Anaerobic Digestion of Tetracycline Spiked Livestock Manure and Poultry Litter Increased the Abundances of Antibiotic and Heavy Metal Resistance Genes

Anaerobic digestion is used for the treatment of animal manure by generating biogas. Heavy metals cause environmental pollutions and co-select for antimicrobial resistance. We evaluated the impact of mesophilic anaerobic digestion of cattle manure (CM), swine manure (SM) and poultry litter (PL) on t...

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Main Authors: Getahun E. Agga, John Kasumba, John H. Loughrin, Eric D. Conte
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.614424/full
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author Getahun E. Agga
John Kasumba
John H. Loughrin
Eric D. Conte
author_facet Getahun E. Agga
John Kasumba
John H. Loughrin
Eric D. Conte
author_sort Getahun E. Agga
collection DOAJ
description Anaerobic digestion is used for the treatment of animal manure by generating biogas. Heavy metals cause environmental pollutions and co-select for antimicrobial resistance. We evaluated the impact of mesophilic anaerobic digestion of cattle manure (CM), swine manure (SM) and poultry litter (PL) on the concentrations of seven tetracycline [tet(A), tet(B), tet(G), tet(M), tet(O), tet(Q), and tet(W)], macrolide [erm(B)], methicillin (mecA and mecC), copper (copB, pcoA, pcoD, and tcrB) and zinc (czrC) resistance genes, and three bacterial species (E. coli, Enterococcus spp. and Staphylococcus aureus). The total bacterial population and total abundance of the seven tet genes significantly increased in the three manure types after digestion. Concentration of tet(M) was strongly correlated with that of erm(B) and enterococci. As concentration of tetracyclines declined during anaerobic digestion, that of four tet genes (A, B, Q, and W) and 16S rRNA increased, that of tet(M) decreased, and that of tet(G) and tet(O) did not change. Concentrations of copB and pcoA did not change; while that of pcoD did not change in the PL, it increased in the SM and CM. While the concentration of enterococci remained unchanged in CM, it significantly increased in the PL and SM. Concentrations of tcrB significantly increased in the three manure types. While concentrations of S. aureus significantly increased in the CM and PL, that of SM was not affected. Concentrations of mecC significantly increased in all manure types after digestion; while mecA concentrations did not change in the SM, they significantly increased in CM and PL. While concentration of czrC remained low in the CM, it increased in the PL but declined in the SM. In conclusion, while mesophilic anaerobic digestion of animal manure decreased concentration of tetracyclines, it increased the concentrations of total bacteria, tet genes, E. coli, enterococci and S. aureus and methicillin resistance genes. It did not have any effect on concentrations of heavy metals; concentrations of heavy metal resistance genes either increased or remained unaffected depending on the animal species. This study showed the need for post-digestion treatments of animal manure to remove bacteria, antibiotic resistance genes, heavy metals and their resistance genes.
