Highlights
- •The first large-scale study to reveal the overview of ARGs in Chinese LPMs.
- •Poultry gut microbiome contains high diversity and abundance of ARGs.
- •TcR genes were the most abundant ARGs in both food animals and humans.
- •The mcr-1, mcr-3, mcr-4 and mcr-5 were prevalent in Chinese LPMs.
- •the mcr-1 gene was presented in 59.63% (449/753) LPM samples.
Summary
Objectives
The heavy use of antibiotics in farm animals contributes to the enrichment and spread
of antibiotic resistance genes (ARGs) in “one-health” settings. Numerous ARGs have
been identified in livestock-associated environments but not in Chinese live poultry
markets (LPMs).
Methods
We collected 753 poultry fecal samples from LPMs of 18 provinces and municipalities
in China and sequenced the metagenomes of 130 samples. Bioinformatic tools were used
to construct the gene catalog and analyze the ARG content. PCR amplification and Sanger
sequencing were used to survey the distribution of mcr-1 gene in all 753 fecal samples.
Results
We found that a low number of genes but a high percentage of gene functions were shared
among the poultry, human and pig gut gene catalogs. The poultry gut possessed 539
ARGs which were classified into 235 types. Both the ARG number and abundance were
significantly higher in poultry than that in either pigs or humans. Fourteen ARG types
were found present in all 130 samples, and tetracycline resistance (TcR) genes were
the most abundant ARGs in both animals and humans. Moreover, 59.63% LPM samples harbored
the colistin resistance gene mcr-1, and other mcr gene variants were also found.
Conclusions
We demonstrated that the Chinese LPMs is a repository for ARGs, posing a high risk
for ARG dissemination from food animals to humans under such a trade system, which
has not been addressed before.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Journal of InfectionAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Antibacterial resistance worldwide: causes, challenges and responses.Nat Med. 2004; 10 (129): S122https://doi.org/10.1038/nm1145
- The review on antimicrobial resistance. Antimicrobial resistance: Tackling a crisis for the health and wealth of nations.Wellcome Trust, London2014
- The antibiotic resistome: gene flow in environments, animals and human beings.Front Med. 2017; 11: 161-168https://doi.org/10.1007/s11684-017-0531-x
- The shared antibiotic resistome of soil bacteria and human pathogens.Science. 2012; 337: 1107-1111https://doi.org/10.1126/science.1220761
- Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study.Lancet Infect Dis. 2010; 10: 597-602https://doi.org/10.1016/S1473-3099(10)70143-2
- Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study.Lancet Infect Dis. 2016; 16: 161-168https://doi.org/10.1016/S1473-3099(15)00424-7
- Towards understanding MCR-like colistin resistance.Trends Microbiol. 2018; https://doi.org/10.1016/j.tim.2018.02.006
- Dissemination of the mcr-1 colistin resistance gene.Lancet Infect Dis. 2016; 16: 146-147https://doi.org/10.1016/S1473-3099(15)00533-2
- Antibiotic resistance is ancient.Nature. 2011; 477: 457-461https://doi.org/10.1038/nature10388
- Antibiotic use and its consequences for the normal microbiome.Science. 2016; 352: 544-545https://doi.org/10.1126/science.aad9358
- Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries.Nat Microbiol. 2018; 3: 898-908https://doi.org/10.1038/s41564-018-0192-9
- Antimicrobial use in food-producing animals: a rapid evidence assessment of stakeholder practices and beliefs.Vet Rec. 2017; 181: 510https://doi.org/10.1136/vr.104304
- Reducing antimicrobial use in food animals.Science. 2017; 357: 1350-1352https://doi.org/10.1126/science.aao1495
- Antibiotic alternatives: the substitution of antibiotics in animal husbandry.Front Microbiol. 2014; 5: 217https://doi.org/10.3389/fmicb.2014.00217
- China takes aim at rampant antibiotic resistance.Science. 2012; 336: 795https://doi.org/10.1126/science.336.6083.795
- Diverse and abundant antibiotic resistance genes in Chinese swine farms.Proc Natl Acad Sci U S A. 2013; 110: 3435-3440https://doi.org/10.1073/pnas.1222743110
- Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes.ISME J. 2015; 9: 2490-2502https://doi.org/10.1038/ismej.2015.59
- Influenza and the live poultry trade.Science. 2014; 344: 235https://doi.org/10.1126/science.1254664
- Dissemination, divergence and establishment of H7N9 influenza viruses in China.Nature. 2015; 522: 102-105https://doi.org/10.1038/nature14348
- Data, information, knowledge and principle: back to metabolism in KEGG.Nucleic Acids Res. 2014; 42 (205): D199https://doi.org/10.1093/nar/gkt1076
- An integrated catalog of reference genes in the human gut microbiome.Nat Biotechnol. 2014; 32: 834-841https://doi.org/10.1038/nbt.2942
- A reference gene catalogue of the pig gut microbiome.Nat Microbiol. 2016; 1: 16161https://doi.org/10.1038/nmicrobiol.2016.161
- The comprehensive antibiotic resistance database.Antimicrob Agents Chemother. 2013; 57: 3348-3357https://doi.org/10.1128/AAC.00419-13
