BglaTNB6, a tailocin produced by a plant-associated nonpathogenic bacterium, prevents rice seed-borne bacterial diseases.

IF 5.5 1区 医学 Q1 MICROBIOLOGY PLoS Pathogens Pub Date : 2024-10-18 eCollection Date: 2024-10-01 DOI:10.1371/journal.ppat.1012645
Yusuke Kouzai, Yoshiyuki Sagehashi, Riku Watanabe, Hideyuki Kajiwara, Nobuhiro Suzuki, Hiroshi Ono, Ken Naito, Chiharu Akimoto-Tomiyama
{"title":"BglaTNB6, a tailocin produced by a plant-associated nonpathogenic bacterium, prevents rice seed-borne bacterial diseases.","authors":"Yusuke Kouzai, Yoshiyuki Sagehashi, Riku Watanabe, Hideyuki Kajiwara, Nobuhiro Suzuki, Hiroshi Ono, Ken Naito, Chiharu Akimoto-Tomiyama","doi":"10.1371/journal.ppat.1012645","DOIUrl":null,"url":null,"abstract":"<p><p>Rice seed-borne diseases caused by the bacterial pathogens Burkholderia glumae and B. plantarii pose a major threat to rice production worldwide. To manage these diseases in a sustainable manner, a biocontrol strategy is crucial. In this study, we showed that B. gladioli NB6 (NB6), a nonpathogenic bacterium, strongly protects rice from infection caused by the above-mentioned pathogens. NB6 was isolated from the indica rice cultivar Nona Bokra seedlings, which possesses genetic resistance to B. glumae. We discovered that cell suspensions of NB6 and its culture filtrate suppressed the disease symptoms caused by B. glumae and B. plantarii in rice seedlings, which indicated that NB6 secretes a plant-protective substance extracellularly. Through purification and mass spectrometry analysis of the culture filtrate, combined with transmission electron microscopy and mutant analysis, the substance was identified as a tailocin and named BglaTNB6. Tailocins are bacteriotoxic multiprotein structures morphologically similar to headless phage tails. BglaTNB6 exhibited antibacterial activity against several Burkholderia species, including B. glumae, B. plantarii, and B. gladioli, suggesting it can prevent pathogen infection. Interestingly, BglaTNB6 greatly contributed only to the biocontrol activity of NB6 cell suspensions against B. plantarii, and not against B. glumae. BglaTNB6 was shown to be encoded by a prophage locus lacking genes for phage head proteins, and a B. gladioli strain with the coded BglaTNB6-like locus equipped with phage head proteins failed to prevent rice seedlings from being infected with B. plantarii. These results suggested that BglaTNB6 may enhance the competitiveness of NB6 against a specific range of bacteria. Our study also highlights the potential of tailocin-producing endophytes for managing crop bacterial diseases.</p>","PeriodicalId":48999,"journal":{"name":"PLoS Pathogens","volume":null,"pages":null},"PeriodicalIF":5.5000,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11524443/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Pathogens","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1371/journal.ppat.1012645","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Rice seed-borne diseases caused by the bacterial pathogens Burkholderia glumae and B. plantarii pose a major threat to rice production worldwide. To manage these diseases in a sustainable manner, a biocontrol strategy is crucial. In this study, we showed that B. gladioli NB6 (NB6), a nonpathogenic bacterium, strongly protects rice from infection caused by the above-mentioned pathogens. NB6 was isolated from the indica rice cultivar Nona Bokra seedlings, which possesses genetic