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Antibiotic resistance gene reservoir in live poultry markets

  • Author Footnotes
    1 These authors contributed equally to this work.
    Yanan Wang
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    Jiangsu Key Laboratory of Zoonosis, Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, Jiangsu 225009, China

    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China

    College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou, Henan 450046, China
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  • Author Footnotes
    1 These authors contributed equally to this work.
    Yongfei Hu
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China

    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China
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  • Jian Cao
    Affiliations
    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China

    University of Chinese Academy of Sciences, Beijing 100049, China
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  • Yuhai Bi
    Affiliations
    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China
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  • Na Lv
    Affiliations
    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China
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  • Fei Liu
    Affiliations
    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China
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  • Shihao Liang
    Affiliations
    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China
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  • Yi Shi
    Affiliations
    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China

    University of Chinese Academy of Sciences, Beijing 100049, China
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  • Xinan Jiao
    Correspondence
    Corresponding author at: Jiangsu Key Laboratory of Zoonosis, Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, Jiangsu 225009, China.
    Affiliations
    Jiangsu Key Laboratory of Zoonosis, Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, Jiangsu 225009, China

    Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agri-Food Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, Jiangsu 225009, China
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  • George Fu Gao
    Correspondence
    Corresponding author.
    Affiliations
    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China

    State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China
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  • Baoli Zhu
    Correspondence
    Corresponding author at: CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China.
    Affiliations
    CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, China

    University of Chinese Academy of Sciences, Beijing 100049, China

    Beijing Key Laboratory of Antimicrobial Resistance and Pathogen Genomics, Beijing 100101, China

    Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases First Attainted Hospital, College of Medicine, Zhejiang University, 310006, China

    Department of Pathogenic Biology, School of Basic Medical Sciences, Southwest Medical University, Sichuan 646000, China
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  • Author Footnotes
    1 These authors contributed equally to this work.
Published:March 29, 2019DOI:https://doi.org/10.1016/j.jinf.2019.03.012

