Isolation of Bartonella species from rodents in Taiwan including a strain closely related to 'Bartonella rochalimae' from Rattus norvegicus.
ABSTRACT An increasing number of Bartonella species originally isolated from small mammals have been identified as emerging human pathogens. During an investigation of Bartonella infection in rodent populations carried out in Taiwan in 2006, a total of 58 rodents were tested. It was determined that 10.3 % (6/58) of the animals were Bartonella bacteraemic. After PCR/RFLP analysis, four isolates were identified as Bartonella elizabethae and one isolate as Bartonella tribocorum. However, there was one specific isolate with an unrecognized PCR/RFLP pattern. After further sequence and phylogenetic analyses of the gltA, ftsZ and rpoB genes, and the 16S-23S rRNA intergenic spacer region, the results indicated that this specific isolate from Rattus norvegicus was closely related to human pathogenic 'Bartonella rochalimae'. Further studies need to be conducted to evaluate whether this rodent species could be a reservoir for 'B. rochalimae'.
- SourceAvailable from: ncbi.nlm.nih.gov[show abstract] [hide abstract]
ABSTRACT: Identification of Bartonella species is of increasing importance as the number of infections in which these bacteria are involved increases. To date, these gram-negative bacilli have been identified by various serological, biochemical, and genotypic methods. However, the development of alternative tools is required, principally to circumvent a major risk of contamination during sample manipulation. The aim of our study was to investigate the possible identification of various Bartonella species by comparison of RNA polymerase beta-subunit gene (rpoB) sequences. This approach has previously been shown to be useful for the identification of members of the family Enterobacteriaceae (C. M. Mollet, M. Drancourt, and D. Raoult, Mol. Microbiol. 26:1005-1011, 1997). Following PCR amplification with specific oligonucleotides, a 825-bp region of the rpoB gene was sequenced from 13 distinct Bartonella strains. Analysis of these sequences allowed selection of three restriction enzymes (ApoI, AluI, and AflIII) useful for discerning the different strains by PCR-restriction fragment length polymorphism (PCR-RFLP) analysis. To confirm the potential value of such an approach for identification of Bartonella, the rpoB PCR was then applied to 94 clinical samples, and the results obtained were identical to those obtained by our reference PCR method. Twenty-four isolates were also adequately identified by PCR-RFLP analysis. In all cases, our results were in accordance with those of the reference method. Moreover, conserved regions of DNA were chosen as suitable primer targets for PCR amplification of a 439-bp fragment which can be easily sequenced.Journal of Clinical Microbiology 03/2001; 39(2):430-7. · 4.07 Impact Factor
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ABSTRACT: The most likely animal source of a human case of cardiac disease in Washoe County, Nev., was identified by comparison of DNA sequences of three genes (citrate synthase gltA, 60-kDa heat shock protein gene groEL, and 16S rRNA gene) of Bartonella washoensis cultured from the human patient in question and of Bartonella isolates obtained from the following Nevada rodents: Peromyscus maniculatus (17 isolates), Tamias minimus (11 isolates), Spermophilus lateralis (3 isolates), and Spermophilus beecheyi (7 isolates). Sequence analyses of gltA amplicons obtained from Bartonella from the rodents demonstrated considerable heterogeneity and resulted in the identification of 16 genetic variants that were clustered within three groups in phylogenetic analysis. Each of the three groups was associated with a rodent genus, Peromyscus, Tamias, or Spermophilus: The gltA, 16S rRNA gene, and groEL sequences of a Bartonella isolate obtained from a California ground squirrel (S. beecheyi) were completely identical to homologous sequences of B. washoensis, strongly suggesting that these animals were the source of infection in the human case.Journal of Clinical Microbiology 03/2003; 41(2):645-50. · 4.07 Impact Factor
