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Characteristics of two transferable aminoglycoside resistance plasmids in Escherichia coli isolated from pig and chicken manure

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Abstract

Plasmid-mediated antibiotic resistance genes (ARGs) have recently become a more prominent concern in the global environment. However, the prevalence of aminoglycoside resistance plasmids in the livestock industry is under reported. In this study, two transferable aminoglycoside resistance plasmids, pRKZ3 and pKANJ7, isolated from pig and chicken manure, were characterized. Results showed that pRKZ3 (8236 bp) is a non-conjugative IncQ plasmid and contains genes encoding for plasmid replication and stabilization (repA, repB and repC), mobilization (mob), and antibiotic resistance (arr-3 and aacA). pKANJ7 (30142 bp) is a conjugative IncX plasmid which codes for a type IV secretion system (T4SS). Conjugative transfer experiments showed that the optimal mating time of pKANJ7 was 8 h under the starvation condition, but the number of tranconjugants increased with time under the nutrient condition. Statistical analysis indicated that the two plasmids had little impact on the growth of their hosts, but a relatively high level of fitness cost due to pKANJ7 was observed. We also found that the fitness cost of plasmids depended on their hosts. Compared with pKANJ7, the relative fitness cost index of pRKZ3 varied within a narrow range during the 10 days of competition. The low level of fitness cost of pRKZ3 might contribute to the persistence of the plasmid in the environment. Our study provides new information for understanding the characterizations of antibiotic resistance plasmids (ARPs) in manure sources and helps to clarify the transfer and persistence of ARPs in the environment following the application of manure.

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References

  • Andrup L, Smidt L, Andersen K, Boe L (1998). Kinetics of conjugative transfer: A study of the plasmid pxo16 from bacillus thuringiensis subsp. Israelensis1. Plasmid, 40: 30–43

    Article  CAS  Google Scholar 

  • Barilla D, Carmelo E, Hayes F (2007). The tail of the parG DNA segregation protein remodels parF polymers and enhances ATP hydrolysis via an arginine finger-like motif. Proceedings of the National Academy of Sciences of the United States of America, 104(6): 1811–1816

    Article  CAS  Google Scholar 

  • Becker K, van Alen S, Idelevich E A, Schleimer N, Seggewi J, Mellmann A, Kaspar U, Peters G (2018). Plasmid-encoded transferable mecb-mediated methicillin resistance in staphylococcus aureus. Emerging Infectious Diseases, 24(2): 242–248

    Article  CAS  Google Scholar 

  • Beranek A, Zettl M, Lorenzoni K, Schauer A, Manhart M, Koraimann G (2004). Thirty-eight c-terminal amino acids of the coupling protein TraD of the F-like conjugative resistance plasmid R1 are required and sufficient to confer binding to the substrate selector protein tram. Journal of Bacteriology, 186(20): 6999–7006

    Article  CAS  Google Scholar 

  • Bien T L T, Sato-Takabe Y, Ogo M, Usui M, Suzuki S (2015). Persistence of multi-drug resistance plasmids in sterile water under very low concentrations of tetracycline. Microbes and Environments, 30(4): 339–343

    Article  Google Scholar 

  • Binh C T, Heuer H, Kaupenjohann M, Smalla K (2008). Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiology Ecology, 66: 25–37

    Article  CAS  Google Scholar 

  • Bousquet A, Henquet S, Compain F, Genel N, Arlet G, Decré D (2015). Partition locus-based classification of selected plasmids in Klebsiella pneumoniae, Escherichia coli and Salmonella enterica spp.: An additional tool. Journal of Microbiological Methods, 110: 85–91

    Article  CAS  Google Scholar 

  • Carattoli A, Zankari E, García-Fernánde A, Voldby L M, Lund O, Villa L, Møller A F, Hasman H (2014). In silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrobial Agents and Chemotherapy, 58(7): 3895–3903

    Article  Google Scholar 

  • Chen L, Hu H Y, Chavda K D, Zhao S L, Liu R K, Liang H, Zhang W, Wang X M, Jacobs M R, Bonomo R A, Kreiswirth B N (2014). Complete sequence of a KPC-producing INCN multidrug-resistant plasmid from an epidemic Escherichia coli sequence type 131 strain in China. Antimicrobial Agents and Chemotherapy, 58(4): 2422–2425

