Sulfonamide-Resistant Bacteria and Their Resistance Genes in Soils Fertilized with Manures from Jiangsu Province, Southeastern China

Wang, Na; Yang, Xiaolu; Jiao, Shaojun; Zhang, Jun; Ye, Boping; Gao, Shixiang

doi:10.1371/journal.pone.0112626

Cited by 80 publications

(52 citation statements)

References 25 publications

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“…In ADS, sul1 (21.2 %) was the ARG with high relative abundance, while the intI genes could not be detected using a metagenomics approach. These findings are consistent with previous studies reporting prevalence of sul1 and sul genes in agriculture impacted environments [37,38]. Other abundant genes in ADS included mexB (7.0 %) and mexY (8.5 %), aadA1 (6.1 %) and strB (6.6 %).…”

Section: Diversity and Distribution Of Antibiotic Resistance Genes Insupporting

confidence: 92%

Antibiotic resistance genes in agriculture and urban influenced watersheds in southwestern British Columbia

Uyaguari

Croxen

Luo

et al. 2017

Preprint

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BackgroundThe dissemination of antibiotic resistance genes (ARGs) from anthropogenic activities into the environment poses an emerging public health threat. Water constitutes a major vehicle for transport of both biological material and chemical substances. The present study focused on putative antibiotic resistance and integrase genes present in the microbiome of agricultural, urban influenced and protected watersheds in southwestern British Columbia, Canada. A metagenomics approach and high throughput quantitative PCR (HT qPCR) were used to screen for elements of resistance including ARGs and integronassociated integrase genes (intI). Sequencing of bacterial genomic DNA was used to characterize the resistome of microbial communities present in watersheds over a one-year period. ResultsData mining using CARD and Integrall databases enabled the identification of putative antibiotic resistance genes present in watershed samples. Antibiotic resistance genes presence in samples from various watershed locations was low relative to the microbial population (<1 %). Analysis of the metagenomic sequences detected a total of 78 ARGs and intI1 across all watershed locations.The relative abundance and richness of antibiotic resistance genes was found to be highest in agriculture impacted watersheds compared to protected and urban watersheds. Gene copy numbers (GCNs) from a subset of 21 different elements of antibiotic resistance were further estimated using HT qPCR. Most GCNs of ARGs were found to be variable over time. A downstream transport pattern was observed in the impacted watersheds (urban and agricultural) during dry months.Urban and agriculture impacted sites had a higher GCNs of ARGs compared to protected sites. Similar to other reports, this study found a strong association between intI1 and ARGs (e. g., sul1), an association which may be used as a proxy for anthropogenic activities. Chemical analysis of water samples for three major groups of antibiotics was negative. However, the high richness and GCNs of ARGs in impacted sites suggest effects of effluents on microbial communities are occurring even at low concentrations of antimicrobials in the water column. ConclusionAntibiotic resistance and integrase genes in a year-long metagenomic study showed that ARGs were driven mainly by environmental factors from anthropogenized sites in agriculture and urban watersheds. Environmental factors accounted for almost 40% of the variability observed in watershed locations.

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Section: Diversity and Distribution Of Antibiotic Resistance Genes Insupporting

confidence: 92%

Antibiotic resistance genes in agriculture and urban influenced watersheds in southwestern British Columbia

Uyaguari

Croxen

Luo

et al. 2017

Preprint

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“…Based on culture-dependent approaches, sulfonamide-resistant bacteria isolated from agriculture sites contaminated by sulfonamides incorporated mainly Bacillus genera (49). Similarly, Bacillus has been found to be the most prevalent genus for all sulfonamide-resistant bacteria isolated from manure samples (50). In another study, a phylogenetic analysis further showed that there were possibilities for the genetic transfer of the sul1 gene from intestinal Enterococcus spp.…”

Section: Fig 5 Network Analyses As Inferred By Pairwise Spearman Corrmentioning

confidence: 95%

Housefly Larva Vermicomposting Efficiently Attenuates Antibiotic Resistance Genes in Swine Manure, with Concomitant Bacterial Population Changes

