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Public Health Microbiology

Prevalence and Genetic Diversity of Bartonella Species Isolated from Wild Rodents in Japan

Kai Inoue, Soichi Maruyama, Hidenori Kabeya, Naoyuki Yamada, Norio Ohashi, Yukita Sato, Masayoshi Yukawa, Toshiyuki Masuzawa, Fumihiko Kawamori, Teruki Kadosaka, Nobuhiro Takada, Hiromi Fujita, Hiroki Kawabata
Kai Inoue
1Laboratory of Veterinary Public Health, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan
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Soichi Maruyama
1Laboratory of Veterinary Public Health, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan
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  • For correspondence: maruyama.soichi@nihon-u.ac.jp
Hidenori Kabeya
1Laboratory of Veterinary Public Health, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan
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Naoyuki Yamada
1Laboratory of Veterinary Public Health, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan
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Norio Ohashi
2Laboratory of Environmental Microbiology, Institute for Environmental Sciences, University of Shizuoka and Global COE Program, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
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Yukita Sato
3Laboratory of Biomedical Science, Department of Veterinary Medicine College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan
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Masayoshi Yukawa
3Laboratory of Biomedical Science, Department of Veterinary Medicine College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan
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Toshiyuki Masuzawa
4Laboratory of Microbiology and Immunology, Faculty of Pharmaceutical Sciences, Chiba Institute of Science, Shiomi 3, Choshi, Chiba 288-0025, Japan
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Fumihiko Kawamori
5Shizuoka Institute of Environment and Hygiene, 4-27-2, Kita-ando, Shizuoka 420-8637, Japan
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Teruki Kadosaka
6Department of Parasitology, Aichi Medical University, Aichi 480-1195, Japan
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Nobuhiro Takada
7Department of Pathological Sciences, Faculty of Medical Sciences, University of Fukui, Fukui 910-1193, Japan
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Hiromi Fujita
8Ohara Research Laboratory, Ohara General Hospital, Fukushima 960-0195, Japan
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Hiroki Kawabata
9Department of Bacteriology, National Institute of Infectious Diseases, Toyama 1-23-1, Shinjuku-ku, Tokyo 162-8640, Japan
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DOI: 10.1128/AEM.00071-08
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    FIG. 1.

    Geographical representation of the locations where wild rodents were captured. Cities, areas, or islands and their prefectures (e.g., Yokohama [city], Kanagawa [Prefecture]) are shown around the map of Japan in the figure. The numbers of rodents captured are indicated in parentheses.

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    FIG. 2.

    Phylogenetic classification of Japanese Bartonella isolates based on sequences of rpoB (left) and gltA (right). The phylogenetic tree was constructed by the neighbor-joining method, and bootstrap values were obtained with 1,000 replicates. Only bootstrap replicates of >70% are noted. The 31 and 29 different sequences of rpoB and gltA, respectively, from Japanese Bartonella isolates were classified into eight clusters, A to H for rpoB and I to P for gltA. Based on the correlation between respective clusters in rpoB and gltA, combinations of clusters such as A-I, B-J, C-K, D-L, E-M, F-N, G-O, and H-P were assigned as Bartonella genetic groups. The numbers of Bartonella isolates with identical DNA sequences are shown in parentheses at the right and left of the respective GenBank accession numbers for the rpoB and gltA sequences, respectively. The rodent species associated with the respective Bartonella genetic groups are shown between the two trees. The rpoB and gltA sequences from Brucella melitensis 16 MT were used as an outgroup bacterium.

Tables

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  • TABLE 1.

    Prevalence of Japanese Bartonella organisms in wild rodents

    EnvironmentPrefectureAreaNo. of bartonella-infected rodents/no. of rodents examined (isolation rate [%])
    A. speciosusA. argenteusC. rufocanus subsp. bedfordiaeM. caroliR. rattusR. norvegicusSubtotalTotal
    SuburbanHokkaidoSapporo29/31 (93.5)3/5 (60.0)4/17 (23.5)36/53 (67.9)
    AomoriTsugaru11/17 (64.7)1/2 (50.0)12/19 (63.2)
    GunmaMinakami26/43 (60.5)3/5 (60.0)29/48 (60.4)
    KanagawaFujisawa1/1 (100)3/3 (100)4/4 (100)
    ShizuokaMt. Fuji13/21 (61.9)8/17 (47.1)21/38 (55.3)
    IshikawaMt. Haku2/7 (28.6)2/7 (28.6)
    NaganoKaruizawa16/20 (80.0)1/1 (100)17/21 (81.0)
    ShimaneMatsue8/40 (20.0)0/2 (0.0)0/1 (0.0)8/43 (18.6)
    TokushimaHiwasa2/6 (33.3)2/6 (33.3)
    EhimeMatsuyama5/6 (83.3)5/6 (83.3)
    KagoshimaNakanoshima Island22/30 (73.3)2/4 (50.0)24/34 (70.6)
    KagoshimaYoroshima Island10/17 (58.8)10/17 (58.8)
    KagoshimaTokunoshima Island4/12 (33.3)4/12 (33.3)
    OkinawaMain Island0/7 (0.0)2/6 (33.3)0/19 (0.0)2/32 (6.3)176/340 (51.8)
    CityKanagawaYokohama0/255 (0.0)0/84 (0.0)0/339 (0.0)
    ShizuokaShimoda0/2 (0.0)0/3 (0.0)0/1 (0.0)0/6 (0.0)0/345 (0.0)
    Total135/224 (60.3)19/35 (54.3)4/17 (23.5)0/7 (0.0)18/297 (6.1)0/105 (0.0)176/685 (25.7)
  • TABLE 2.

