Early life exposure of infants to benzylpenicillin and gentamicin is associated with a persistent amplification of the gut resistome

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Abstract

Background

Infant gut microbiota is highly malleable, but the long-term longitudinal impact of antibiotic exposure in early life, together with the mode of delivery on infant gut microbiota and resistome, is not extensively studied.

Methods

Two hundred and eight samples from 45 infants collected from birth until 2 years of age over five time points (week 1, 4, 8, 24, year 2) were analysed. Based on shotgun metagenomics, the gut microbial composition and resistome profile were compared in the early life of infants divided into three groups: vaginal delivery/no-antibiotic in the first 4 days of life, C-section/no-antibiotic in the first 4 days of life, and C-section/antibiotic exposed in first 4 days of life. Gentamycin and benzylpenicillin were the most commonly administered antibiotics during this cohort’s first week of life.

Results

Newborn gut microbial composition differed in all three groups, with higher diversity and stable composition seen at 2 years of age, compared to week 1. An increase in microbial diversity from week 1 to week 4 only in the C-section/antibiotic-exposed group reflects the effect of antibiotic use in the first 4 days of life, with a gradual increase thereafter. Overall, a relative abundance of Actinobacteria and Bacteroides was significantly higher in vaginal delivery/no-antibiotic while Proteobacteria was higher in C-section/antibiotic-exposed infants. Strains from species belonging to Bifidobacterium and Bacteroidetes were generally persistent colonisers, with Bifidobacterium breve and Bifidobacterium bifidum species being the major persistent colonisers in all three groups. Bacteroides persistence was dominant in the vaginal delivery/no-antibiotic group, with species Bacteroides ovatus and Phocaeicola vulgatus found to be persistent colonisers in the no-antibiotic groups. Most strains carrying antibiotic-resistance genes belonged to phyla Proteobacteria and Firmicutes, with the C-section/antibiotic-exposed group presenting a higher frequency of antibiotic-resistance genes (ARGs).

Conclusion

These data show that antibiotic exposure has an immediate and persistent effect on the gut microbiome in early life. As such, the two antibiotics used in the study selected for strains (mainly Proteobacteria) which were multiple drug-resistant (MDR), presumably a reflection of their evolutionary lineage of historical exposures—leading to what can be an extensive and diverse resistome.

Supplementary Information

The online version contains supplementary material available at 10.1186/s40168-023-01732-6.

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Most cited references 77

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phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data

Paul McMurdie, Susan Holmes (2013)

Background The analysis of microbial communities through DNA sequencing brings many challenges: the integration of different types of data with methods from ecology, genetics, phylogenetics, multivariate statistics, visualization and testing. With the increased breadth of experimental designs now being pursued, project-specific statistical analyses are often needed, and these analyses are often difficult (or impossible) for peer researchers to independently reproduce. The vast majority of the requisite tools for performing these analyses reproducibly are already implemented in R and its extensions (packages), but with limited support for high throughput microbiome census data. Results Here we describe a software project, phyloseq, dedicated to the object-oriented representation and analysis of microbiome census data in R. It supports importing data from a variety of common formats, as well as many analysis techniques. These include calibration, filtering, subsetting, agglomeration, multi-table comparisons, diversity analysis, parallelized Fast UniFrac, ordination methods, and production of publication-quality graphics; all in a manner that is easy to document, share, and modify. We show how to apply functions from other R packages to phyloseq-represented data, illustrating the availability of a large number of open source analysis techniques. We discuss the use of phyloseq with tools for reproducible research, a practice common in other fields but still rare in the analysis of highly parallel microbiome census data. We have made available all of the materials necessary to completely reproduce the analysis and figures included in this article, an example of best practices for reproducible research. Conclusions The phyloseq project for R is a new open-source software package, freely available on the web from both GitHub and Bioconductor.

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CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes

Donovan Parks, Michael Imelfort, Connor Skennerton … (2015)

Large-scale recovery of genomes from isolates, single cells, and metagenomic data has been made possible by advances in computational methods and substantial reductions in sequencing costs. Although this increasing breadth of draft genomes is providing key information regarding the evolutionary and functional diversity of microbial life, it has become impractical to finish all available reference genomes. Making robust biological inferences from draft genomes requires accurate estimates of their completeness and contamination. Current methods for assessing genome quality are ad hoc and generally make use of a limited number of “marker” genes conserved across all bacterial or archaeal genomes. Here we introduce CheckM, an automated method for assessing the quality of a genome using a broader set of marker genes specific to the position of a genome within a reference genome tree and information about the collocation of these genes. We demonstrate the effectiveness of CheckM using synthetic data and a wide range of isolate-, single-cell-, and metagenome-derived genomes. CheckM is shown to provide accurate estimates of genome completeness and contamination and to outperform existing approaches. Using CheckM, we identify a diverse range of errors currently impacting publicly available isolate genomes and demonstrate that genomes obtained from single cells and metagenomic data vary substantially in quality. In order to facilitate the use of draft genomes, we propose an objective measure of genome quality that can be used to select genomes suitable for specific gene- and genome-centric analyses of microbial communities.