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ABSTRACT: Currently, 19 species are recognized in the genus Bartonella, 7 of which are involved in an increasing variety of human diseases. Development of molecular tools for detection, identification, and subtyping of strains and isolates has promoted research on Bartonella spp. We amplified and sequenced the portion of the ftsZ gene encoding the N-terminal region of the cell division protein for 13 Bartonella species: Bartonella alsatica, B. birtlesii, B. doshiae, B. elizabethae, B. grahami, B. koehlerae, B. schoenbuchensis, B. taylorii, B. tribocorum, Bartonella vinsonii subsp. arupensis, Bartonella vinsonii subsp. berkhoffii, Bartonella vinsonii subsp. vinsonii, and B. bovis Bermond et al.("B. weissii"). Phylogenetically derived trees revealed four statistically supported groups, indicating that sequencing of the ftsZ gene is a useful tool for identifying evolutionary relationships among Bartonella species. Furthermore, we amplified and sequenced the portion of the ftsZ gene encoding the C-terminal region of the protein for 4 B. bacilliformis isolates, 14 B. clarridgeiae isolates, 14 B. quintana isolates, and 30 B. henselae isolates that were obtained from different geographic regions, hosts, and clinical specimens. B. clarridgeiae and B. quintana sequences were highly conserved, while those of the four B. bacilliformis isolates differed from the type strain at 5 positions. Among B. henselae strains isolated from cats and patients, only two genotypes were detected: Houston and Marseille. Among 80 clinical samples we detected Bartonella spp. in 35 (43.75%) and found the assay to be comparable to that of a combined intergenic-spacer-region- and pap31-based PCR assay. Our results show the usefulness of the portion of the ftsZ gene encoding the C-terminal region for diagnosis of Bartonella infections. More samples should be tested to study its usefulness for epidemiological investigations.Journal of Clinical Microbiology 11/2002; 40(10):3641-7. · 4.07 Impact Factor
Isolation of Bartonella species from rodents in
Taiwan including a strain closely related to
‘Bartonella rochalimae’ from Rattus norvegicus
Jen-Wei Lin,1Chun-Yu Chen,2Wan-Ching Chen,3Bruno B. Chomel4
and Chao-Chin Chang2
1Department of Veterinary Medicine, College of Veterinary Medicine, National Chung Hsing
University, Taichung 402, Taiwan
2Graduate Institute of Veterinary Public Health, National Chung Hsing University, Taichung 402,
3Department of Safety Health and Environmental Engineering, Central Taiwan University of Science
and Technology, Taichung 406, Taiwan
4Department of Population Health and Reproduction, School of Veterinary Medicine, University of
California, Davis, CA, USA
Received 2 July 2008
Accepted 20 August 2008
An increasing number of Bartonella species originally isolated from small mammals have been
identified as emerging human pathogens. During an investigation of Bartonella infection in rodent
populations carried out in Taiwan in 2006, a total of 58 rodents were tested. It was determined
that 10.3% (6/58) of the animals were Bartonella bacteraemic. After PCR/RFLP analysis, four
isolates were identified as Bartonella elizabethae and one isolate as Bartonella tribocorum.
However, there was one specific isolate with an unrecognized PCR/RFLP pattern. After further
sequence and phylogenetic analyses of the gltA, ftsZ and rpoB genes, and the 16S–23S rRNA
intergenic spacer region, the results indicated that this specific isolate from Rattus norvegicus
was closely related to human pathogenic ‘Bartonella rochalimae’. Further studies need to be
conducted to evaluate whether this rodent species could be a reservoir for ‘B. rochalimae’.
Bartonella species are short rod, fastidious, Gram-negative
and oxidase-negative bacteria (Boulouis et al., 2005;
Breitschwerdt & Kordick, 2000). Since the early 1990s, more
than 20 species within the genus Bartonella have been
recognized (Eremeeva et al., 2007; Zeaiter et al., 2002). These
intracellular bacteria are regarded as emerging zoonotic
pathogens, which can cause serious diseases in humans
worldwide (Boulouis et al., 2005). A new species, ‘Bartonella
rochalimae’, was recently isolated from a case of splenomeg-
aly in a patient who had travelled to South America
(Eremeeva et al., 2007). This event raised the concern that
it could be a newly emerged zoonotic pathogen. However, to
date, little is known regarding to the reservoirs and vectors
for the transmission of ‘B. rochalimae’.
