Infectious phage particles packaging antibiotic resistance genes found in meat products and chicken feces

Abstract Bacteriophages can package part of their host’s genetic material, including antibiotic resistance genes (ARGs), contributing to a rapid dissemination of resistances among bacteria. Phage particles containing ARGs were evaluated in meat, pork, beef and chicken minced meat, and ham and mortadella, purchased in local retailer. Ten ARGs (blaTEM, blaCTX-M-1, blaCTX-M-9, blaOXA-48, blaVIM, qnrA, qnrS, mecA, armA and sul1) were analyzed by qPCR in the phage DNA fraction. The genes were quantified, before and after propagation experiments in Escherichia coli, to evaluate the ability of ARG-carrying phage particles to infect and propagate in a bacterial host. According to microbiological parameters, all samples were acceptable for consumption. ARGs were detected in most of the samples after particle propagation indicating that at least part of the isolated phage particles were infectious, being sul1the most abundant ARG in all the matrices followed by β-lactamase genes. ARGs were also found in the phage DNA fraction of thirty-seven archive chicken cecal samples, confirming chicken fecal microbiota as an important ARG reservoir and the plausible origin of the particles found in meat. Phages are vehicles for gene transmission in meat that should not be underestimated as a risk factor in the global crisis of antibiotic resistance.

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Association of nanoparticles with extracellular genetic material and implications for the fate of antibiotic resistance genes in environmental systems

10.1021/scimeetings.0c07368 ◽

2020 ◽

Author(s):

Nadrat Chowdhury

Keyword(s):

Antibiotic Resistance ◽

Resistance Genes ◽

Genetic Material ◽

Antibiotic Resistance Genes ◽

Environmental Systems

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The In-Feed Antibiotic Carbadox Induces Phage Gene Transcription in the Swine Gut Microbiome

mBio ◽

10.1128/mbio.00709-17 ◽

2017 ◽

Vol 8 (4) ◽

Cited By ~ 18

Author(s):

Timothy A. Johnson ◽

Torey Looft ◽

Andrew J. Severin ◽

Darrell O. Bayles ◽

Daniel J. Nasko ◽

...

Keyword(s):

Gene Expression ◽

Antibiotic Resistance ◽

Genetic Material ◽

Clinical Importance ◽

Antibiotic Resistance Genes ◽

Antibiotic Use ◽

Human Medicine ◽

Phage Dna ◽

Pig Farms ◽

Collateral Effects

ABSTRACT Carbadox is a quinoxaline-di-N-oxide antibiotic fed to over 40% of young pigs in the United States that has been shown to induce phage DNA transduction in vitro; however, the effects of carbadox on swine microbiome functions are poorly understood. We investigated the in vivo longitudinal effects of carbadox on swine gut microbial gene expression (fecal metatranscriptome) and phage population dynamics (fecal dsDNA viromes). Microbial metagenome, transcriptome, and virome sequences were annotated for taxonomic inference and gene function by using FIGfam (isofunctional homolog sequences) and SEED subsystems databases. When the beta diversities of microbial FIGfam annotations were compared, the control and carbadox communities were distinct 2 days after carbadox introduction. This effect was driven by carbadox-associated lower expression of FIGfams (n = 66) related to microbial respiration, carbohydrate utilization, and RNA metabolism (q < 0.1), suggesting bacteriostatic or bactericidal effects within certain populations. Interestingly, carbadox treatment caused greater expression of FIGfams related to all stages of the phage lytic cycle 2 days following the introduction of carbadox (q ≤0.07), suggesting the carbadox-mediated induction of prophages and phage DNA recombination. These effects were diminished by 7 days of continuous carbadox in the feed, suggesting an acute impact. Additionally, the viromes included a few genes that encoded resistance to tetracycline, aminoglycoside, and beta-lactam antibiotics but these did not change in frequency over time or with treatment. The results show decreased bacterial growth and metabolism, prophage induction, and potential transduction of bacterial fitness genes in swine gut bacterial communities as a result of carbadox administration. IMPORTANCE FDA regulations on agricultural antibiotic use have focused on antibiotics that are important for human medicine. Carbadox is an antibiotic not used in humans but frequently used on U.S. pig farms. It is important to study possible side effects of carbadox use because it has been shown to promote bacterial evolution, which could indirectly impact antibiotic resistance in bacteria of clinical importance. Interestingly, the present study shows greater prophage gene expression in feces from carbadox-fed animals than in feces from nonmedicated animals 2 days after the initiation of in-feed carbadox treatment. Importantly, the phage genetic material isolated in this study contained genes that could provide resistance to antibiotics that are important in human medicine, indicating that human-relevant antibiotic resistance genes are mobile between bacteria via phages. This study highlights the collateral effects of antibiotics and demonstrates the need to consider diverse antibiotic effects whenever antibiotics are being used or new regulations are considered. FDA regulations on agricultural antibiotic use have focused on antibiotics that are important for human medicine. Carbadox is an antibiotic not used in humans but frequently used on U.S. pig farms. It is important to study possible side effects of carbadox use because it has been shown to promote bacterial evolution, which could indirectly impact antibiotic resistance in bacteria of clinical importance. Interestingly, the present study shows greater prophage gene expression in feces from carbadox-fed animals than in feces from nonmedicated animals 2 days after the initiation of in-feed carbadox treatment. Importantly, the phage genetic material isolated in this study contained genes that could provide resistance to antibiotics that are important in human medicine, indicating that human-relevant antibiotic resistance genes are mobile between bacteria via phages. This study highlights the collateral effects of antibiotics and demonstrates the need to consider diverse antibiotic effects whenever antibiotics are being used or new regulations are considered.

