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Journal of Clinical Microbiology, December 1998, p. 3497-3504, Vol. 36, No. 12
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Expanded Diversity among Californian
Borrelia Isolates and Description of Borrelia
bissettii sp. nov. (Formerly Borrelia Group
DN127)
D.
Postic,1,*
N. Marti
Ras,1
R. S.
Lane,2
M.
Hendson,2 and
G.
Baranton1
Unité de Bactériologie
Moléculaire et Médicale, Institut Pasteur, 75724 Paris
Cedex 15, France,1 and
Department of
Environmental Science, Policy and Management, Division of Insect
Biology, University of California, Berkeley, Berkeley, California
947202
Received 2 July 1998/Returned for modification 27 August
1998/Accepted 15 September 1998
 |
ABSTRACT |
Up to now, the only species in the complex Borrelia
burgdorferi sensu lato known to cause Lyme borreliosis in the
United States has been B. burgdorferi sensu stricto.
However, some atypical strains closely related to the previously
designated genomic group DN127 have been isolated in the United States,
mostly in California. To explore the diversity of B. burgdorferi sensu lato group DN127, we analyzed the nucleotide
sequences of the rrf-rrl intergenic spacer regions from 19 atypical strains (18 from California and one from New York) and 13 North American B. burgdorferi sensu stricto strains (6 from
California). The spacer region sequences from the entire B. burgdorferi sensu lato complex available in data banks were used
for comparison. Phylogenetic analysis of sequences shows that the main
species of the B. burgdorferi sensu lato complex (B. afzelii, B. garinii, B. andersonii,
B. japonica, B. burgdorferi sensu stricto,
B. valaisiana, and B. lusitaniae) each form a
coherent cluster. A heterogeneous group comprising strains belonging to
the previously designated group DN127 clustered separately from
B. burgdorferi sensu stricto. Within this cluster, the deep
branches expressing the distances between the rrf-rrl sequences reflect a high level of divergence. This unexpected diversity
contrasts with the monomorphism exhibited by B. burgdorferi sensu stricto. To clarify the taxonomic status of this highly heterogeneous group, analysis of the rrs sequences of
selected strains chosen from deeply separated branches was performed.
The results show that these strains significantly diverge at a level that is compatible with several distinct genomic groups. We conclude that the taxonomy and phylogeny of North American B. burgdorferi sensu lato should be reevaluated. For now, we propose
that the genomic group DN127 should be referred to as a new species,
B. bissettii sp. nov., and that other related but distinct
strains, which require further characterization, be referred to as
Borrelia spp.
| |
INTRODUCTION |
In Eurasia, seven species of the
complex Borrelia burgdorferi sensu lato have been reported.
Only three of these species are associated with Lyme borreliosis. It
has also been shown that each pathogenic species is associated
predominantly with a given clinical presentation; Borrelia
burgdorferi sensu stricto is associated with arthritis, B. garinii is associated with neuroborreliosis, and B. afzelii is associated with late cutaneous symptoms (2, 39). Up to now, B. burgdorferi sensu stricto is the
only species associated with Lyme borreliosis in North America.
However, two other B. burgdorferi sensu lato genospecies
coexist in the United States, B. andersonii (22)
and the genomic group DN127 (3, 32). B. andersonii seems to be restricted to a limited ecosystem involving
cottontail rabbits and Ixodes dentatus ticks. In contrast, the genomic group DN127 appears to be involved in several enzootic transmission cycles (6, 29). A recent study demonstrated substantial genetic heterogeneity among Californian and other American
strains (24). We took advantage of the unique structure of
ribosomal genes in B. burgdorferi sensu lato to analyze the polymorphism of some strains isolated in California. A single copy of
the rrs gene is separated by a large spacer
(rrs-rrl; 3,000 to 5,000 bp) from two tandemly duplicated
copies of rrl and rrf genes (13, 36).
These two copies are separated by a small spacer, rrf-rrl,
which is approximately 250 bp long. The genetic heterogeneity of the
group DN127 was first evidenced by analysis of the restriction patterns
of the rrf-rrl spacer (32). However, the results
of DNA-DNA hybridization on a limited number of strains (32)
allowed us to place them in a single genomic group. To clarify the
genetic relationships between diverse North American strains, 20 atypical strains were compared with 13 B. burgdorferi sensu
stricto strains. Identification procedures involved restriction
polymorphism and sequencing studies of both the variable rrf-rrl spacer and the conserved rrs gene.