Small mammals are natural hosts for several Bartonella
species, some of which can cause human diseases (Boulouis
et al., 2005; Zeaiter et al., 2002). The order Rodentia has
been reported as the reservoir for several Bartonella species
(Ellis et al., 1999) that are pathogens for humans, such as
Bartonella elizabethae reported in a case of endocarditis
(Daly et al., 1993). Bartonella grahamii, isolated primarily
from bank voles (Clethrionomys glareolus), was identified to
be the causative agent of neuroretinitis in humans (Baker,
1946; Kerkhoff et al., 1999). Although the main route of
transmission for rodent Bartonella species is still unclear,
these infections are likely to be vector-borne, mainly by fleas.
For instance, Ctenophthalmus nobilis, collected on bank voles
in the UK, was shown to be a competent vector for B.
al., 1993). In Kabul, Afghanistan, B. taylorii was also detected
by molecular methods in fleas collected from gerbils
(Meriones libycus), and B. elizabethae and Bartonella doshiae
were identified in rat fleas (Marie ´ et al., 2006). More recently,
Bartonella clarridgeiae-like bacteria were detected in rat fleas
(Xenopsylla cheopis) collected from brown rats (Rattus
norvegicus) from Egypt (Loftis et al., 2006). Similarly, when
studying Bartonella infection in flea vectors (Polygenis gwyni)
parasitizing cotton rats (Sigmodon hispidus), some samples
were co-infected with a strain phylogenetically related to B.
clarridgeiae (Abbot et al., 2007).
Abbreviation: ITS, intergenic spacer region.
The GenBank/EMBL/DDBJ accession numbers for the gltA, ftsZ and
rpoB genes and the 16S–23S rRNA ITS sequence of Bartonella 1-1C
strain are EU551154, EU551155, EU551156 and EU551157.
Journal of Medical Microbiology (2008), 57, 1496–1501
1496 2008/004671G2008 SGMPrinted in Great Britain
Our laboratory has been collaborating with the Center for
Disease Control, Taiwan, to conduct an epidemiological
survey of Bartonella species in small mammals in central
Taiwan. In this study, using molecular methods and
sequencing various genes for the obtained isolates, our
aim was to determine if a ‘B. rochalimae’-like organism
could be isolated from rodents and the prevalence of
Bartonella infection in rodents in Taiwan.
Sample collection. Between March and October 2006, a total of 58
rodents (53 R. norvegicus, 2 Mus musculus and 3 Rattus rattus) were
captured in Taichung, a city located in central Taiwan. After being
humanely anaesthetized with zoletil 50 (Virbac Laboratories), the
animals were bled to death via cardiac puncture by using 3 ml
syringes fitted with 22 gauge, 3.8 cm needles. The blood was then
collected in a tube containing 10 ml (1.5 mg ml21) EDTA, and was
stored at 280 uC for isolation and molecular identification of
Blood culture for Bartonella species. For bacterial culture, 200 ml
thawed whole blood sample was plated onto both fresh 10% sheep
blood-enriched Columbia agar and chocolate agar. The plates were
incubated at 35 uC in 5% CO2for at least 1 month and checked for
growth of Bartonella species on a weekly basis (Boulouis et al., 2005).
The suspected colonies were subcultured onto a fresh agar plate for
further molecular identification of Bartonella species by PCR/RFLP
and sequence analyses.