    Article  Google Scholar 

  • Chen P, Chen C, Li X (2018). Transport of antibiotic resistance plasmids in porous media and the influence of surfactants. Frontiers of Environmental Science & Engineering, 12(2): 5

    Article  Google Scholar 

  • Christie P J, Vogel J P (2000). Bacterial type IV secretion: Conjugation systems adapted to deliver effector molecules to host cells. Trends in Microbiology, 8(8): 354–360

    Article  CAS  Google Scholar 

  • Coros A M, Twiss E, Tavakoli N P, Derbyshire K M (2005). Genetic evidence that GTP is required for transposition of IS903 and Tn552 in Escherichia coli. Journal of Bacteriology, 187(13): 4598–4606

    Article  CAS  Google Scholar 

  • Cottell J L, Webber M A, Piddock L J (2012). Persistence of transferable extended-spectrum-beta-lactamase resistance in the absence of antibiotic pressure. Antimicrobial Agents and Chemotherapy, 56(9): 4703–4706

    Article  CAS  Google Scholar 

  • Dang B J, Mao D Q, Xu Y, Luo Y (2017). Conjugative multi-resistant plasmids in Haihe River and their impacts on the abundance and spatial distribution of antibiotic resistance genes. Water Research, 111: 81–91

    Article  CAS  Google Scholar 

  • Datta N, Kontomichalou P (1965). Penicillinase synthesis controlled by infectious R factors in Enterobacteriaceae. Nature, 208: 239–241

    Article  CAS  Google Scholar 

  • Devendec L L, Mourand G, Bougeard S, Léaustic J, Jouy E, Keita A, Couet W, Rousset N, Kempf I (2016). Impact of colistin sulfate treatment of broilers on the presence of resistant bacteria and resistance genes in stored or composted manure. Veterinary Microbiology, 194: 98–106

    Article  Google Scholar 

  • Dobiasova H, Dolejska M (2016). Prevalence and diversity of IncX plasmids carrying fluoroquinolone and β-lactam resistance genes in Escherichia coli originating from diverse sources and geographical areas. Journal of Antimicrobial Chemotherapy, 71: 2118–2124

    Article  Google Scholar 

  • Foucault M L, Courvalin P, Grillot-Courvalin C (2009). Fitness cost of VanA-type vancomycin resistance in methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 53(6): 2354–2359

    Article  CAS  Google Scholar 

  • Garnier F, Debat H, Nadal M (2018). Type IA DNA topoisomerases: A universal core and multiple activities. In: Drolet M, eds. DNA topoisomerases. Methods in Molecular Biology, 1703: 1–20.

  • Giangrossi M, Wintraecken K, Spurio R, Vries R D (2014). Probing the relation between protein-protein interactions and DNA binding for a linker mutant of the bacterial nucleoid protein H-NS. Biochimica et Biophysica Acta, 1844: 339–345

    Article  CAS  Google Scholar 

  • Goessweiner-Mohr N, Arends K, Keller W, Grohmann E (2014). Conjugation in gram-positive bacteria. Microbiology Spectrum, 2: 1–19

    Article  Google Scholar 

  • Guo M T, Yuan Q B, Yang J (2015). Distinguishing effects of ultraviolet exposure and chlorination on the horizontal transfer of antibiotic resistance genes in municipal wastewater. Environmental Science & Technology, 49: 5771–5778

    Article  CAS  Google Scholar 

  • Guo Q L, Tomich A D, McElheny C L, Cooper V S, Stoesser N, Wang M, Sluis-Cremer N, Doi Y (2016a). Glutathione-S-transferase FosA6 of Klebsiella pneumoniae origin conferring fosfomycin resistance in ESBL-producing Escherichia coli. Journal of Antimicrobial Chemotherapy, 71: 2460–2465

    Article  CAS  Google Scholar 

  • Guo X Y, Hao L J, Qiu P Z, Chen R, Xu J, Kong X J, Shan Z J, Wang N (2016b). Pollution characteristics of 23 veterinary antibiotics in livestock manure and manure-amended soils in Jiangsu Province, China. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 51(6): 383–392

