Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes
Abstract Background Research is needed to delineate the relative and combined effects of different antibiotic administration and manure management practices in either amplifying or attenuating the potential for antibiotic resistance to spread. Here, we carried out a comprehensive parallel examinatio...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2021-04-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-021-01006-z |
| _version_ | 1818611180138135552 |
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| author | Ishi Keenum Robert K. Williams Partha Ray Emily D. Garner Katharine F. Knowlton Amy Pruden |
| author_facet | Ishi Keenum Robert K. Williams Partha Ray Emily D. Garner Katharine F. Knowlton Amy Pruden |
| author_sort | Ishi Keenum |
| collection | DOAJ |
| description | Abstract Background Research is needed to delineate the relative and combined effects of different antibiotic administration and manure management practices in either amplifying or attenuating the potential for antibiotic resistance to spread. Here, we carried out a comprehensive parallel examination of the effects of small-scale (> 55 °C × 3 days) static and turned composting of manures from dairy and beef cattle collected during standard antibiotic administration (cephapirin/pirlimycin or sulfamethazine/chlortetracycline/tylosin, respectively), versus from untreated cattle, on “resistomes” (total antibiotic resistance genes (ARGs) determined via shotgun metagenomic sequencing), bacterial microbiota, and indicator ARGs enumerated via quantitative polymerase chain reaction. To gain insight into the role of the thermophilic phase, compost was also externally heated to > 55 °C × 15 days. Results Progression of composting with time and succession of the corresponding bacterial microbiota was the overarching driver of the resistome composition (ANOSIM; R = 0.424, p = 0.001, respectively) in all composts at the small-scale. Reduction in relative abundance (16S rRNA gene normalized) of total ARGs in finished compost (day 42) versus day 0 was noted across all conditions (ANOSIM; R = 0.728, p = 0.001), except when externally heated. Sul1, intI1, beta-lactam ARGs, and plasmid-associated genes increased in all finished composts as compared with the initial condition. External heating more effectively reduced certain clinically relevant ARGs (bla OXA, bla CARB), fecal coliforms, and resistome risk scores, which take into account putative pathogen annotations. When manure was collected during antibiotic administration, taxonomic composition of the compost was distinct according to nonmetric multidimensional analysis and tet(W) decayed faster in the dairy manure with antibiotic condition and slower in the beef manure with antibiotic condition. Conclusions This comprehensive, integrated study revealed that composting had a dominant effect on corresponding resistome composition, while little difference was noted as a function of collecting manure during antibiotic administration. Reduction in total ARGs, tet(W), and resistome risk suggested that composting reduced some potential for antibiotic resistance to spread, but the increase and persistence of other indicators of antibiotic resistance were concerning. Results indicate that composting guidelines intended for pathogen reduction do not necessarily provide a comprehensive barrier to ARGs or their mobility prior to land application and additional mitigation measures should be considered. Video Abstract. |
| first_indexed | 2024-12-16T15:26:14Z |
| format | Article |
| id | doaj.art-2afa88b003ed40c898ae5044dc49d478 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-16T15:26:14Z |
| publishDate | 2021-04-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-2afa88b003ed40c898ae5044dc49d4782022-12-21T22:26:30ZengBMCMicrobiome2049-26182021-04-019111610.1186/s40168-021-01006-zCombined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genesIshi Keenum0Robert K. Williams1Partha Ray2Emily D. Garner3Katharine F. Knowlton4Amy Pruden5Department of Civil and Environmental Engineering, Virginia TechDepartment of Civil and Environmental Engineering, Virginia TechDepartment of Animal Sciences, School of Agriculture, Policy and Development, University of ReadingDepartment of Civil and Environmental Engineering, Virginia TechDepartment of Dairy Science, Virginia TechDepartment of Civil and Environmental Engineering, Virginia TechAbstract Background Research is needed to delineate the relative and combined effects of different antibiotic administration and manure management practices in either amplifying or attenuating the potential for antibiotic resistance to spread. Here, we carried out a comprehensive parallel examination of the effects of small-scale (> 55 °C × 3 days) static and turned composting of manures from dairy and beef cattle collected during standard antibiotic administration (cephapirin/pirlimycin or sulfamethazine/chlortetracycline/tylosin, respectively), versus from untreated cattle, on “resistomes” (total antibiotic resistance genes (ARGs) determined via shotgun metagenomic sequencing), bacterial microbiota, and indicator ARGs enumerated via quantitative polymerase chain reaction. To gain insight into the role of the thermophilic phase, compost was also externally heated to > 55 °C × 15 days. Results Progression of composting with time and succession of the corresponding bacterial microbiota was the overarching driver of the resistome composition (ANOSIM; R = 0.424, p = 0.001, respectively) in all composts at the small-scale. Reduction in relative abundance (16S rRNA gene normalized) of total ARGs in finished compost (day 42) versus day 0 was noted across all conditions (ANOSIM; R = 0.728, p = 0.001), except when externally heated. Sul1, intI1, beta-lactam ARGs, and plasmid-associated genes increased in all finished composts as compared with the initial condition. External heating more effectively reduced certain clinically relevant ARGs (bla OXA, bla CARB), fecal coliforms, and resistome risk scores, which take into account putative pathogen annotations. When manure was collected during antibiotic administration, taxonomic composition of the compost was distinct according to nonmetric multidimensional analysis and tet(W) decayed faster in the dairy manure with antibiotic condition and slower in the beef manure with antibiotic condition. Conclusions This comprehensive, integrated study revealed that composting had a dominant effect on corresponding resistome composition, while little difference was noted as a function of collecting manure during antibiotic administration. Reduction in total ARGs, tet(W), and resistome risk suggested that composting reduced some potential for antibiotic resistance to spread, but the increase and persistence of other indicators of antibiotic resistance were concerning. Results indicate that composting guidelines intended for pathogen reduction do not necessarily provide a comprehensive barrier to ARGs or their mobility prior to land application and additional mitigation measures should be considered. Video Abstract.https://doi.org/10.1186/s40168-021-01006-zCompostMicrobial community SuccessionThermophilic stressSelection pressureAntibiotic resistance |
| spellingShingle | Ishi Keenum Robert K. Williams Partha Ray Emily D. Garner Katharine F. Knowlton Amy Pruden Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes Microbiome Compost Microbial community Succession Thermophilic stress Selection pressure Antibiotic resistance |
| title | Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes |
| title_full | Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes |
| title_fullStr | Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes |
| title_full_unstemmed | Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes |
| title_short | Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes |
| title_sort | combined effects of composting and antibiotic administration on cattle manure borne antibiotic resistance genes |
| topic | Compost Microbial community Succession Thermophilic stress Selection pressure Antibiotic resistance |
| url | https://doi.org/10.1186/s40168-021-01006-z |
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