噬菌体,如ϕPB2,可以感染茄枯萎病菌,成为土壤中潜在的生物防治剂。此外,一些纳米颗粒,尤其是铜制剂,也显示出对茄碱菌的高毒性和对植物的低毒性。然而,这些纳米颗粒是否可以联合施用,以及它们对茄腐镰刀菌引起的植物病害的抑制效果如何,目前还知之甚少。在这项研究中,利用扫描电子显微镜、透射电子显微镜、X 射线光电子能谱、傅立叶变换红外光谱和 X 射线衍射对 CuONPs 进行了表征,结果发现 CuONPs 为 83 nm 的纳米颗粒。随后发现,CuONPs 与噬菌体(jPB2)的联合应用在控制烟草细菌性枯萎病方面优于单独使用 jPB2 或 CuONPs,其中 CuONPs(250 毫克/毫升)与噬菌体(106 PFU/毫升)的比例最佳,达到 79.1%。与单施 CuONPs 或 ϕPB2 的对照组相比,CuONPs 和 ϕPB2 的组合对烟草生长也没有明显的毒性。此外,R. solanacearum 的转录组变化分析表明,联合施用和单一施用 CuONPs 可抑制 "生物膜形成"、分子功能、生物过程、细胞成分、代谢过程等。此外,与单一施用 CuONPs 或噬菌体(jPB2)相比,联合施用对运动和生物膜的抑制作用更强,对细胞膜通透性、蛋白质渗漏、MDA 浓度及其呼吸链脱氢酶活性的增强效果更好。转录组分析也证明,ϕPB2 的添加通过影响 R. solanacearum 的 ABC 转运体和法定量感应、代谢过程和细胞生物合成过程,增强了 CuONPs 的毒性。总之,我们的研究不仅提出了一种通过添加噬菌体来提高纳米材料杀菌效果的新方法,而且发现了其影响、协同效应和机制,有助于设计新的方法来对付复杂环境中的植物病原菌。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Chemical and Biological Technologies in Agriculture
Chemical and Biological Technologies in Agriculture Biochemistry, Genetics and Molecular Biology-Biotechnology
CiteScore
6.80
自引率
3.00%
发文量
83
审稿时长
15 weeks
期刊介绍: Chemical and Biological Technologies in Agriculture is an international, interdisciplinary, peer-reviewed forum for the advancement and application to all fields of agriculture of modern chemical, biochemical and molecular technologies. The scope of this journal includes chemical and biochemical processes aimed to increase sustainable agricultural and food production, the evaluation of quality and origin of raw primary products and their transformation into foods and chemicals, as well as environmental monitoring and remediation. Of special interest are the effects of chemical and biochemical technologies, also at the nano and supramolecular scale, on the relationships between soil, plants, microorganisms and their environment, with the help of modern bioinformatics. Another special focus is the use of modern bioorganic and biological chemistry to develop new technologies for plant nutrition and bio-stimulation, advancement of biorefineries from biomasses, safe and traceable food products, carbon storage in soil and plants and restoration of contaminated soils to agriculture. This journal presents the first opportunity to bring together researchers from a wide number of disciplines within the agricultural chemical and biological sciences, from both industry and academia. The principle aim of Chemical and Biological Technologies in Agriculture is to allow the exchange of the most advanced chemical and biochemical knowledge to develop technologies which address one of the most pressing challenges of our times - sustaining a growing world population. Chemical and Biological Technologies in Agriculture publishes original research articles, short letters and invited reviews. Articles from scientists in industry, academia as well as private research institutes, non-governmental and environmental organizations are encouraged.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信