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Mechanisms of Resistance

Mutational and Transcriptomic Changes Involved in the Development of Macrolide Resistance in Campylobacter jejuni

Haihong Hao, Zonghui Yuan, Zhangqi Shen, Jing Han, Orhan Sahin, Peng Liu, Qijing Zhang
Haihong Hao
National Reference Laboratory of Veterinary Drug Residues (HZAU)/MOA Key Laboratory for Detection of Veterinary Drug Residues in Foods, Huazhong Agricultural University, Wuhan, People's Republic of ChinaDepartment of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, Iowa, USA
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Zonghui Yuan
National Reference Laboratory of Veterinary Drug Residues (HZAU)/MOA Key Laboratory for Detection of Veterinary Drug Residues in Foods, Huazhong Agricultural University, Wuhan, People's Republic of China
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Zhangqi Shen
Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, Iowa, USA
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Jing Han
Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, Iowa, USA
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Orhan Sahin
Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, Iowa, USA
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Peng Liu
Department of Statistics, Iowa State University, Ames, Iowa, USA
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Qijing Zhang
Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, Iowa, USA
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DOI: 10.1128/AAC.01927-12
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  • Fig 1
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    Fig 1

    Differential expression of four efflux genes in selected mutant strains in four different lineages. The data were generated by real-time RT-PCR in comparison with the parent strain (NCTC 11168 or 81-176).

  • Fig 2
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    Fig 2

    Immunoblotting analysis of CmeABC expression in selected strains in four different lineages. In panel A, numbers 1, 2, 3, 4, 5, and 6 represent C. jejuni NCTC 11168, 68E1-3, 68E4-3, 68E8-3, 68E32-3, and 68E64-3, respectively. In panel B, numbers 1, 2, 3, 4, 5, and 6 correspond to C. jejuni NCTC 11168, 68E1-1, 68E4-1, 68E8-1, 68E32-1, and 68E64-1. In panel C, numbers 1, 2, 3, and 4 correspond to C. jejuni 81-176, 76E2-6, 76E8-6, and 76E64-6. In panel D, numbers 1, 2, 3, and 4 correspond to C. jejuni 81-176, 76T8-7, 76T16-7, and 76T32-7. Cell envelopes prepared from each strain were blotted with polyclonal antibodies to CmeA, CmeB, and CmeC. The same amount of total proteins was loaded in each lane. Prestained molecular mass markers (lane M; Bio-Rad) were used to estimate the sizes of the proteins (shown in kilodaltons). The positions of CmeA, CmeB, and CmeC are indicated.

  • Fig 3
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    Fig 3

    HCL analysis of C. jejuni genes differentially expressed in the three strains (68E1-3, 68E8-3, and 68E64-3) in lineage 68Ex-3. For each of the four clusters, hierarchical clustering was performed both on the genes and on the strains to visualize the relationships among the genes and strains, respectively. Four clusters are presented in four different panels. For each cluster, the color scale shows the n-fold change range of up- and down-regulated genes. The three mutant strains are indicated at the top of each panel.

Tables

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  • Table 1

    Primers used for PCR amplification and real-time RT-PCR

    PrimerSequence (5′–3′)Reference
    23S rRNA gene amplification
        FICCCTAAGTCAAGCCTTTCAATCC20
        FIICGTTATAGATACGCTTAGCGGTTATG20
        FIIICATCGAGCAAGAGTTTATGCAAGC20
        CJ-copy-RCTACCCACCAGACATTGTCCCAC20
    Fragment of 23S rRNA gene
        23S-domV-FGTAAACGGCGGCCGTAACTAThis study
        23S-domV-RGACCGAACTGTCTCACGACGThis study
        23S-2611FATGTCGGCTCATCGCATCCTGG20
        23S-2611RCATCCATTACACACCCAGCCTATC20
    Ribosomal protein L4
        L4-FGTAGTTAAAGGTGCAGTACCAThis study
        L4-RGCGAAGTTTGAATAACTACGThis study
    Ribosomal protein L22
        L22-FGAATTTGCTCCAACACGCThis study
        L22-RACCATCTTGATTCCCAGTTTCThis study
    CmeR and cmeABC promoter
        cmeR-FTAGAAAAGTATATTTGTATACCCT16
        cmeR-RCGCCACTAACTTGAGGCTTTA16
    Real-time RT-PCRa
        16S-FTACCTGGGCTTGATATCCTA21
        16S-RGGACTTAACCCAACATCTCA21
        CmeB-FACGATTCAACCTTTTCCCAGCThis study
        CmeB-RTTTGCTACTTGAGCAATCGCTTCThis study
        Cj1687-FTGGTGGTTTGGACTCTTTCTGGGAThis study
        Cj1687-FTCTCTGCGATTAAAGCCACCACGAThis study
        Cj1375-FGCTTTACCACGATTTTCTTCTGTGAThis study
        Cj1375-RTACACCATGCTTTTAGGAAGAATGCThis study
        Cj1257c-FATCGCCGTGATAGCGCCTAAAGAAThis study
        Cj1257c-RGCCACCAAACAAAGGCCCAAGTAAThis study
    • ↵a Sequences and gene names are based on C. jejuni NCTC 11168.