    CAS  Google Scholar 

  • Haldorsen B C, Simonsen G S, Sundsfjord A, Samuelsen Ø (2014). Increased prevalence of aminoglycoside resistance in clinical isolates of Escherichia coli and Klebsiella spp. in Norway is associated with the acquisition of AAC(3)-II and AAC(6′)-Ib. Diagnostic Microbiology and Infectious Disease, 78: 66–69

    Article  CAS  Google Scholar 

  • Harrison E, Brockhurst M A (2012). Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends in Microbiology, 20(6): 262–267

    Article  CAS  Google Scholar 

  • Harrison E, Guymer D, Spiers A J, Paterson S, Brockhurst M A (2015). Parallel compensatory evolution stabilizes plasmids across the parasitism-mutualism continuum. Current Biology, 25(15): 2034–2039

    Article  CAS  Google Scholar 

  • Hirt H, Greenwood-Quaintance K E, Karau M J, Till L M, Kashyap P C, Patel R, Dunny G M (2018). Enterococcus faecalis sex pheromone cCF10 enhances conjugative plasmid transfer in vivo. mBio, 9(1): 1–13

    Article  Google Scholar 

  • Huang P, Zhang Y, Xiao K, Jiang F, Wang H, Tang D, Liu D, Liu B, Liu Y, He X, Liu H, Liu X, Qing Z, Liu C, Huang J, Ren Y, Yun L, Yin L, Lin Q, Zeng C, Su X, Yuan J, Lin L, Hu N, Cao H, Huang S, Guo Y, Fan W, Zeng J (2018). The chicken gut metagenome and the modulatory effects of plant-derived benzylisoquinoline alkaloids. Microbiome, 6(1): 1–17

    Article  CAS  Google Scholar 

  • Ito H, Ishii H, Akiba M (2004). Analysis of the complete nucleotide sequence of an Actinobacillus pleuropneumoniae streptomycin-sulfonamide resistance plasmid, pMS260. Plasmid, 51: 41–47

    Article  CAS  Google Scholar 

  • Johnson T J, Bielak E M, Fortini D, Hansen L H, Hasman H, Debroy C, Nolan L K, Carattoli A (2012). Expansion of the IncX plasmid family for improved identification and typing of novel plasmids in drugresistant Enterobacteriaceae. Plasmid, 68: 43–50

    Article  CAS  Google Scholar 

  • Joy S R, Bartelt-Hunt S L, Snow D D, Gilley J E, Woodbury B L, Parker D B, Marx D B, Li X (2013). Fate and transport of antimicrobials and antimicrobial resistance genes in soil and runoff following land application of swine manure slurry. Environmental Science & Technology, 47: 12081–12088

    Article  CAS  Google Scholar 

  • Kassis-Chikhani N, Frangeul L, Drieux L, Sengelin C, Jarlier V, Brisse S, Arlet G, Decré D (2012). Complete nucleotide sequence of the first KPC-2- and SHV-12-encoding IncX plasmid, pKpS90, from Klebsiella pneumoniae. Antimicrobial Agents and Chemotherapy, 57(1): 618–620

    Article  Google Scholar 

  • Ke Y H, Wang Y F, Li W F, Chen Z L (2015). Type IV secretion system of Brucella spp. and its effectors. Frontiers in Cellular and Infection Microbiology, 5: 1–10

    Article  Google Scholar 

  • Kottara A, Hall J P J, Harrison E, Brockhurst M A (2017). Variable plasmid fitness effects and mobile genetic element dynamics across Pseudomonas species. FEMS Microbiology Ecology, 94(1): 1–7

    Google Scholar 

  • Krishnasamy V, Otte J, Silbergeld E (2015). Antimicrobial use in Chinese swine and broiler poultry production. Antimicrobial Resistance and Infection Control, 4(17): 1–9

    Google Scholar 

  • Kubori T, Koike M, Bui X T, Higaki S, Aizawa S I, Nagai H (2014). Native structure of a type IV secretion system core complex essential for Legionella pathogenesis. Proceedings of the National Academy of Sciences of the United States of America, 111(32): 11804–11809

