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Microbial Ecology

Gut Symbiotic Bacteria of the Genus Burkholderia in the Broad-Headed Bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae)

Yoshitomo Kikuchi, Xian-Ying Meng, Takema Fukatsu
Yoshitomo Kikuchi
Natural History Laboratory, Faculty of Science, Ibaraki University, Mito 310-8512Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan
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  • For correspondence: yoshitomo.kikuchi@uconn.edu
Xian-Ying Meng
Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan
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Takema Fukatsu
Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan
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DOI: 10.1128/AEM.71.7.4035-4043.2005
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  • FIG. 1.
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    FIG. 1.

    Midgut organization of R. clavatus and L. chinensis. (A) Dissected midgut of R. clavatus. (B) Dissected midgut of L. chinensis. (C) Tissue section of midgut crypts of R. clavatus, stained with hematoxylin and eosin. (D) Fluorescent in situ hybridization of a tissue section of midgut crypts of R. clavatus, targeting 16S rRNA of the Burkholderia symbiont. Green signals are due to the Burkholderia-specific probe Cy3-Alsym16S. Blue signals are nuclei of the host cells visualized by DAPI. The arrows indicate the Burkholderia signals in the main tract of the midgut and signals in the ducts connecting the crypts with the main tract. (A) Bar = 0.5 mm. (B) Bar = 0.2 mm. (C and D) Bars = 100 μm. Abbreviations: C, crypt: G, gut; M1, first midgut section; M2, second midgut section; M3, third midgut section; M4, fourth midgut section (symbiotic organ); H, hindgut.

  • FIG. 2.
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    FIG. 2.

    Phylogenetic relationship of the Burkholderia symbionts from R. clavatus and L. chinensis on the basis of 16S rRNA gene sequences. (A) Neighbor-joining tree. (B) Maximum-parsimony tree based on 50% majority-rule consensus. Pandoraea spp. were used as outgroup taxa for the genus Burkholderia. Bootstrap values greater than 50% are shown at the nodes. The numbers in brackets are nucleotide sequence accession numbers.

  • FIG. 3.
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    FIG. 3.

    Transmission electron microscopy of the midgut crypts of R. clavatus and L. chinensis. (A) Crypt of R. clavatus harboring many rod-shaped bacteria. Bar = 2 μm. (B) Enlarged image of the interface between the lumen and the epithelium of the crypt in R. clavatus. The bacteria are present only in the lumen. Bar = 1 μm. (C) Enlarged image of the rod-shaped bacteria in R. clavatus. A well-developed cell wall and a particle-like structure are present. Bar = 300 nm. (D) Crypt of L. chinensis harboring many rod-shaped bacteria. Bar = 2 μm. Abbreviations: B, symbiotic bacterium; M, mitochondrion; N, nucleus.

Tables

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  • TABLE 1.

    Alydid stinkbug samples used in this study

    SpeciesSampleLocalityCollection dateCollector
    Riptortus clavatusaIB1Mito, Ibaraki30 June 2001Y. Kikuchi
    IB2Tomobe, Ibaraki22 August 2002M. Ishizaki
    IB3Tsukuba, ibaraki5 May 2001Y. Kikuchi
    GNNumata, Gunma15 July 2003Y. Kikuchi
    NGJoetsu, Nigata6 October 2003c,dH. Higuchi
    KYKyoto, Kyoto29 September 2003dC. Himuro
    NRNara, Nara16 October 2003dC. Himuro
    KCNakamura, Kochi26 September 2003M. Takai
    SGKanzaki, Saga7 May 2002T. Kashima
    KMKikuchi, Kumamoto3 October 2003dY. Kikuchi
    OKIshigaki, Okinawa25 July 2002K. Kohno
    Leptocorisa chinensisaFKHanawa, Fukushima14 August 2002Y. Kikuchi
    IB1Mito, Ibaraki29 August 2002Y. Kikuchi
    IB2Tsukuba, Ibaraki10 August 2002dY. Kikuchi
    10 October 2003cY. Kikuchi
    GNKiryu, Gunma18 November 2003E. Hara
    CBMaruyama, Chiba8 September 2002Y. Kikuchi
    KYKyoto, Kyoto29 September 2003dC. Himuro
    NRNara, Nara16 October 2003dC. Himuro
    SGSaga, Saga3 June 2002T. Kashima
    KMKikuchi, Kumamoto3 October 2003dY. Kikuchi
    Riptortus linearisbNaha, Okinawa20 June 2002T. Fukatsu
    Leptocorisa acutabIriomote, Okinawa26 May 2004T. Yasuda
    Leptocorisa oratoriabIriomote, Okinawa26 May 2004T. Yasuda
    Megalotomus costalisbSapporo, Hokkaido26 August 2002K. Ito
    Daclera levanabIshigaki, Okinawa23 July 2002K. Kohno
    Paraplesius unicolorbMonobe, Kochi27 July 2002M. Takai
    • ↵a One individual from each population was subjected to cloning and sequencing.

    • ↵b One individual was subjected to diagnostic PCR analysis.

    • ↵c Subjected to diagnostic PCR analysis to examine the localization in a body.

    • ↵d Subjected to diagnostic PCR analysis to survey the infection rate in a natural population.

  • TABLE 2.

