Characterization of the Microbial Resistome in Conventional and “Raised Without Antibiotics” Beef and Dairy Production Systems
Metagenomic investigations have the potential to provide unprecedented insights into microbial ecologies, such as those relating to antimicrobial resistance (AMR). We characterized the microbial resistome in livestock operations raising cattle conventionally (CONV) or without antibiotic exposures (R...
| Main Authors: | , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-09-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.01980/full |
| _version_ | 1828875806026235904 |
|---|---|
| author | Pablo Rovira Tim McAllister Steven M. Lakin Shaun R. Cook Enrique Doster Noelle R. Noyes Maggie D. Weinroth Xiang Yang Jennifer K. Parker Christina Boucher Calvin W. Booker Dale R. Woerner Keith E. Belk Paul S. Morley |
| author_facet | Pablo Rovira Tim McAllister Steven M. Lakin Shaun R. Cook Enrique Doster Noelle R. Noyes Maggie D. Weinroth Xiang Yang Jennifer K. Parker Christina Boucher Calvin W. Booker Dale R. Woerner Keith E. Belk Paul S. Morley |
| author_sort | Pablo Rovira |
| collection | DOAJ |
| description | Metagenomic investigations have the potential to provide unprecedented insights into microbial ecologies, such as those relating to antimicrobial resistance (AMR). We characterized the microbial resistome in livestock operations raising cattle conventionally (CONV) or without antibiotic exposures (RWA) using shotgun metagenomics. Samples of feces, wastewater from catchment basins, and soil where wastewater was applied were collected from CONV and RWA feedlot and dairy farms. After DNA extraction and sequencing, shotgun metagenomic reads were aligned to reference databases for identification of bacteria (Kraken) and antibiotic resistance genes (ARGs) accessions (MEGARes). Differences in microbial resistomes were found across farms with different production practices (CONV vs. RWA), types of cattle (beef vs. dairy), and types of sample (feces vs. wastewater vs. soil). Feces had the greatest number of ARGs per sample (mean = 118 and 79 in CONV and RWA, respectively), with tetracycline efflux pumps, macrolide phosphotransferases, and aminoglycoside nucleotidyltransferases mechanisms of resistance more abundant in CONV than in RWA feces. Tetracycline and macrolide–lincosamide–streptogramin classes of resistance were more abundant in feedlot cattle than in dairy cow feces, whereas the β-lactam class was more abundant in dairy cow feces. Lack of congruence between ARGs and microbial communities (procrustes analysis) suggested that other factors (e.g., location of farms, cattle source, management practices, diet, horizontal ARGs transfer, and co-selection of resistance), in addition to antimicrobial use, could have impacted resistome profiles. For that reason, we could not establish a cause–effect relationship between antimicrobial use and AMR, although ARGs in feces and effluents were associated with drug classes used to treat animals according to farms’ records (tetracyclines and macrolides in feedlots, β-lactams in dairies), whereas ARGs in soil were dominated by multidrug resistance. Characterization of the “resistance potential” of animal-derived and environmental samples is the first step toward incorporating metagenomic approaches into AMR surveillance in agricultural systems. Further research is needed to assess the public-health risk associated with different microbial resistomes. |
| first_indexed | 2024-12-13T08:06:49Z |
| format | Article |
| id | doaj.art-1438d350ff714b3b9f45a93f5805736b |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-13T08:06:49Z |
| publishDate | 2019-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-1438d350ff714b3b9f45a93f5805736b2022-12-21T23:54:18ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-09-011010.3389/fmicb.2019.01980460814Characterization of the Microbial Resistome in Conventional and “Raised Without Antibiotics” Beef and Dairy Production SystemsPablo Rovira0Tim McAllister1Steven M. Lakin2Shaun R. Cook3Enrique Doster4Noelle R. Noyes5Maggie D. Weinroth6Xiang Yang7Jennifer K. Parker8Christina Boucher9Calvin W. Booker10Dale R. Woerner11Keith E. Belk12Paul S. Morley13Department of Animal Sciences, College of Agricultural Sciences, Colorado State University, Fort Collins, CO, United StatesLethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, AB, CanadaDepartment of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, United StatesAlberta Agriculture and Forestry, Lethbridge, AB, CanadaDepartment of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, United StatesVeterinary Population Medicine Department, University of Minnesota, St. Paul, MN, United StatesDepartment of Animal Sciences, College of Agricultural Sciences, Colorado State University, Fort Collins, CO, United StatesDepartment of Animal Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Molecular Biosciences, University of Texas, Austin, TX, United StatesDepartment of Computer and Information Science and Engineering, University of Florida, Gainesville, FL, United StatesFeedlot Health Management Services, Ltd., Okotoks, AB, Canada0Department of Animal and Food Sciences, College of Agricultural Sciences & Natural Resources, Texas Tech University, Lubbock, TX, United