- Rapid resistome mapping using nanopore sequencing.Nucleic Acids Res. 2017; 45: e61https://doi.org/10.1093/nar/gkw1328
- Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses.ISME J. 2017; 11: 237-247https://doi.org/10.1038/ismej.2016.90
- Metagenomic assembly reveals hosts of antibiotic resistance genes and the shared resistome in pig, chicken, and human feces.Environ Sci Technol. 2016; 50: 420-427https://doi.org/10.1021/acs.est.5b03522
- Antimicrobial use in Chinese swine and broiler poultry production.Antimicrob Resist Infect Control. 2015; 4: 17https://doi.org/10.1186/s13756-015-0050-y
- Global trends in antimicrobial use in food animals.Proc Natl Acad Sci U S A. 2015; 112: 5649-5654https://doi.org/10.1073/pnas.1503141112
- Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota.Nat Commun. 2013; 4: 2151https://doi.org/10.1038/ncomms3151
- Prevalence and characterisation of CTX-M beta-lactamases amongst Escherichia coli isolates from healthy food animals in China.Int J Antimicrob Agents. 2012; 39: 305-310https://doi.org/10.1016/j.ijantimicag.2011.12.001
- Dissemination of the fosfomycin resistance gene fosA3 with CTX-M beta-lactamase genes and rmtB carried on IncFII plasmids among Escherichia coli isolates from pets in China.Antimicrob Agents Chemother. 2012; 56: 2135-2138https://doi.org/10.1128/AAC.05104-11
- First detection of conjugative plasmid-borne fosfomycin resistance gene fosA3 in Salmonella isolates of food origin.Antimicrob Agents Chemother. 2015; 59: 1381-1383https://doi.org/10.1128/AAC.04750-14
- Prevalence of the fosfomycin-resistance determinant, fosB3, in Enterococcus faecium clinical isolates from China.J Med Microbiol. 2014; 63: 1484-1489https://doi.org/10.1099/jmm.0.077701-0
- Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production.Nat Microbiol. 2017; 2: 16260https://doi.org/10.1038/nmicrobiol.2016.260
- Structure of the catalytic domain of the colistin resistance enzyme MCR-1.BMC Biology. 2016; 14: 81https://doi.org/10.1186/s12915-016-0303-0
- Insights into the mechanistic basis of plasmid-mediated colistin resistance from crystal structures of the catalytic domain of MCR-1.Sci Rep. 2017; 7: 39392https://doi.org/10.1038/srep39392
- Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016.Euro Surveill. 2016; 21: 30280https://doi.org/10.2807/1560-7917.ES.2016.21.27.30280
- Novel plasmid-mediated colistin resistance gene mcr-3 in.Escherichia coli. mBio. 2017; 8 (17): e00543https://doi.org/10.1128/mBio.00543-17
- Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016.Euro Surveill. 2017; 22: 30589https://doi.org/10.2807/1560-7917.ES.2017.22.31.30589
- Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B.J Antimicrob Chemother. 2017; 72: 3317-3324https://doi.org/10.1093/jac/dkx327
- mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015.J Antimicrob Chemother. 2017; 72: 2745-2749https://doi.org/10.1093/jac/dkx286
- Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae.J Antimicrob Chemother. 2018; 17: 1791-1795https://doi.org/10.1093/jac/dky111
- Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae.Emerg Microbes Infect. 2018; 7: 122https://doi.org/10.1038/s41426-018-0124-z
- China bans colistin as a feed additive for animals.Lancet Infect Dis. 2016; 16: 1102-1103https://doi.org/10.1016/S1473-3099(16)30329-2
- Haunted with and hunting for viruses.Sci China Life Sci. 2013; 56: 675-677https://doi.org/10.1007/s11427-013-4525-x
- Genesis, evolution and prevalence of H5N6 avian influenza viruses in China.Cell Host & Microbe. 2016; 20: 810-821https://doi.org/10.1016/j.chom.2016.10.022
- SOAP2: an improved ultrafast tool for short read alignment.Bioinformatics. 2009; 25: 1966-1967https://doi.org/10.1093/bioinformatics/btp336
- SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler.Gigascience. 2012; 1: 18https://doi.org/10.1186/2047-217X-1-18
- MOCAT2: a metagenomic assembly, annotation and profiling framework.Bioinformatics. 2016; 32: 2520-2523https://doi.org/10.1093/bioinformatics/btw183
- MOCAT: A metagenomics assembly and gene prediction toolkit.PloS One. 2012; 7: e47656https://doi.org/10.1371/journal.pone.0047656
- Ab initio gene identification in metagenomic sequences.Nucleic Acids Res. 2010; 38: e132https://doi.org/10.1093/nar/gkq275
- CD-HIT: accelerated for clustering the next-generation sequencing data.Bioinformatics. 2012; 28: 3150-3152https://doi.org/10.1093/nar/gkq275
- MetaPhlAn2 for enhanced metagenomic taxonomic profiling.Nat Methods. 2015; 12: 902-903https://doi.org/10.1038/nmeth.3589
- A new subclass of intrinsic aminoglycoside nucleotidyltransferases, ANT(3")-II, is horizontally transferred among Acinetobacter spp. by homologous recombination.PLoS Genet. 2017; 13e1006602https://doi.org/10.1371/journal.pgen.1006602
Article info
Publication history
Published online: March 29, 2019
Accepted:
March 28,
2019
Identification
Copyright
© 2019 The British Infection Association. Published by Elsevier Ltd. All rights reserved.