Sequences of the rrf-rrl spacer and the rrs gene
were used in a phylogenetic analysis. Some Californian strains are
closely related to the genomic group DN127, for which we propose the
name of B. bissettii sp. nov. Other atypical strains which
do not fall into this group are designated merely as
Borrelia spp. in this study. The latter strains cannot be
assigned to specific genomic groups until more isolates representative of each group are available for further characterization.
| |
MATERIALS AND METHODS |
Bacterial strains and DNA preparation.
The designations and
origins of the Borrelia strains used in this study are given
in Table 1. The uncloned strains were
grown in BSK II medium at 30°C. DNA was extracted by using the
Dynabeads DNA direct kit (Dynal), a method based on DNA separation by
biomagnetic beads as previously described (17). DNA samples
were stored at 
20°C until use for PCRs.
Analysis of restriction patterns of rrf-rrl spacer
and sequencing.
The restriction pattern analysis of amplified
rrf-rrl spacer was performed by using primers 1 and 2 as
described previously (32). MseI and
DraI restriction patterns were used to compare the strains.
The rrf-rrl spacer was sequenced by a solid-phase approach,
using the Cy5-AutoRead sequencing kit with an ALF express automatic
sequencer (Pharmacia) (17). To amplify the
rrf-rrl spacer, we used primers A
(5'-ATTACCCGTATCTTTGGC-3') and D
(5'-TCAATAAATGTTTGCTTCTC-3'), with one of the two primers
biotinylated at the 5' end. The biotinylated strand was then
immobilized through the interaction between biotin and
streptavidin by using the Dynabeads M-280 streptavidin kit (Dynal) according to the manufacturer's instructions. Sequencing was
performed by using the sequencing primers INS1
(5'-GAAAAGAGGAAACACCTGTT-3') in the rrf gene and
INS4 (5'-AGCTCCTAGGCATTCACCAT-3') at the 5' end of the
rrl gene.
rrs sequencing.
Amplification and sequencing of
the rrs gene were done as previously described
(17).
Sequence alignments and phylogenetic analysis.
Sequences
were aligned both manually on VSM software V.2.0 written by B. Lafay
and R. Christen (33) as described recently (10)
and by using the multisequence alignment program Clustal V
(10). Phylogenetic trees were constructed with distance
matrix data (calculated by the method of Jukes of Cantor
[14]) and both the neighbor-joining (NJ) method
(34) and the unweighted pair group with mathematical average
(UPGMA) (37) methods in MEGA software (15). A
parsimony method in MEGA was used to analyze the rrf-rrl
intergenic spacer sequences of select strains.
Characterization of the rrs-rrl spacer.
The size
of the rrs-rrl spacer was determined after amplification by
using primer S15 (5'-GGGCCTTGTACACACCGCCC-3') at the 3' end
of rrs and primer INS4 as given above. The PCR mixture (50 µl) contained 10 ng of DNA in 5 µl, 50 mM Tris-HCl, 1.5 mM MgCl2, 20 mM NH4SO4, 200 µM each
of the four deoxynucleoside triphosphates, 10 pmol of each primer, and
0.45 U of Hot Tub DNA polymerase (Amersham Life Science).
The PCR was carried out for 30 cycles with an amplification profile of
denaturation at 93°C for 15 s and then simultaneous annealing
and extension at 60°C for 8 min, with a final extension step at
60°C for 10 min.
PCR products (10 µl) were digested with 5 U of
HinfI
(Biolabs) in a total volume of 20 µl. Digested fragments were
analyzed
by electrophoresis on a 1.2% agarose gel stained with
ethidium
bromide.
Nucleotide sequence accession numbers.
The nucleotide
sequences of rrf-rrl spacer regions or
rrs genes from B. burgdorferi sensu lato isolates
have been deposited in EMBL data bank and assigned accession nos.
AJ006359 to AJ006375, AJ006503 to AJ006512, and AJ224130 to AJ224141
(see Table 1).
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RESULTS |
Individualization of B. bissettii deduced from the
analysis of the rrf-rrl spacer.
Analysis of
MseI restriction patterns of amplification products of the
spacer between the two tandem copies of the rrl-rrf ribosomal genes from North American strains revealed 11 different patterns (Table 2). These patterns were
not identical to any of the patterns recorded previously for B. burgdorferi sensu lato species and genomic groups. However, they
were very similar to the pattern of strains belonging to B. burgdorferi sensu stricto (Fig. 1).
The analysis of patterns obtained after restriction by DraI
confirmed this heterogeneity (Table 2).
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FIG. 1.