      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

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      References

        • Levy SB
        • Marshall B.
        Antibacterial resistance worldwide: causes, challenges and responses.
        Nat Med. 2004; 10 (129): S122https://doi.org/10.1038/nm1145
        • O'Neill J.
        The review on antimicrobial resistance. Antimicrobial resistance: Tackling a crisis for the health and wealth of nations.
        Wellcome Trust, London2014
        • Hu Y
        • Gao GF
        • Zhu B
        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
        • Forsberg KJ
        • Reyes A
        • Wang B
        • Selleck EM
        • Sommer MO
        • Dantas G
        The shared antibiotic resistome of soil bacteria and human pathogens.
        Science. 2012; 337: 1107-1111https://doi.org/10.1126/science.1220761
        • Kumarasamy KK
        • Toleman MA
        • Walsh TR
        • Bagaria J
        • Butt F
        • Balakrishnan R
        • et al.
        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
        • Liu YY
        • Wang Y
        • Walsh TR
        • Yi LX
        • Zhang R
        • Spencer J
        • et al.
        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
        • Sun J
        • Zhang H
        • Liu YH
        • Feng Y
        Towards understanding MCR-like colistin resistance.
        Trends Microbiol. 2018; https://doi.org/10.1016/j.tim.2018.02.006
        • Hu YF
        • Liu F
        • Lin YC
        • Gao GF
        • Zhu B
        Dissemination of the mcr-1 colistin resistance gene.
        Lancet Infect Dis. 2016; 16: 146-147https://doi.org/10.1016/S1473-3099(15)00533-2
        • D'Costa VM
        • King CE
        • Kalan L
        • Morar M
        • Sung WW
        • Schwarz C
        • et al.
        Antibiotic resistance is ancient.
        Nature. 2011; 477: 457-461https://doi.org/10.1038/nature10388
        • Blaser MJ.
        Antibiotic use and its consequences for the normal microbiome.
        Science. 2016; 352: 544-545https://doi.org/10.1126/science.aad9358
        • Munk P
        • Knudsen BE
        • Lukjancenko O
        • Duarte ASR
        • Van Gompel L
        • Luiken REC
        • et al.
        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
        • Hockenhull J
        • Turner AE
        • Reyher KK
        • Barrett DC
        • Jones L
        • Hinchliffe S
        • et al.
        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
        • Van Boeckel TP
        • Glennon EE
        • Chen D
        • Gilbert M
        • Robinson TP
        • Grenfell BT
        • et al.
        Reducing antimicrobial use in food animals.
        Science. 2017; 357: 1350-1352https://doi.org/10.1126/science.aao1495
        • Cheng G
        • Hao H
        • Xie S
        • Wang X
        • Dai M
        • Huang L
        • et al.
        Antibiotic alternatives: the substitution of antibiotics in animal husbandry.
        Front Microbiol. 2014; 5: 217https://doi.org/10.3389/fmicb.2014.00217
        • Hvistendahl M.
        China takes aim at rampant antibiotic resistance.
        Science. 2012; 336: 795https://doi.org/10.1126/science.336.6083.795
        • Zhu YG
        • Johnson TA
        • Su JQ
        • Qiao M
        • Guo GX
        • Stedtfeld RD
        • et al.
        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
        • Li B
        • Yang Y
        • Ma L
        • Ju F
        • Guo F
        • Tiedje JM
        • et al.
        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
        • Gao GF.
        Influenza and the live poultry trade.
        Science. 2014; 344: 235https://doi.org/10.1126/science.1254664
        • Lam TT
        • Zhou B
        • Wang J
        • Chai Y
        • Shen Y
        • Chen X
        • et al.
        Dissemination, divergence and establishment of H7N9 influenza viruses in China.
        Nature. 2015; 522: 102-105https://doi.org/10.1038/nature14348
        • Kanehisa M
        • Goto S
        • Sato Y
        • Kawashima M
        • Furumichi M
        • Tanabe M
        Data, information, knowledge and principle: back to metabolism in KEGG.
        Nucleic Acids Res. 2014; 42 (205): D199https://doi.org/10.1093/nar/gkt1076
        • Li J
        • Jia H
        • Cai X
        • Zhong H
        • Feng Q
        • Sunagawa S
        • et al.
        An integrated catalog of reference genes in the human gut microbiome.
        Nat Biotechnol. 2014; 32: 834-841https://doi.org/10.1038/nbt.2942
        • Xiao L
        • Estellé J
        • Kiilerich P
        • Ramayo-Caldas Y
        • Xia Z
        • Feng Q
        • et al.
        A reference gene catalogue of the pig gut microbiome.
        Nat Microbiol. 2016; 1: 16161https://doi.org/10.1038/nmicrobiol.2016.161
        • McArthur AG
        • Waglechner N
        • Nizam F
        • Yan A
        • Azad MA
        • Baylay AJ
        • et al.
        The comprehensive antibiotic resistance database.
        Antimicrob Agents Chemother. 2013; 57: 3348-3357https://doi.org/10.1128/AAC.00419-13
        • Van der Helm E
        • Imamovic L
        • Hashim Ellabaan MM
        • van Schaik W
        • Koza A
        • Sommer MO
        Rapid resistome mapping using nanopore sequencing.
        Nucleic Acids Res. 2017; 45: e61https://doi.org/10.1093/nar/gkw1328
        • Enault F
        • Briet A
        • Bouteille L
        • Roux S
        • Sullivan MB
        • Petit MA
        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
        • Ma L
        • Xia Y
        • Li B
        • Yang Y
        • Li LG
        • Tiedje JM
        • et al.
