{"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.
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.