Characterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes

ABSTRACT Environmental microbes have harbored the capacity for antibiotic production for millions of years, spanning the evolution of humans and other vertebrates. However, the industrial-scale use of antibiotics in clinical and agricultural practice over the past century has led to a substantial in...

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Autores principales: Pablo Tsukayama, Manish Boolchandani, Sanket Patel, Erica C. Pehrsson, Molly K. Gibson, Kenneth L. Chiou, Clifford J. Jolly, Jeffrey Rogers, Jane E. Phillips-Conroy, Gautam Dantas
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:346f1c8b27664300ac546deffba0b4bd2021-12-02T19:47:34ZCharacterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes10.1128/mSystems.00016-182379-5077https://doaj.org/article/346f1c8b27664300ac546deffba0b4bd2018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00016-18https://doaj.org/toc/2379-5077ABSTRACT Environmental microbes have harbored the capacity for antibiotic production for millions of years, spanning the evolution of humans and other vertebrates. However, the industrial-scale use of antibiotics in clinical and agricultural practice over the past century has led to a substantial increase in exposure of these agents to human and environmental microbiota. This perturbation is predicted to alter the ecology of microbial communities and to promote the evolution and transfer of antibiotic resistance (AR) genes. We studied wild and captive baboon populations to understand the effects of exposure to humans and human activities (e.g., antibiotic therapy) on the composition of the primate fecal microbiota and the antibiotic-resistant genes that it collectively harbors (the “resistome”). Using a culture-independent metagenomic approach, we identified functional antibiotic resistance genes in the gut microbiota of wild and captive baboon groups and saw marked variation in microbiota architecture and resistomes across habitats and lifeways. Our results support the view that antibiotic resistance is an ancient feature of gut microbial communities and that sharing habitats with humans may have important effects on the structure and function of the primate microbiota. IMPORTANCE Antibiotic exposure results in acute and persistent shifts in the composition and function of microbial communities associated with vertebrate hosts. However, little is known about the state of these communities in the era before the widespread introduction of antibiotics into clinical and agricultural practice. We characterized the fecal microbiota and antibiotic resistomes of wild and captive baboon populations to understand the effect of human exposure and to understand how the primate microbiota may have been altered during the antibiotic era. We used culture-independent and bioinformatics methods to identify functional resistance genes in the guts of wild and captive baboons and show that exposure to humans is associated with changes in microbiota composition and resistome expansion compared to wild baboon groups. Our results suggest that captivity and lifestyle changes associated with human contact can lead to marked changes in the ecology of primate gut communities.Pablo TsukayamaManish BoolchandaniSanket PatelErica C. PehrssonMolly K. GibsonKenneth L. ChiouClifford J. JollyJeffrey RogersJane E. Phillips-ConroyGautam DantasAmerican Society for Microbiologyarticleantibioticsantimicrobial resistancebaboonmetagenomicsmicrobial ecologymicrobiomeMicrobiologyQR1-502ENmSystems, Vol 3, Iss 3 (2018)
institution DOAJ
collection DOAJ
language EN
topic antibiotics
antimicrobial resistance
baboon
metagenomics
microbial ecology
microbiome
Microbiology
QR1-502
spellingShingle antibiotics
antimicrobial resistance
baboon
metagenomics
microbial ecology
microbiome
Microbiology
QR1-502
Pablo Tsukayama
Manish Boolchandani
Sanket Patel
Erica C. Pehrsson
Molly K. Gibson
Kenneth L. Chiou
Clifford J. Jolly
Jeffrey Rogers
Jane E. Phillips-Conroy
Gautam Dantas
Characterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes
description ABSTRACT Environmental microbes have harbored the capacity for antibiotic production for millions of years, spanning the evolution of humans and other vertebrates. However, the industrial-scale use of antibiotics in clinical and agricultural practice over the past century has led to a substantial increase in exposure of these agents to human and environmental microbiota. This perturbation is predicted to alter the ecology of microbial communities and to promote the evolution and transfer of antibiotic resistance (AR) genes. We studied wild and captive baboon populations to understand the effects of exposure to humans and human activities (e.g., antibiotic therapy) on the composition of the primate fecal microbiota and the antibiotic-resistant genes that it collectively harbors (the “resistome”). Using a culture-independent metagenomic approach, we identified functional antibiotic resistance genes in the gut microbiota of wild and captive baboon groups and saw marked variation in microbiota architecture and resistomes across habitats and lifeways. Our results support the view that antibiotic resistance is an ancient feature of gut microbial communities and that sharing habitats with humans may have important effects on the structure and function of the primate microbiota. IMPORTANCE Antibiotic exposure results in acute and persistent shifts in the composition and function of microbial communities associated with vertebrate hosts. However, little is known about the state of these communities in the era before the widespread introduction of antibiotics into clinical and agricultural practice. We characterized the fecal microbiota and antibiotic resistomes of wild and captive baboon populations to understand the effect of human exposure and to understand how the primate microbiota may have been altered during the antibiotic era. We used culture-independent and bioinformatics methods to identify functional resistance genes in the guts of wild and captive baboons and show that exposure to humans is associated with changes in microbiota composition and resistome expansion compared to wild baboon groups. Our results suggest that captivity and lifestyle changes associated with human contact can lead to marked changes in the ecology of primate gut communities.
format article
author Pablo Tsukayama
Manish Boolchandani
Sanket Patel
Erica C. Pehrsson
Molly K. Gibson
Kenneth L. Chiou
Clifford J. Jolly
Jeffrey Rogers
Jane E. Phillips-Conroy
Gautam Dantas
author_facet Pablo Tsukayama
Manish Boolchandani
Sanket Patel
Erica C. Pehrsson
Molly K. Gibson
Kenneth L. Chiou
Clifford J. Jolly
Jeffrey Rogers
Jane E. Phillips-Conroy
Gautam Dantas
author_sort Pablo Tsukayama
title Characterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes
title_short Characterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes
title_full Characterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes
title_fullStr Characterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes
title_full_unstemmed Characterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes
title_sort characterization of wild and captive baboon gut microbiota and their antibiotic resistomes
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/346f1c8b27664300ac546deffba0b4bd
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