Farm dust resistomes and bacterial microbiomes in European poultry and pig farms

Luiken, Roosmarijn E C; Gompel, Liese Van; Bossers, Alex; Munk, Patrick; Joosten, Philip; Hansen, Rasmus Borup; Knudsen, Berith Elkær; García-Cobos, Silvia; Dewulf, Jeroen; Aarestrup, Frank Møller; Wagenaar, Jaap A.; Smit, Lidwien A M; Mevius, Dik; Heederik, Dick; Schmitt, Heike

doi:10.1016/j.envint.2020.105971

Cited by 80 publications

(81 citation statements)

References 37 publications

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“…In addition, the strong effect shown by sample type in the resistome was also observed for the bacterial microbiome composition, with, for instance, the dominance of Proteobacteria in environmental samples, in contrast with a more diverse taxonomy in feces and slurry, with the predominance of members of the Firmicutes phylum. These findings suggested an association between the resistome and the microbiome, which was further supported by Procrustes analyses, evidencing that changes in the environment and slurry resistomes were linked to shifts in the microbial populations dominating these niches, as it has been recently reported on pig farms [29]. Some major differences between the resistome of feces and farm environments were found, for instance, in the abundance of ARGs assigned to Enterobacteriaceae.…”

Section: Discussionsupporting

confidence: 76%

“…A total of 105 DNA samples were sequenced from these 38 independent herds, including three DNA extraction negative controls. The samples were divided into environment (38), feces (38), and slurry (29). Prior to DNA extraction, fecal samples from each farm were pooled by stirring thoroughly with a sterile tongue depressor using 3 g per individual sample, obtaining a final composite sample of 15 g. After its homogenization, 2 g were soaked in 18 ml of PBS 1× and vigorously mixed for 5 min using a Stomacher Laboratory Blender (Seward, Worthing, UK).…”

Section: Sample Processing Dna Extraction Library Preparation and mentioning

confidence: 99%

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Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms

et al. 2020

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Background The global threat of antimicrobial resistance (AMR) is a One Health problem impacted by antimicrobial use (AMU) for human and livestock applications. Extensive Iberian swine production is based on a more sustainable and eco-friendly management system, providing an excellent opportunity to evaluate how sustained differences in AMU impact the resistome, not only in the animals but also on the farm environment. Here, we evaluate the resistome footprint of an extensive pig farming system, maintained for decades, as compared to that of industrialized intensive pig farming by analyzing 105 fecal, environmental and slurry metagenomes from 38 farms. Results Our results evidence a significantly higher abundance of antimicrobial resistance genes (ARGs) on intensive farms and a link between AMU and AMR to certain antimicrobial classes. We observed differences in the resistome across sample types, with a higher richness and dispersion of ARGs within environmental samples than on those from feces or slurry. Indeed, a deeper analysis revealed that differences among the three sample types were defined by taxa-ARGs associations. Interestingly, mobilome analyses revealed that the observed AMR differences between intensive and extensive farms could be linked to differences in the abundance of mobile genetic elements (MGEs). Thus, while there were no differences in the abundance of chromosomal-associated ARGs between intensive and extensive herds, a significantly higher abundance of integrons in the environment and plasmids, regardless of the sample type, was detected on intensive farms. Conclusions Overall, this study shows how AMU, production system, and sample type influence, mainly through MGEs, the profile and dispersion of ARGs in pig production.

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Section: Discussionsupporting

confidence: 76%

Section: Sample Processing Dna Extraction Library Preparation and mentioning

confidence: 99%

Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms

et al. 2020

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“…Phylogenetic analyses indicated that viruses identified from farm dust samples were genetically closely related to viruses identified from chicken feces collected from the same farm, suggesting that viruses identified in dust were attributed to the viruses circulating in the chicken feces that is also source of farm dust. This observation is in agreement with a previous study that reported the correlation found in the resistomes between animal feces and farm dust (46). More importantly, the detection of chicken-related virus sequences in dust samples raises the possibility of dust-borne transmission of viruses especially important in the cases of chicken and/or zoonotic pathogenic viruses (47), although infectivity of the viruses identified was not confirmed as no virus culture was performed in our study.…”

