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Research Article | Molecular Biology and Physiology

MITEAba12, a Novel Mobile Miniature Inverted-Repeat Transposable Element Identified in Acinetobacter baumannii ATCC 17978 and Its Prevalence across the Moraxellaceae Family

Felise G. Adams, Melissa H. Brown
Craig D. Ellermeier, Editor
Felise G. Adams
aCollege of Science and Engineering, Flinders University, Bedford Park, South Australia, Australia
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Melissa H. Brown
aCollege of Science and Engineering, Flinders University, Bedford Park, South Australia, Australia
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Craig D. Ellermeier
University of Iowa
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Sally Partridge
University of Sydney
Roles: Solicited external reviewer
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John Boyce
Monash University
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DOI: 10.1128/mSphereDirect.00028-19
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  • FIG 1
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    FIG 1

    Identification of hypermotile variants from A. baumannii ATCC 17978 WT, ΔqseBC, and ΔygiW strains after desiccation stress. (A) Desiccation survival was determined by enumeration of viable cells (CFU/ml) over a 30-day period. Markers represent mean values of viable cells and error bars the standard errors of the means calculated on days 0, 1, 3, 5, 7, 9, 15, 21, and 30. Four biological replicates were undertaken over two independent experiments. The pink arrow indicates the day that hypermotile variants were identified. (B) Images of hypermotile variants (blue arrows) obtained from rehydrated desiccated cells after ON incubation at 37°C on 1% LB agar.

  • FIG 2
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    FIG 2

    Insertions in the hns locus from hypermotile variants and relationship between ISAba12 and MITEAba12. (A) Examples of amplicons generated from PCR across the hns locus from hypermotile isolates compared to the wild type and the previously identified Δhns mutant (27). The amplicon from the ΔygiW Δhns::MITEAba12 strain (663 bp) was 122 bp larger than that from the wild-type control (541 bp), while the ΔygiW Δhns::ISAba12 strain yielded the same size product as the Δhns control (1,590 bp). (B) The open white arrow depicts the hns gene (ACX60_16755) and direction of transcription, and black triangles with green nucleotide sequences represent the TSD for the two integration sites identified previously (29) as well as in this study. The 113-bp MITE is comprised of an 81-bp central region (CR; blue) flanked by 16-bp imperfect inverted repeat sequences (IRL and IRR; purple). //, break in DNA sequence. The novel insertion site/TSD sequences are in pink. The figure is not drawn to scale. (C) Location of MITEAba12 in the A. baumannii ATCC 17978 genome. The 3′ end of ACX60_04650 is fused to MITEAba12, leading to a truncation and the formation of a pseudogene. The deduced amino acid sequence for the modified ACX60_04650 is designated by a single letter code above the underlined nucleotide sequence, and the asterisk indicates the proposed stop codon. Purple and blue nucleotides represent TIR and CR, respectively, of MITEAba12. (D) Nucleotide alignment of 12 bp up- and downstream of the MITEAba12 element in hns of the A. baumannii ATCC 17978 ΔygiW strain, ISAba12 elements present in ATCC 17978, and ISAba12 in hns [ISAba12 (hns)] (27). TIR and TSD are in purple and pink, respectively. Purple underlined nucleotides represent the mismatching base in IRR. The black bracket indicates the size of the region between IRL and IRR, either 81 bp for MITEAba12 or up to 1,008 bp for ISAba12.

  • FIG 3
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    FIG 3

    Nucleotide alignment of all MITEAba12 elements identified in this study. The nucleotide sequence above the alignment (black box) denotes the consensus sequence, MITEAba12(c), derived using WebLogo software (35). MITEAba12 sequences with nucleotide variations are displayed. Subgroup representatives are numbered and in boldface type with numbers in parentheses indicating the total number of MITEAba12 copies with that sequence. A, T, G, and C nucleotides are denoted in blue, yellow, purple, and green boxes, respectively. Black lines and asterisks represent the terminal inverted repeats (IRL and IRR) and conserved bases, respectively. See Table S1 for a full list of MITEAba12 elements included in each subgroup and Table 1 for strain accession numbers.

