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Cited by 160Antibiotic Resistance in BacteriaPharmaceutical and Antibiotic Environmental ImpactsGut microbiota and health

The DOI matches its Crossref record; 115 of the 115 references it cites were found in a registry or an index.

Good microbes, bad genes? The dissemination of antimicrobial resistance in the human microbiome

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Crits-Christoph, Alexander, Hallowell, Haley Anne, Koutouvalis, Kalia, Suez, Jotham·2022·Gut Microbes
DOI 10.1080/19490976.2022.2055944PMC PMC8959533
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Abstract

A global rise in antimicrobial resistance among pathogenic bacteria has proved to be a major public health threat, with the rate of multidrug-resistant bacterial infections increasing over time. The gut microbiome has been studied as a reservoir of antibiotic resistance genes (ARGs) that can be transferred to bacterial pathogens via horizontal gene transfer (HGT) of conjugative plasmids and mobile genetic elements (the gut resistome). Advances in metagenomic sequencing have facilitated the identification of resistome modulators, including live microbial therapeutics such as probiotics and fecal microbiome transplantation that can either expand or reduce the abundances of ARG-carrying bacteria in the gut. While many different gut microbes encode for ARGs, they are not uniformly distributed across, or transmitted by, various members of the microbiome, and not all are of equal clinical relevance. Both experimental and theoretical approaches in microbial ecology have been applied to understand differing frequencies of ARG horizontal transfer between commensal microbes as well as between commensals and pathogens. In this commentary, we assess the evidence for the role of commensal gut microbes in encoding antimicrobial resistance genes, the degree to which they are shared both with other commensals and with pathogens, and the host and environmental factors that can impact resistome dynamics. We further discuss novel sequencing-based approaches for identifying ARGs and predicting future transfer events of clinically relevant ARGs from commensals to pathogens.

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Figure 1. Host and Environmental Factors that Impact the Gut Resistome. The abundance and composition of the gut resistome are influenced by a multitude of factors. (1) Live Microbial Therapeutics; Live Microbial Therapeutics can reduce or expand the resistome depending on the environmental context, such as the administration of antibiotics. (2) Antibiotics; Antibiotic usage can select for resident antibiotic-resistant microbes and leads to an overall expansion of the resistome. (3) Disease State; Certain disease states, such as IBD, are correlated with the overall expansion of the resistome through boosting horizontal gene transfer. (4) Hospital Environment; Hospital settings provide an ideal environment for the dissemination of antibiotic resistance genes between patients. (5) Breastfeeding; Antibiotic resistance genes can be vertically transmitted through breastmilk. Breast milk is associated with a suppressive effect on the resistome of infants. (6) Agriculture; Working or living in close proximity to livestock serves as an exposure route of antimicrobial resistance genes. Additionally, antibiotic resistance genes can be acquired from food itself. (7) Geographical Location; Geographical location is correlated with variations in the resistome. Additionally, depending on the destination, international travel leads to changes in the composition of the resistome. (8) Diet; Antibiotic-resistance genes can be derived from food itself, which can be driven by use of antibiotics in livestock. Additionally, certain diets, such as ones high in whole grains, have been correlated with a reduction in the resistome.
Figure 1. Host and Environmental Factors that Impact the Gut Resistome. The abundance and composition of the gut resistome are influenced by a multitude of factors. (1) Live Microbial Therapeutics; Live Microbial Therapeutics can reduce or expand the resistome depending on the environmental context, such as the administration of antibiotics. (2) Antibiotics; Antibiotic usage can select for resident antibiotic-resistant microbes and leads to an overall expansion of the resistome. (3) Disease State; Certain disease states, such as IBD, are correlated with the overall expansion of the resistome through boosting horizontal gene transfer. (4) Hospital Environment; Hospital settings provide an ideal environment for the dissemination of antibiotic resistance genes between patients. (5) Breastfeeding; Antibiotic resistance genes can be vertically transmitted through breastmilk. Breast milk is associated with a suppressive effect on the resistome of infants. (6) Agriculture; Working or living in close proximity to livestock serves as an exposure route of antimicrobial resistance genes. Additionally, antibiotic resistance genes can be acquired from food itself. (7) Geographical Location; Geographical location is correlated with variations in the resistome. Additionally, depending on the destination, international travel leads to changes in the composition of the resistome. (8) Diet; Antibiotic-resistance genes can be derived from food itself, which can be driven by use of antibiotics in livestock. Additionally, certain diets, such as ones high in whole grains, have been correlated with a reduction in the resistome.CC BY · PubMed Central
Figure 2. Effects of Live Microbial Therapeutics (LMT) on the Gut Resistome. When LMTs are administered, they can have a variety of consequences on gut commensals. Left to right; LMTs can directly reduce the overall number of ARG-carrying bacteria. However, this may depend on whether the LMTs are able to colonize the gut of the host. Colonization resistance to LMT may limit their effect on ARG-carrying bacteria. Second, LMTs containing ARGs can transfer antibiotic resistance to endogenous microbes. For example, many LMTs utilize lactic acid bacteria, which are known to be antibiotic-resistant, and are able to undergo horizontal gene transfer with commensal species. Finally, LMTs may indirectly promote expansion of the resistome, by supporting the bloom of ARG-carrying bacteria in the antibiotic-perturbed gut.
Figure 2. Effects of Live Microbial Therapeutics (LMT) on the Gut Resistome. When LMTs are administered, they can have a variety of consequences on gut commensals. Left to right; LMTs can directly reduce the overall number of ARG-carrying bacteria. However, this may depend on whether the LMTs are able to colonize the gut of the host. Colonization resistance to LMT may limit their effect on ARG-carrying bacteria. Second, LMTs containing ARGs can transfer antibiotic resistance to endogenous microbes. For example, many LMTs utilize lactic acid bacteria, which are known to be antibiotic-resistant, and are able to undergo horizontal gene transfer with commensal species. Finally, LMTs may indirectly promote expansion of the resistome, by supporting the bloom of ARG-carrying bacteria in the antibiotic-perturbed gut.CC BY · PubMed Central

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  1. 10.3201/1106.041204 · DOI
  2. 10.1101/2022.01.12.476061v1.full · DOI

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Metadata

Authors
Crits-Christoph, A., Hallowell, H. A., Koutouvalis, K., & Suez, J.
Affiliations
  • Johns Hopkins Bloomberg School of Public Health
  • Johns Hopkins University (US)
Corresponding author
Suez, Jotham
ORCID
Venue
Gut Microbes
Publisher
Informa UK Limited
Published
2022-03-25
Volume
14
Issue
1
Pages
2055944-2055944
ISSN
  • 1949-0976 (ISSN-L)
  • 1949-0984
DOI
10.1080/19490976.2022.2055944
PMC
PMC8959533
OpenAlex
W4221117022
Cited by
156
References
115
Citations by year
2026: 34 · 2025: 36 · 2024: 45 · 2023: 35 · 2022: 6
FWCI
2.33
Type
journal article
Language
en
Open access
Licence
doi.org/10.1080/policies-text-data-mining (tdm)
Locations
  • Gut Microbes (publishedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
article
Topics
  • Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
  • Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
antimicrobial resistance genes, gut microbiota, horizontal gene transfer, commensal bacteria, gut resistome, probiotics, conjugative plasmids, mobile genetic elements, multidrug resistance
MeSH terms
Gastrointestinal Microbiome, Anti-Bacterial Agents, Bacteria, Genes, Bacterial, Humans, Drug Resistance, Bacterial, Metagenomics, Microbiota

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