    Article  CAS  Google Scholar 

  • Leon I M, Lawhon S D, Norman K N, Threadgill D S, Ohta N, Vinasco J, Scott H M (2018). Serotype diversity and antimicrobial resistance among Salmonella enterica isolates from patients at an equine referral hospital. Applied and Environmental Microbiology, 84(13): 1–15

    Article  CAS  Google Scholar 

  • Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J (2010). De novo assembly of human genomes with massively parallel short read sequencing. Genome Research, 20: 265–272

    Article  CAS  Google Scholar 

  • Li R C, Ye L W, Zheng Z W, Chan E W C, Chen S (2017). Genetic characterization of broad-host range IncQ plasmids harboring blaVEB-18 in vibrio species. Antimicrobial Agents and Chemotherapy, 61(7): 1–3

    Article  Google Scholar 

  • Li Y, Currie D, Zydney A L (2016). Enhanced purification of plasmid DNA isoforms by exploiting ionic strength effects during ultrafiltration. Biotechnology and Bioengineering, 113(4): 783–789

    Article  CAS  Google Scholar 

  • Liu C, Zheng H, Yang M, Xu Z, Wang X, Wei L, Tang B, Liu F, Zhang Y, Ding Y, Tang X, Wu B, Johnson T J, Chen H, Tan C (2015a). Genome analysis and in vivo virulence of porcine extraintestinal pathogenic Escherichia coli strain PCN033. BMC Genomics, 16: 1–18

    Article  Google Scholar 

  • Liu C C, Kuo H Y, Tang C Y, Chang K C, Liou M L (2014). Prevalence and mapping of a plasmid encoding a type IV secretion system in Acinetobacter baumannii. Genomics, 104: 215–223

    Article  CAS  Google Scholar 

  • Liu Z B, Zhang Z G, Yan H, Li J R, Shi L (2015b). Isolation and molecular characterization of multidrug-resistant Enterobacteriaceae strains from pork and environmental samples in Xiamen, China. Journal of Food Protection, 78(1): 78–88

    Article  CAS  Google Scholar 

  • Lo W U, Chow K H, Law P Y, Ng K Y, Cheung Y Y, Lai E L, Ho P L (2014). Highly conjugative IncX4 plasmids carrying bla CTX-M in Escherichia coli from humans and food animals. Journal of Medical Microbiology, 63: 835–840

    Article  CAS  Google Scholar 

  • Loftie-Eaton W, Bashford K, Quinn H, Dong K, Millstein J, Hunter S, Thomason M K, Merrikh H, Ponciano J M, Top E M (2017). Compensatory mutations improve general permissiveness to antibiotic resistance plasmids. Nature Ecology & Evolution, 1(9): 1354–1363

    Article  Google Scholar 

  • Madsen J S, Riber L, Kot W, Basfeld A, Burmølle M, Hansen L H, Sørensen S J (2016). Type 3 fimbriae encoded on plasmids are expressed from a unique promoter without affecting host motility, facilitating an exceptional phenotype that enhances conjugal plasmid transfer. PLoS One, 11(9): 1–19

    Article  Google Scholar 

  • McKinney C W, Dungan R S, Moore A, Leytem A B (2018). Occurrence and abundance of antibiotic resistance genes in agricultural soil receiving dairy manure. FEMS Microbiology Ecology, 94: 1–10

    Article  Google Scholar 

  • Millan A S, Peña-Miller R, Toll-Riera M, Halbert Z V, McLean A R, Cooper B S, MacLean R C (2014). Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids. Nature Communications, 10(5): 1–11

    Google Scholar 

  • Mollenkopf D X F, Stull J W, Mathys D A, Bowman A S, Feicht S M, Grooters S V, Daniels J B, Wittum T E (2017). Carbapenemase-producing Enterobacteriaceae recovered from the environment of a swine farrow-to-finish operation in the United States. Antimicrobial Agents and Chemotherapy, 61(2): 1–9

    Article  Google Scholar 

  • Nakaminami H, Noguchi N, Nishijima S, Kurokawa I, Sasatsu M (2008). Characterization of the pTZ2162 encoding multidrug efflux gene qacB from Staphylococcus aureus. Plasmid, 60: 108–117

