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Gut-derived Enterococcus faecium from ulcerative colitis patients promotes colitis in a genetically susceptible mouse host.

ABSTRACT: BACKGROUND:Recent metagenomic analyses have revealed dysbiosis of the gut microbiota of ulcerative colitis (UC) patients. However, the impacts of this dysbiosis are not fully understood, particularly at the strain level. RESULTS:We perform whole-genome shotgun sequencing of fecal DNA extracts from 13 healthy donors and 16 UC and 8 Crohn's disease (CD) patients. The microbiota of UC and CD patients is taxonomically and functionally divergent from that of healthy donors, with E. faecium being the most differentially abundant species between the two microbial communities. Transplantation of feces from UC or CD patients into Il10-/- mice promotes pathological inflammation and cytokine expression in the mouse colon, although distinct cytokine expression profiles are observed between UC and CD. Unlike isolates derived from healthy donors, E. faecium isolates from the feces of UC patients, along with E. faecium strain ATCC 19434, promotes colitis and colonic cytokine expression. Inflammatory E. faecium strains, including ATCC 19434 and a UC-derived strain, cluster separately from commercially available probiotic strains based on whole-genome shotgun sequencing analysis. The presence of E. faecium in fecal samples is associated with large disease extent and the need for multiple medications in UC patients. CONCLUSIONS:E. faecium strains derived from UC patients display an inflammatory genotype that causes colitis.

SUBMITTER: Seishima J

PROVIDER: S-EPMC6876129 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Gut-derived Enterococcus faecium from ulcerative colitis patients promotes colitis in a genetically susceptible mouse host.

Seishima Jun J Iida Noriho N Kitamura Kazuya K Yutani Masahiro M Wang Ziyu Z Seki Akihiro A Yamashita Taro T Sakai Yoshio Y Honda Masao M Yamashita Tatsuya T Kagaya Takashi T Shirota Yukihiro Y Fujinaga Yukako Y Mizukoshi Eishiro E Kaneko Shuichi S

Genome biology 20191125 1

<h4>Background</h4>Recent metagenomic analyses have revealed dysbiosis of the gut microbiota of ulcerative colitis (UC) patients. However, the impacts of this dysbiosis are not fully understood, particularly at the strain level.<h4>Results</h4>We perform whole-genome shotgun sequencing of fecal DNA extracts from 13 healthy donors and 16 UC and 8 Crohn's disease (CD) patients. The microbiota of UC and CD patients is taxonomically and functionally divergent from that of healthy donors, with E. fae ...[more]

PMID: 31767028

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Project description:BackgroundBecause of its social nature, the honeybee is regularly exposed to environmental toxicants such as heavy metals and xenobiotics. These toxicants are known to exert strong selective pressure on the gut microbiome's structure and diversity. For example, resistant microbial members are more likely to dominate in maintaining a stable microbiome, which is critical for bee health. Therefore, the aim of this study was to examine the Enterococcus faecium strains isolated from bee guts for their in vitro growth and tolerability to diverse heavy metals and xenobiotics. An additional aim was to analyze the genomes of E. faecium isolates to assess the molecular bases of resistance and compare them with E. faecium species isolated from other environmental sources.ResultsThe E. faecium bee isolates were able to tolerate high levels (up to 200 mg/L) of toxicants, including cadmium, zinc, benzoate, phenol and hexane. Moreover, the isolates could tolerate toluene and copper at up to 100 mg/L. The genome of E. faecium Am5, isolated from the larval stage of Apis mellifera gut, was about 2.7 Mb in size, had a GC content of 37.9% and 2,827 predicted coding sequences. Overall, the Am5 genome features were comparable with previously sequenced bee-gut isolates, E. faecium Am1, Bee9, SM21, and H7. The genomes of the bee isolates provided insight into the observed heavy metal tolerance. For example, heavy metal tolerance and/or regulation genes were present, including czcD (cobalt/zinc/cadmium resistance), cadA (exporting ATPase), cutC (cytoplasmic copper homeostasis) and zur (zinc uptake regulation). Additionally, genes associated with nine KEGG xenobiotic biodegradation pathways were detected, including γ-hexachlorocyclohexane, benzoate, biphenyl, bisphenol A, tetrachloroethene, 1,4-dichlorobenzene, ethylbenzene, trinitrotoluene and caprolactam. Interestingly, a comparative genomics study demonstrated the conservation of toxicant resistance genes across a variety of E. faecium counterparts isolated from other environmental sources such as non-human mammals, humans, avians, and marine animals.ConclusionsHoneybee gut-derived E. faecium strains can tolerate a variety of heavy metals. Moreover, their genomes encode many xenobiotic biodegradation pathways. Further research is required to examine E. faecium strains potential to boost host resistance to environmental toxins.

Project description:ObjectiveThe pathogenesis of UC relates to gut microbiota dysbiosis. We postulate that alterations in the viral community populating the intestinal mucosa play an important role in UC pathogenesis. This study aims to characterise the mucosal virome and their functions in health and UC.DesignDeep metagenomics sequencing of virus-like particle preparations and bacterial 16S rRNA sequencing were performed on the rectal mucosa of 167 subjects from three different geographical regions in China (UC=91; healthy controls=76). Virome and bacteriome alterations in UC mucosa were assessed and correlated with patient metadata. We applied partition around medoids clustering algorithm and classified mucosa viral communities into two clusters, referred to as mucosal virome metacommunities 1 and 2.ResultsIn UC, there was an expansion of mucosa viruses, particularly Caudovirales bacteriophages, and a decrease in mucosa Caudovirales diversity, richness and evenness compared with healthy controls. Altered mucosal virome correlated with intestinal inflammation. Interindividual dissimilarity between mucosal viromes was higher in UC than controls. Escherichia phage and Enterobacteria phage were more abundant in the mucosa of UC than controls. Compared with metacommunity 1, metacommunity 2 was predominated by UC subjects and displayed a significant loss of various viral species. Patients with UC showed substantial abrogation of diverse viral functions, whereas multiple viral functions, particularly functions of bacteriophages associated with host bacteria fitness and pathogenicity, were markedly enriched in UC mucosa. Intensive transkingdom correlations between mucosa viruses and bacteria were significantly depleted in UC.ConclusionWe demonstrated for the first time that UC is characterised by substantial alterations of the mucosa virobiota with functional distortion. Enrichment of Caudovirales bacteriophages, increased phage/bacteria virulence functions and loss of viral-bacterial correlations in the UC mucosa highlight that mucosal virome may play an important role in UC pathogenesis.

Dataset Information

Gut-derived Enterococcus faecium from ulcerative colitis patients promotes colitis in a genetically susceptible mouse host.

Publications

Gut-derived Enterococcus faecium from ulcerative colitis patients promotes colitis in a genetically susceptible mouse host.

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