  • FIG 4
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    FIG 4

    Characterization of target site duplications flanking MITEAba12. (A) Graphical representation of AT richness (%) identified from all target site duplications flanking MITEAba12 elements. (B) Nucleotide logo generated from all target site duplication events using WebLogo software (35).

  • FIG 5
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    FIG 5

    MITEAba12 is located within Tn6645 in Moraexella osloensis CCUG 350. Gray arrows indicate the direction of transcription, and blue arrows represent ISAba3 elements forming the boundaries of Tn6645. Identity between regions is indicated by the color gradient. (A) Alignment of nucleotide sequence from AXE82_04585 to AXE82_06445 in M. osloensis CCUG 350 and the corresponding region in strain KSH (73) (GenBank accession numbers CP014234.1 and CP024180.2, respectively). Gene names and locus tags are derived from M. osloensis CCUG 350 annotation. (B) Alignment of Tn6645 from M. osloensis CCUG 350 and part of the A. guillouiae NBRC 110550 chromosome (GenBank accession number AP014630.1 [43]). Identity between Tn6645 and A. guillouiae NBRC 110550 starts 80 bp downstream from the TIR of ISAba11. The 8-bp TSDs flanking Tn6645 are shown. The location of MITEAba12 is indicated by the orange triangle. Sequences were obtained from the NCBI database and aligned and visualized using the Easyfig 2.2.2 tool (74).

Tables

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  • Supplemental Material
  • TABLE 1

    Bacterial strains that harbor full-length MITEAba12 elements

    Strain or plasmidNo. of MITEAba12
    elements per strain
    Isolation source/originAccession no. and
    reference or source
    Strain
     A. baumannii DS00222Soil, IndiaCP027704.1, unpublished
     A. indicus SGAir056410Air, SingaporeCP024620.1 (75)
     A. johnsonii XBB1a7Hospital sewage, USACP010350.1 (76)
     A. junii 655Limnetic water, RussiaCP019041 (77)
     Acinetobacter sp. strain SWBY1a5Hospital sewage, ChinaCP026616.1, unpublished
     A. baumannii B83004Human bloodstream,
    southern India
    LFYY00000000.1 (78)
     Acinetobacter sp. strain ACNIH13Hospital plumbing, USACP026420.1 (79)
     A. baumannii ABNIH283Hospital plumbing, USACP026125 (79)
     Acinetobacter sp. strain TGL-Y22Frozen soil, ChinaCP015110.1, unpublished
     A. baumannii B83422Human bloodstream,
    southern India
    LFYZ00000000.1, (80)
     M. osloensis CCUG 3501Human cerebrospinal fluid, USACP014234.1, unpublished
     A. haemolyticus TJS011Human respiratory tract, ChinaCP018871.1, unpublished
     Acinetobacter sp. strain NCu2D-21Murine trachea, GermanyCP015594 (81)
     Acinetobacter sp. strain ACNIH2a1Hospital plumbing, USACP026412.1 (79)
     A. baumannii ATCC 179781Human meninges, FranceCP012004.1 (5)
     A. junii WCHAJ591Hospital sewage, ChinaCP028800.1, unpublished
     A. baumannii AR_00831UnknownCP027528.1, unpublished
     Acinetobacter sp. strain WCHA45a1Sewage, ChinaCP028561.1, unpublished
     A. baumannii MADb1Human skin, FranceAY665723.1 (82)
    Plasmids
     A. schindleri SGAir0122, pSGAir01222Air, SingaporeCP025619.1 (83)
     A. baumannii A297 (RUH875), pA297-31Human urinary tract, NetherlandsKU744946 (46)
     A. johnsonnii XBB1, pXBB1-91Hospital sewage, USACP010351.1 (76)
     A. lwoffii ED45-23, pALWED2.11Permafrost, RussiaKX426229 (53)
     A. baumannii AbPK1, pAbPK1a1Ovine respiratory tract, PakistanCP024577 (84)
     Acinetobacter sp. strain DUT-2, unnamed 11Marine sediment, ChinaCP014652, unpublished
     Acinetobacter sp. strain BW3, pKLH2071Stream water, USAAJ486856 (85)
     A. towneri strain G165, pNDM-GJ011Human stool, ChinaKT965092 (86)
     A. baumannii D46, pD46-41Human urine, AustraliaMF399199 (52)
     Acinetobacter sp. strain ACNIH2, pACl-35691Hospital plumbing, USACP026416.1 (79)
     Acinetobacter sp. strain WCHA45, pNDM1_1000451Hospital sewage, ChinaCP028560.1, unpublished
     A. baumannii CHI-32, pNDM-321Human bloodstream, IndiaLN833432.1, unpublished
     A. defluvii WCHA30, pOXA58_0100301Hospital sewage, ChinaCP029396.1, unpublished
     A. pittii WCHAP005069, pOXA58_0050691Clinical isolate, ChinaCP026086.1, unpublished
     A. pittii WCHAP100004, pOXA58_1000041Clinical isolate, ChinaCP027249.1, unpublished
     A. pittii WCHAP005046, pOXA58_0050461Clinical isolate, ChinaCP028573.1, unpublished
     Acinetobacter sp. strain SWBY1, pSWBY11Hospital sewage, ChinaCP026617.1, unpublished
    • ↵a Strains where MITEAba12 is present on both chromosomal and plasmid DNA.