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The Influencing Factors of Bacterial Resistance Related to Livestock Farm: Sources and Mechanisms

Frontiers in Animal Science ◽

10.3389/fanim.2021.650347 ◽

2021 ◽

Vol 2 ◽

Author(s):

Kaixuan Guo ◽

Yue Zhao ◽

Luqing Cui ◽

Zhengzheng Cao ◽

Fan Zhang ◽

...

Keyword(s):

Antibiotic Resistance ◽

Influencing Factors ◽

Resistance Genes ◽

Bacterial Resistance ◽

Genetic Material ◽

Resistance Mechanism ◽

Antibiotic Resistance Genes ◽

Direct Selection ◽

Adaptive Mutation ◽

Specific Response

Bacterial resistance is a complex scientific issue. To manage this issue, we need to deeply understand the influencing factors and mechanisms. Based on the background of livestock husbandry, this paper reviews the factors that affect the acquisition of bacterial resistance. Meanwhile, the resistance mechanism is also discussed. “Survival of the fittest” is the result of genetic plasticity of bacterial pathogens, which brings about specific response, such as producing adaptive mutation, gaining genetic material or changing gene expression. To a large extent, bacterial populations acquire resistance genes directly caused by the selective pressure of antibiotics. However, mobile resistance genes may be co-selected by other existing substances (such as heavy metals and biocides) without direct selection pressure from antibiotics. This is because the same mobile genetic elements as antibiotic resistance genes can be co-located by the resistance determinants of some of these compounds. Furthermore, environmental factors are a source of resistance gene acquisition. Here, we describe some of the key measures that should be taken to mitigate the risk of antibiotic resistance. We call on the relevant governments or organizations around the world to formulate and improve the monitoring policies of antibiotic resistance, strengthen the supervision, strengthen the international cooperation and exchange, and curb the emergence and spread of drug-resistant strains.

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Fecal Microbiota Transplant in Cirrhosis Reduces Gut Microbial Antibiotic Resistance Genes: Analysis of Two Trials

Hepatology Communications ◽

10.1002/hep4.1639 ◽

2020 ◽

Author(s):

Jasmohan S. Bajaj ◽

Amirhossein Shamsaddini ◽

Andrew Fagan ◽

Richard K. Sterling ◽

Edith Gavis ◽

...

Keyword(s):

Antibiotic Resistance ◽

Resistance Genes ◽

Antibiotic Resistance Genes ◽

Fecal Microbiota ◽

Fecal Microbiota Transplant

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Antibiotic Resistance Genes in the Bacteriophage DNA Fraction of Human Fecal Samples

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.01684-13 ◽

2013 ◽

Vol 58 (1) ◽

pp. 606-609 ◽

Cited By ~ 63

Author(s):

Pablo Quirós ◽

Marta Colomer-Lluch ◽

Alexandre Martínez-Castillo ◽

Elisenda Miró ◽

Marc Argente ◽

...