MseI restriction polymorphism of the
amplified rrf-rrl spacer from Californian strains. DNA was
electrophoresed on a 16% acrylamide gel, stained with ethidium
bromide, and UV illuminated. The species assignment of strains is given
in Table 1. The molecular sizes of DNA fragments (in base pairs) are
shown to the left of the gel.
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|
Some strains (CA27, CA372, CA378, and CA394) exhibited exactly the same
pattern as strain DN127, the type strain of the previous
genomic group
DN127.
The
rrf-rrl spacer region (
32) of strains tested
ranged from 216 to 257 bp. The percent identity in pairwise alignments
of sequences from
Borrelia spp. strains ranged from 85.3 to
100
(data not shown). However, all strains with identical
MseI or
DraI patterns exhibited 100% sequence
identity, except strain
CA404 which differed by one nucleotide from
strains CA31, CA443,
and CA446. To compare the polymorphism, the spacer
regions from
10 American strains previously identified as
B. burgdorferi sensu
stricto were sequenced. In contrast with the
extreme diversity
in
Borrelia spp., considerable homogeneity
characterized the sequences
of
B. burgdorferi sensu stricto
strains, as nucleotide substitutions
or deletions occurred in only five
positions.
The NJ and UPGMA distance methods were used to construct phylogenetic
trees from sequences obtained in this study. An example
of a tree drawn
by the UPGMA distance method is shown in Fig.
2. Each previous species, namely,
B. garinii,
B. afzelii,
B. valaisiana,
B. lusitaniae,
B. tanukii,
B. turdi,
B. andersonii, and
B. japonica,
clustered
separately. One large and heterogeneous cluster of 32
sequences
comprises
B. burgdorferi sensu stricto, the strains
identified as belonging to
B. bissettii sp. nov. (formerly
the
genomic group DN127, DN127, CA128, CA55, and 25015), and all
strains
with atypical
MseI and
DraI patterns
(
Borrelia spp.). Within this
cluster, all strains belonging
to
B. burgdorferi sensu stricto
are closely related, which
contrasts with the strains of
Borrelia spp. that are
scattered on several branches. Among the atypical
strains, two strains
(CA19 and CA423), despite slight differences
in their
MseI
patterns, fell into the
B. burgdorferi sensu stricto
cluster. Given the large diversity exhibited by the
Borrelia
spp.,
segregation of some strains did not correlate precisely with
different
trees drawn by phenetic (Fig.
2) or cladistic methods (data
not
shown). For example, the placement of strain CA2 was uncertain,
as
was the placement of strains CA29 and CA8, because they constituted
a
separate cluster comprising four distinct branches together
with
Californian strains CA404, CA443, CA446, and CA31 and
B. andersonii in the tree drawn with the NJ distance method (data
not
shown).
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FIG. 2.
Phylogenetic tree based on a comparison of the
rrf-rrl sequences of B. burgdorferi sensu lato.
The branching pattern was generated by the UPGMA method. The bar
represents 1% divergence.
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However, the branch consisting of strains previously placed in the
group DN127 (DN127, CA55, CA128, and 25015), and six additional
strains
(CA27, CA370, CA372, CA378, CA394, and CA395) was constant,
irrespective of the method used to construct the
trees.
New genomic groups deduced from rrs sequences.
To
provide an alternative assessment of phylogenetic relationships between
such divergent strains, we sequenced the entire rrs gene
from strains representing each of the main branches in the
rrf-rrl trees. A phylogenetic tree showing the result of the NJ analysis of sequences is shown in Fig.
3. The assignment of strain CA19 in
B. burgdorferi sensu stricto was confirmed. The results
showed that strains of Borrelia spp. significantly diverge at a level compatible with distinct genomic groups. Strains CA31 and
CA446 constituted one group. Strains CA8 and CA29 comprised another
group. Strains CA2 and CA28 were located on two different branches
according to the rrf-rrl sequence. They clustered together by rrs sequence, but their genetic distance is relatively
large. The status of strain CA2 was not clear on the basis of DNA-DNA hybridization data (32). However, our present results
suggest that strains CA2 and CA28 should constitute a new genomic
group. Strains CA128, CA55, and 25015 segregated with strain DN127.
Whether strain CA13 belong to the latter genomic group remains unknown. The clustering of strains of Borrelia spp. was consistent
with that obtained by the UPGMA analysis (data not shown).
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FIG. 3.
Phylogenetic tree based on a comparison of the
rrs sequences of B. burgdorferi sensu lato. The
branching pattern was generated by the NJ method. The bar represents
0.1% divergence.
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Polymorphism of the rrs-rrl spacer.