        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
        • Krishnasamy V
        • Otte J
        • Silbergeld E
        Antimicrobial use in Chinese swine and broiler poultry production.
        Antimicrob Resist Infect Control. 2015; 4: 17https://doi.org/10.1186/s13756-015-0050-y
        • Van Boeckel TP
        • Brower C
        • Gilbert M
        • Grenfell BT
        • Levin SA
        • Robinson TP
        • et al.
        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
        • Hu Y
        • Yang X
        • Qin J
        • Lu N
        • Cheng G
        • Wu N
        • et al.
        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
        • Zheng H
        • Zeng Z
        • Chen S
        • Liu Y
        • Yao Q
        • Deng Y
        • et al.
        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
        • Hou J
        • Huang X
        • Deng Y
        • He L
        • Yang T
        • Zeng Z
        • et al.
        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
        • Lin D
        • Chen S.
        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
        • Chen C
        • Xu X
        • Qu T
        • Yu Y
        • Ying C
        • Liu Q
        • et al.
        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
        • Wang Y
        • Zhang R
        • Li J
        • Wu Z
        • Yin W
        • Schwarz S
        • et al.
        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
        • Stojanoski V
        • Sankaran B
        • Prasad BV
        • Poirel L
        • Nordmann P
        • Palzkill T
        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
        • Hinchliffe P
        • Yang QE
        • Portal E
        • Young T
        • Li H
        • Tooke CL
        • et al.
        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
        • Xavier BB
        • Lammens C
        • Ruhal R
        • Kumar-Singh S
        • Butaye P
        • Goossens H
        • et al.
        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
        • Yin W
        • Li H
        • Shen Y
        • Liu Z
        • Wang S
        • Shen Z
        • et al.
        Novel plasmid-mediated colistin resistance gene mcr-3 in.
        Escherichia coli. mBio. 2017; 8 (17): e00543https://doi.org/10.1128/mBio.00543-17
        • Carattoli A
        • Villa L
        • Feudi C
        • Curcio L
        • Orsini S
        • Luppi A
        • et al.
        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
        • Borowiak M
        • Fischer J
        • Hammerl JA
        • Hendriksen RS
        • Szabo I
        • Malorny B
        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
        • Abuoun M
        • Stubberfield EJ
        • Duggett NA
        • Kirchner M
        • Dormer L
        • Nunezgarcia J
        • et al.
        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
        • Yang YQ
        • Li YX
        • Lei CW
        • Zhang AY
        • Wang HN
        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
        • Wang X
        • Wang Y
        • Zhou Y
        • Li J
        • Yin W
        • Wang S
        • et al.
        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
        • Walsh TR
        • Wu Y.
        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
        • Gao GF
        • Wu Y.
        Haunted with and hunting for viruses.
        Sci China Life Sci. 2013; 56: 675-677https://doi.org/10.1007/s11427-013-4525-x
        • Bi Y
        • Chen Q
        • Wang Q
        • Chen J
        • Jin T
        • Wong G
        • et al.
        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
        • Li R
        • Yu C
        • Li Y
        • Lam TW
        • Yiu SM
        • Kristiansen K
        • et al.
        SOAP2: an improved ultrafast tool for short read alignment.
        Bioinformatics. 2009; 25: 1966-1967https://doi.org/10.1093/bioinformatics/btp336
        • Luo R
        • Liu B
        • Xie Y
        • Li Z
        • Huang W
        • Yuan J
        • et al.
        SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler.
        Gigascience. 2012; 1: 18https://doi.org/10.1186/2047-217X-1-18
        • Kultima JR
        • Coelho LP
        • Forslund K
        • Huerta-Cepas J
        • Li SS
        • Driessen M
        • et al.
        MOCAT2: a metagenomic assembly, annotation and profiling framework.
        Bioinformatics. 2016; 32: 2520-2523https://doi.org/10.1093/bioinformatics/btw183
        • Kultima JR
        • Sunagawa S
        • Li J
        • Chen W
        • Chen H
        • Mende DR
        • et al.
        MOCAT: A metagenomics assembly and gene prediction toolkit.
        PloS One. 2012; 7: e47656https://doi.org/10.1371/journal.pone.0047656
        • Zhu W
        • Lomsadze A
        • Borodovsky M
        Ab initio gene identification in metagenomic sequences.
        Nucleic Acids Res. 2010; 38: e132https://doi.org/10.1093/nar/gkq275
        • Fu L
        • Niu B
        • Zhu Z
        • Wu S
        • Li W
        CD-HIT: accelerated for clustering the next-generation sequencing data.
        Bioinformatics. 2012; 28: 3150-3152https://doi.org/10.1093/nar/gkq275
        • Truong DT
        • Franzosa EA
        • Tickle TL
        • Scholz M
        • Weingart G
        • Pasolli E
        • et al.
        MetaPhlAn2 for enhanced metagenomic taxonomic profiling.
        Nat Methods. 2015; 12: 902-903https://doi.org/10.1038/nmeth.3589
        • Zhang G
        • Leclercq SO
        • Tian J
        • Wang C
        • Yahara K
        • Ai G
        • et al.
        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