Low-Concentration Ciprofloxacin Selects Plasmid-Mediated Quinolone Resistance Encoding Genes and Affects Bacterial Taxa in Soil Containing Manure

Huang, Ting; Xü, Ying; Zeng, Jie; Zhao, Dong-Hao; Li, Liang; Liao, Xiao‐Ping; Liu, Yahong; Sun, Jian

doi:10.3389/fmicb.2016.01730

Cited by 16 publications

(5 citation statements)

References 45 publications

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“…Two possible explanations are suggested to account for the significant enrichment of these genera under the pressure of enrofloxacin treatment. Firstly, several previous studies reported that Lactococcus , Burkholderia and Bacillus were associated with intrinsic ciprofloxacin resistance ( Mathur and Singh, 2005 ; Fajardo et al, 2008 ; Walsh and Duffy, 2013 ; Huang et al, 2016 ). Secondly, resistant mutant might be selected under the antibiotic pressure and lead to the propagation.…”

Section: Discussionmentioning

confidence: 99%

“… Videnska et al (2013) reported that Enterococcus in the chicken fecal microbiota was increased in response to the single or repeated therapy with tetracycline and streptomycin. Lower concentrations of ciprofloxacin in soil also enriched the genus Enterococcus ( Huang et al, 2016 ) Enterococcus has shown to be intrinsically resistant to several antibiotics, such as β-lactams and aminoglycosides. The emergence of virulent Enterococcus that is resistant to vancomycin (VRE) has widely raised public concern.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Microbial Shifts in the Intestinal Microbiota of Salmonella Infected Chickens in Response to Enrofloxacin

Hao

Cheng

et al. 2017

Front. Microbiol.

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Fluoroquinolones (FQs) are important antibiotics used for treatment of Salmonella infection in poultry in many countries. However, oral administration of fluoroquinolones may affect the composition and abundance of a number of bacterial taxa in the chicken intestine. Using 16S rRNA gene sequencing, the microbial shifts in the gut of Salmonella infected chickens in response to enrofloxacin treatments at different dosages (0, 0.1, 4, and 100 mg/kg b.w.) were quantitatively evaluated. The results showed that the shedding levels of Salmonella were significantly reduced in the high dosage group as demonstrated by both the culturing method and 16S rRNA sequencing method. The average values of diversity indices were higher in the control group than in the three medicated groups. Non-metric multidimensional scaling (NMDS) analysis results showed that the microbial community of high dosage group was clearly separated from the other three groups. In total, 25 genera were significantly enriched (including 6 abundant genera: Lactococcus, Bacillus, Burkholderia, Pseudomonas, Rhizobium, and Acinetobacter) and 23 genera were significantly reduced in the medicated groups than in the control group for the treatment period, but these bacterial taxa recovered to normal levels after therapy withdrawal. Additionally, 5 genera were significantly reduced in both treatment and withdrawal periods (e.g., Blautia and Anaerotruncus) and 23 genera (e.g., Enterobacter and Clostridium) were significantly decreased only in the withdrawal period, indicating that these genera might be the potential targets for the fluoroquinolones antimicrobial effects. Specially, Enterococcus was significantly reduced under high dosage of enrofloxacin treatment, while significantly enriched in the withdrawal period, which was presumably due to the resistance selection. Predicted microbial functions associated with genetic information processing were significantly decreased in the high dosage group. Overall, enrofloxacin at a dosage of 100 mg/kg b.w. significantly altered the microbial community membership and structure, and microbial functions in the chicken intestine during the medication. This study fully investigates the chicken intestinal microbiota in response to enrofloxacin treatment and identifies potential targets against which the fluoroquinolones may have potent antimicrobial effects. These results provide insights into the effects of the usage of enrofloxacin on chicken and will aid in the prudent and rational use of antibiotics in poultry industry.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Microbial Shifts in the Intestinal Microbiota of Salmonella Infected Chickens in Response to Enrofloxacin

Hao

Cheng

et al. 2017

Front. Microbiol.

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“…However, the rate of spread of ARGs depends on the antibiotic concentration in the soil. Huang et al ( 2016 ) showed that the dissipation rate of plasmid-located genes [i.e., qnrS, oqxA, aac(6 ′ )-Ib-cr ] was significantly lower in soil treated with ciprofloxacin at concentrations of 0.04 and 0.4 mg/kg soil compared to soil treated with antibiotic at 4 mg/kg and controls. Forsberg et al ( 2012 ) also found little evidence for HGT in soil.…”

Section: Diversity Of Antimicrobial Resistance Genesmentioning

confidence: 99%

Antibiotics in the Soil Environment—Degradation and Their Impact on Microbial Activity and Diversity