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spelling doaj.art-c6668a75ef0a4776ab9a65007608b14a2022-12-21T19:00:48ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-12-011110.3389/fmicb.2020.614424614424Anaerobic Digestion of Tetracycline Spiked Livestock Manure and Poultry Litter Increased the Abundances of Antibiotic and Heavy Metal Resistance GenesGetahun E. Agga0John Kasumba1John H. Loughrin2Eric D. Conte3USDA, Agricultural Research Service, Food Animal Environmental Systems Research Unit, Bowling Green, KY, United StatesDepartment of Chemistry, Western Kentucky University, Bowling Green, KY, United StatesUSDA, Agricultural Research Service, Food Animal Environmental Systems Research Unit, Bowling Green, KY, United StatesDepartment of Chemistry, Western Kentucky University, Bowling Green, KY, United StatesAnaerobic digestion is used for the treatment of animal manure by generating biogas. Heavy metals cause environmental pollutions and co-select for antimicrobial resistance. We evaluated the impact of mesophilic anaerobic digestion of cattle manure (CM), swine manure (SM) and poultry litter (PL) on the concentrations of seven tetracycline [tet(A), tet(B), tet(G), tet(M), tet(O), tet(Q), and tet(W)], macrolide [erm(B)], methicillin (mecA and mecC), copper (copB, pcoA, pcoD, and tcrB) and zinc (czrC) resistance genes, and three bacterial species (E. coli, Enterococcus spp. and Staphylococcus aureus). The total bacterial population and total abundance of the seven tet genes significantly increased in the three manure types after digestion. Concentration of tet(M) was strongly correlated with that of erm(B) and enterococci. As concentration of tetracyclines declined during anaerobic digestion, that of four tet genes (A, B, Q, and W) and 16S rRNA increased, that of tet(M) decreased, and that of tet(G) and tet(O) did not change. Concentrations of copB and pcoA did not change; while that of pcoD did not change in the PL, it increased in the SM and CM. While the concentration of enterococci remained unchanged in CM, it significantly increased in the PL and SM. Concentrations of tcrB significantly increased in the three manure types. While concentrations of S. aureus significantly increased in the CM and PL, that of SM was not affected. Concentrations of mecC significantly increased in all manure types after digestion; while mecA concentrations did not change in the SM, they significantly increased in CM and PL. While concentration of czrC remained low in the CM, it increased in the PL but declined in the SM. In conclusion, while mesophilic anaerobic digestion of animal manure decreased concentration of tetracyclines, it increased the concentrations of total bacteria, tet genes, E. coli, enterococci and S. aureus and methicillin resistance genes. It did not have any effect on concentrations of heavy metals; concentrations of heavy metal resistance genes either increased or remained unaffected depending on the animal species. This study showed the need for post-digestion treatments of animal manure to remove bacteria, antibiotic resistance genes, heavy metals and their resistance genes.https://www.frontiersin.org/articles/10.3389/fmicb.2020.614424/fullantimicrobial resistanceantimicrobial resistance genesanaerobic digestiontetracycline resistanceheavy metal resistanceanimal manure
spellingShingle Getahun E. Agga
John Kasumba
John H. Loughrin
Eric D. Conte
Anaerobic Digestion of Tetracycline Spiked Livestock Manure and Poultry Litter Increased the Abundances of Antibiotic and Heavy Metal Resistance Genes
Frontiers in Microbiology
antimicrobial resistance
antimicrobial resistance genes
anaerobic digestion
tetracycline resistance
heavy metal resistance
animal manure
title Anaerobic Digestion of Tetracycline Spiked Livestock Manure and Poultry Litter Increased the Abundances of Antibiotic and Heavy Metal Resistance Genes
title_full Anaerobic Digestion of Tetracycline Spiked Livestock Manure and Poultry Litter Increased the Abundances of Antibiotic and Heavy Metal Resistance Genes
title_fullStr Anaerobic Digestion of Tetracycline Spiked Livestock Manure and Poultry Litter Increased the Abundances of Antibiotic and Heavy Metal Resistance Genes
title_full_unstemmed Anaerobic Digestion of Tetracycline Spiked Livestock Manure and Poultry Litter Increased the Abundances of Antibiotic and Heavy Metal Resistance Genes
title_short Anaerobic Digestion of Tetracycline Spiked Livestock Manure and Poultry Litter Increased the Abundances of Antibiotic and Heavy Metal Resistance Genes
title_sort anaerobic digestion of tetracycline spiked livestock manure and poultry litter increased the abundances of antibiotic and heavy metal resistance genes
topic antimicrobial resistance
antimicrobial resistance genes
anaerobic digestion
tetracycline resistance
heavy metal resistance
animal manure
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.614424/full
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AT johnkasumba anaerobicdigestionoftetracyclinespikedlivestockmanureandpoultrylitterincreasedtheabundancesofantibioticandheavymetalresistancegenes
AT johnhloughrin anaerobicdigestionoftetracyclinespikedlivestockmanureandpoultrylitterincreasedtheabundancesofantibioticandheavymetalresistancegenes
AT ericdconte anaerobicdigestionoftetracyclinespikedlivestockmanureandpoultrylitterincreasedtheabundancesofantibioticandheavymetalresistancegenes