Department of Cell and Molecular Biology, Colorado State University, Plant Sciences Bldg. 307 University Ave, Fort Collins, CO 80523, United States.
Department of Soil and Crop Sciences, Colorado State University, Plant Sciences Bldg. 307 University Ave, Fort Collins, CO 80523, United States.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrae187.
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 seven 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 support 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.
鼠伤寒沙门氏菌是一种普遍存在的肠道病原体,也是全球公共卫生的持续威胁。在受沙门氏菌影响的肠道中进行的生态研究在文献中仍然代表性不足,忽略了可能在定植和感染期间为沙门氏菌生理学提供信息的微生物组介导的相互作用。为了了解沙门氏菌重塑肠道微生物组的微生物生态学,我们对未经处理和感染沙门氏菌的小鼠的粪便微生物群落进行了多组学分析。重建的基因组招募了宏转录组和代谢组学数据,为沙门氏菌感染期间微生物组表达的代谢物提供了菌株解析的视图。这些数据为沙门氏菌与肠道微生物组中以前未表征的成员可能发生的相互作用提供了信息。沙门氏菌诱导的炎症显著降低了招募肠道微生物组中转录本的基因组多样性,但观察到七种成员的转录本映射增加,其中 Luxibacter 和 Ligilactobacillus 的转录本募集最为普遍。来自沙门氏菌和炎症微生物组中其他持久性分类群的宏转录组见解进一步阐述了氧化应激耐受机制的必要性,以耐受感染引起的宿主炎症反应。在炎症肠道中,乳酸是一种关键代谢物,在检测到转录本募集的成员中报告了其产生和消耗。我们还表明,肠道微生物群可以将有机硫源转化为无机硫库,这些硫库在炎症肠道中被氧化,产生支持沙门氏菌呼吸的硫代硫酸盐和连四硫酸盐。这项研究超越了基于扩增子的方法,提供了关于生理微生物组的深入见解,这里概述的转录活性生物体和代谢途径为感染沙门氏菌的肠道提供了有趣的干预靶点。