Evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattle
IntroductionUse of antimicrobial drugs (AMDs) in food producing animals has received increasing scrutiny because of concerns about antimicrobial resistance (AMR) that might affect consumers. Previously, investigations regarding AMR have focused largely on phenotypes of selected pathogens and indicat...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.970358/full |
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| author | Enrique Doster Enrique Doster Lee J. Pinnell Noelle R. Noyes Jennifer K. Parker Cameron A. Anderson Calvin W. Booker Sherry J. Hannon Tim A. McAllister Sheryl P. Gow Keith E. Belk Paul S. Morley |
| author_facet | Enrique Doster Enrique Doster Lee J. Pinnell Noelle R. Noyes Jennifer K. Parker Cameron A. Anderson Calvin W. Booker Sherry J. Hannon Tim A. McAllister Sheryl P. Gow Keith E. Belk Paul S. Morley |
| author_sort | Enrique Doster |
| collection | DOAJ |
| description | IntroductionUse of antimicrobial drugs (AMDs) in food producing animals has received increasing scrutiny because of concerns about antimicrobial resistance (AMR) that might affect consumers. Previously, investigations regarding AMR have focused largely on phenotypes of selected pathogens and indicator bacteria, such as Salmonella enterica or Escherichia coli. However, genes conferring AMR are known to be distributed and shared throughout microbial communities. The objectives of this study were to employ target-enriched metagenomic sequencing and 16S rRNA gene amplicon sequencing to investigate the effects of AMD use, in the context of other management and environmental factors, on the resistome and microbiome in beef feedlot cattle.MethodsThis study leveraged samples collected during a previous longitudinal study of cattle at beef feedlots in Canada. This included fecal samples collected from randomly selected individual cattle, as well as composite-fecal samples from randomly selected pens of cattle. All AMD use was recorded and characterized across different drug classes using animal defined daily dose (ADD) metrics.ResultsOverall, fecal resistome composition was dominated by genes conferring resistance to tetracycline and macrolide-lincosamide-streptogramin (MLS) drug classes. The diversity of bacterial phyla was greater early in the feeding period and decreased over time in the feedlot. This decrease in diversity occurred concurrently as the microbiome represented in different individuals and different pens shifted toward a similar composition dominated by Proteobacteria and Firmicutes. Some antimicrobial drug exposures in individuals and groups were associated with explaining a statistically significant proportion of the variance in the resistome, but the amount of variance explained by these important factors was very small (<0.6% variance each), and smaller than associations with other factors measured in this study such as time and feedlot ID. Time in the feedlot was associated with greater changes in the resistome for both individual animals and composite pen-floor samples, although the proportion of the variance associated with this factor was small (2.4% and 1.2%, respectively).DiscussionResults of this study are consistent with other investigations showing that, compared to other factors, AMD exposures did not have strong effects on antimicrobial resistance or the fecal microbial ecology of beef cattle. |
| first_indexed | 2024-04-11T06:01:40Z |
| format | Article |
| id | doaj.art-2450750e988649a1951162950791635f |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-11T06:01:40Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-2450750e988649a1951162950791635f2022-12-22T04:41:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-12-011310.3389/fmicb.2022.970358970358Evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattleEnrique Doster0Enrique Doster1Lee J. Pinnell2Noelle R. Noyes3Jennifer K. Parker4Cameron A. Anderson5Calvin W. Booker6Sherry J. Hannon7Tim A. McAllister8Sheryl P. Gow9Keith E. Belk10Paul S. Morley11Department of Microbiology, Immunology, & Pathology, Colorado State University, Fort Collins, CO, United StatesVeterinary Education, Research, and Outreach Program, Texas A&M University, Canyon, TX, United StatesVeterinary Education, Research, and Outreach Program, Texas A&M University, Canyon, TX, United StatesDepartment of Veterinary Population Medicine, University of Minnesota, Minneapolis, MN, United StatesDepartment of Microbiology, Immunology, & Pathology, Colorado State University, Fort Collins, CO, United StatesDepartment of Microbiology, Immunology, & Pathology, Colorado State University, Fort Collins, CO, United StatesFeedlot Health Management Services, Okotoks, AB, CanadaFeedlot Health Management Services, Okotoks, AB, CanadaAgriculture and Agri-Food Canada, Lethbridge, AB, CanadaPublic Health Agency of Canada, Saskatoon, SK, CanadaDepartment of Microbiology, Immunology, & Pathology, Colorado State University, Fort Collins, CO, United StatesVeterinary Education, Research, and Outreach Program, Texas A&M University, Canyon, TX, United StatesIntroductionUse of antimicrobial drugs (AMDs) in food producing animals has received increasing scrutiny because of concerns about antimicrobial resistance (AMR) that might affect consumers. Previously, investigations regarding AMR have focused largely on phenotypes of selected pathogens and indicator bacteria, such as Salmonella enterica or Escherichia coli. However, genes conferring AMR are known to be distributed and shared throughout microbial communities. The objectives of this study were to employ target-enriched metagenomic sequencing and 16S rRNA gene amplicon sequencing to investigate the effects of AMD use, in the context of other management and environmental factors, on the resistome and microbiome in beef feedlot cattle.MethodsThis study leveraged samples collected during a previous longitudinal study of cattle at beef feedlots in Canada. This included fecal samples collected from randomly selected individual cattle, as well as composite-fecal samples from randomly selected pens of cattle. All AMD use was recorded and characterized across different drug classes using animal defined daily dose (ADD) metrics.ResultsOverall, fecal resistome composition was dominated by genes conferring resistance to tetracycline and macrolide-lincosamide-streptogramin (MLS) drug classes. The diversity of bacterial phyla was greater early in the feeding period and decreased over time in the feedlot. This decrease in diversity occurred concurrently as the microbiome represented in different individuals and different pens shifted toward a similar composition dominated by Proteobacteria and Firmicutes. Some antimicrobial drug exposures in individuals and groups were associated with explaining a statistically significant proportion of the variance in the resistome, but the amount of variance explained by these important factors was very small (<0.6% variance each), and smaller than associations with other factors measured in this study such as time and feedlot ID. Time in the feedlot was associated with greater changes in the resistome for both individual animals and composite pen-floor samples, although the proportion of the variance associated with this factor was small (2.4% and 1.2%, respectively).DiscussionResults of this study are consistent with other investigations showing that, compared to other factors, AMD exposures did not have strong effects on antimicrobial resistance or the fecal microbial ecology of beef cattle.https://www.frontiersin.org/articles/10.3389/fmicb.2022.970358/fullresistomemicrobiomemicrobial ecologyantimicrobial drug exposureantimicrobial resistancecattle |
| spellingShingle | Enrique Doster Enrique Doster Lee J. Pinnell Noelle R. Noyes Jennifer K. Parker Cameron A. Anderson Calvin W. Booker Sherry J. Hannon Tim A. McAllister Sheryl P. Gow Keith E. Belk Paul S. Morley Evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattle Frontiers in Microbiology resistome microbiome microbial ecology antimicrobial drug exposure antimicrobial resistance cattle |
| title | Evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattle |
| title_full | Evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattle |
| title_fullStr | Evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattle |
| title_full_unstemmed | Evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattle |
| title_short | Evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattle |
| title_sort | evaluating the effects of antimicrobial drug use on the ecology of antimicrobial resistance and microbial community structure in beef feedlot cattle |
| topic | resistome microbiome microbial ecology antimicrobial drug exposure antimicrobial resistance cattle |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.970358/full |
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