Keyword(s):

Antibiotic Resistance ◽

Real Time ◽

Quantitative Pcr ◽

Resistance Genes ◽

Antibiotic Resistance Genes ◽

Fecal Samples ◽

Real Time Quantitative Pcr ◽

Healthy Humans ◽

Phage Dna

ABSTRACTA group of antibiotic resistance genes (ARGs) (blaTEM,blaCTX-M-1,mecA,armA,qnrA, andqnrS) were analyzed by real-time quantitative PCR (qPCR) in bacteriophage DNA isolated from feces from 80 healthy humans. Seventy-seven percent of the samples were positive in phage DNA for one or more ARGs.blaTEM,qnrA, and,blaCTX-M-1were the most abundant, andarmA,qnrS, andmecAwere less prevalent. Free bacteriophages carrying ARGs may contribute to the mobilization of ARGs in intra- and extraintestinal environments.

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Reduction of Antibiotic Resistance Genes in Intestinal Microbiota of Patients With RecurrentClostridium difficileInfection After Fecal Microbiota Transplantation

Clinical Infectious Diseases ◽

10.1093/cid/ciw390 ◽

2016 ◽

Vol 63 (5) ◽

pp. 710-711 ◽

Cited By ~ 23

Author(s):

Hanne Jouhten ◽

Eero Mattila ◽

Perttu Arkkila ◽

Reetta Satokari

Keyword(s):

Antibiotic Resistance ◽

Intestinal Microbiota ◽

Resistance Genes ◽

Fecal Microbiota Transplantation ◽

Antibiotic Resistance Genes ◽

Fecal Microbiota

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Joining the resistance

Science Translational Medicine ◽

10.1126/scitranslmed.aar7519 ◽

2018 ◽

Vol 10 (425) ◽

pp. eaar7519

Author(s):

Stephanie A. Christenson

Keyword(s):

Antibiotic Resistance ◽

Preterm Infants ◽

Resistance Genes ◽

Gut Microbiome ◽

Antibiotic Resistance Genes ◽

Antibiotic Administration ◽

Before And After

The effect of antibiotic resistance genes on the gut microbiome is examined in preterm infants before and after antibiotic administration.

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Isolation and Antibiotic Resistant Research of Tetragenococcus halophilus from Xuanwei Ham, A China High-Salt-Fermented Meat Products

Antibiotics ◽

10.3390/antibiotics8030151 ◽

2019 ◽

Vol 8 (3) ◽

pp. 151

Author(s):

Yinjiao Li ◽

Luying Shan ◽

Chen Zhang ◽

Zhan Lei ◽

Ying Shang

Keyword(s):

Antibiotic Resistance ◽

Resistance Genes ◽

Safety Assessment ◽

Meat Products ◽

Antibiotic Resistance Genes ◽

Chain Reaction ◽

Detection Rates ◽

Antibiotic Resistant ◽

Tetragenococcus Halophilus ◽

Polymerase Chain

We assessed the prevalence of antibiotic resistant and antibiotic resistance genes for 49 Tetragenococcus halophilus (T. halophilus) strains isolated from Xuawei ham in China. The antibiotic resistance phenotype was detected by the Bauer–Kirby (K–B) method and the results showed that 49 isolates can be considered completely susceptible to penicillin, ampicillin, amoxicillin, cefradine, cefotaxime, tetracyclines, minocycline, doxycycline, and vancomycin, but resistant to gentamicin, streptomycin, neomycin, polymyxinB, cotrimoxazole. This resistance was sufficiently high to consider the potential for acquisition of transmissible determinants. A total of 32 isolates were resistant to ofloxacin, 4 isolates were resistant to ciprofloxacin and chloramphenicol, and 2 isolates were resistant to ceftazidime and ticarcillin. The antibiotic resistance genes were detected by routine polymerase chain reaction (PCR). Among the 26 antibiotic resistance genes, 5 varieties of antibiotic resistance genes, including acrB, blaTEM, AAda1, SulII, and GyrB were detected and the detection rates were 89.79%, 47.7%, 16.33%, 77.55%, and 75.51%, respectively. The potential acquisition of transmissible determinants for antibiotic resistance and antibiotic resistance genes identified in this study necessitate the need for a thorough antibiotic resistance safety assessment of T. halophilus before it can be considered for use in food fermentation processes.

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