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Volume 25, Number 12—December 2019

Genomic Analysis of Fluoroquinolone- and Tetracycline-Resistant Campylobacter jejuni Sequence Type 6964 in Humans and Poultry, New Zealand, 2014–2016

Nigel P. FrenchComments to Author , Ji Zhang, Glen P. Carter, Anne C. Midwinter, Patrick J. Biggs, Kristin Dyet, Brent J. Gilpin, Danielle J. Ingle, Kerry Mulqueen, Lynn E. Rogers, David A. Wilkinson, Sabrina S. Greening, Petra Muellner, Ahmed Fayaz, and Deborah A. Williamson
Author affiliations: Massey University, Palmerston North, New Zealand (N.P. French, J. Zhang, A.C. Midwinter, P.J. Biggs, L.E. Rogers, D.A. Wilkinson, S.S. Greening, A. Fayaz); New Zealand Food Safety Science and Research Centre, Palmerston North (N.P. French, D.A. Wilkinson); The University of Melbourne, Melbourne, Victoria, Australia (G.P. Carter, D.J. Ingle, D.A. Williamson); Institute of Environmental Science and Research Limited, Christchurch, New Zealand (K. Dyet, B.J. Gilpin); Australian National University, Canberra, Australian Capital Territory, Australia (D.J. Ingle); Poultry Industry Association of New Zealand, Auckland, New Zealand (K. Mulqueen); EPI-interactive, Wellington, New Zealand (P. Muellner)

Main Article

Figure 2

Population structure of 227 sequence type 6964 Campylobacter jejuni isolates from humans and poultry, New Zealand, 2014–2016. The tree is the inferred midpoint rooted phylogeny of the isolates, including the reference 15AR0984 genome. The tips are colored by source of the C. jejuni isolate. The heatmap indicates the likelihoods of the presence of mobile elements including CJIE1 variant (cjie1_15AR0984), CJIEs 1–4, and the plasmid 15AR0984-m. Dark shading on the heatmap indicates 100% likelihood;

Figure 2. Population structure of 227 sequence type 6964 Campylobacter jejuni isolates from humans and poultry, New Zealand, 2014–2016. The tree is the inferred midpoint rooted phylogeny of the isolates, including the reference 15AR0984 genome. The tips are colored by source of the C. jejuni isolate. The heatmap indicates the likelihoods of the presence of mobile elements including CJIE1 variant (cjie1_15AR0984), CJIEs 1–4, and the plasmid 15AR0984-m. Dark shading on the heatmap indicates 100% likelihood; white indicates absence. Scale bar indicates nucleotide substitutions per site.