DNA extraction and PCR/RFLP procedures for Bartonella
species. After culturing a single colony pick from the original plate,
DNA of the cultured isolates was extracted using a Viogene DNA/
RNA extraction kit (Viogene Biotek) following the manufacturer’s
instructions. The primers used for DNA amplification and sequencing
in this study are shown in Table 1. The primers BhCS.781p and
BhCS.1137n were used first for amplifying a partial fragment, ranging
from 380 to 400 bp, of the gltA gene of Bartonella species. PCR
mixtures were set up as follows: 5 ml DNA template, 0.5 ml 100 mM
each primer, 4 ml 2.5 mM dNTPs, 5 ml 106 PCR buffer, 3 ml 25 mM
MgCl2, 31.75 ml sterile distilled H2O and 0.25 ml DNA polymerase
(AmpliTaq Gold; Applied Biosystems). The PCR amplification was
executed as follows: 1 cycle of 10 min at 95 uC, followed by 45 cycles
of 30 s at 95 uC, 1 min at 57 uC and 2 min at 72 uC, and then 1 cycle
of 5 min at 72 uC for final extension (Norman et al., 1995). Primers
bartsppA and bartsppB amplified a fragment of the 16S–23S rRNA
intergenic spacer region (ITS) by single-step PCR (Jensen et al., 2000);
the different molecular size of the PCR products allowed for quick
differentiation of various Bartonella species. The PCR program for the
ITS was as follows: 1 cycle of 2 min at 95 uC, followed by 45 cycles of
1 min at 95 uC, 1 min at 52 uC and 30 s at 72 uC, and 1 cycle of
10 min at 72 uC for complete extension (Jensen et al., 2000). The
primers for the amplification of the ftsZ gene were Bfp1 and Bfp2. A
900 bp fragment was expected from the amplification. The PCR
program consisted of: 1 cycle of 4 min at 94 uC, followed by 44 cycles
of 30 s at 94 uC, 30 s at 55 uC and 1 min at 68 uC, and then 1 cycle of
10 min at 68 uC for complete extension (Zeaiter et al., 2002). For
PCR amplification of the rpoB gene, a set of primers 1400F and 2300R
was used to amplify an expected 900 bp DNA fragment. The PCR was
performed as follows: 1 cycle of 2 min at 94 uC, 35 cycles of 30 s at
94 uC, 30 s at 53 uC and 1 min at 72 uC, and then 1 cycle of 2 min at
72 uC for complete extension (Renesto et al., 2001). RFLP of the gltA
gene was also used for quick identification of Bartonella organisms at
the species level with restriction enzyme digestion with TaqI (New
England BioLabs), HhaI (New England BioLabs) and MseI (New
England BioLabs) following the manufacturer’s instructions. The
RFLP banding patterns were then compared to the patterns of
Bartonella type strains, including Bartonella alsatica (IBS382T) CIP
105477, Bartonella birtlesii (IBS 325T) CIP 106294, Bartonella bovis
(91-4T) CIP 106692, B. clarridgeiae (Houston-2T) ATCC 51734, B.
doshiae (R18T) NCTC 12862, B. elizabethae (F9251T) ATCC 49927,
B. grahamii (V2T) NCTC 12860 b, Bartonella henselae (Houston-1T)
ATCC 49882, Bartonella koehlerae (C-29T) ATCC 700693, Bartonella
quintana (FullerT) ATCC VR-358, B. taylorii (M6T) NCTC 12861,
Bartonella tribocorum (IBS 506T) CIP 104576, Bartonella. vinsonii
subsp. arupensis (OK 94-513T) ATCC 700727, B. vinsonii subsp.
berkhoffii (93-CO1T) ATCC 51672, B. vinsonii subsp. vinsonii
(BakerT) ATCC VR-152.
Sequencing and phylogenetic analyses for Bartonella species.
The confirmed PCR products were sent for automated sequencing
using the primers listed in Table 1 (Mission Biotech). Sequences of
several Bartonella species were downloaded for comparison from
GenBank. The sequences of the gltA, ftsZ and rpoB genes, and the
16S–23S rRNA ITS, of the Bartonella strain (1-1C) isolated in this
study have been submitted to the GenBank. The accession numbers
are EU551154 for the gltA gene, EU551155 for the ftsZ gene,
EU551156 for the rpoB gene and EU551157 for the 16S–23S rRNA
ITS. Sequences were first aligned by the CLUSTAL W method of the
BioEdit program (Tom Hall, Ibis Biosciences, Isis Pharmaceuticals).
Phylogenetic analysis was performed on the aligned DNA sequences
using maximum-parsimony as implemented in PHYLIP version 3.6
(Joseph Felsenstein, Department
Department of Biology, University of Washington, Seattle, WA,
Table 1. Primers used for PCR amplification and sequencing
Primer setTarget genePrimer sequenceSize of PCR product (bp) Reference
380–400 Norman et al. (1995)
16S–23S rRNA ITS Molecular size dependent on
Jensen et al. (2000)
ftsZ900 Zeaiter et al. (2002)
rpoB900Renesto et al. (2001)
‘Bartonella rochalimae’ and Rattus norvegicus
Fig. 1. Phylogenetic analysis of different Bartonella species on the
basis of partial DNA sequences of: (a) the gltA gene, (b) the ftsZ
gene and (c) the rpoB gene. The phylogenetic relationship was
constructed by using the maximum-parsimony method of the PHYLIP
version 3.6 program, and bootstrap analysis was performed with
1000 trials of bootstrap data (bootstrap values not shown if lower
J.-W. Lin and others
1498 Journal of Medical Microbiology 57
USA). Bootstrap support was calculated by using 1000 bootstrap data
replicates as implemented by SEQBOOT of the PHYLIP program.