    Levels of similarity for the Burkholderia symbionts detected in local samples of R. clavatus and L. chinensis and other Burkholderia strains based on 16S rRNA gene sequencesa

    SampleR. clavatusL. chinensisBurkholderia sp.B. kurkiiB. glatheiB. sordidicolaB. capaciaB. graminis
    IB1IB2IB3GNKYNRKCSGKMOK type 1OK type 2FKIB1IB2GNCBKYNRSGKM type 1KM type 2S4.9AK-5WD206NF100
    R. clavatus
        IB110.980.9830.9740.980.9780.9770.9740.9840.9710.9690.9910.9810.9780.9920.9830.9830.9830.980.9850.9830.9780.9790.9810.9960.9720.9710.9720.9680.954
        IB210.9740.9810.9850.9830.9910.9760.9820.9820.9770.980.9730.9810.980.9770.9740.9740.9760.9740.9770.9830.9740.9730.9810.9690.9690.9650.9590.957
        IB310.9820.980.9830.9770.9850.9910.9740.9770.9870.9980.9830.9880.98810.9920.9770.9910.9870.9840.9920.9980.9850.9690.9740.9710.9610.952
        GN10.9860.9910.9820.9850.9880.9860.9880.9820.9810.9890.9810.9830.9820.9870.980.9870.9890.9910.9880.980.9790.9760.9740.9610.9580.953
        KY10.9930.990.980.9850.9850.9790.9810.9790.9940.980.980.980.980.9760.980.9830.9950.980.9770.9840.9760.9790.9680.9620.96
        NR10.9860.9830.9890.9860.9820.9850.9830.9960.9850.9830.9830.9840.9790.9840.9860.9990.9840.9810.9830.9730.9740.9650.960.959
        KC10.9760.9810.9860.9770.9760.9740.9860.9770.9760.9770.9740.9710.9740.9760.9870.9740.9750.9770.9710.9710.9610.9560.957
        SG10.9830.9830.9910.9830.9840.9820.9830.990.9850.9890.9910.9890.9850.9830.9890.9820.9790.9730.9710.9630.9590.958
        KM10.980.980.9880.9890.9880.9880.9870.9910.9880.9760.9910.9940.990.9880.9880.9860.9740.9770.9670.9650.953
        OK type 110.9850.9760.9730.9880.9750.9770.9740.9810.9790.9810.9830.9880.9780.9730.9710.9710.9660.9550.9490.953
        OK type 210.9780.9770.980.9770.9830.9770.9820.9870.9820.9830.9830.9820.9760.9740.9730.970.9590.9550.957
    L. chinensis
        FK10.9860.9840.9990.990.9870.9870.9880.9880.9860.9850.9870.9850.9960.9660.9720.9720.9670.955
        IB110.9820.9870.9880.9980.9910.9760.990.9860.9830.9910.9960.9840.6680.9730.9710.960.949
        IB210.9830.9830.9830.9850.9770.9850.9870.9980.9830.980.9810.9730.9740.9630.9590.956
        GN10.9910.9880.9860.9880.9880.9850.9850.9860.9850.9950.9670.9710.9710.9660.955
        CB10.9880.990.9850.9910.9870.9840.990.9860.9850.9710.970.9660.9650.952
        KY10.9920.9770.9910.9870.9840.9920.9980.9850.9690.9740.9710.9610.952
        NR10.9810.9970.9930.9850.9970.990.9840.9740.9740.9660.960.95
        SG10.9810.9790.9790.9810.9740.9840.9670.9650.9660.9590.956
        KM type 110.9960.9850.9940.9880.9870.9750.9730.9650.9630.95
        KM type 210.9870.9910.9850.9850.9770.9750.9650.9640.951
    Burkholderia sp.
        S4.910.9850.9820.9830.9740.9750.9650.9610.959
        AK-510.990.9840.9720.9740.9660.9610.951
        WD20610.9820.9670.9710.9690.9580.949
        NF10010.9710.9750.9760.9710.957
    B. kirkii10.9680.9550.9590.952
    B. glathei10.9720.960.956
    B. sordidicola10.9670.952
    B. cepacia10.948
    B. graminis1
    • a The levels of similarity were calculated by using Kimura's two-parameter model.

  • TABLE 3.

    Diagnostic PCR detection of the Burkholderia symbionts in the tissues of R. clavatus and L. chinensis

    SpeciesSexNo. positivea
    ForelegProboscisForegutMidgut section 1Midgut sections 2 and 3Midgut section 4 (crypts)HindgutTestis or ovary
    R. clavatusMale000021041
    Female000221010
    L. chinensisMale000001000
    Female001011010
    • ↵a Ten individuals were examined for each species and each sex.

  • TABLE 4.

    Detection of the Burkholderia symbionts in midgut crypts in natural populations of R. clavatus and L. chinensis

    SpeciesSample% Detection (no. positive/total no.)
    R. clavatusNG100 (26/26)
    KY100 (11/11)
    NR100 (10/10)
    KM95 (40/42)
    Total98 (87/89)
    L. chinensisIB297 (70/72)
    KY100 (12/12)
    NR100 (11/11)
    KM100 (21/21)
    Total98 (114/116)
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Gut Symbiotic Bacteria of the Genus Burkholderia in the Broad-Headed Bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae)
Yoshitomo Kikuchi, Xian-Ying Meng, Takema Fukatsu
Applied and Environmental Microbiology Jul 2005, 71 (7) 4035-4043; DOI: 10.1128/AEM.71.7.4035-4043.2005

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Gut Symbiotic Bacteria of the Genus Burkholderia in the Broad-Headed Bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae)
Yoshitomo Kikuchi, Xian-Ying Meng, Takema Fukatsu
Applied and Environmental Microbiology Jul 2005, 71 (7) 4035-4043; DOI: 10.1128/AEM.71.7.4035-4043.2005
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