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  1. Kaakoush  NO, Castaño-Rodríguez  N, Mitchell  HM, Man  SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev. 2015;28:687720. DOIPubMed
  2. Sproston  EL, Wimalarathna  HML, Sheppard  SK. Trends in fluoroquinolone resistance in Campylobacter. Microb Genom. 2018;4.
  3. The Institute of Environmental Science and Research Ltd. Notifiable diseases in New Zealand: annual report 2017 [cited 2019 Oct 9].
  4. Sears  A, Baker  MG, Wilson  N, Marshall  J, Muellner  P, Campbell  DM, et al. Marked campylobacteriosis decline after interventions aimed at poultry, New Zealand. Emerg Infect Dis. 2011;17:100715. DOIPubMed
  5. Müllner  P, Collins-Emerson  JM, Midwinter  AC, Carter  P, Spencer  SE, van der Logt  P, et al. Molecular epidemiology of Campylobacter jejuni in a geographically isolated country with a uniquely structured poultry industry. Appl Environ Microbiol. 2010;76:214554. DOIPubMed
  6. McTavish  SM, Pope  CE, Nicol  C, Sexton  K, French  N, Carter  PE. Wide geographical distribution of internationally rare Campylobacter clones within New Zealand. Epidemiol Infect. 2008;136:124452. DOIPubMed
  7. Mullner  P, Spencer  SEF, Wilson  DJ, Jones  G, Noble  AD, Midwinter  AC, et al. Assigning the source of human campylobacteriosis in New Zealand: a comparative genetic and epidemiological approach. Infect Genet Evol. 2009;9:13119. DOIPubMed
  8. Sheppard  SK, Cheng  L, Méric  G, de Haan  CP, Llarena  A-K, Marttinen  P, et al. Cryptic ecology among host generalist Campylobacter jejuni in domestic animals. Mol Ecol. 2014;23:244251. DOIPubMed
  9. Bolwell  CF, Gilpin  BJ, Campbell  D, French  NP. Evaluation of the representativeness of a sentinel surveillance site for campylobacteriosis. Epidemiol Infect. 2015;143:19902002. DOIPubMed
  10. Williamson  D, Dyet  K, Heffernan  H. Antimicrobial resistance in human isolates of Campylobacter jejuni, 2015 [cited 2019 Oct 9].
  11. Nohra  A, Grinberg  A, Midwinter  AC, Marshall  JC, Collins-Emerson  JM, French  NP. Molecular epidemiology of Campylobacter coli strains isolated from different sources in New Zealand between 2005 and 2014. Appl Environ Microbiol. 2016;82:436370. DOIPubMed
  12. Wang  G, Clark  CG, Taylor  TM, Pucknell  C, Barton  C, Price  L, et al. Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J Clin Microbiol. 2002;40:47447. DOIPubMed
  13. Clinical and Laboratory Standards Institute. Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria, 3rd edition (M45). Wayne (PA): The Institute; 2016.
  14. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 5.0. 2015 [cited 2018 Oct 10].
  15. Dingle  KE, McCarthy  ND, Cody  AJ, Peto  TE, Maiden  MC. Extended sequence typing of Campylobacter spp., United Kingdom. Emerg Infect Dis. 2008;14:16202. DOIPubMed
  16. Baines  SL, Howden  BP, Heffernan  H, Stinear  TP, Carter  GP, Seemann  T, et al. Rapid emergence and evolution of Staphylococcus aureus clones harboring fusC-containing staphylococcal cassette chromosome elements. Antimicrob Agents Chemother. 2016;60:235965. DOIPubMed
  17. Bankevich  A, Nurk  S, Antipov  D, Gurevich  AA, Dvorkin  M, Kulikov  AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:45577. DOIPubMed
  18. Zhang  J, Xiong  Y, Rogers  L, Carter  GP, French  N. Genome-by-genome approach for fast bacterial genealogical relationship evaluation. Bioinformatics. 2018;34:30257. DOIPubMed
  19. Huson  DH, Bryant  D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23:25467. DOIPubMed
  20. Croucher  NJ, Page  AJ, Connor  TR, Delaney  AJ, Keane  JA, Bentley  SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43:e15. DOIPubMed
  21. Cody  AJ, Bray  JE, Jolley  KA, McCarthy  ND, Maiden  MCJ. Core genome multilocus sequence typing scheme for stable, comparative analyses of Campylobacter jejuni and C. coli human disease isolates. J Clin Microbiol. 2017;55:208697. DOIPubMed
  22. Page  AJ, Taylor  B, Delaney  AJ, Soares  J, Seemann  T, Keane  JA, et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom. 2016;2:e000056. DOIPubMed
  23. Nguyen  LT, Schmidt  HA, von Haeseler  A, Minh  BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:26874. DOIPubMed
  24. Minh  BQ, Nguyen  MA, von Haeseler  A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013;30:118895. DOIPubMed
  25. Yu  G, Lam  TT, Zhu  H, Guan  Y. Two methods for mapping and visualizing associated data on phylogeny using ggtree. Mol Biol Evol. 2018;35:30413. DOIPubMed
  26. Hadfield  J, Croucher  NJ, Goater  RJ, Abudahab  K, Aanensen  DM, Harris  SR. Phandango: an interactive viewer for bacterial population genomics. Bioinformatics. 2017. [Epub ahead of print].