Section: Discussionsupporting

confidence: 94%

Establishing farm dust as a useful viral metagenomic surveillance matrix

Kwok¹,

Rooij

et al. 2021

Preprint

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Livestock animals housed in close proximity to humans can act as sources or intermediate hosts facilitating animal-to-human transmission of zoonotic diseases. Understanding virus diversity in livestock is important for identifying potential zoonotic threats and for ensuring animal health and safe livestock production. Here, we report viral metagenomic characterization of chicken feces (N=51) and paired farm dust samples (N=13) using metagenomic deep sequencing. Samples were collected at 4-5 time points in three broiler farms in the Netherlands. Viruses in the Parvoviridae and Picornaviridae families were the most prevalent, detected in all feces and dust samples and in all feces and 85% of dust samples, respectively. Virus composition found in chicken feces and corresponding dust samples were similar. Great genomic diversity was identified in Picornaviridae and 46 sequences from five picornavirus genera (Sicinivirus, Megrivirus, Anatvirus, Gallivirus and Avisvirus) were detected. For calicivirus, Basovirus and an unclassified novel chicken calicivirus were identified in 13 fecal and 1 dust samples. Two distinct types of chicken astroviruses were identified. Phylogenetic analyses of identified virus sequences from Picornaviridae, Astroviridae and Caliciviridae suggested that viral sequences obtained from different farms are often more closely related to each other than global reference sequences, and sequences from feces and paired dust samples also clustered together. Importantly, our sequencing methodology enabled the recover viral genome sequences from farm dusts, allowing the tracking of virus chatter between livestock animals and their farm environment. This study, albeit relative sample size, does expand current knowledge of virus communities in chickens and surrounding dusts.

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“…Furthermore, the E. coli from farm 5 had lower resistance rates for 8 of the antibiotic types tested ( Figure 2 A). Some studies have reported that animal feces and farm dust were important reservoirs for resistant bacteria and antibiotic resistance genes ( Furtula et al., 2010 ; Chuppava et al., 2019 ; Luiken et al., 2019 , 2020 ), and that antibiotic-resistant bacteria can spread antibiotic resistance to the environment through animal manure. This suggests that there is an accumulation of resistance in response to the long-term use of antibiotics, leading to a higher prevalence of drug-resistant microbes on older farms than on newer ones; however, other environmental factors cannot be discounted.…”

Section: Discussionmentioning

confidence: 99%

Longitudinal monitoring of multidrug resistance in Escherichia coli on broiler chicken fattening farms in Shandong, China

et al. 2021

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The extensive use of antibiotics has, in recent years, caused antimicrobial resistance and multidrug resistance in Escherichia coli to gradually develop into a worldwide problem. These resistant E. coli could be transmitted to humans through animal products and animal feces in the environment, thereby creating a problem for bacterial treatment for humans and animals and resulting in a public health issue. Monitoring the resistance of E. coli throughout the broiler fattening period is therefore of great significance for both the poultry industry and public health. In this longitudinal study, samples were taken from 6 conventional broiler fattening farms in Shandong Province, China, at 3 different times within 1 fattening period. The overall isolation rate of E. coli was 53.04% (375/707). Antibiotic resistance was very common in the E. coli isolated from these farms, and differed for different antibiotics, with ampicillin having the highest rate (92.86%) and cefoxitin the lowest (10.12%). Multidrug resistance was as high as 91.07%. More importantly, both the resistance rate of E. coli to the different drugs and the detection rate of drug resistance genes increased over time. The mobile colistin resistance ( mcr-1 ) gene was detected in 24.40% of the strains, and these strains often carried other drug resistance genes, such as those conferring aminoglycoside, β-lactamase, tetracycline, and sulfonamide resistance. Antimicrobial resistance and drug resistance genes in E. coli were least common in the early fattening stage. The individual detection rates of sul1 , sul3 , aacC4 , aphA3 , and mcr-1 were significantly lower ( P < 0.05) for the early fattening stage than for the middle and late stages. The rational use of antibiotics, in conjunction with the improvement of the breeding environment during the entire broiler fattening cycle, will be helpful in the development of the poultry industry and the protection of public health.

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Farm dust resistomes and bacterial microbiomes in European poultry and pig farms

Cited by 80 publications

References 37 publications

Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms

Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms

Establishing farm dust as a useful viral metagenomic surveillance matrix

Longitudinal monitoring of multidrug resistance in Escherichia coli on broiler chicken fattening farms in Shandong, China

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