Wang

Gilbert

et al. 2015

Appl Environ Microbiol

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h Manure from swine treated with antimicrobials as feed additives is a major source for the expansion of the antibiotic resistance gene (ARG) reservoir in the environment. Vermicomposting via housefly larvae (Musca domestica) can be efficiently used to treat manure and regenerate biofertilizer, but few studies have investigated its effect on ARG attenuation. Here, we tracked the abundances of 9 ARGs and the composition and structure of the bacterial communities in manure samples across 6 days of fullscale manure vermicomposting. On day 6, the abundances of genes encoding tetracycline resistance [tet(M), tet(O), tet(Q), and tet(W)] were reduced (P < 0.05), while those of genes encoding sulfonamide resistance (sul1 and sul2) were increased (P < 0.05) when normalized to 16S rRNA. The abundances of tetracycline resistance genes were correlated (P < 0.05) with the changing concentrations of tetracyclines in the manure. The overall diversity and richness of the bacteria significantly decreased during vermicomposting, accompanied by a 100 times increase in the relative abundance of Flavobacteriaceae spp. Variations in the abundances of ARGs were correlated with the changing microbial community structure and the relative abundances of the family Ruminococcaceae, class Bacilli, or phylum Proteobacteria. Vermicomposting, as a waste management practice, can reduce the overall abundance of ARGs. More research is warranted to assess the use of this waste management practice as a measure to attenuate the dissemination of antimicrobial residues and ARGs from livestock production before vermicompost can be safely used as biofertilizer in agroecosystems.A ntimicrobials have been widely used at therapeutic levels for microbial infection control and at subtherapeutic levels for growth promotion as veterinary feed additives, administered in water or parenterally in animal husbandry (1). Antimicrobials can select for antibiotic resistance genes (ARGs) in host-associated bacteria from concentrated animal feeding operations and in the environment where antimicrobial-containing feces are excreted or applied to fields (2). Through horizontal gene transfer mechanisms triggered by mobile genetic elements, such as conjugative plasmids, integrons, and transposons (3, 4), different microbes can share their genetic information, potentially causing the transfer and dissemination of ARGs from feces-associated bacteria to indigenous environmental microbes. For instance, an intI1 gene encoding a site-specific integrase responsible for integration is closely related to the transfer of sulfonamide resistance genes among bacteria (5). Specifically, swine manure increases the resistant gene reservoir in the environment, as most applied veterinary antimicrobials are poorly absorbed by livestock (6). These antimicrobials are largely excreted in feces and then dispersed to soil when the manure is used as fertilizer. Unmanaged waste disposal is commonly regarded as one of the major sources for the environmental expansion of ARGs (3); therefore, it is ext...

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“…A larger number of studies have shown that manure application is a major source of agricultural soil contamination with veterinary pharmaceuticals (Christian et al, 2003;Karcı & Balcıoğlu, 2009;Wang et al, 2014). Such findings are necessary for an evidence-based risk assessment of the effects of veterinary pharmaceuticals in the environment and subsequent policies and regulatory measures aiming to monitor and minimise these effects (Kaczala & Blum, 2016).…”

Section: Thielementioning

confidence: 99%

Antibiotics and microbial resistance in Brazilian soils under manure application

et al. 2018

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Animal manure is commonly used in agriculture as fertiliser. This practice could represent, however, a risk of soil degradation through the accumulation of pharmaceutical residues or resistant microorganisms. Thus, 12 pharmaceuticals (11 antibiotics and 1 nonsteroidal anti‐inflammatory drug) were quantified in soil samples from 15 sites regularly fertilised with different animal manures (dairy cow, pig or poultry litter manure) and from forest sites in southern Brazil. This study (a) investigated the impacts of Brazilian animal waste application on antibiotic levels and induced bacterial resistance of soils and (b) determined whether one type of waste is more polluting than others. Three bacterial resistance genes, namely, sul1, qnr A, and erm, were also quantified to determine the impacts of manure application on the resistance of soil microbial communities. The effect of manure application was confirmed by the presence of antibiotic residues (up to 38.3 μg kg−1) and bacterial resistance modifications of the bacterial community (up to 8.97 × 10−3 copies of genes per bacteria) in the studied soils. Soils amended with pig manure presented the highest antibiotic concentrations. However, soils subjected to dairy cow grazing over long periods of time presented the highest concentrations of sulfonamide resistance gene (sul1). Our results lead us to infer that the type of manure can induce a “specific pollution fingerprint.”

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Sulfonamide-Resistant Bacteria and Their Resistance Genes in Soils Fertilized with Manures from Jiangsu Province, Southeastern China

Cited by 80 publications

References 25 publications

Antibiotic resistance genes in agriculture and urban influenced watersheds in southwestern British Columbia

Antibiotic resistance genes in agriculture and urban influenced watersheds in southwestern British Columbia

Housefly Larva Vermicomposting Efficiently Attenuates Antibiotic Resistance Genes in Swine Manure, with Concomitant Bacterial Population Changes

Antibiotics and microbial resistance in Brazilian soils under manure application

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