Using whole blood culture, 6 (10.3%) of the 58 animals
were Bartonella bacteraemic. Among the six bacteraemic
animals, five were R. norvegicus and one was R. rattus. After
PCR/RFLP analysis and pattern comparisons of Bartonella
type strains, it was determined that four of the five isolates
from R. norvegicus were B. elizabethae and the isolate from
R. rattus was B. tribocorum. However, there was one
specific isolate with an unrecognized PCR/RFLP pattern,
which was one undigested band (380 bp) by TaqI, two
bands (285 and 94 bp) by HhaI and two bands (199 and
132 bp) by MseI digestion. Therefore, this isolate was
further characterized by direct DNA sequencing for species
For this specific isolate, three randomly picked colonies
from the original plate were subcultured and harvested for
DNA extraction after 1 week. There was no gltA sequence
variation between the isolates, thus a single isolate
(designated 1-1C) was used for subsequent sequencing of
the other genes. The accession numbers of the Bartonella
reference strains used for comparison are shown in Table 2.
In comparison with partial sequences of the gltA gene of
Bartonella species in GenBank, the DNA similarity value of
this specific isolate was highest, 95.6% with ‘B. rochalimae’,
followed by B. clarridgeiae (95%), Bartonella schoenbu-
chensis (90.8%) and ‘Bartonella washoensis subsp. cynomy-
Table 2. Accession numbers of the reference Bartonella species sequences used for phylogenetic
analysis in this study
Bartonella strain Sequence accession no.
B. bovis isolate 23MI
B. bovis isolate N 05-1406N05
B. elizabethae strain F9251
B. grahamii strain V2
‘B. phoceensis’ strain 16120
B. quintana strain Fuller
‘B. rattimassiliensis’ strain 15908
‘B. rattimassiliensis’ strain16115
‘B. rochalimae’ isolate BMGH
‘B. rochalimae’ SM318006
B. schoenbuchii strain R6
B. tribocorum isolate IBS 506
B. vinsonii strain Baker
B. vinsonii subsp. arupensis
B. vinsonii subsp. berkhoffii
B. vinsonii subsp. vinsonii
B. washoensis subsp. cynomysii strain
‘Bartonella rochalimae’ and Rattus norvegicus
sii’ strain CL8606co (90.2%). DNA similarity was less than
90% to all other Bartonella species tested.
After sequence analysis of the ftsZ and rpoB genes, as well as
the 16S–23S rRNA ITS, the isolate 1-1C sequences were still
closest to ‘B. rochalimae’ (similarity values: 97.1, 97.1 and
96%, respectively). Similarly, phylogenetic analysis of the
gltA, ftsZ and rpoB genes strongly supported that isolate 1-
1C and ‘B. rochalimae’ belonged to the same clade, as
indicated by the high bootstrap value (.90%) on the basis
of 1000 replicates (Fig. 1). This clade also includes B.
clarridgeiae and is clearly separated from other Bartonella
species. When we further compared sequence relatedness
between the 1-1C strain and B. clarridgeiae, we found that
the similarity values were 94.3% for the ftsZ gene and
93.2% for the rpoB gene, and the similarity value for the
16S–23S rRNA ITS was only 69.1%.