    Article  CAS  Google Scholar 

  • Norman A, Hansen L H, She Q X, Sørensen S J (2008). Nucleotide sequence of pOLA52: A conjugative IncX1 plasmid from Escherichia coli which enables biofilm formation and multidrug efflux. Plasmid, 60: 59–74

    Article  CAS  Google Scholar 

  • Nunez B, Avila P, Cruz F D L (1997). Genes involved in conjugative DNA processing of plasmid R6K. Molecular Microbiology, 24(6): 1157–1168

    Article  CAS  Google Scholar 

  • Oshima K, Nishida H (2007). Phylogenetic relationships among Mycoplasmas based on the whole genomic information. Journal of Molecular Evolution, 65(3): 249–258

    Article  CAS  Google Scholar 

  • Partridge S R, Ellem J A, Tetu S G, Zong Z Y, Paulsen I T, Iredell J R (2011). Complete sequence of pJIE143, apir-type plasmid carrying ISEcp1-blaCTX-M-15 from an Escherichia coli ST131 isolate. Antimicrobial Agents and Chemotherapy, 55(12): 5933–5935

    Article  CAS  Google Scholar 

  • Patel J B, Cockerill F R (2016). Performance standards for antimicrobial susceptibility testing. M100S, 26th ed

  • Paulander W, Maisnier-Patin S, Andersson D I (2009). The fitness cost of streptomycin resistance depends on rpsL mutation, carbon source and RpoS (σS). Genetics, 183: 539–546

    Article  CAS  Google Scholar 

  • Peng S, Wang Y M, Zhou B B, Lin X G (2015). Long-term application of fresh and composted manure increase tetracycline resistance in the arable soil of eastern China. Science of the Total Environment, 506–507: 279–286

    Article  Google Scholar 

  • Pérez-Segura G, Pérez-Oseguera Á, Cevallos M A (2013). The repAC replication system of the Rhizobium leguminosarum pRL7 plasmid is functional: Implications regarding the origin and evolution of repABC plasmids. Plasmid, 69: 49–57

    Article  Google Scholar 

  • Porse A, Schønning K, Munck C, Sommer M O A (2016). Survival and evolution of a large multidrug resistance plasmid in new clinical bacterial hosts. Molecular Biology and Evolution, 33(11): 2860–2873

    Article  CAS  Google Scholar 

  • Pu C J, Lv M H, Zeng Y H, Gong X Y, Sun Y (2017). Drug resistance to four antibiotics of Escherichia coli in chicken and pig feces. Asian Journal of Ecotoxicology, 12(1): 141–147 (in Chinese)

    Google Scholar 

  • Qian X, Gu J, Sun W, Wang X J, Su J Q, Stedfeld R (2018). Diversity, abundance, and persistence of antibiotic resistance genes in various types of animal manure following industrial composting. Journal of Hazardous Materials, 344: 716–722

    Article  CAS  Google Scholar 

  • Qiu Z G, Yu Y M, Chen Z L, Jin M, Yan D, Zhao Z G, Wang J F, Shen Z Q, Wang X W, Qian D, Huang A H, Zhang B C, Li J W (2012). Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proceedings of the National Academy of Sciences of the United States of America, 109(13): 4944–4949

    Article  CAS  Google Scholar 

  • Rahube T O, Yost C K (2012). Characterization of a mobile and multiple resistance plasmid isolated from swine manure and its detection in soil after manure application. Journal of Applied Microbiology, 112: 1123–1133

    Article  CAS  Google Scholar 

  • Rakowski S A, Filutowicz M (2013). Plasmid R6K replication control. Plasmid, 69: 231–242

    Article  CAS  Google Scholar 

  • Redzej A, Ukleja M, Connery S, Trokter M, Felisberto-Rodrigues C, Cryar A, Thalassinos K, Hayward R D, Orlova E V, Waksman G (2017). Structure of a VirD4 coupling protein bound to a VirB type IV secretion machinery. EMBO Journal, 36(20): 3080–3095

    Article  CAS  Google Scholar 

  • Ribeiro S C, Monteiro G A, Prazeres D M F (2009). Evaluation of the effect of non-B DNA structures on plasmid integrity via accelerated stability studies. Journal of Pharmaceutical Sciences, 98(4): 1400–1408

