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Antibiotic Treatment Drives the Diversification of the Human Gut Resistome.

ABSTRACT: Despite the documented antibiotic-induced disruption of the gut microbiota, the impact of antibiotic intake on strain-level dynamics, evolution of resistance genes, and factors influencing resistance dissemination potential remains poorly understood. To address this gap we analyzed public metagenomic datasets from 24 antibiotic treated subjects and controls, combined with an in-depth prospective functional study with two subjects investigating the bacterial community dynamics based on cultivation-dependent and independent methods. We observed that short-term antibiotic treatment shifted and diversified the resistome composition, increased the average copy number of antibiotic resistance genes, and altered the dominant strain genotypes in an individual-specific manner. More than 30% of the resistance genes underwent strong differentiation at the single nucleotide level during antibiotic treatment. We found that the increased potential for horizontal gene transfer, due to antibiotic administration, was ∼3-fold stronger in the differentiated resistance genes than the non-differentiated ones. This study highlights how antibiotic treatment has individualized impacts on the resistome and strain level composition, and drives the adaptive evolution of the gut microbiota.

SUBMITTER: Li J

PROVIDER: S-EPMC6520913 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Antibiotic Treatment Drives the Diversification of the Human Gut Resistome.

Li Jun J Rettedal Elizabeth A EA van der Helm Eric E Ellabaan Mostafa M Panagiotou Gianni G Sommer Morten O A MOA

Genomics, proteomics & bioinformatics 20190201 1

Despite the documented antibiotic-induced disruption of the gut microbiota, the impact of antibiotic intake on strain-level dynamics, evolution of resistance genes, and factors influencing resistance dissemination potential remains poorly understood. To address this gap we analyzed public metagenomic datasets from 24 antibiotic treated subjects and controls, combined with an in-depth prospective functional study with two subjects investigating the bacterial community dynamics based on cultivatio ...[more]

PMID: 31026582

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Project description:Industrialization has driven lifestyle changes in eastern and western Chinese populations, yet we have a poor understanding of the dynamic changes in their gut microbiome and resistome under industrialization, which is essential for the scientific management of public health. Here, this study employed metagenomics to analyze the gut microbiota of 1,382 healthy individuals from China, including 415 individuals from the eastern region of advanced industrialization and 967 individuals from the western region of developing industrialization. Compared with western populations, eastern populations show a significant increase in interindividual dissimilarity of microbial species composition and metabolic pathways but a significant decrease in intraindividual species and functional diversity. Furthermore, our results found significantly less abundance and richness of antibiotic resistance genes (ARGs) in the gut microbiota of eastern populations, alongside a lower prevalence of unique core ARG subtypes. For the 12 core ARG types shared between eastern and western populations, the mean relative abundance of two types was notably higher in the eastern populations, while eight core ARG types had significantly higher mean relative abundance in the western populations. Based on the reconstruction of metagenomic assembled genomes, we found that Escherichia coli genomes from western populations carried more virulence factor genes (VFGs) and mobile genetic elements (MGEs) compared to those from eastern populations. This large-scale study for the first time revealed industrialization potentially led to unexpected alterations of the gut microbiome and resistome between eastern and western populations that provide a vital implication for Chinese public health and may aid in the development of region-specific strategies for managing pathogenic infections.ImportanceAs China experiences rapid but uneven industrialization, understanding its effect on people's gut bacteria is critical for public health. This study reveals how industrialization may reshape the health risks related to gut bacteria and antibiotic resistance. This work provides crucial information to help create customized public health policies for different regions.

Project description:BackgroundChronic diarrhea is a common disease causing morbidity and mortality of captive rhesus macaques (RMs, Macaca mulatta). Chronic diarrhea in RMs is typically characterized by long-term diarrhea and a weak response to antibiotic treatment. Diarrhea is also a common disease in humans and can cause death. However, the etiology of about half of diarrheal cases of humans is still unclear. Therefore, we performed shotgun metagenomic sequencing to characterize the differences in the gut microbiome and resistome of chronic diarrhea RMs and asymptomatic individuals.ResultsOur results showed Lactobacillus spp. (mainly L. johnsonii, L. reuteri and L. amylovorus) were significantly depleted in chronic diarrhea RM guts compared to asymptomatic individuals (5.2 vs 42.4%). Functional annotation of genes suggested these Lactobacillus spp. carried genes involved in the adhesion of intestinal epithelial cells and production of bacteriocin. Chronic diarrhea RM guts also had a significantly greater abundance of many other gut bacteria, including mucin-degrading bacteria and opportunistic pathogens. The metabolic pathways of chronic diarrhea RM gut microbiome were enriched in aerobactin biosynthesis, while the metabolic pathways of asymptomatic RM gut microbiome were enriched in the production of short-chain fatty acids (SCFAs). Chronic diarrhea RM guts had a significantly greater abundance of antibiotic resistance genes (ARGs), such as ermF, aph(3')-IIIa, ermB, and floR. The strains isolated from feces and tissue fluid of chronic diarrhea RMs had higher resistance rates to the majority of tested antibiotics, but not cephamycin and carbapenem antibiotics. Gut microbial composition comparisons showed that several captive nonhuman primate (NHP) guts were more similar to the guts of humans with a non-westernized diet than humans with a westernized diet. Chronic diarrhea RM gut microbiome was strikingly similar to rural-living humans with diarrhea and humans with a non-westernized diet than asymptomatic RMs.ConclusionsOur results suggested chronic diarrhea significantly altered the composition and metabolic pathways of the RM gut microbiome. The frequent use of antibiotics caused antibiotic resistance in chronic diarrhea RM gut microbiome with serious consequences for individual treatment and survival. The findings of this study will help us to improve the effective prevention and treatment of diarrhea in RMs. Video Abstract.

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Antibiotic Treatment Drives the Diversification of the Human Gut Resistome.

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Antibiotic Treatment Drives the Diversification of the Human Gut Resistome.

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