    Closest relatives of Japanese Bartonella isolates and relationships between organisms and their host species based on sequence analysis of rpoB and gltA

    Genetic groupClosest relativea% similarities to rpoB and gltANo. of isolates
    A. speciosusA. argenteusC. rufocanus subsp. bedfordiaeR. rattusTotal
    A-I B. grahamii 94.7-97.3, 96.8-98.41161300129
    B-J B. tribocorum 95.0-96.4, 93.6-96.542028
    B. elizabethae 93.8-94.4, 92.6-94.2
    C-K B. tribocorum 95.9, 92.6-92.900044
    B. rattimassiliensis 91.2, 96.2-96.5
    D-L B. rattimassiliensis 98.3, 97.1-97.400033
    E-MNA51006
    F-N B. phoceensis 100, 1000001111
    G-O B. taylorii 97.1-98.1, 94.1-97.020406
    H-PNA1330016
    Total14019420183
    • ↵ a NA, not applicable.

  • TABLE 3.

    Dual infection with two different Bartonella genetic groups in wild rodents

    Rodent no.PrefectureAreaRodent speciesDetails of dual infection
    Genetic groupClosest relative(s)GenBank accession no. for identical rpoB and gltA sequencesGenetic groupClosest relative(s)aGenBank accession no. for identical rpoB and gltA sequences
    1AomoriTsugaru A. speciosus A-I B. grahamii AB259944 , AB242284E-MNA AB259953 , AB259956
    2AomoriTsugaru A. speciosus A-I B. grahamii AB259946 , AB242284B-J B. tribocorum, B. elizabethae AB242279 , AB261693
    3ShimaneMatsue A. speciosus A-I B. grahamii AB242283 , AB242284E-MNA AB259952 , AB242287
    4KagoshimaNakanoshima A. speciosus A-I B. grahamii AB259949 , AB259955H-PNA AB290273 , AB290295
    5KagoshimaNakanoshima A. speciosus A-I B. grahamii AB259949 , AB259955H-PNA AB290273 , AB290296
    6KagoshimaYoroshima R. rattus B-J B. tribocorum, B. elizabethae AB290270 , AB290281F-N B. phoceensis AB290278 , AB290292
    7OkinawaMain Island R. rattus B-J B. tribocorum, B. elizabethae AB290266 , AB290280D-L B. rattimassiliensis AB290272 , AB290283
    • ↵ a NA, not applicable.

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Prevalence and Genetic Diversity of Bartonella Species Isolated from Wild Rodents in Japan
Kai Inoue, Soichi Maruyama, Hidenori Kabeya, Naoyuki Yamada, Norio Ohashi, Yukita Sato, Masayoshi Yukawa, Toshiyuki Masuzawa, Fumihiko Kawamori, Teruki Kadosaka, Nobuhiro Takada, Hiromi Fujita, Hiroki Kawabata
Applied and Environmental Microbiology Aug 2008, 74 (16) 5086-5092; DOI: 10.1128/AEM.00071-08

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Prevalence and Genetic Diversity of Bartonella Species Isolated from Wild Rodents in Japan
Kai Inoue, Soichi Maruyama, Hidenori Kabeya, Naoyuki Yamada, Norio Ohashi, Yukita Sato, Masayoshi Yukawa, Toshiyuki Masuzawa, Fumihiko Kawamori, Teruki Kadosaka, Nobuhiro Takada, Hiromi Fujita, Hiroki Kawabata
Applied and Environmental Microbiology Aug 2008, 74 (16) 5086-5092; DOI: 10.1128/AEM.00071-08
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KEYWORDS

Bartonella
Bartonella Infections
Disease Reservoirs
Genetic Variation
Rodent Diseases

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