Dissecting the impact of Anaplasma phagocytophilum infection on functional networks and community stability of the tick microbiome.

IF 2.3 4区 生物学 Q3 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
International Microbiology Pub Date : 2024-08-01 Epub Date: 2023-12-28 DOI:10.1007/s10123-023-00473-8
Patrícia Gonzaga Paulino, Lianet Abuin-Denis, Apolline Maitre, Elianne Piloto-Sardiñas, Dasiel Obregon, Huarrisson Azevedo Santos, Alejandro Cabezas-Cruz
{"title":"Dissecting the impact of Anaplasma phagocytophilum infection on functional networks and community stability of the tick microbiome.","authors":"Patrícia Gonzaga Paulino, Lianet Abuin-Denis, Apolline Maitre, Elianne Piloto-Sardiñas, Dasiel Obregon, Huarrisson Azevedo Santos, Alejandro Cabezas-Cruz","doi":"10.1007/s10123-023-00473-8","DOIUrl":null,"url":null,"abstract":"<p><strong>Context: </strong>Pathogens can manipulate microbial interactions to ensure survival, potentially altering the functional patterns and microbiome assembly. The present study investigates how Anaplasma phagocytophilum infection affects the functional diversity, composition, and assembly of the Ixodes scapularis microbiome, with a focus on high central pathways-those characterized by elevated values in centrality metrics such as eigenvector, betweenness, and degree measures, in the microbial community.</p><p><strong>Methods: </strong>Using previously published data from nymphs' gut V4 region's amplicons of bacterial 16S rRNA, we predicted the functional diversity and composition in control and A. phagocytophilum-infected ticks and inferred co-occurrence networks of taxa and ubiquitous pathways in each condition to associate the high central pathways to the microbial community assembly.</p><p><strong>Results: </strong>Although no differences were observed concerning pathways richness and diversity, there was a significant impact on taxa and functional assembly when ubiquitous pathways in each condition were filtered. Moreover, a notable shift was observed in the microbiome's high central functions. Specifically, pathways related to the degradation of nucleosides and nucleotides emerged as the most central functions in response to A. phagocytophilum infection. This finding suggests a reconfiguration of functional relationships within the microbial community, potentially influenced by the pathogen's limited metabolic capacity. This limitation implies that the tick microbiome may provide additional metabolic resources to support the pathogen's functional needs.</p><p><strong>Conclusions: </strong>Understanding the metabolic interactions within the tick microbiome can enhance our knowledge of pathogen colonization mechanisms and uncover new disease control and prevention strategies. For example, certain pathways that were more abundant or highly central during infection may represent potential targets for microbiota-based vaccines.</p>","PeriodicalId":14318,"journal":{"name":"International Microbiology","volume":" ","pages":"1205-1218"},"PeriodicalIF":2.3000,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"International Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1007/s10123-023-00473-8","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2023/12/28 0:00:00","PubModel":"Epub","JCR":"Q3","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Context: Pathogens can manipulate microbial interactions to ensure survival, potentially altering the functional patterns and microbiome assembly. The present study investigates how Anaplasma phagocytophilum infection affects the functional diversity, composition, and assembly of the Ixodes scapularis microbiome, with a focus on high central pathways-those characterized by elevated values in centrality metrics such as eigenvector, betweenness, and degree measures, in the microbial community.

Methods: Using previously published data from nymphs' gut V4 region's amplicons of bacterial 16S rRNA, we predicted the functional diversity and composition in control and A. phagocytophilum-infected ticks and inferred co-occurrence networks of taxa and ubiquitous pathways in each condition to associate the high central pathways to the microbial community assembly.

Results: Although no differences were observed concerning pathways richness and diversity, there was a significant impact on taxa and functional assembly when ubiquitous pathways in each condition were filtered. Moreover, a notable shift was observed in the microbiome's high central functions. Specifically, pathways related to the degradation of nucleosides and nucleotides emerged as the most central functions in response to A. phagocytophilum infection. This finding suggests a reconfiguration of functional relationships within the microbial community, potentially influenced by the pathogen's limited metabolic capacity. This limitation implies that the tick microbiome may provide additional metabolic resources to support the pathogen's functional needs.

Conclusions: Understanding the metabolic interactions within the tick microbiome can enhance our knowledge of pathogen colonization mechanisms and uncover new disease control and prevention strategies. For example, certain pathways that were more abundant or highly central during infection may represent potential targets for microbiota-based vaccines.

Abstract Image

剖析噬细胞原虫感染对蜱微生物群功能网络和群落稳定性的影响。
背景:病原体可以操纵微生物之间的相互作用以确保生存,从而可能改变功能模式和微生物组的组合。本研究调查了噬吞噬细胞阿纳疟原虫感染如何影响黄斑伊蚊微生物组的功能多样性、组成和组合,重点是高中心通路--在微生物群落中以中心度量(如特征向量、间隔度和程度度量)值升高为特征的通路:方法:利用之前发表的若虫肠道 V4 区域细菌 16S rRNA 扩增子数据,我们预测了对照组和噬细胞甲虫感染蜱的功能多样性和组成,并推断了每种情况下类群和普遍途径的共现网络,从而将高中心途径与微生物群落的组装联系起来:结果:虽然在通路的丰富度和多样性方面没有观察到差异,但在过滤每个条件下的泛在通路后,对分类群和功能组合产生了显著影响。此外,还观察到微生物群的核心功能发生了显著变化。具体来说,与核苷酸和核苷酸降解相关的途径成为应对噬细胞甲虫感染的最核心功能。这一发现表明,微生物群落内部的功能关系发生了重新配置,这可能受到病原体代谢能力有限的影响。这种限制意味着蜱微生物群落可能会提供额外的代谢资源来支持病原体的功能需求:结论:了解蜱微生物组内的代谢相互作用可以增强我们对病原体定植机制的了解,并发现新的疾病控制和预防策略。例如,在感染期间更丰富或高度集中的某些途径可能是基于微生物群的疫苗的潜在靶标。
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
International Microbiology
International Microbiology 生物-生物工程与应用微生物
CiteScore
5.50
自引率
3.20%
发文量
67
审稿时长
3 months
期刊介绍: International Microbiology publishes information on basic and applied microbiology for a worldwide readership. The journal publishes articles and short reviews based on original research, articles about microbiologists and their work and questions related to the history and sociology of this science. Also offered are perspectives, opinion, book reviews and editorials. A distinguishing feature of International Microbiology is its broadening of the term microbiology to include eukaryotic microorganisms.
×
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