StatesDepartment of Animal Sciences, College of Agricultural Sciences, Colorado State University, Fort Collins, CO, United States1VERO - Veterinary Education, Research, and Outreach Program, Texas A&M University and West Texas A&M University, Canyon, TX, United StatesMetagenomic investigations have the potential to provide unprecedented insights into microbial ecologies, such as those relating to antimicrobial resistance (AMR). We characterized the microbial resistome in livestock operations raising cattle conventionally (CONV) or without antibiotic exposures (RWA) using shotgun metagenomics. Samples of feces, wastewater from catchment basins, and soil where wastewater was applied were collected from CONV and RWA feedlot and dairy farms. After DNA extraction and sequencing, shotgun metagenomic reads were aligned to reference databases for identification of bacteria (Kraken) and antibiotic resistance genes (ARGs) accessions (MEGARes). Differences in microbial resistomes were found across farms with different production practices (CONV vs. RWA), types of cattle (beef vs. dairy), and types of sample (feces vs. wastewater vs. soil). Feces had the greatest number of ARGs per sample (mean = 118 and 79 in CONV and RWA, respectively), with tetracycline efflux pumps, macrolide phosphotransferases, and aminoglycoside nucleotidyltransferases mechanisms of resistance more abundant in CONV than in RWA feces. Tetracycline and macrolide–lincosamide–streptogramin classes of resistance were more abundant in feedlot cattle than in dairy cow feces, whereas the β-lactam class was more abundant in dairy cow feces. Lack of congruence between ARGs and microbial communities (procrustes analysis) suggested that other factors (e.g., location of farms, cattle source, management practices, diet, horizontal ARGs transfer, and co-selection of resistance), in addition to antimicrobial use, could have impacted resistome profiles. For that reason, we could not establish a cause–effect relationship between antimicrobial use and AMR, although ARGs in feces and effluents were associated with drug classes used to treat animals according to farms’ records (tetracyclines and macrolides in feedlots, β-lactams in dairies), whereas ARGs in soil were dominated by multidrug resistance. Characterization of the “resistance potential” of animal-derived and environmental samples is the first step toward incorporating metagenomic approaches into AMR surveillance in agricultural systems. Further research is needed to assess the public-health risk associated with different microbial resistomes.https://www.frontiersin.org/article/10.3389/fmicb.2019.01980/fullcattleantibiotic resistanceresistomemicrobiomemetagenomics |
| spellingShingle | Pablo Rovira Tim McAllister Steven M. Lakin Shaun R. Cook Enrique Doster Noelle R. Noyes Maggie D. Weinroth Xiang Yang Jennifer K. Parker Christina Boucher Calvin W. Booker Dale R. Woerner Keith E. Belk Paul S. Morley Characterization of the Microbial Resistome in Conventional and “Raised Without Antibiotics” Beef and Dairy Production Systems Frontiers in Microbiology cattle antibiotic resistance resistome microbiome metagenomics |
| title | Characterization of the Microbial Resistome in Conventional and “Raised Without Antibiotics” Beef and Dairy Production Systems |
| title_full | Characterization of the Microbial Resistome in Conventional and “Raised Without Antibiotics” Beef and Dairy Production Systems |
| title_fullStr | Characterization of the Microbial Resistome in Conventional and “Raised Without Antibiotics” Beef and Dairy Production Systems |
| title_full_unstemmed | Characterization of the Microbial Resistome in Conventional and “Raised Without Antibiotics” Beef and Dairy Production Systems |
| title_short | Characterization of the Microbial Resistome in Conventional and “Raised Without Antibiotics” Beef and Dairy Production Systems |
| title_sort | characterization of the microbial resistome in conventional and raised without antibiotics beef and dairy production systems |
| topic | cattle antibiotic resistance resistome microbiome metagenomics |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.01980/full |
| work_keys_str_mv | AT pablorovira characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT timmcallister characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT stevenmlakin characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT shaunrcook characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT enriquedoster characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT noellernoyes characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT maggiedweinroth characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT xiangyang characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT jenniferkparker characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT christinaboucher characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT calvinwbooker characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT dalerwoerner characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT keithebelk characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems AT paulsmorley characterizationofthemicrobialresistomeinconventionalandraisedwithoutantibioticsbeefanddairyproductionsystems |