It has been
shown previously that the size of the spacer between the rrs
gene and the first copy of the rrl gene varied among different Borrelia species (28). The size of the
rrs-rrl spacer allowed Borrelia species to be
distinguished by decreasing size order from 5,000 bp for B. afzelii to 3,000 bp for B. burgdorferi sensu stricto
and B. andersonii (Fig. 4). As
shown in Fig. 4, strains evaluated in this work exhibited PCR products
of two different sizes. All strains assigned to B. bissettii
sp. nov. (DN127, CA55, 25015, CA27, CA394, CA395, CA370, CA372, and
CA378), as well as four strains of Borrelia spp. (CA31,
CA404, CA443, and CA446) exhibited a rrs-rrl spacer with an
identical size of approximately 500 bp larger than that of B. burgdorferi sensu stricto. Other strains of Borrelia
spp. had a rrs-rrl spacer whose size was the same as that of
B. burgdorferi sensu stricto. The analysis of the
HinfI restriction pattern of the rrs-rrl spacer
PCR product has been proposed for typing of B. burgdorferi
sensu stricto (18, 19). As described earlier
(18), we also found two DNA fragment patterns among strains
of B. burgdorferi sensu stricto. In contrast to these
findings, a strong polymorphism was observed among atypical strains
(Fig. 5). Ten distinctive patterns
recorded from 17 atypical strains are shown in Fig. 5. Notably, the
analyses of polymorphism of both the large rrs-rrl spacer
and the small rrf-rrl spacer produced comparable groupings
of strains.
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FIG. 4.
PCR products of rrs-rrl spacer from B. burgdorferi sensu lato strains. The species assignment of strains
is given in Table 1. Amplification was carried out by using the
S15-INS4 primer set. DNAs were electrophoresed on a 0.6% agarose gel,
stained with ethidium bromide, and UV illuminated. Molecular size
standards Raoul (Appligene) were used.
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FIG. 5.
Restriction patterns of Californian strains. The species
assignment of strains is indicated in Table 1. DNAs from amplified
rrs-rrl spacers were digested by HinfI. DNAs were
electrophoresed on a 1.2% agarose gel, stained with ethidium bromide,
and UV illuminated. Molecular size standards Raoul (Appligene) were
used.
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DISCUSSION |
Since the first description of B. burgdorferi in 1982 (7), it has been assumed that strains in the United States
were more homogeneous than the European strains (8, 9).
However, an increasing number of atypical strains have been recognized
in the United States, particularly in the 1990s (1, 5, 9, 12, 16,
21, 24, 35, 41, 42). Some of these strains were identified as
belonging to the species B. andersonii (22), whereas others constituted a new genomic group called group DN127 (3, 32). Considerable phenotypic heterogeneity was found among strains described from California and Colorado (26,
35), and substantial genetic diversity was reported among a large
number of North American strains (24) on the basis of
genomic macrorestriction analysis and ospA and
rrl gene sequencing. Our study emphasizes that the genetic
diversity among American strains is much greater than previously thought.
Phylogenetic analyses of rrs gene sequences have often been
used to evaluate the taxonomic relatedness of B. burgdorferi
sensu lato strains (11, 17, 20, 40). The results of these
analyses correlated well with data from DNA-DNA hybridizations
(32). The rrs gene sequence analysis of atypical
strains confirmed the foregoing results and revealed at least four
groups which appear to represent heretofore undescribed genospecies.
CA19 belongs to B. burgdorferi sensu stricto. Three new
genomic groups were CA29-CA8, CA2-CA28, and CA31-CA446, respectively.
The taxonomic position of strain CA13 remains unclear. A polymorphism
was observed in the rrf-rrl restriction patterns of the
strains within the genomic group DN127. Also, some differences were
previously reported for the physical maps of strains DN127 and CA55,
which were classified in two separate groups (8). However,
data originated from the single gene locus hbb
(38), as well as information acquired by multilocus enzyme
electrophoresis, involving the whole genome (4) were
consistent with data from DNA-DNA hybridizations showing that DN127 and
CA55 do belong to the same species (32). Moreover, the
rrs sequences of these two strains are 100% identical. To clarify the taxonomic status of B. burgdorferi sensu lato in
the United States, we propose the name B. bissettii sp. nov.