  27. Seemann  T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:20689. DOIPubMed
  28. Llarena  A-K, Zhang  J, Vehkala  M, Välimäki  N, Hakkinen  M, Hänninen  M-L, et al. Monomorphic genotypes within a generalist lineage of Campylobacter jejuni show signs of global dispersion. Microb Genom. 2016;2:e000088. DOIPubMed
  29. Parker  CT, Quiñones  B, Miller  WG, Horn  ST, Mandrell  RE. Comparative genomic analysis of Campylobacter jejuni strains reveals diversity due to genomic elements similar to those present in C. jejuni strain RM1221. J Clin Microbiol. 2006;44:412535. DOIPubMed
  30. Darling  AC, Mau  B, Blattner  FR, Perna  NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14:1394403. DOIPubMed
  31. Alikhan  NF, Petty  NK, Ben Zakour  NL, Beatson  SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 2011;12:402. DOIPubMed
  32. Poly  F, Read  TD, Chen  YH, Monteiro  MA, Serichantalergs  O, Pootong  P, et al. Characterization of two Campylobacter jejuni strains for use in volunteer experimental-infection studies. Infect Immun. 2008;76:565567. DOIPubMed
  33. Wang  Y, Huang  WM, Taylor  DE. Cloning and nucleotide sequence of the Campylobacter jejuni gyrA gene and characterization of quinolone resistance mutations. Antimicrob Agents Chemother. 1993;37:45763. DOIPubMed
  34. Marasini  D, Fakhr  MK. Whole-genome sequencing of a Campylobacter jejuni strain isolated from retail chicken meat reveals the presence of a megaplasmid with Mu-like prophage and multidrug resistance genes. Genome Announc. 2016;4:e0046016. DOIPubMed
  35. Fouts  DE, Mongodin  EF, Mandrell  RE, Miller  WG, Rasko  DA, Ravel  J, et al. Major structural differences and novel potential virulence mechanisms from the genomes of multiple campylobacter species. PLoS Biol. 2005;3:e15. DOIPubMed
  36. The Institute of Environmental Science and Research Ltd. General antimicrobial susceptibility data collected from hospital and community laboratories [cited 2018 Aug 1].
  37. Pleydell  EJ, Rogers  L, Kwan  E, French  NP. Low levels of antibacterial drug resistance expressed by Gram-negative bacteria isolated from poultry carcasses in New Zealand. N Z Vet J. 2010;58:22936. DOIPubMed
  38. Heffernen  H, Wong  T, Lindsay  J, Bowen  B, Woodhouse  R. A baseline survey of antimicrobial resistance in bacteria from selected New Zealand foods, 2009–2010 [cited 2019 Oct 9].
  39. New Zealand Food Safety. Antibiotic sales analysis 2014–2016. Technical paper no. 2018/08 [cited 2019 Oct 9].
  40. Ministry for Primary Industries. 2011–2014 Antibiotic Sales Analysis. MPI technical paper no. 2016/65 [cited 2019 Oct 9].
  41. Huang  JY, Henao  OL, Griffin  PM, Vugia  DJ, Cronquist  AB, Hurd  S, et al. Infection with pathogens transmitted commonly through food and the effect of increasing use of culture-independent diagnostic tests on surveillance—Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2012–2015. MMWR Morb Mortal Wkly Rep. 2016;65:36871. DOIPubMed
  42. May  FJ, Stafford  RJ, Carroll  H, Robson  JM, Vohra  R, Nimmo  GR, et al. The effects of culture independent diagnostic testing on the diagnosis and reporting of enteric bacterial pathogens in Queensland, 2010 to 2014. Commun Dis Intell Q Rep. 2017;41:E22330.PubMed
  43. Whitehouse  CA, Young  S, Li  C, Hsu  CH, Martin  G, Zhao  S. Use of whole-genome sequencing for Campylobacter surveillance from NARMS retail poultry in the United States in 2015. Food Microbiol. 2018;73:1228. DOIPubMed
  44. Clark  CG, Grant  CC, Pollari  F, Marshall  B, Moses  J, Tracz  DM, et al. Effects of the Campylobacter jejuni CJIE1 prophage homologs on adherence and invasion in culture, patient symptoms, and source of infection. BMC Microbiol. 2012;12:269. DOIPubMed
  45. Clark  CG, Chong  PM, McCorrister  SJ, Simon  P, Walker  M, Lee  DM, et al. The CJIE1 prophage of Campylobacter jejuni affects protein expression in growth media with and without bile salts. BMC Microbiol. 2014;14:70. DOIPubMed
  46. Gaasbeek  EJ, Wagenaar  JA, Guilhabert  MR, van Putten  JP, Parker  CT, van der Wal  FJ. Nucleases encoded by the integrated elements CJIE2 and CJIE4 inhibit natural transformation of Campylobacter jejuni. J Bacteriol. 2010;192:93641. DOIPubMed
  47. Gaasbeek  EJ, Wagenaar  JA, Guilhabert  MR, Wösten  MM, van Putten  JP, van der Graaf-van Bloois  L, et al. A DNase encoded by integrated element CJIE1 inhibits natural transformation of Campylobacter jejuni. J Bacteriol. 2009;191:2296306. DOIPubMed

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