Gut microbiota carbon and sulfur metabolisms support Salmonella infections.

Ikaia Leleiwi,Katherine Kokkinias,Yongseok Kim,Maryam Baniasad,Michael Shaffer,Anice Sabag-Daigle,Rebecca A Daly,Rory M Flynn,Vicki H Wysocki,Brian M M Ahmer,Mikayla A Borton,Kelly C Wrighton
{"title":"Gut microbiota carbon and sulfur metabolisms support Salmonella infections.","authors":"Ikaia Leleiwi,Katherine Kokkinias,Yongseok Kim,Maryam Baniasad,Michael Shaffer,Anice Sabag-Daigle,Rebecca A Daly,Rory M Flynn,Vicki H Wysocki,Brian M M Ahmer,Mikayla A Borton,Kelly C Wrighton","doi":"10.1093/ismejo/wrae187","DOIUrl":null,"url":null,"abstract":"Salmonella enterica serovar Typhimurium is a pervasive enteric pathogen and ongoing global threat to public health. Ecological studies in the Salmonella impacted gut remain underrepresented in the literature, discounting microbiome mediated interactions that may inform Salmonella physiology during colonization and infection. To understand the microbial ecology of Salmonella remodeling of the gut microbiome, we performed multi-omics on fecal microbial communities from untreated and Salmonella-infected mice. Reconstructed genomes recruited metatranscriptomic and metabolomic data providing a strain-resolved view of the expressed metabolisms of the microbiome during Salmonella infection. These data informed possible Salmonella interactions with members of the gut microbiome that were previously uncharacterized. Salmonella-induced inflammation significantly reduced the diversity of genomes that recruited transcripts in the gut microbiome, yet increased transcript mapping was observed for 7 members, among which Luxibacter and Ligilactobacillus transcript read recruitment was most prevalent. Metatranscriptomic insights from Salmonella and other persistent taxa in the inflamed microbiome further expounded the necessity for oxidative tolerance mechanisms to endure the host inflammatory responses to infection. In the inflamed gut lactate was a key metabolite, with microbiota production and consumption reported amongst members with detected transcript recruitment. We also showed that organic sulfur sources could be converted by gut microbiota to yield inorganic sulfur pools that become oxidized in the inflamed gut, resulting in thiosulfate and tetrathionate that supports Salmonella respiration. This research advances physiological microbiome insights beyond prior amplicon-based approaches, with the transcriptionally active organismal and metabolic pathways outlined here offering intriguing intervention targets in the Salmonella-infected intestine.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"193 1","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"The ISME Journal","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/ismejo/wrae187","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0

Abstract

Salmonella enterica serovar Typhimurium is a pervasive enteric pathogen and ongoing global threat to public health. Ecological studies in the Salmonella impacted gut remain underrepresented in the literature, discounting microbiome mediated interactions that may inform Salmonella physiology during colonization and infection. To understand the microbial ecology of Salmonella remodeling of the gut microbiome, we performed multi-omics on fecal microbial communities from untreated and Salmonella-infected mice. Reconstructed genomes recruited metatranscriptomic and metabolomic data providing a strain-resolved view of the expressed metabolisms of the microbiome during Salmonella infection. These data informed possible Salmonella interactions with members of the gut microbiome that were previously uncharacterized. Salmonella-induced inflammation significantly reduced the diversity of genomes that recruited transcripts in the gut microbiome, yet increased transcript mapping was observed for 7 members, among which Luxibacter and Ligilactobacillus transcript read recruitment was most prevalent. Metatranscriptomic insights from Salmonella and other persistent taxa in the inflamed microbiome further expounded the necessity for oxidative tolerance mechanisms to endure the host inflammatory responses to infection. In the inflamed gut lactate was a key metabolite, with microbiota production and consumption reported amongst members with detected transcript recruitment. We also showed that organic sulfur sources could be converted by gut microbiota to yield inorganic sulfur pools that become oxidized in the inflamed gut, resulting in thiosulfate and tetrathionate that supports Salmonella respiration. This research advances physiological microbiome insights beyond prior amplicon-based approaches, with the transcriptionally active organismal and metabolic pathways outlined here offering intriguing intervention targets in the Salmonella-infected intestine.
肠道微生物群碳和硫代谢支持沙门氏菌感染。
伤寒沙门氏菌(Salmonella enterica serovar Typhimurium)是一种普遍存在的肠道病原体,对全球公共卫生构成持续威胁。受沙门氏菌影响的肠道生态学研究在文献中的代表性仍然不足,忽略了微生物组介导的相互作用,而这种相互作用可能为沙门氏菌在定植和感染期间的生理学提供信息。为了了解沙门氏菌重塑肠道微生物组的微生物生态学,我们对未经处理的小鼠和沙门氏菌感染小鼠的粪便微生物群落进行了多组学研究。重建的基因组招募了元转录组和代谢组数据,提供了沙门氏菌感染期间微生物组表达代谢的菌株分辨视图。这些数据揭示了沙门氏菌与以前未定性的肠道微生物群成员之间可能存在的相互作用。沙门氏菌诱导的炎症大大降低了肠道微生物组招募转录本的基因组多样性,但观察到 7 个成员的转录本映射增加,其中卢克氏菌和半乳杆菌的转录本读取招募最为普遍。沙门氏菌和发炎微生物群中其他持久性类群的元转录组学研究进一步说明了氧化耐受机制对于维持宿主对感染的炎症反应的必要性。在发炎的肠道中,乳酸是一种关键的代谢产物,据报道,在检测到转录本招募的微生物群成员中,乳酸的产生和消耗量都很大。我们还发现,有机硫源可被肠道微生物群转化为无机硫池,这些无机硫池在发炎的肠道中被氧化,产生硫代硫酸盐和四硫酸盐,支持沙门氏菌的呼吸作用。这项研究推动了对生理微生物组的深入了解,超越了之前基于扩增子的方法,其中概述的转录活跃的生物体和代谢途径为沙门氏菌感染的肠道提供了令人感兴趣的干预目标。
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
自引率
0.00%
发文量
0
×
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