Fusobacterium nucleatum metabolically integrates commensals and pathogens in oral biofilms

Author:

Sakanaka AkitoORCID,Kuboniwa MasaeORCID,Shimma ShuichiORCID,Alghamdi Samar A.ORCID,Mayumi ShotaORCID,Lamont Richard J.ORCID,Fukusaki EiichiroORCID,Amano AtsuoORCID

Abstract

AbstractFusobacterium nucleatum is a common constituent of the oral microbiota in both periodontal health and disease. Previously, we discovered ornithine cross-feeding between F. nucleatum and Streptococcus gordonii, where S. gordonii secretes ornithine via an arginine-ornithine antiporter (ArcD), which in turn supports the growth and biofilm development of F. nucleatum; however, broader metabolic aspects of F. nucleatum within polymicrobial communities and their impact on periodontal pathogenesis have not been addressed. Here, we show that when co-cultured with S. gordonii, F. nucleatum increased amino acid availability to enhance the production of butyrate and putrescine, a polyamine produced by ornithine decarboxylation. Co-culture with Veillonella parvula, another common inhabitant of the oral microbiota, also increased lysine availability, promoting cadaverine production by F. nucleatum. We confirmed that ArcD-dependent ornithine excretion by S. gordonii results in synergistic putrescine production, and mass spectrometry imaging revealed this metabolic capability creates a putrescine-rich microenvironment inside F. nucleatum biofilms. We further demonstrated that polyamines caused significant changes in the biofilm phenotype of a periodontal pathogen, Porphyromonas gingivalis, with putrescine being a potent stimulator of biofilm development and dispersal, and confirmed that F. nucleatum-mediated conversion of ornithine to putrescine enhances biofilm formation by P. gingivalis. Lastly, analysis of plaque samples revealed cooccurrence of P. gingivalis with genetic modules for putrescine production by S. gordonii and F. nucleatum. Overall, our results highlight the ability of F. nucleatum to induce synergistic polyamine production within multi-species consortia, and provide insight into how the trophic web in oral biofilm ecosystems can eventually shape disease-associated communities.Significance StatementPeriodontitis is caused by the pathogenic transition of subgingival microbiota ecosystems, which is accompanied by alterations to microbiome functions including metabolic systems and the establishment of metabolic cross-feeding. While Fusobacterium nucleatum is a major constituent of the periodontal microbiota, its metabolic integration within polymicrobial communities and the impact on periodontal pathogenesis are poorly understood. Here, we report that amino acids supplied by other commensal bacteria induce polyamine production by F. nucleatum, creating polyamine-rich microenvironments. We further show that this trophic web results in enhancement of biofilm formation and dispersal of a periodontal pathogen, Porphyromonas gingivalis. This work provides mechanistic insight into how cooperative metabolism within oral biofilms can tip the balance toward periodontitis.

Publisher

Cold Spring Harbor Laboratory

Reference55 articles.

1. Staging and grading of periodontitis: framework and proposal of a new classification and case definition;J. Periodontol.,2018

2. The oral microbiota: dynamic communities and host interactions

3. Polymicrobial synergy and dysbiosis in inflammatory disease

4. Metatranscriptomics of the human oral microbiome during health and disease;mBio,2014

5. The social network of microorganisms — how auxotrophies shape complex communities

Cited by 1 articles. 订阅此论文施引文献 订阅此论文施引文献,注册后可以免费订阅5篇论文的施引文献,订阅后可以查看论文全部施引文献

同舟云学术

1.学者识别学者识别

2.学术分析学术分析

3.人才评估人才评估

"同舟云学术"是以全球学者为主线,采集、加工和组织学术论文而形成的新型学术文献查询和分析系统,可以对全球学者进行文献检索和人才价值评估。用户可以通过关注某些学科领域的顶尖人物而持续追踪该领域的学科进展和研究前沿。经过近期的数据扩容,当前同舟云学术共收录了国内外主流学术期刊6万余种,收集的期刊论文及会议论文总量共计约1.5亿篇,并以每天添加12000余篇中外论文的速度递增。我们也可以为用户提供个性化、定制化的学者数据。欢迎来电咨询!咨询电话:010-8811{复制后删除}0370

www.globalauthorid.com

TOP

Copyright © 2019-2024 北京同舟云网络信息技术有限公司
京公网安备11010802033243号  京ICP备18003416号-3