A multiplayer game: species of Clostridium, Acinetobacter, and Pseudomonas are responsible for the persistence of antibiotic resistance genes in manure‐treated soils

Leclercq, Sébastien; Wang, Chao; Sui, Zhi-Hai; Wu, Hai; Zhu, Baoli; Deng, Ye; Feng, Jie

doi:10.1111/1462-2920.13337

Cited by 92 publications

(35 citation statements)

References 77 publications

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“…This prevalence is considerably higher than the levels reported before [27]. Although some studies report that Salmonella can survive up to four months on the soils upon fertilization, it can be assumed that the majority of the manure-associated bacteria including pathogens die off within two weeks after fertilization [28]. It cannot be excluded that this pathogen is further spread by wild fauna, e.g., by wild birds picking grains after sowing.…”

Section: Discussionmentioning

confidence: 83%

Antibiotic Residues and Antibiotic-Resistant Bacteria in Pig Slurry Used to Fertilize Agricultural Fields

et al. 2020

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Pig manure may contain antibiotic residues, antibiotic-resistant bacteria or pathogens, which may reach the environment upon fertilization. During this study, 69 antibiotic residues belonging to 12 classes were quantified in 89 pig slurry samples. These samples were also studied for the presence of Salmonella and for E. coli resistant to meropenem, colistin, ciprofloxacin, or cefotaxim. The obtained isolates were further tested for antibacterial susceptibility. No antibiotic residues were detected in four samples, whereas in the other samples, up to 12 antibiotics were found. The most frequently detected antibiotic residues were doxycycline, sulfadiazine, and lincomycin. Doxycycline was found in the highest concentration with a mean of 1476 µg/kg manure (range: 18–13632 µg/kg). Tylosin and oxytetracycline were found with mean concentrations of 784 µg/kg (range: 17–5599 µg/kg) and 482 µg/kg (range: 11–3865 µg/kg), respectively. Lincomycin, had a mean concentration of 177 µg/kg manure (range: 9–3154 µg/kg). All other 18 antibiotic residues were found with mean concentrations of less than 100 µg/kg manure. Fifty-one slurry samples harbored Salmonella; 35% of the Salmonella isolates were sensitive to a panel of 14 antibiotics, whereas the other 65% were resistant up to five antibiotics. For E. coli, 52 manure samples contained E. coli isolates which were resistant to ciprofloxacin and 22 resistant to cefotaxime. All ciprofloxacin and cefotaxime-resistant isolates were multi-resistant, with resistance up to nine and eight antibiotics, respectively. This research indicates that pig slurry used for fertilization often contains antibiotic residues and antibiotic-resistant bacteria, including pathogens.

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Section: Discussionmentioning

confidence: 83%

Antibiotic Residues and Antibiotic-Resistant Bacteria in Pig Slurry Used to Fertilize Agricultural Fields

et al. 2020

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“…have been shown to increase Pseudomonas spp. populations by ten-fold in field soil (Gotz and Smalla, 1997) and to be the largest contributors of class 1 integrons and ARGs to soils after manure slurry application (Partridge et al, 2009;Leclercq et al, 2016). Pseudomonas are of further interest for future study given their relevance to multiantibiotic resistance in clinical settings (Micek et al, 2015).…”

Section: Effect Of Vegetable Type: Lettuce and Radishmentioning

confidence: 99%

Microbiota and Antibiotic Resistome of Lettuce Leaves and Radishes Grown in Soils Receiving Manure-Based Amendments Derived From Antibiotic-Treated Cows

Fogler

Guron

Wind

et al. 2019

Front. Sustain. Food Syst.

