Destination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in Dutch travelers
Abstract Background Antimicrobial-resistant bacteria and their antimicrobial resistance (AMR) genes can spread by hitchhiking in human guts. International travel can exacerbate this public health threat when travelers acquire AMR genes endemic to their destinations and bring them back to their home...
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doaj-1320836afcd4449184bf3388301f7b162021-06-13T11:13:01ZengBMCGenome Medicine1756-994X2021-06-0113112110.1186/s13073-021-00893-zDestination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in Dutch travelersAlaric W. D’Souza0Manish Boolchandani1Sanket Patel2Gianluca Galazzo3Jarne M. van Hattem4Maris S. Arcilla5Damian C. Melles6Menno D. de Jong7Constance Schultsz8COMBAT ConsortiumGautam Dantas9John Penders10The Edison Family Center for Genome Sciences and Systems Biology, Washington University School of MedicineThe Edison Family Center for Genome Sciences and Systems Biology, Washington University School of MedicineThe Edison Family Center for Genome Sciences and Systems Biology, Washington University School of MedicineDepartment of Medical Microbiology, Care and Public Health Research Institute (CAPHRI), Maastricht University Medical CenterDepartment of Medical Microbiology, Amsterdam University Medical Center, Location AMCDepartment of Medical Microbiology and Infectious Diseases, Erasmus University Medical CentreDepartment of Medical Microbiology and Infectious Diseases, Erasmus University Medical CentreDepartment of Medical Microbiology, Amsterdam University Medical Center, Location AMCDepartment of Medical Microbiology, Amsterdam University Medical Center, Location AMCThe Edison Family Center for Genome Sciences and Systems Biology, Washington University School of MedicineDepartment of Medical Microbiology, Care and Public Health Research Institute (CAPHRI), Maastricht University Medical CenterAbstract Background Antimicrobial-resistant bacteria and their antimicrobial resistance (AMR) genes can spread by hitchhiking in human guts. International travel can exacerbate this public health threat when travelers acquire AMR genes endemic to their destinations and bring them back to their home countries. Prior studies have demonstrated travel-related acquisition of specific opportunistic pathogens and AMR genes, but the extent and magnitude of travel’s effects on the gut resistome remain largely unknown. Methods Using whole metagenomic shotgun sequencing, functional metagenomics, and Dirichlet multinomial mixture models, we investigated the abundance, diversity, function, resistome architecture, and context of AMR genes in the fecal microbiomes of 190 Dutch individuals, before and after travel to diverse international locations. Results Travel markedly increased the abundance and α-diversity of AMR genes in the travelers’ gut resistome, and we determined that 56 unique AMR genes showed significant acquisition following international travel. These acquisition events were biased towards AMR genes with efflux, inactivation, and target replacement resistance mechanisms. Travel-induced shaping of the gut resistome had distinct correlations with geographical destination, so individuals returning to The Netherlands from the same destination country were more likely to have similar resistome features. Finally, we identified and detailed specific acquisition events of high-risk, mobile genetic element-associated AMR genes including qnr fluoroquinolone resistance genes, bla CTX-M family extended-spectrum β-lactamases, and the plasmid-borne mcr-1 colistin resistance gene. Conclusions Our results show that travel shapes the architecture of the human gut resistome and results in AMR gene acquisition against a variety of antimicrobial drug classes. These broad acquisitions highlight the putative risks that international travel poses to public health by gut resistome perturbation and the global spread of locally endemic AMR genes.https://doi.org/10.1186/s13073-021-00893-zResistomeAntibiotic resistanceTravelmcr-1β-LactamasesESBL |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Alaric W. D’Souza Manish Boolchandani Sanket Patel Gianluca Galazzo Jarne M. van Hattem Maris S. Arcilla Damian C. Melles Menno D. de Jong Constance Schultsz COMBAT Consortium Gautam Dantas John Penders |
spellingShingle |
Alaric W. D’Souza Manish Boolchandani Sanket Patel Gianluca Galazzo Jarne M. van Hattem Maris S. Arcilla Damian C. Melles Menno D. de Jong Constance Schultsz COMBAT Consortium Gautam Dantas John Penders Destination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in Dutch travelers Genome Medicine Resistome Antibiotic resistance Travel mcr-1 β-Lactamases ESBL |
author_facet |
Alaric W. D’Souza Manish Boolchandani Sanket Patel Gianluca Galazzo Jarne M. van Hattem Maris S. Arcilla Damian C. Melles Menno D. de Jong Constance Schultsz COMBAT Consortium Gautam Dantas John Penders |
author_sort |
Alaric W. D’Souza |
title |
Destination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in Dutch travelers |
title_short |
Destination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in Dutch travelers |
title_full |
Destination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in Dutch travelers |
title_fullStr |
Destination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in Dutch travelers |
title_full_unstemmed |
Destination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in Dutch travelers |
title_sort |
destination shapes antibiotic resistance gene acquisitions, abundance increases, and diversity changes in dutch travelers |
publisher |
BMC |
series |
Genome Medicine |
issn |
1756-994X |
publishDate |
2021-06-01 |
description |
Abstract Background Antimicrobial-resistant bacteria and their antimicrobial resistance (AMR) genes can spread by hitchhiking in human guts. International travel can exacerbate this public health threat when travelers acquire AMR genes endemic to their destinations and bring them back to their home countries. Prior studies have demonstrated travel-related acquisition of specific opportunistic pathogens and AMR genes, but the extent and magnitude of travel’s effects on the gut resistome remain largely unknown. Methods Using whole metagenomic shotgun sequencing, functional metagenomics, and Dirichlet multinomial mixture models, we investigated the abundance, diversity, function, resistome architecture, and context of AMR genes in the fecal microbiomes of 190 Dutch individuals, before and after travel to diverse international locations. Results Travel markedly increased the abundance and α-diversity of AMR genes in the travelers’ gut resistome, and we determined that 56 unique AMR genes showed significant acquisition following international travel. These acquisition events were biased towards AMR genes with efflux, inactivation, and target replacement resistance mechanisms. Travel-induced shaping of the gut resistome had distinct correlations with geographical destination, so individuals returning to The Netherlands from the same destination country were more likely to have similar resistome features. Finally, we identified and detailed specific acquisition events of high-risk, mobile genetic element-associated AMR genes including qnr fluoroquinolone resistance genes, bla CTX-M family extended-spectrum β-lactamases, and the plasmid-borne mcr-1 colistin resistance gene. Conclusions Our results show that travel shapes the architecture of the human gut resistome and results in AMR gene acquisition against a variety of antimicrobial drug classes. These broad acquisitions highlight the putative risks that international travel poses to public health by gut resistome perturbation and the global spread of locally endemic AMR genes. |
topic |
Resistome Antibiotic resistance Travel mcr-1 β-Lactamases ESBL |
url |
https://doi.org/10.1186/s13073-021-00893-z |
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