for the genomic group DN127 in honor of Marjorie L. Bissett, who with her coworker Warren Hill, first described a member of this group in
1987 (5). We refrain from naming the other genomic groups until hybridization data are available for genetic characterization. Instead, we lump them here as Borrelia spp. The noncoding
region between the two copies of rrf and rrl
genes was shown previously to reflect the taxonomic status of strains
(32). The phylogenetic study of this region showed that
strains from each B. burgdorferi sensu lato species
clustered as expected taxonomically, and each cluster clearly diverged
from others. In contrast with the high conservation of sequences within
the B. burgdorferi sensu stricto cluster, rrf-rrl
sequences from Borrelia strains exhibited an unexpected broad diversity. This region is not constrained
genetically, so the number of mutational events found should
reflect the relative antiquity of the members of this bacterial
complex. Californian strains were found scattered in different
clusters. Within each cluster, the deep branches expressing the
distances between the rrf-rrl sequences reflect a high
divergence level. According to previous studies (23, 32),
these results strongly suggest that these strains should constitute new
genomic groups. Despite some discrepancies between the different trees,
all are consistent with the placement of strains belonging to B. bissettii sp. nov. in a distinct cluster. Within this cluster,
only strain 25015 was located on a separate branch.
In opposition with what is usually thought, more than two B. burgdorferi sensu lato species (B. burgdorferi sensu
stricto and B. andersonii) seem to occur in the United
States. B. burgdorferi sensu stricto is transmitted
primarily by Ixodes scapularis and Ixodes
pacificus ticks, whereas the new genomic groups described here are
associated with these two ticks plus Ixodes neotomae (now
Ixodes spinipalpis [27]) and some of its
rodent hosts. Moreover, I. spinipalpis also can harbor
Borrelia from other genomic groups, since strains CA2 and
CA13 represent two distinct groups. Thus, there are a variety of ticks
and reservoir host for B. burgdorferi sensu lato in the
United States. It is not known whether B. bissettii sp. nov.
and the other novel genomic groups can infect humans. All the strains
used in this study were isolated from ticks or small mammals. As stated
by Oliver (29), clinical manifestations of Lyme borreliosis
in the southern United States are mild and some cases may be
asymptomatic. Thus, the roles of B. bissettii sp. nov. and
Borrelia spp. in producing Lyme borreliosis remain to be
demonstrated. In addition, Picken et al. (30, 31) recently described human strains from Slovenia related to strain 25015, which
belongs to B. bissettii sp. nov. on the basis of large
restriction fragment pattern, protein, and plasmid profile analyses. If
the strains from Slovenia are true members of B. bissettii
sp. nov., the pathogenicity of this species should be evaluated there
as well as in the United States. In Europe, three species are known to
be pathogenic for humans; in the United States, all strains isolated
from humans so far belong to B. burgdorferi sensu stricto. This could mean that I. spinipalpis does not transmit
Borrelia to humans or that these new genomic groups are
nonpathogenic for humans. This latter hypothesis seems more likely,
since I. pacificus and I. scapularis frequently
bite humans and occasionally harbor such strains. Moreover, I. spinipalpis primarily infests rodents and lagomorphs and rarely
attaches to humans (25). However, despite the great number
of strains isolated from I. scapularis in the United States,
25015 is the only strain recovered from this tick that belongs to a
species other than B. burgdorferi sensu stricto. Also, this
strain is genetically distant from other strains within B. bissettii sp. nov. This fact could reflect genetic adaptation to
an unusual vector. The heterogeneity encountered among B. burgdorferi sensu lato in the United States might be compared to
that described in Europe and Asia. On the latter two continents,
B. garinii comprises a more heterogenous collection than
B. afzelii and B. burgdorferi sensu stricto.
Aside from the three pathogenic species, nonpathogenic species, such as
B. valaisiana, B. lusitaniae, or B. japonica, coexist. More data are needed to understand the
significance of the diversity of B. burgdorferi sensu lato
and their role in human Lyme borreliosis.
| |
ACKNOWLEDGMENTS |
We thank T. G. Schwan and R. N. Brown for supplying
some of the strains, I. Saint Girons for critical reading of the
manuscript, and E. Bellenger for technical assistance.
We thank the Pasteur Institute for supporting this work. Also, many of
the Californian strains were acquired during ecologic studies supported
in part by funding to R.S.L. from the U.S. National Institutes of
Health (grant AI22501) and the Centers for Disease Control and
Prevention (cooperative agreement U50/CCU906594).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Unité de
Bactériologie Moléculaire et Médicale, Institut
Pasteur, 28 rue du Docteur Roux, 75724 Paris Cedex 15, France. Phone:
33 1 45 68 83 37. Fax: 33 1 40 61 30 01. E-mail:
dpostic{at}pasteur.fr.
| |
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Journal of Clinical Microbiology, December 1998, p. 3497-3504, Vol. 36, No. 12
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Abstract
Introduction