2019

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Antibiotics play a key role in the management of infectious diseases in humans, animals, livestock, and aquacultures all over the world. The release of increasing amount of antibiotics into waters and soils creates a potential threat to all microorganisms in these environments. This review addresses issues related to the fate and degradation of antibiotics in soils and the impact of antibiotics on the structural, genetic and functional diversity of microbial communities. Due to the emergence of bacterial resistance to antibiotics, which is considered a worldwide public health problem, the abundance and diversity of antibiotic resistance genes (ARGs) in soils are also discussed. When antibiotic residues enter the soil, the main processes determining their persistence are sorption to organic particles and degradation/transformation. The wide range of DT50 values for antibiotic residues in soils shows that the processes governing persistence depend on a number of different factors, e.g., physico-chemical properties of the residue, characteristics of the soil, and climatic factors (temperature, rainfall, and humidity). The results presented in this review show that antibiotics affect soil microorganisms by changing their enzyme activity and ability to metabolize different carbon sources, as well as by altering the overall microbial biomass and the relative abundance of different groups (i.e., Gram-negative bacteria, Gram-positive bacteria, and fungi) in microbial communities. Studies using methods based on analyses of nucleic acids prove that antibiotics alter the biodiversity of microbial communities and the presence of many types of ARGs in soil are affected by agricultural and human activities. It is worth emphasizing that studies on ARGs in soil have resulted in the discovery of new genes and enzymes responsible for bacterial resistance to antibiotics. However, many ambiguous results indicate that precise estimation of the impact of antibiotics on the activity and diversity of soil microbial communities is a great challenge.

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“…This has been seen for quinolone resistance since PMQR genes have become prevalent in clinical and environmental settings. 133,146,[157][158][159][160][161][162][163][164] One of PMQR genes that have emerged rapidly in these settings are qnr genes incurring fitness advantages in the presence of fluoroquinolones. It has been shown through biochemical assays that Qnr proteins can reduce the amount of enzyme-DNA targets for ciprofloxacin inhibition.…”

Section: Qnr Prevalencementioning

confidence: 99%

Prevalence and Characterization of Plasmid-Mediated Quinolone Resistance in Various Aquatic Sources

Yusuf¹,

Gilbride²

2022

Preprint

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Bacterial isolates found in aquatic ecosystems often carry antibiotic resistance genes (ARGs). These ARGs are often found on plasmids and transposons, which allows them to be proliferate throughout bacterial communities via horizontal gene transfer (HGT) causing dissemination of multidrug resistance. The increase in antibiotic resistance has raised concerns about the ability to continue to use these drugs to fight infectious diseases. Novel synthetic antibiotics like ciprofloxacin that are not naturally found in the environment were developed to prevent resistances. However, ciprofloxacin resistance has occurred through chromosomal gene mutations of type 2 topoisomerases or by the acquisition of plasmid-mediated quinolone resistances (PMQR). A particular PMQR, qnr genes, encoding for pentapeptide repeat proteins that confer low levels of quinolone resistance and protect DNA gyrase and topoisomerase IV from antibacterial activity. These qnr genes have been identified globally in both clinical and environmental isolates. The aim of this study was to determine the prevalence of ciprofloxacin-resistant bacteria in aquatic environments in the Greater Toronto Area and the potential dissemination of ciprofloxacin resistance. With the selective pressure of ciprofloxacin, we hypothesize that ciprofloxacin-resistant bacteria (CipR) in the environment may carry PMQR mechanisms while the sensitive population (CipS) would not carry PMQR genes. Isolates were tested for resistance to an additional 12 different antibiotics and identified using Sanger sequencing PCR products of the 16S rRNA gene. To determine which genes are responsible for ciprofloxacin resistance, multiplex PCR of associated qnr genes, qnrA, qnrB, and qnrS, was carried out on 202 environmental isolates. Our data demonstrate a similar prevalence of qnr genes was found in CipR (19%) and CipS (14%) populations suggesting that the presence of these genes was not necessarily correlated with the phenotypic resistance to the antibiotic. Furthermore, ciprofloxacinresistant bacteria were found in all locations at similar frequencies suggesting that resistance genes are widespread and could possibly arise through HGT events. Overall, determining the underlying cause and prevalence of ciprofloxacin resistance could help re-establish the effectiveness of these antimicrobial compounds.

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Low-Concentration Ciprofloxacin Selects Plasmid-Mediated Quinolone Resistance Encoding Genes and Affects Bacterial Taxa in Soil Containing Manure

Cited by 16 publications

References 45 publications

Microbial Shifts in the Intestinal Microbiota of Salmonella Infected Chickens in Response to Enrofloxacin

Microbial Shifts in the Intestinal Microbiota of Salmonella Infected Chickens in Response to Enrofloxacin

Antibiotics in the Soil Environment—Degradation and Their Impact on Microbial Activity and Diversity

Prevalence and Characterization of Plasmid-Mediated Quinolone Resistance in Various Aquatic Sources

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