Upper respiratory microbial communities of healthy populations are shaped by niche and age.

IF 13.8 1区 生物学 Q1 MICROBIOLOGY
Susan Zelasko, Mary Hannah Swaney, Shelby Sandstrom, Timothy C Davenport, Christine M Seroogy, James E Gern, Lindsay R Kalan, Cameron R Currie
{"title":"Upper respiratory microbial communities of healthy populations are shaped by niche and age.","authors":"Susan Zelasko, Mary Hannah Swaney, Shelby Sandstrom, Timothy C Davenport, Christine M Seroogy, James E Gern, Lindsay R Kalan, Cameron R Currie","doi":"10.1186/s40168-024-01940-8","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Alterations in upper respiratory microbiomes have been implicated in shaping host health trajectories, including by limiting mucosal pathogen colonization. However, limited comparative studies of respiratory microbiome development and functioning across age groups have been performed. Herein, we perform shotgun metagenomic sequencing paired with pathogen inhibition assays to elucidate differences in nasal and oral microbiome composition and intermicrobial interactions across healthy 24-month-old infant (n = 229) and adult (n = 100) populations.</p><p><strong>Results: </strong>We find that beta diversity of nasal and oral microbiomes varies with age, with nasal microbiomes showing greater population-level variation compared to oral microbiomes. Infant microbiome alpha diversity was significantly lower across nasal samples and higher in oral samples, relative to adults. Accordingly, we demonstrate significant differences in genus- and species-level composition of microbiomes between sites and age groups. Antimicrobial resistome patterns likewise varied across body sites, with oral microbiomes showing higher resistance gene abundance compared to nasal microbiomes. Biosynthetic gene clusters encoding specialized metabolite production were found in higher abundance across infant oral microbiomes, relative to adults. Investigation of pathogen inhibition revealed greater inhibition of gram-negative and gram-positive bacteria by oral commensals, while nasal isolates had higher antifungal activity.</p><p><strong>Conclusions: </strong>In summary, we identify significant differences in the microbial communities inhabiting nasal and oral cavities of healthy infants relative to adults. These findings inform our understanding of the interactions impacting respiratory microbiome composition and functions related to colonization resistance, with important implications for host health across the lifespan. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8000,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11490146/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-024-01940-8","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Background: Alterations in upper respiratory microbiomes have been implicated in shaping host health trajectories, including by limiting mucosal pathogen colonization. However, limited comparative studies of respiratory microbiome development and functioning across age groups have been performed. Herein, we perform shotgun metagenomic sequencing paired with pathogen inhibition assays to elucidate differences in nasal and oral microbiome composition and intermicrobial interactions across healthy 24-month-old infant (n = 229) and adult (n = 100) populations.

Results: We find that beta diversity of nasal and oral microbiomes varies with age, with nasal microbiomes showing greater population-level variation compared to oral microbiomes. Infant microbiome alpha diversity was significantly lower across nasal samples and higher in oral samples, relative to adults. Accordingly, we demonstrate significant differences in genus- and species-level composition of microbiomes between sites and age groups. Antimicrobial resistome patterns likewise varied across body sites, with oral microbiomes showing higher resistance gene abundance compared to nasal microbiomes. Biosynthetic gene clusters encoding specialized metabolite production were found in higher abundance across infant oral microbiomes, relative to adults. Investigation of pathogen inhibition revealed greater inhibition of gram-negative and gram-positive bacteria by oral commensals, while nasal isolates had higher antifungal activity.

Conclusions: In summary, we identify significant differences in the microbial communities inhabiting nasal and oral cavities of healthy infants relative to adults. These findings inform our understanding of the interactions impacting respiratory microbiome composition and functions related to colonization resistance, with important implications for host health across the lifespan. Video Abstract.

健康人群的上呼吸道微生物群落由生态位和年龄决定。
背景:上呼吸道微生物组的变化与宿主健康轨迹的形成有关,包括通过限制粘膜病原体定植。然而,关于不同年龄组呼吸道微生物组发育和功能的比较研究还很有限。在此,我们进行了霰弹枪元基因组测序,并配以病原体抑制试验,以阐明健康的 24 个月大婴儿(n = 229)和成人(n = 100)人群的鼻腔和口腔微生物组组成及微生物间相互作用的差异:结果:我们发现鼻腔和口腔微生物组的β多样性随年龄而变化,与口腔微生物组相比,鼻腔微生物组显示出更大的群体水平变化。与成人相比,鼻腔样本中婴儿微生物组的α多样性明显较低,而口腔样本中的α多样性较高。因此,我们证明了不同部位和年龄组的微生物组在属种和物种组成上存在显著差异。抗微生物耐药性基因组模式在不同身体部位同样存在差异,与鼻腔微生物组相比,口腔微生物组显示出更高的耐药性基因丰度。与成人相比,婴儿口腔微生物组中编码特殊代谢物生产的生物合成基因簇的丰度更高。对病原体抑制作用的调查显示,口腔共生菌对革兰氏阴性菌和革兰氏阳性菌的抑制作用更强,而鼻腔分离菌的抗真菌活性更高:总之,我们发现健康婴儿的鼻腔和口腔中栖息的微生物群落与成人有显著差异。这些发现有助于我们了解影响呼吸道微生物群组成的相互作用以及与抗定植有关的功能,对宿主一生的健康具有重要意义。视频摘要。
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
Microbiome
Microbiome MICROBIOLOGY-
CiteScore
21.90
自引率
2.60%
发文量
198
审稿时长
4 weeks
期刊介绍: Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.
×
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