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Cattle are commonly administered antibiotics, resulting in excretion of antibiotics, antibiotic-resistant bacteria (ARB), and antibiotic resistance genes (ARGs). The aim of this study was to determine if the use of dairy manure collected during antibiotic administration influences the bacterial microbiota of lettuce and radishes, including carriage of ARB and ARGs, when applied as a soil amendment and if composting mitigates the effects. Lettuce and radishes were grown in field-plots amended with raw manure from antibiotic-treated (cephapirin, pirlimycin) cows, composted manure from antibiotic-treated cows, composted manure from antibiotic-free cows, or an inorganic chemical fertilizer (control; 12 plots, n = 3). Surficial vegetable bacteria and antibiotic resistomes (i.e., total ARGs) were characterized using heterotrophic plate counts (HPCs) on antibiotic-containing media, 16S rRNA gene amplicon sequencing, quantitative polymerase chain reaction (qPCR), and shotgun metagenomics. The different manure and compost amendments did not result in significant changes to the surficial vegetable bacteria at the phylum level; however, some minor changes at the class and family level were observed. Beta-diversities of the ARGs detected by shotgun metagenomic sequencing were distinctly different between vegetable type (R = 0.30, p = 0.04), with small separations between the resistomes associated with amendment type in unrarefied analysis (R = 0.27, p = 0.02), but not rarefied analysis, of the data. Network analysis highlighted that multi-drug ARG classes commonly co-occurred with plasmid-associated genes and could be a driver of co-and cross-selection of ARGs in the different conditions. Carriage of sul1 and tet(W) ARGs on vegetables quantified by qPCR were strong indicators of manure-based amendment relative to chemical fertilizer, with some reduction incurred via composting (p < 0.05). Also, increased HPCs resistant/tolerant to clindamycin, a class of antibiotics administered to cattle, were on lettuce grown in biological soil amendments relative to chemical fertilizer (p < 0.05). This study demonstrates that amending soil with raw manure collected from dairy cows during Fogler et al. Biological Amendment Affects Vegetable Resistome antibiotic administration may affect the composition of microbiota and resistomes associated with vegetable surfaces. Composting may be an important strategy to reduce some ARGs on fresh produce, but differences in the resistomes of lettuce and radishes suggest the extent of soil contact should be considered.

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“…Second, culture‐based methods facilitate establishing links between ARGs and their bacterial hosts (Fig. ) . Identifying the hosts of ARGs is particularly important to determine the origin of ARGs and to assess the dispersion of ARGs between environmental bacteria and pathogens .…”

Section: Culture‐based Genomic Identification Of Argsmentioning

confidence: 99%

“…1). 67 Identifying the hosts of ARGs is particularly important to determine the origin of ARGs and to assess the dispersion of ARGs between environmental bacteria and pathogens. 68,69 However, it is challenging to determine ARG hosts in complex environmental microbial communities using metagenomic technology; to accomplish that requires increased sequencing depth and greater expertise in bioinformatics.…”

Section: Culture-based Genomic Identification Of Argsmentioning

confidence: 99%

Application of genomic technologies to measure and monitor antibiotic resistance in animals

Chen

et al. 2016

Annals of the New York Academy of Sciences

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One of the richest reservoirs of antibiotic-resistant bacteria and genes, animal intestinal microbiota contributes to the spread of antibiotic resistance in the environment and, potentially, to human pathogens. Both culture-based genomic technology and culture-independent metagenomics have been developed to investigate the abundance and diversity of antibiotic resistance genes. The characteristics, strengths, limitations, and challenges of these genomic approaches are discussed in this review in the context of antibiotic resistance in animals. We also discuss the advances in single-cell genomics and its potential for surveillance of antibiotic resistance in animals.

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A multiplayer game: species of Clostridium, Acinetobacter, and Pseudomonas are responsible for the persistence of antibiotic resistance genes in manure‐treated soils

Cited by 92 publications

References 77 publications

Antibiotic Residues and Antibiotic-Resistant Bacteria in Pig Slurry Used to Fertilize Agricultural Fields

Antibiotic Residues and Antibiotic-Resistant Bacteria in Pig Slurry Used to Fertilize Agricultural Fields

Microbiota and Antibiotic Resistome of Lettuce Leaves and Radishes Grown in Soils Receiving Manure-Based Amendments Derived From Antibiotic-Treated Cows

Application of genomic technologies to measure and monitor antibiotic resistance in animals

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