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Characterization of the resistome in manure, soil and wastewater from dairy and beef production systems.

Noyes NR, Yang X, Linke LM, Magnuson RJ, Cook SR, Zaheer R, Yang H, Woerner DR, Geornaras I, McArt JA, Gow SP, Ruiz J, Jones KL, Boucher CA, McAllister TA, Belk KE, Morley PS - Sci Rep (2016)

Bottom Line: We utilized shotgun metagenomics to provide a first description of the resistome of North American dairy and beef production effluents, and identify factors that significantly impact this resistome.The majority of resistance-associated sequences found in all samples belonged to tetracycline resistance mechanisms.We found that the ranch samples contained significantly fewer resistance mechanisms than dairy and feedlot samples, and that the resistome of dairy operations differed significantly from that of feedlots.

View Article: PubMed Central - PubMed

Affiliation: Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, USA.

ABSTRACT
It has been proposed that livestock production effluents such as wastewater, airborne dust and manure increase the density of antimicrobial resistant bacteria and genes in the environment. The public health risk posed by this proposed outcome has been difficult to quantify using traditional microbiological approaches. We utilized shotgun metagenomics to provide a first description of the resistome of North American dairy and beef production effluents, and identify factors that significantly impact this resistome. We identified 34 mechanisms of antimicrobial drug resistance within 34 soil, manure and wastewater samples from feedlot, ranch and dairy operations. The majority of resistance-associated sequences found in all samples belonged to tetracycline resistance mechanisms. We found that the ranch samples contained significantly fewer resistance mechanisms than dairy and feedlot samples, and that the resistome of dairy operations differed significantly from that of feedlots. The resistome in soil, manure and wastewater differed, suggesting that management of these effluents should be tailored appropriately. By providing a baseline of the cattle production waste resistome, this study represents a solid foundation for future efforts to characterize and quantify the public health risk posed by livestock effluents.

No MeSH data available.


Beef and dairy systems have different resistomes.NMDS ordination at the mechanism level of (A) (adult) fecal, soil and wastewater samples and (B) only adult fecal samples were both significantly different based on system, e.g., beef vs. dairy (ANOSIM P < 0.05).
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f3: Beef and dairy systems have different resistomes.NMDS ordination at the mechanism level of (A) (adult) fecal, soil and wastewater samples and (B) only adult fecal samples were both significantly different based on system, e.g., beef vs. dairy (ANOSIM P < 0.05).

Mentions: Resistome composition at the mechanism and class levels differed between beef (feedlot and pasture) and dairy operations, for all sample matrices (NMDS Stress = 0.11 and 0.06, ANOSIM R = 0.15 and 0.11, and ANOSIM P = 0.01 and 0.03, respectively, Fig. 3A). However, Shannon’s diversity and richness indices did not differ between beef and dairy cattle (data not shown). Sequencing depth and DNA quality and quantity did not differ significantly between beef and dairy samples. Within fecal samples, ordination at the mechanism level showed clear separation of beef and dairy resistomes (NMDS Stress = 0.006, ANOSIM R = 0.38 and ANOSIM P = 0.03, Fig. 3B); soil and wastewater resistomes of beef versus dairy could not be compared due to data sparseness. Of the 13 classes of resistance identified in all samples collected from adult cattle, 5 were more abundant in beef samples versus dairy, 2 were more abundant in dairy samples, 1 was nearly equally abundant in dairy and beef samples, and 5 did not pass filtering criteria due to low prevalence across samples. Even among classes that did pass filtering, several were present in very low abundance, and therefore estimates of log-fold differences in abundance may not be reliable. Consequently, the discussion is restricted to resistance classes present in at least 10 of the 30 soil, wastewater and adult fecal samples, i.e., tetracyclines, MLS, aminoglycosides, beta-lactams, and general-purpose mechanisms. The MLS resistance class was nearly equally abundant between dairy and beef samples. Alignments to tetracycline ARGs were more abundant in feedlots than in dairies, while aminoglycoside acetyltransferases and phosphotransferases were significantly more abundant in dairy samples. This pattern could reflect differential antimicrobial use practices in feedlots and dairies. Although the American Association of Bovine Practitioners strongly discourages dairy and beef veterinarians from administering aminoglycosides to cattle, nationwide surveys suggest that they are still being used with some frequency in dairies16, much less so in beef feedlots13. In addition, tetracyclines are used more frequently by US feedlots than US dairies, both in-feed and parenterally1316. However, many other factors could account for these differences, including frequency of pen cleaning (which could influence the soil resistome), lagoon construction and management (which could impact the lagoon resistome), and feed composition (which could affect the fecal resistome). In addition, alignments to beta-lactam ARGs were more abundant in feedlot samples, even though these antimicrobial drugs are reported to be much more widely used in dairy production1352. These findings highlight the complexity of dynamics between antimicrobial use and AMR, and suggest that use practices do not solely or directly influence AMR patterns in livestock production.