    Article  CAS  Google Scholar 

  • Rodriguez-Bonano N M, Torres-Bauza L J (2004). Molecular analysis of oriT and MobA protein in the 7.4kb mobilizable β-lactamase plasmid pSJ7.4 from Neisseria gonorrhoeae. Plasmid, 52(2): 89–101

    Article  CAS  Google Scholar 

  • Rysz M, Mansfield W R, Fortner J D, Alvarez P J J (2013). Tetracycline resistance gene maintenance under varying bacterial growth rate, substrate and oxygen availability, and tetracycline concentration. Environmental Science & Technology, 47(13): 6995–7001

    Article  CAS  Google Scholar 

  • San Millan A, Garcia-Cobos S, Escudero J A, Hidalgo L, Gutierrez B, Carrilero L, Campos J, Gonzalez-Zorn B (2010). Haemophilus influenzae clinical isolates with plasmid pB1000 bearing blaROB-1: Fitness cost and interspecies dissemination. Antimicrobial Agents and Chemotherapy, 54(4): 1506–1511

    Article  CAS  Google Scholar 

  • Scott A B, Singh M, Toribio J, Hernandez-Jover M, Barnes B, Glass K, Moloney B, Lee A, Groves P (2017). Comparisons of management practices and farm design on Australian commercial layer and meat chicken farms: Cage, barn and free range. PLoS One, 12(11): 1–17

    Article  Google Scholar 

  • Shen P, Yi M L, Fu Y, Ruan Z, Du X X, Yu Y S, Xie X Y (2017). Detection of an Escherichia coli sequence type 167 strain with two tandem copies of blaNDM-1 in the chromosome. Journal of Clinical Microbiology, 55(1): 199–204

    Article  CAS  Google Scholar 

  • Silva F, Queiroz J A, Domingues F C (2012). Evaluating metabolic stress and plasmid stability in plasmid DNA production by Escherichia coli. Biotechnology Advances, 30(3): 691–708

    Article  CAS  Google Scholar 

  • Smalla K, Heuer H, Gotz A, Niemeyer D, Krogerrecklenfort E, Tietze E (2000). Exogenous isolation of antibiotic resistance plasmids from piggery manure slurries reveals a high prevalence and diversity of IncQ-like plasmids. Applied and Environmental Microbiology, 66(11): 4854–4862

    Article  CAS  Google Scholar 

  • Smillie C, Garcillan-Barcia M P, Francia M V, Rocha E P C, de la Cruz F (2010). Mobility of plasmids. Microbiology and Molecular Biology Reviews, 74(3): 434–452

    Article  CAS  Google Scholar 

  • Sumrall E T, Gallo E B, Aboderin A O, Lamikanra A, Okeke I N (2014). Dissemination of the transmissible quinolone-resistance gene qnrS1 by IncX plasmids in Nigeria. PLoS One, 9: e110279

    Article  Google Scholar 

  • Sun J, Li X P, Fang L X, Sun R Y, He Y Z, Lin J X, Liao X P, Feng Y J, Liu Y H (2018). Co-occurrence of mcr-1 in the chromosome and on an IncHI2 plasmid: Persistence of colistin resistance in Escherichia coli. International Journal of Antimicrobial Agents, 51: 842–847

    Article  CAS  Google Scholar 

  • Tokajian S, Moghnieh R, Salloum T, Arabaghian H, Alousi S, Moussa J, Abboud E, Youssef S, Husni R (2018). Extended-spectrum β-lactamase-producing Escherichia coli in wastewaters and refugee camp in Lebanon. Future Microbiology, 13(1): 81–95

    Article  CAS  Google Scholar 

  • Unterholzner S J, Hailer B, Poppenberger B, Rozhon W (2013). Characterisation of the stbD/E toxin-antitoxin system of pEP36, a plasmid of the plant pathogen Erwinia pyrifoliae. Plasmid, 70: 216–225

    Article  CAS  Google Scholar 

  • Wang N, Guo X, Xu J, Kong X, Gao S, Shan Z (2014). Pollution characteristics and environmental risk assessment of typical veterinary antibiotics in livestock farms in Southeastern China. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 49: 468–479

