A metalloprotease secreted by an environmentally acquired gut bacterium hinders Borrelia afzelii colonization in Ixodes ricinus.

IF 4.6 2区 医学 Q2 IMMUNOLOGY
Frontiers in Cellular and Infection Microbiology Pub Date : 2024-10-10 eCollection Date: 2024-01-01 DOI:10.3389/fcimb.2024.1476266
Adnan Hodžić, Gorana Veinović, Amer Alić, David Seki, Martin Kunert, Georgi Nikolov, Ratko Sukara, Jovana Šupić, Snežana Tomanović, David Berry
{"title":"A metalloprotease secreted by an environmentally acquired gut bacterium hinders <i>Borrelia afzelii</i> colonization in <i>Ixodes ricinus</i>.","authors":"Adnan Hodžić, Gorana Veinović, Amer Alić, David Seki, Martin Kunert, Georgi Nikolov, Ratko Sukara, Jovana Šupić, Snežana Tomanović, David Berry","doi":"10.3389/fcimb.2024.1476266","DOIUrl":null,"url":null,"abstract":"<p><p>Although the importance of the microbiome in the context of tick biology and vector competence has recently come into a broader research focus, the field is still in its infancy and the complex ecological interactions between the tick residential bacteria and pathogens are obscure. Here, we show that an environmentally acquired gut bacterium has the potential to impair <i>Borrelia afzelii</i> colonization within the tick vector through a secreted metalloprotease. Oral introduction of either <i>Bacillus cereus</i> LTG-1 isolate or its purified enhancin (<i>Bc</i>Enhancin) protein significantly reduces <i>B. afzelii</i> burden in the guts of <i>Ixodes ricinus</i> ticks. This effect is attributed to the ability of <i>Bc</i>Enhancin to degrade a glycan-rich peritrophic matrix (PM), which is a gut protective barrier essential for <i>Borrelia</i> survival. Our study highlights the importance of the gut microbiome in determining tick vector competence and provides a deeper mechanistic insight into the complex network of interactions between <i>Borrelia</i>, the tick, and the tick microbiome.</p>","PeriodicalId":12458,"journal":{"name":"Frontiers in Cellular and Infection Microbiology","volume":null,"pages":null},"PeriodicalIF":4.6000,"publicationDate":"2024-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11499241/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Cellular and Infection Microbiology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3389/fcimb.2024.1476266","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"IMMUNOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Although the importance of the microbiome in the context of tick biology and vector competence has recently come into a broader research focus, the field is still in its infancy and the complex ecological interactions between the tick residential bacteria and pathogens are obscure. Here, we show that an environmentally acquired gut bacterium has the potential to impair Borrelia afzelii colonization within the tick vector through a secreted metalloprotease. Oral introduction of either Bacillus cereus LTG-1 isolate or its purified enhancin (BcEnhancin) protein significantly reduces B. afzelii burden in the guts of Ixodes ricinus ticks. This effect is attributed to the ability of BcEnhancin to degrade a glycan-rich peritrophic matrix (PM), which is a gut protective barrier essential for Borrelia survival. Our study highlights the importance of the gut microbiome in determining tick vector competence and provides a deeper mechanistic insight into the complex network of interactions between Borrelia, the tick, and the tick microbiome.

一种由环境获得的肠道细菌分泌的金属蛋白酶阻碍了阿夫泽尔氏包柔氏菌(Borrelia afzelii)在蓖麻线虫体内的定植。
尽管微生物组在蜱生物学和载体能力方面的重要性最近已成为更广泛的研究焦点,但该领域仍处于起步阶段,蜱栖息地细菌与病原体之间复杂的生态相互作用还不明显。在这里,我们发现一种从环境中获得的肠道细菌有可能通过分泌金属蛋白酶来损害阿夫泽尔氏包柔氏菌在蜱载体内的定殖。口服蜡样芽孢杆菌 LTG-1 分离物或其纯化的增强素(BcEnhancin)蛋白可显著降低蓖麻弓形虫蜱肠道中的阿夫泽氏包柔氏菌负担。这种效果归因于 BcEnhancin 降解富含糖的营养周基质(PM)的能力,而营养周基质是鲍瑞氏菌生存所必需的肠道保护屏障。我们的研究强调了肠道微生物组在决定蜱载体能力方面的重要性,并从机理上更深入地揭示了鲍瑞氏菌、蜱和蜱微生物组之间复杂的相互作用网络。
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
CiteScore
7.90
自引率
7.00%
发文量
1817
审稿时长
14 weeks
期刊介绍: Frontiers in Cellular and Infection Microbiology is a leading specialty journal, publishing rigorously peer-reviewed research across all pathogenic microorganisms and their interaction with their hosts. Chief Editor Yousef Abu Kwaik, University of Louisville is supported by an outstanding Editorial Board of international experts. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide. Frontiers in Cellular and Infection Microbiology includes research on bacteria, fungi, parasites, viruses, endosymbionts, prions and all microbial pathogens as well as the microbiota and its effect on health and disease in various hosts. The research approaches include molecular microbiology, cellular microbiology, gene regulation, proteomics, signal transduction, pathogenic evolution, genomics, structural biology, and virulence factors as well as model hosts. Areas of research to counteract infectious agents by the host include the host innate and adaptive immune responses as well as metabolic restrictions to various pathogenic microorganisms, vaccine design and development against various pathogenic microorganisms, and the mechanisms of antibiotic resistance and its countermeasures.
×
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