Characterization of the resistome in manure, soil and wastewater from dairy and beef production systems.

Noyes NR, Yang X, Linke LM, Magnuson RJ, Cook SR, Zaheer R, Yang H, Woerner DR, Geornaras I, McArt JA, Gow SP, Ruiz J, Jones KL, Boucher CA, McAllister TA, Belk KE, Morley PS - Sci Rep (2016)

Beef and dairy systems have different resistomes.NMDS ordination at the mechanism level of (A) (adult) fecal, soil and wastewater samples and (B) only adult fecal samples were both significantly different based on system, e.g., beef vs. dairy (ANOSIM P < 0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4837390&req=5

f3: Beef and dairy systems have different resistomes.NMDS ordination at the mechanism level of (A) (adult) fecal, soil and wastewater samples and (B) only adult fecal samples were both significantly different based on system, e.g., beef vs. dairy (ANOSIM P < 0.05).
Mentions: Resistome composition at the mechanism and class levels differed between beef (feedlot and pasture) and dairy operations, for all sample matrices (NMDS Stress = 0.11 and 0.06, ANOSIM R = 0.15 and 0.11, and ANOSIM P = 0.01 and 0.03, respectively, Fig. 3A). However, Shannon’s diversity and richness indices did not differ between beef and dairy cattle (data not shown). Sequencing depth and DNA quality and quantity did not differ significantly between beef and dairy samples. Within fecal samples, ordination at the mechanism level showed clear separation of beef and dairy resistomes (NMDS Stress = 0.006, ANOSIM R = 0.38 and ANOSIM P = 0.03, Fig. 3B); soil and wastewater resistomes of beef versus dairy could not be compared due to data sparseness. Of the 13 classes of resistance identified in all samples collected from adult cattle, 5 were more abundant in beef samples versus dairy, 2 were more abundant in dairy samples, 1 was nearly equally abundant in dairy and beef samples, and 5 did not pass filtering criteria due to low prevalence across samples. Even among classes that did pass filtering, several were present in very low abundance, and therefore estimates of log-fold differences in abundance may not be reliable. Consequently, the discussion is restricted to resistance classes present in at least 10 of the 30 soil, wastewater and adult fecal samples, i.e., tetracyclines, MLS, aminoglycosides, beta-lactams, and general-purpose mechanisms. The MLS resistance class was nearly equally abundant between dairy and beef samples. Alignments to tetracycline ARGs were more abundant in feedlots than in dairies, while aminoglycoside acetyltransferases and phosphotransferases were significantly more abundant in dairy samples. This pattern could reflect differential antimicrobial use practices in feedlots and dairies. Although the American Association of Bovine Practitioners strongly discourages dairy and beef veterinarians from administering aminoglycosides to cattle, nationwide surveys suggest that they are still being used with some frequency in dairies16, much less so in beef feedlots13. In addition, tetracyclines are used more frequently by US feedlots than US dairies, both in-feed and parenterally1316. However, many other factors could account for these differences, including frequency of pen cleaning (which could influence the soil resistome), lagoon construction and management (which could impact the lagoon resistome), and feed composition (which could affect the fecal resistome). In addition, alignments to beta-lactam ARGs were more abundant in feedlot samples, even though these antimicrobial drugs are reported to be much more widely used in dairy production1352. These findings highlight the complexity of dynamics between antimicrobial use and AMR, and suggest that use practices do not solely or directly influence AMR patterns in livestock production.

Bottom Line: We utilized shotgun metagenomics to provide a first description of the resistome of North American dairy and beef production effluents, and identify factors that significantly impact this resistome.The majority of resistance-associated sequences found in all samples belonged to tetracycline resistance mechanisms.We found that the ranch samples contained significantly fewer resistance mechanisms than dairy and feedlot samples, and that the resistome of dairy operations differed significantly from that of feedlots.

View Article: PubMed Central - PubMed

Affiliation: Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, USA.

ABSTRACT
It has been proposed that livestock production effluents such as wastewater, airborne dust and manure increase the density of antimicrobial resistant bacteria and genes in the environment. The public health risk posed by this proposed outcome has been difficult to quantify using traditional microbiological approaches. We utilized shotgun metagenomics to provide a first description of the resistome of North American dairy and beef production effluents, and identify factors that significantly impact this resistome. We identified 34 mechanisms of antimicrobial drug resistance within 34 soil, manure and wastewater samples from feedlot, ranch and dairy operations. The majority of resistance-associated sequences found in all samples belonged to tetracycline resistance mechanisms. We found that the ranch samples contained significantly fewer resistance mechanisms than dairy and feedlot samples, and that the resistome of dairy operations differed significantly from that of feedlots. The resistome in soil, manure and wastewater differed, suggesting that management of these effluents should be tailored appropriately. By providing a baseline of the cattle production waste resistome, this study represents a solid foundation for future efforts to characterize and quantify the public health risk posed by livestock effluents.

No MeSH data available.