    • ↵b In A. baumannii MAD, MITEAba12 was found on a 7.8-kb stretch of sequenced DNA rather than a full-length chromosome (82).

  • TABLE 2

    IS with TIR closely related to those of ISAba12 and MITEAba12

    IS nameaIRL sequenceIRR sequenceLength (bp)TSD (bp)
    MITEAba12GGCTTTGTTGCACAAAGGCTTTGTTGCATAAA1139
    ISAba12GGCTTTGTTGCACAAAGGCTTTGTTGCACAAA1,0399
    IS17GGCTTTGTTGCACAAAGGCTTTGTTGCACAAA1,0409
    ISAba5bGGCTTTGTTGCACAAAGGCTTTGTTGCATAAA1,044ND
    ISAba7GGCTTTGTTGCATAAAGGCTTTGTTGCACAAA1,0399
    ISAba10GGCTTTGTTGCATAAATAGGCTTTGTTGCACAAATA1,0239
    ISAba13GGCTTTGTTGCACAAAGGCTTTGTTGCACAAA1,0399
    ISAba40GGCTTTGTTGCACAAAGGCTTTGTTGCACAAA1,0399
    ISAha1GGCTTTGTTGCACAAACGGCTTTGTTGCACAAAC1,0394
    ISAha2GGCTTTGTTGCACAAAGGCTTTGTTGCACAAA1,040ND
    ISAha3GGCTTTGTTGCACAAAGGCTTTGTTGCATAAA1,039ND
    ISAjo1GGCTTTGTTGCACAAAGGCTTTGTTGCATAAA1,0393
    ISAlw1GGCTTTGTTGCACAAAGGGCTTTGTTGCACAAAG1,038ND
    ISEcl7GGCTTTGTTGCACAAAGGCTTTGTTGCATAAA1,0529
    ISNov2GGCTTTGTTGCGCAAATGGCTTTGTTGCATAAAT1,0489
    • ↵a Abbreviations: IS, insertion sequence; IRL, inverted repeat left; IRR, inverted repeat right; TSD, target site duplication; ND, not determined.

    • ↵b The transposase of ISAba5 is thought to be inactive (28).