‘B. rochalimae’ has recently been isolated from a human
infection (Eremeeva et al., 2007); however, the reservoir of
this new human pathogen remains unknown. We report
what is believed to be the first isolation of a Bartonella
strain closely related to ‘B. rochalimae’ from a brown rat
captured in central Taiwan. As the data are limited by the
small sample size of rats tested and the lack of a further
inoculation test in laboratory animals in this study, this
unique isolate does not allow confirmation of rats as a
possible reservoir of ‘B. rochalimae’. However, several
Bartonella species have been shown to use various species
of small mammals as their natural reservoirs (Baker, 1946;
Birtles et al., 1995; Brenner et al., 1993; Heller et al., 1998;
Kordick et al., 1996). Of major importance, several rodent
Bartonella species have been shown to be emerging
zoonotic pathogens. The first rodent-associated zoonotic
Bartonella species was B. elizabethae (Daly et al., 1993), and
R. norvegicus was considered to be its main reservoir (Ellis
et al., 1999). ‘B. washoensis’ and B. vinsonii subsp.
arupensis, which cause human myocarditis and neuro-
logical disorders, respectively, were also suggested to be
rodent associated (Kosoy et al., 2003; Welch et al., 1999).
The present study clearly showed that rodents in Taiwan
can harbour Bartonella species, including B. elizabethae, B.
tribocorum and a strain closely related to ‘B. rochalimae’.
B. clarridgeiae is considered to be an agent possibly causing
human cat-scratch disease, with cats being the natural
reservoir (Boulouis et al., 2005), and recently ‘B. rochalimae’,
the closest Bartonella species to B. clarridgeiae, was isolated
from a human patient (Eremeeva et al., 2007). In a study
conducted in northern California, researchers identified a
novel B. clarridgeiae-like bacterium from 3 dogs and 22 grey
foxes (Henn et al., 2007). These data raise concerns about the
existence of other reservoirs and vectors for this emerging
infection. For instance, a novel Bartonella species close but
distinct from B. clarridgeiae was identified in a striped field
mouse (Apodemus agrarius) and a yellow-necked field mouse
(Apodemus flavicollis) from Slovenia (Knap et al., 2007). B.
clarridgeiae-like bacteria were also detected in rat fleas (X.
cheopis) collected on brown rats (R. norvegicus) from Egypt
(Loftis et al., 2006) and from P. gwyni fleas parasitizing
cotton rats (S. hispidus) in the United States (Abbot et al.,
2007). Furthermore, according to a phylogenetic analysis of
Bartonella species detected in rodent fleas, a genotype
designated F15YN, most closely related to B. clarridgeiae,
was identified in a Ctenophthalmus lushuiensis flea in China
(Li et al., 2007). Because Taiwan is geographically located
close to mainland China, the sequence of the gltA gene of the
F15YN strain was further compared to the one of our 1-1C
strain. After sequence comparison, it showed that a 5%
divergence existed between these two strains. Unfortunately,
no sequences for other genes of the F15YN were available for
comparison. In this study, we determined that the 1-1C
strain was most closely related to ‘B. rochalimae’, on the basis
of more than 95% similarity values for the sequences of gltA,
ftsZ and rpoB genes, and the 16S–23S rRNA ITS region.
Although 95% similarity for the gltA gene was also observed
between the 1-1C strain and B. clarridgeiae, more divergence
was observed by the sequence comparisons of the ftsZ and
rpoB genes, as well as the 16S–23S rRNA ITS (similarity
values: 94.3, 93.2 and 69.1%, respectively). The partial
sequence of the 16S–23S rRNA ITS region was shown to be
useful to differentiate ‘B. rochalimae’ and B. clarridgeiae. As
the phylogenetic analysis showed a specific clade including
‘B. rochalimae’, B. clarridgeiae and the 1-1C strain, it will be
important to further determine the relationship and
biological differences of these B. clarridgeiae-like isolates in
the future. Although the mode of infection of humans from
vectors. Unfortunately, no ectoparasites were collected for
detection of Bartonella infection on the bacteraemic rats in
In conclusion, the most significant finding of this study is
the identification of a ‘B. rochalimae’-like organism from R.
norvegicus, on the basis of sequence and phylogenetic
analyses of gltA, ftsZ and rpoB genes. Due to the small
sample size of animals tested, this study cannot conclude
that R. norvegicus is the reservoir for ‘B. rochalimae’, but it
certainly warrants further investigation.
This project was supported by grants DOH 95-DC1035 from the
Department of Health, Taiwan, and NSC 95-2313-B-005-028-MY2
from the National Science Council, Taiwan.
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