  • Table 2

    Characteristics of C. jejuni mutants selected by Ery

    Lineagea and strainbMIC (μg/ml)Mutation in 23S rRNA genecChange in protein L4Change(s) in protein L22Mutation in cmeR
    EryTyl
    Parent, NCTC 1116814—d——
    68Ex-1
        68E1-148——A88E—
        68E4-132256——A88EDel490A
        68E8-164128——A88EDel490A
        68E32-1256128—G67VA88EDel490A
        68E64-1>512256C2627A (3)G67VA88EDel490A
    68Ex-2
        68E1-248—59-G-60—
        68E4-232128—59-G-60G86E—
        68E8-264128—59-G-60A84D, G86E—
        68E32-2128128—59-G-60A84D, G86V—
        68E64-2512256—59-G-60A84D, G86V—
    68Ex-268Ex-3
        68E1-3416—R72I——
        68E4-36464—R72IV100LH174N
        68E8-3128256—R72I91-S-92H174N
        68E32-3>512>512—R72I—H174N
        68E64-3>512>512A2074C (3)R72I—H174N
    Parent, 8117614————
    68Ex-268Ex-376Ex-6
        76E2-63264————
        76E8-6256>512A2074C (2)———
        76E64-6>512>512A2074C (3)———
    • ↵a The lineages are named according to the parent strain and the antibiotic used for selection. 68 and 76 indicate that the parent strains are 11168 and 81-176, respectively, E represents selection by Ery, x depicts the various concentrations used for selection, and the last number indicates the lineage number.

    • ↵b The strains in the lineages are named similarly to the lineages, except that x is replaced by the actual antibiotic concentration from which the mutant was selected.

    • ↵c Each number in parentheses is the number of mutated copies of the 23S rRNA gene.

    • ↵d —, no mutations detected.

  • Table 3

    Characteristics of C. jejuni mutants selected by Tyl

    Lineagea and strainbMIC (μg/ml)Mutation in 23S rRNA geneChange in protein L4Change(s) in protein L22Mutation in cmeR
    EryTyl
    Parent, NCTC 1116814—c——
    68Tx-1
        68T4-148——A88E
        68T16-132256—R72IA88EH174N
        68T32-164256—R72IA88EH174N
        68T128-1128256—R72IA88EH174N
    68Tx-2
        68T4-248———
        68T16-2128256—G57V——
        68T32-2256512—G57VG86E—
        68T128-2128256—G57VG86E—
    68 Tx-3
        68T4-328————
        68T16-332256—A71D—S117Y
        68T32-364512—A71DA88ES117Y
        68T64-316256—A71DA88ES117Y
    68Tx-4
        68T4-428————
        68T8-41664—A71D——
        68T16-432128—A71DA88EG204L
        68T32-464256—A71DA88EG204L
        68T64-4128512—A71DA88E, G86VG204L
    Parent, 8117614————
    76Tx-7
        76T8-7832————
        76T16-732128—G57DG86E—
        76T32-764256—G57DG86E—
    • ↵a See Table 2 footnote a for an explanation of the lineage names. T represents selection by Tyl.

    • ↵b See Table 2 footnote b for an explanation of the strain names.

    • ↵c —, no mutations detected.

Additional Files

  • Figures
  • Tables
  • Supplemental material

    Files in this Data Supplement:

    • Supplemental file 1 -

      Figure S1, Venn diagram showing the numbers of genes differentially expressed in three selected mutant strains (68E1-3, 68E8-3, and 68E64-3) of lineage 68Ex-3 in comparison with wild-type NCTC 11168.

      PDF, 34K

    • Supplemental file 2 -

      Supplemental Table S1

      XLSX, 35K

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Mutational and Transcriptomic Changes Involved in the Development of Macrolide Resistance in Campylobacter jejuni
Haihong Hao, Zonghui Yuan, Zhangqi Shen, Jing Han, Orhan Sahin, Peng Liu, Qijing Zhang
Antimicrobial Agents and Chemotherapy Feb 2013, 57 (3) 1369-1378; DOI: 10.1128/AAC.01927-12

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Mutational and Transcriptomic Changes Involved in the Development of Macrolide Resistance in Campylobacter jejuni
Haihong Hao, Zonghui Yuan, Zhangqi Shen, Jing Han, Orhan Sahin, Peng Liu, Qijing Zhang
Antimicrobial Agents and Chemotherapy Feb 2013, 57 (3) 1369-1378; DOI: 10.1128/AAC.01927-12
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