  • TABLE 3

    Strains and plasmids used in this study

    Strain or plasmidGenotype or descriptionaReference or source
    Strains
     A. baumannii
            ATCC 17978Noninternational type clone (wild type)ATCC (70)
            ΔqseBCATCC 17978 with Eryr insertion disruption in qseBCThis study
            ΔygiWATCC 17978 with Eryr insertion disruption in ygiWThis study
            ΔhnsATCC 17978 with hns disrupted by ISAba1227
            Δhns::ISAba12ATCC 17978 with hns disrupted by ISAba12This study
            ΔqseBC Δhns::ISAba12ΔqseBC with hns disrupted by ISAba12This study
            ΔygiW Δhns::ISAba12ΔygiW with hns disrupted by ISAba12This study
            ΔygiW Δhns::MITEAba12ΔygiW with hns disrupted by MITEAba12This study
            Δhns pWH0268Δhns with pWH026827
            Δhns::ISAba12 pWH0268Δhns::ISAba12 with pWH0268This study
            ΔqseBC Δhns::ISAba12 pWH0268ΔqseBC Δhns::ISAba12 with pWH0268This study
            ΔygiW Δhns::ISAba12 pWH0268ΔygiW Δhns::ISAba12 with pWH0268This study
            ΔygiW Δhns::MITEAba12 pWH0268ΔygiW Δhns::MITEAba12 with pWH0268This study
     E. coli
            DH5α λpirF– Φ80lacZΔM15 Δ(lacZYA-argF)U169 recA1 endA1 hsdR17(rK, mK+)
    phoA supE44 λ– thi-1 gyrA96 relA1 λpir,
    conjugative strain which can host λ-pir-dependent plasmids
    87
    Plasmids
        pAT04Tetr; pMMB67EH with RecAb system71
        pGEM-T EasyAmpr; T-overhang cloning vectorPromega
        pVA891Cmlr Eryr; Source of Eryr cassette88
        pWH0268Ampr; pWH1266 with hns cloned via BamHI restriction site27
    • ↵a Abbreviations: Amp, ampicillin; Cml, chloramphenicol; Ery, erythromycin; Tet, tetracycline.

  • TABLE 4

    Primers used in this study

    Primer function and nameSequencea (5′–3′)Reference or source
    Cloning and sequencing of hns genes
    with integrated mobile genetic elements
     hns_FGAGACATATGATGCATCATCATCATCATCATATAAATATTAAGAAAATATATTA27
     hns_RTCTCGGATCCTTAGATTAAGAAATCTTCAAG27
        M13 FGTAAAACGACGGCCAGPromega
        M13 RCAGGAAACAGCTATGACPromega
    Identification of presence of IS
        ACX60_04650_FCGTATTTGGGTCTTGGGGAAThis study
        ACX60_04650_RCCTTTGGTAAGTACTTTATThis study
        ACX60_18935_FAGCAACTGAAGCTGAAATTCG27
        ACX60_18935_RTTGGTTCCGAATTAGACTTGC27
        ACX60_04795_FCAGTCAGGTTCGCCATThis study
        ACX60_04795_RGACCAGACAATACAATGThis study
    Construction of ΔqseBC and ΔygiW
        ΔqseBC
        ΔqseBC_UFR_FCAATTCCGCGATAAGAGCThis study
        ΔqseBC_UFR_RCTATCAACACACTCTTAAGCCTGTTATATCCTGATThis study
        ΔqseBC_DFR_FCGGGAGGAAATAATTCTATTTGCAGTCACAACTGGThis study
        ΔqseBC_DFR_RGTAGTAACCAGAACAGCACThis study
        ΔqseBC_NOL_FGGCAAGGACGTCCTGTTTThis study
        ΔqseBC_NOL_RGGGCTGAAAAACTTCAACThis study
        ΔqseBC_Ery_FCTTAAGAGTGTGTTGATAG39
        ΔqseBC_Ery_RATAGAATTATTTCCTCCCG39
        ΔygiW
        ΔygiW_UFR_FCAGTTGAAATGGCATCCATTACThis study
        ΔygiW_UFR_RCTCTTAAGGTATAGGAACTTCAAAATTACCCTCTGTTAThis study
        ΔygiW_DFR_FGAGGAAATAAGAAGTTCCTATACTAAATTAATTTCTACATTTATTCCThis study
        ΔygiW_DFR_RGAGAGCGGCCGCCTCATTTTAAGTCTCCCATACThis study
        ΔygiW_NOL_FCGGCATTTATGAGTTTATGCCAGThis study
        ΔygiW_NOL_RGGCTTGCCCCAACTGAThis study
        ΔygiW_Ery FGAAGTTCCTATACCTTAAGAGTGTGTTGATAGThis study
        ΔygiW_Ery RGTATAGGAACTTCTTATTTCCTCCCGTTAAATAATAGATAACThis study
    • ↵a Nucleotides in boldface represent incorporated restriction sites: NdeI, CATATG; BamHI, GGATCC; NotI, GCGGCCGC.

