Episymbiotic Saccharibacteria TM7x modulates the susceptibility of its host bacteria to phage infection and promotes their coexistence

• 成果类型: Article
• 署名作者: Zhong, Qiu; Liao, Binyou; Liu, Jiazhen; Shen, Wei; Wang, Jing; Wei, Leilei; Ma, Yansong; Dong, Pu-Ting; Bor, Batbileg; McLean, Jeffrey S.; Chang, Yunjie; Shi, Wenyuan; Cen, Lujia; Wu, Miaomiao; Liul, Jun; Li, Yan; He, Xuesong; Le, Shuai
• 署名单位: Sichuan University; Chongqing Medical University; Army Medical University; Capital Medical University; Harvard University; Harvard School of Dental Medicine; University of Washington; University of Washington Seattle; University of Washington; University of Washington Seattle; Zhejiang University; Zhejiang University; Yale University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-9812
• DOI: 10.1073/pnas.2319790121
• 发表日期: 2024-04-09
• 关键词: teichoic-acids; antagonistic coevolution; phase variation

摘要

Bacteriophages (phages) play critical roles in modulating microbial ecology. Within the human microbiome, the factors influencing the long - term coexistence of phages and bacteria remain poorly investigated. Saccharibacteria (formerly TM7) are ubiquitous members of the human oral microbiome. These ultrasmall bacteria form episymbiotic relationships with their host bacteria and impact their physiology. Here, we showed that during surface- associated growth, a human oral Saccharibacteria isolate (named TM7x) protects its host bacterium, a Schaalia odontolytica strain (named XH001) against lytic phage LC001 predation. RNA- Sequencing analysis identified in XH001 a gene cluster with predicted functions involved in the biogenesis of cell wall polysaccharides (CWP), whose expression is significantly down- regulated when forming a symbiosis with TM7x. Through genetic work, we experimentally demonstrated the impact of the expression of this CWP gene cluster on bacterial-phage interaction by affecting phage binding. In vitro coevolution experiments further showed that the heterogeneous populations of TM7x- associated and TM7x-free XH001, which display differential susceptibility to LC001 predation, promote bacteria and phage coexistence. Our study highlights the tripartite interaction between the bacterium, episymbiont, and phage. More importantly, we present a mechanism, i.e., episymbiont- mediated modulation of gene expression in host bacteria, which impacts their susceptibility to phage predation and contributes to the formation of source- sink dynamics between phage and bacteria in biofilm, promoting their long - term coexistence within the human microbiome.