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In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing.

Alessandra Carattoli, Ea Zankari, Aurora García-Fernández … (2014)

In the work presented here, we designed and developed two easy-to-use Web tools for in silico detection and characterization of whole-genome sequence (WGS) and whole-plasmid sequence data from members of the family Enterobacteriaceae. These tools will facilitate bacterial typing based on draft genomes of multidrug-resistant Enterobacteriaceae species by the rapid detection of known plasmid types. Replicon sequences from 559 fully sequenced plasmids associated with the family Enterobacteriaceae in the NCBI nucleotide database were collected to build a consensus database for integration into a Web tool called PlasmidFinder that can be used for replicon sequence analysis of raw, contig group, or completely assembled and closed plasmid sequencing data. The PlasmidFinder database currently consists of 116 replicon sequences that match with at least at 80% nucleotide identity all replicon sequences identified in the 559 fully sequenced plasmids. For plasmid multilocus sequence typing (pMLST) analysis, a database that is updated weekly was generated from www.pubmlst.org and integrated into a Web tool called pMLST. Both databases were evaluated using draft genomes from a collection of Salmonella enterica serovar Typhimurium isolates. PlasmidFinder identified a total of 103 replicons and between zero and five different plasmid replicons within each of 49 S. Typhimurium draft genomes tested. The pMLST Web tool was able to subtype genomic sequencing data of plasmids, revealing both known plasmid sequence types (STs) and new alleles and ST variants. In conclusion, testing of the two Web tools using both fully assembled plasmid sequences and WGS-generated draft genomes showed them to be able to detect a broad variety of plasmids that are often associated with antimicrobial resistance in clinically relevant bacterial pathogens. Copyright © 2014, American Society for Microbiology. All Rights Reserved.

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Author and article information

Contributors

R. Paul Ross: p.ross@ucc.ie

Journal

Journal ID (nlm-ta): Microbiome

Journal ID (iso-abbrev): Microbiome

Title: Microbiome

Publisher: BioMed Central (London )

ISSN (Electronic): 2049-2618

Publication date (Electronic): 3 February 2024

Publication date PMC-release: 3 February 2024

Publication date Collection: 2024

Volume: 12

Electronic Location Identifier: 19

Affiliations

[1 ]School of Microbiology, University College Cork, ( https://ror.org/03265fv13) Cork, Ireland

[2 ]GRID grid.6435.4, ISNI 0000 0001 1512 9569, Teagasc Food Research Centre, ; Moorepark, Fermoy Co., Cork, Ireland

[3 ]APC Microbiome Ireland, Cork, Ireland

[4 ]Department of Paediatrics and Child Health, University College Cork, ( https://ror.org/03265fv13) Cork, Ireland

[5 ]GRID grid.7872.a, ISNI 0000000123318773, Infant Research Centre, , University College Cork, ; Cork, Ireland

Article

Publisher ID: 1732

DOI: 10.1186/s40168-023-01732-6

PMC ID: 10837951

PubMed ID: 38310316

SO-VID: 8d9e07ef-7f02-41bb-84d1-83eda69f41aa

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 9 May 2023

Date accepted : 24 November 2023

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001602, Science Foundation Ireland;

Award ID: 12/RC/2273_P2 and 19/SP/6989

Award Recipient : Dhrati V. Patangia Ghjuvan Grimaud Carol-Anne O’Shea C. A. Ryan Eugene Dempsey Catherine Stanton R. Paul Ross

Funded by: FundRef http://dx.doi.org/10.13039/501100004963, Seventh Framework Programme;

Award ID: 613979

Award Recipient : Carol-Anne O’Shea C. A. Ryan Eugene Dempsey Catherine Stanton R. Paul Ross

Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;

Award ID: 101054719

Award Recipient : R. Paul Ross

Custom metadata

Keywords: infant gut,gut microbiota,shotgun metagenomics,resistome profile,strain persistence

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Keywords: infant gut, gut microbiota, shotgun metagenomics, resistome profile, strain persistence

Early life exposure of infants to benzylpenicillin and gentamicin is associated with a persistent amplification of the gut resistome

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Abstract

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Supplementary Information

Related collections

Tick microbiome

Most cited references 77

phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes

In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing.

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