    CAS  Google Scholar 

  • Wang W, Baloch Z, Peng Z X, Hu Y J, Xu J, Fanning S, Li F X (2017). Genomic characterization of a large plasmid containing a blaNDM-1 gene carried on Salmonella enterica serovar Indiana C629 isolate from China. BMC Infectious Diseases, 17: 479

    Article  Google Scholar 

  • Wetzel M E, Olsen G J, Chakravartty V, Farrand S K (2015). The repABC plasmids with quorum-regulated transfer systems in members of the Rhizobiales divide into two structurally and separately evolving groups. Genome Biology and Evolution, 7(12): 3337–3357

    Article  CAS  Google Scholar 

  • Wild J, Czyz A, Rakowski S A, Filutowicz M (2004). g Origin plasmids of R6K lineage replicate in diverse genera of Gram-negative bacteria. Annals of Microbiology, 54(4): 119–128

    Google Scholar 

  • Wong M H, Chan E W, Chen S (2017). IS26-mediated formation of a virulence and resistance plasmid in Salmonella Enteritidis. Journal of Antimicrobial Chemotherapy, 72(10): 2750–2754

    Article  CAS  Google Scholar 

  • Yan J J, Wu J J, Ko W C, Tsai S H, Chuang C L, Wu H M, Lu Y J, Li J D (2004). Plasmid-mediated 16S rRNA methylases conferring highlevel aminoglycoside resistance in Escherichia coli and Klebsiella pneumoniae isolates from two Taiwanese hospitals. Journal of Antimicrobial Chemotherapy, 54: 1007–1012

    Article  CAS  Google Scholar 

  • Yang Y X, Yang Y Q, Lei C W, Liu B H, Jiang W, Wang H N, Gazitúa M C, Zhang A Y (2017). Characterization of pHeBE7, an IncFII-type virulence-resistance plasmid carrying bla CTX-M-98b, bla TEM-1, and rmtB genes, detected in Escherichia coli from a chicken isolate in China. Plasmid, 92: 37–42

    Article  CAS  Google Scholar 

  • Zhang M L, Chen S, Gnegy M, Ye C S, Lin W F, Lin H R, Yu X (2018). Environmental strains potentially contribute to the proliferation and maintenance of antibiotic resistance in drinking water: A case study of Cupriavidus metallidurans. Science of the Total Environment, 643: 819–826

    Article  CAS  Google Scholar 

  • Zhang N, Liu X, Liu R, Zhang T, Li M, Zhang Z R, Qu Z T, Yuan Z T, Yu H C (2019). Influence of reclaimed water discharge on the dissemination and relationships of sulfonamide, sulfonamide resistance genes along the Chaobai River, Beijing. Frontiers of Environmental Science & Engineering, 13(1): 1–12

    Article  Google Scholar 

  • Zhang Q, Ying G, Pan C, Liu Y, Zhao J (2015). Comprehensive evaluation of antibiotics emission and fate in the river basins of china: Source analysis, multimedia modeling, and linkage to bacterial resistance. Environmental Science & Technology, 49(11): 6772–6782

    Article  CAS  Google Scholar 

  • Zhang Y, Gu A Z, He M, Li D, Chen J M (2016). Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera. Environmental Science & Technology, 51: 570–580

    Article  Google Scholar 

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Acknowledgements

This work is financially supported by the National Key Research and Development Plan of China (No. 2016YFD0501404). We greatly appreciate Professor Congming Wu, College of Veterinary Medicine, China Agricultural University, for kindly providing E. coli J53. We also thank Rory Vu Mather (a research student at Washington University in St. Louis) for his linguistic assistance in manuscript preparation.

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Correspondence to Ying Sun.

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Highlights

• pRKZ3 is a non-conjugative IncQ plasmid, while pKANJ7 is a conjugative IncX plasmid.

• The optimal mating time of pKANJ7 varied under different conditions.

• Both of the two transferable ARPs had little impact on the growth of their hosts.

• A relatively high level of fitness cost was observed for pKANJ7.

• The fitness cost of ARPs depended on their hosts.

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Pu, C., Gong, X. & Sun, Y. Characteristics of two transferable aminoglycoside resistance plasmids in Escherichia coli isolated from pig and chicken manure. Front. Environ. Sci. Eng. 13, 35 (2019). https://doi.org/10.1007/s11783-019-1119-2

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