Supplemental Material

  • Figures
  • Tables
  • FIG S1

    Motility of A. baumannii ATCC 17978 variants and complemented derivatives. Cells grown overnight were used as the inoculum for motility assays on LB medium containing 0.25% agar. WT ATCC 17978, ΔqseBC, and ΔygiW cells displayed a nonmotile phenotype. Derivatives of these strains with an hns gene interrupted by ISAba12 or MITEAba12 and Δhns (27) displayed a hypermotile phenotype, dispersing from the original inoculum site to cover the entire plate surface. Reintroduction of a WT copy of hns on the shuttle vector pWH1266 (pWH0268) returned strains to the parental nonmotile phenotype. Images are a representative example of results obtained. Download FIG S1, TIF file, 1.9 MB.

    Copyright © 2019 Adams and Brown.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S1

    List of MITEAba12 elements and their corresponding strain names that formulate MITEAba12 subgroups 1 to 10. Download Table S1, DOCX file, 0.01 MB.

    Copyright © 2019 Adams and Brown.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    Putative σ70 promoter sequences identified in MITEAba12(c). The σ70 promoter sequences were predicted using the Softberry BPROM tool. (A) Pink and blue nucleotide sequences represent outward-facing promoters, reading out through the IRL and IRR sequences (Pout IRL and Pout IRR, respectively), and the orientation of transcription is shown by arrows. Nucleotides underlined and double underlined denote −10 box and −35 box sequences, respectively. Purple nucleotides denote IRL and IRR, with putative translational start codons in boldface with their corresponding putative ribosome binding sites (RBS) shaded in pink and blue, respectively. (B) Alignment of the putative Pout IRL and Pout IRR and RBSs in MITEAba12(c) against the E. coli σ70 promoter and RBS consensus and Pout of ISAba1 coupled with the adjacent region and RBS in the ISAba1-activated blaampC gene of A. baumannii CLA-1 (38). The nucleotide length between the −10 and −35 boxes [Sep. (bp)] is indicated. Download FIG S2, TIF file, 1.5 MB.

    Copyright © 2019 Adams and Brown.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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MITEAba12, a Novel Mobile Miniature Inverted-Repeat Transposable Element Identified in Acinetobacter baumannii ATCC 17978 and Its Prevalence across the Moraxellaceae Family
Felise G. Adams, Melissa H. Brown
mSphere Feb 2019, 4 (1) e00028-19; DOI: 10.1128/mSphereDirect.00028-19

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MITEAba12, a Novel Mobile Miniature Inverted-Repeat Transposable Element Identified in Acinetobacter baumannii ATCC 17978 and Its Prevalence across the Moraxellaceae Family
Felise G. Adams, Melissa H. Brown
mSphere Feb 2019, 4 (1) e00028-19; DOI: 10.1128/mSphereDirect.00028-19
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    • ABSTRACT
    • INTRODUCTION
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KEYWORDS

Acinetobacter
genetic evolution
insertion sequences
nonautonomous elements
transposons

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