resistance to B. glumae. We discovered that cell suspensions of NB6 and its culture filtrate suppressed the disease symptoms caused by B. glumae and B. plantarii in rice seedlings, which indicated that NB6 secretes a plant-protective substance extracellularly. Through purification and mass spectrometry analysis of the culture filtrate, combined with transmission electron microscopy and mutant analysis, the substance was identified as a tailocin and named BglaTNB6. Tailocins are bacteriotoxic multiprotein structures morphologically similar to headless phage tails. BglaTNB6 exhibited antibacterial activity against several Burkholderia species, including B. glumae, B. plantarii, and B. gladioli, suggesting it can prevent pathogen infection. Interestingly, BglaTNB6 greatly contributed only to the biocontrol activity of NB6 cell suspensions against B. plantarii, and not against B. glumae. BglaTNB6 was shown to be encoded by a prophage locus lacking genes for phage head proteins, and a B. gladioli strain with the coded BglaTNB6-like locus equipped with phage head proteins failed to prevent rice seedlings from being infected with B. plantarii. These results suggested that BglaTNB6 may enhance the competitiveness of NB6 against a specific range of bacteria. Our study also highlights the potential of tailocin-producing endophytes for managing crop bacterial diseases.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
BglaTNB6是一种由植物相关非致病菌产生的尾孢菌素,可预防水稻种子传播的细菌性病害。
由细菌病原体伯克霍尔德氏菌(Burkholderia glumae)和植株伯克霍尔德氏菌(B. plantarii)引起的水稻种子病害对全球水稻生产构成了重大威胁。要以可持续的方式管理这些病害,生物防治策略至关重要。在这项研究中,我们发现一种非致病性细菌 B. gladioli NB6(NB6)能有效保护水稻免受上述病原体的感染。NB6 是从籼稻栽培品种 Nona Bokra 的幼苗中分离出来的,该品种对 B. glumae 具有遗传抗性。我们发现,NB6 的细胞悬浮液及其培养滤液可抑制水稻秧苗由枯萎病菌和植病菌引起的病害症状,这表明 NB6 在细胞外分泌一种植物保护物质。通过对培养滤液进行纯化和质谱分析,并结合透射电子显微镜和突变体分析,确定该物质为尾孢菌素,并将其命名为 BglaTNB6。尾蛋白是一种具有细菌毒性的多蛋白结构,在形态上类似于无头噬菌体的尾巴。BglaTNB6 对几种伯克霍尔德菌(包括 B.glumae、B.plantarii 和 B.gladioli)具有抗菌活性,表明它可以防止病原体感染。有趣的是,BglaTNB6 只对 NB6 细胞悬浮液对植物伯克霍尔德氏菌的生物控制活性有很大贡献,而对 Glumae 伯克霍尔德氏菌没有贡献。研究表明,BglaTNB6 是由一个缺乏噬菌体头部蛋白基因的噬菌体基因座编码的,而一个具有编码的 BglaTNB6 类基因座并带有噬菌体头部蛋白的 B. gladioli 菌株不能阻止水稻幼苗感染植物疫霉菌。这些结果表明,BglaTNB6 可能会增强 NB6 对特定范围细菌的竞争力。我们的研究还凸显了产生尾孢素的内生菌在控制作物细菌性病害方面的潜力。
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 去求助
来源期刊
PLoS Pathogens
PLoS Pathogens MICROBIOLOGY-PARASITOLOGY
自引率
3.00%
发文量
598
期刊介绍: Bacteria, fungi, parasites, prions and viruses cause a plethora of diseases that have important medical, agricultural, and economic consequences. Moreover, the study of microbes continues to provide novel insights into such fundamental processes as the molecular basis of cellular and organismal function.
期刊最新文献
Retraction: p53 promotes ZDHHC1-mediated IFITM3 palmitoylation to inhibit Japanese encephalitis virus replication. Structural basis for human DPP4 receptor recognition by a pangolin MERS-like coronavirus. Use of the Puccinia sorghi haustorial transcriptome to identify and characterize AvrRp1-D recognized by the maize Rp1-D resistance protein. A viral p3a protein targets and inhibits TaDOF transcription factors to promote the expression of susceptibility genes and facilitate viral infection. A major role of class III HD-ZIPs in promoting sugar beet cyst nematode parasitism in Arabidopsis.
×
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
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 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 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1