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Tracking microbial evolution in the human gut using Hi-C reveals extensive horizontal gene transfer, persistence and adaptation.

ABSTRACT: Despite the importance of horizontal gene transfer for rapid bacterial evolution, reliable assignment of mobile genetic elements to their microbial hosts in natural communities such as the human gut microbiota is lacking. We used high-throughput chromosomal conformation capture coupled with probabilistic modelling of experimental noise to resolve 88 strain-level metagenome-assembled genomes of distal gut bacteria from two participants, including 12,251 accessory elements. Comparisons of two samples collected 10 years apart for each of the participants revealed extensive in situ exchange of accessory elements as well as evidence of adaptive evolution in core genomes. Accessory elements were predominantly promiscuous and prevalent in the distal gut metagenomes of 218 adult individuals. This research provides a foundation and approach for studying microbial evolution in natural environments.

SUBMITTER: Yaffe E

PROVIDER: S-EPMC6992475 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Tracking microbial evolution in the human gut using Hi-C reveals extensive horizontal gene transfer, persistence and adaptation.

Yaffe Eitan E Relman David A DA

Nature microbiology 20191223 2

Despite the importance of horizontal gene transfer for rapid bacterial evolution, reliable assignment of mobile genetic elements to their microbial hosts in natural communities such as the human gut microbiota is lacking. We used high-throughput chromosomal conformation capture coupled with probabilistic modelling of experimental noise to resolve 88 strain-level metagenome-assembled genomes of distal gut bacteria from two participants, including 12,251 accessory elements. Comparisons of two samp ...[more]

PMID: 31873203

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Project description:BackgroundSymbiotic relationships between animals and bacteria have profound impacts on the evolutionary trajectories of each partner. Animals and gut bacteria engage in a variety of relationships, occasionally persisting over evolutionary timescales. Ants are a diverse group of animals that engage in many types of associations with taxonomically distinct groups of bacterial associates. Here, we bring into culture and characterize two closely-related strains of gut associated Acetobacteraceae (AAB) of the red carpenter ant, Camponotus chromaiodes.ResultsGenome sequencing, assembly, and annotation of both strains delineate stark patterns of genomic erosion and sequence divergence in gut associated AAB. We found widespread horizontal gene transfer (HGT) in these bacterial associates and report elevated gene acquisition associated with energy production and conversion, amino acid and coenzyme transport and metabolism, defense mechanisms, and lysine export. Both strains have acquired the complete NADH-quinone oxidoreductase complex, plausibly from an Enterobacteriaceae origin, likely facilitating energy production under diverse conditions. Conservation of several lysine biosynthetic and salvage pathways and accumulation of lysine export genes via HGT implicate L-lysine supplementation by both strains as a potential functional benefit for the host. These trends are contrasted by genome-wide erosion of several amino acid biosynthetic pathways and pathways in central metabolism. We perform phylogenomic analyses on both strains as well as several free living and host associated AAB. Based on their monophyly and deep divergence from other AAB, these C. chromaiodes gut associates may represent a novel genus. Together, our results demonstrate how extensive horizontal transfer between gut associates along with genome-wide deletions leads to mosaic metabolic pathways. More broadly, these patterns demonstrate that HGT and genomic erosion shape metabolic capabilities of persistent gut associates and influence their genomic evolution.ConclusionsUsing comparative genomics, our study reveals substantial changes in genomic content in persistent associates of the insect gastrointestinal tract and provides evidence for the evolutionary pressures inherent to this environment. We describe patterns of genomic erosion and horizontal acquisition that result in mosaic metabolic pathways. Accordingly, the phylogenetic position of both strains of these associates form a divergent, monophyletic clade sister to gut associates of honey bees and more distantly to Gluconobacter.

Project description:Transposons, plasmids, bacteriophages, and other mobile genetic elements facilitate horizontal gene transfer in the gut microbiota, allowing some pathogenic bacteria to acquire antibiotic resistance genes (ARGs). Currently, the relationship between specific ARGs and specific transposons in the comprehensive infant gut microbiome has not been elucidated. In this study, ARGs and transposons were annotated from the Unified Human Gastrointestinal Genome (UHGG) and the Early-Life Gut Genomes (ELGG). Association rules mining was used to explore the association between specific ARGs and specific transposons in UHGG, and the robustness of the association rules was validated using the external database in ELGG. Our results suggested that ARGs and transposons were more likely to be relevant in infant gut microbiota compared to adult gut microbiota, and nine robust association rules were identified, among which Klebsiella pneumoniae, Enterobacter hormaechei_A, and Escherichia coli_D played important roles in this association phenomenon. The emphasis of this study is to investigate the synergistic transfer of specific ARGs and specific transposons in the infant gut microbiota, which can contribute to the study of microbial pathogenesis and the ARG dissemination dynamics.IMPORTANCEThe transfer of transposons carrying antibiotic resistance genes (ARGs) among microorganisms accelerates antibiotic resistance dissemination among infant gut microbiota. Nonetheless, it is unclear what the relationship between specific ARGs and specific transposons within the infant gut microbiota. K. pneumoniae, E. hormaechei_A, and E. coli_D were identified as key players in the nine robust association rules we discovered. Meanwhile, we found that infant gut microorganisms were more susceptible to horizontal gene transfer events about specific ARGs and specific transposons than adult gut microorganisms. These discoveries could enhance the understanding of microbial pathogenesis and the ARG dissemination dynamics within the infant gut microbiota.

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Tracking microbial evolution in the human gut using Hi-C reveals extensive horizontal gene transfer, persistence and adaptation.

Publications

Tracking microbial evolution in the human gut using Hi-C reveals extensive horizontal gene transfer, persistence and adaptation.

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