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. 2016 Mar;66(3):1447–1452. doi: 10.1099/ijsem.0.000897

Borrelia bissettiae sp. nov. and Borrelia californiensis sp. nov. prevail in diverse enzootic transmission cycles

Gabriele Margos 1,✉, Robert S Lane 2, Natalia Fedorova 2, Johannes Koloczek 1, Joseph Piesman 3, Andrias Hojgaard 3, Andreas Sing 1, Volker Fingerle 1
PMCID: PMC5801759  NIHMSID: NIHMS936228  PMID: 26813420

Abstract

Two species of the genus Borrelia, Borrelia bissettiae sp. nov. and Borrelia californiensis sp. nov., were first described by Postic and co-workers on the basis of genetic analyses of several loci. Multilocus sequence analysis of eight housekeeping loci confirmed that these two Borrelia genomospecies are distinct members of the Borrelia burgdorferi sensu lato complex. B. bissettiae sp. nov. was initially described in transmission cycles involving Neotoma fuscipes wood rats and Ixodes pacificus ticks in California, and Neotoma mexicana and Ixodes spinipalpis in Colorado. The preferred host of B. californiensis sp. nov. appears to be the California kangaroo rat, Dipodomys californicus; Ixodes jellisoni, I. spinipalipis and I. pacificus ticks are naturally infected with it. Thus, the ecological associations of the two genomospecies and their genetic distance from all other known Borrelia genomospecies species justify their description as separate genomospecies: B. bissettiae sp. nov. (type strain DN127T = DSM 17990T =  CIP 109136T) and B. californiensis (type strain CA446T = DSM 17989T = ATCC BAA-2689T).

Lyme borreliosis (LB) is caused by several species of bacteria belonging to the LB group of spirochaetes, also referred to as Borrelia burgdorferi sensu lato. B. burgdorferi sensu lato is a heterogeneous species complex that currently consists of at least 20 recognized or proposed genomospecies. These bacteria are maintained in natural transmission cycles among vertebrate reservoir hosts and ticks of the Ixodes persulcatus species complex or other species of the genus Ixodes, such as Ixodes spinipalpis (Brown & Lane, 1992, 1996; Kurtenbach et al., 2006).

The strain designated the Borrelia bissettiae sp. nov. type strain, DN127T, was isolated from a questing Ixodes pacificus tick collected in Del Norte County, California, during the 1980s (Bissett & Hill, 1987). Additional strains of this genomospecies have been isolated from I. pacificus or Ixodes neotomae (now I. spinipalpis) in California and Colorado (Bissett & Hill, 1987; Brown & Lane, 1992; Maupin et al., 1994; Schneider et al., 2000) and from rodents captured in the Chicago area of Illinois (Picken & Picken, 2000). Postic et al. (1998) proposed that these strains constitute a distinct genomospecies within the B. burgdorferi sensu lato complex and named it B. bissettii sp. nov. In the USA, B. bissettiae enzootic transmission cycles were also found in some southern states involving Ixodes affinis and various rodent-host species (Oliver et al., 2003). In the far west of the USA, B. bissettiae was associated with the dusky-footed woodrat, Neotoma fuscipes Baird (Brown et al., 2006). In the same geographical region, B. bissettiae was detected in a host-seeking avian tick, Ixodes auritulus, co-infected with B. burgdorferi (Padgett & Bonilla, 2011) and, more recently, in the blood of several bird species and I. pacificus immatures infesting birds (Newman et al., 2015). In the latter study, the infection prevalence in I. pacificus larvae was much lower for B. bissettiae than it was for B. burgdorferi; thus, the role of birds as either primary or secondary reservoir hosts for B. bissettiae remains to be established.

Of the tick species known to transmit B. bissettiae sp. nov. in the USA, i.e. I. pacificus and I. spinipalpis in the far west and south-west, and I. affinis in the south-east (Bissett & Hill, 1987; Lin et al., 2001, 2003; Maupin et al., 1994), only I. pacificus attaches to humans with any frequency. This may partly explain why B. bissettiae is not considered to be a human pathogen in the USA (Maupin et al., 1994). On the other hand, B. bissettiae occasionally infects humans in northern California as demonstrated by the presence of its DNA in a few serum specimens, but signs or symptoms suggestive of clinical Lyme disease are lacking in this region (Girard et al., 2011).

In Europe, B. bissettiae sp. nov. DNA has been detected in human patients (Picken et al., 1996a, b; Rudenko et al., 2008, 2009; Strle et al., 1997), and in questing Ixodes ricinus ticks (Hulínská et al., 2007; Tappe et al., 2014). One human isolate of B. bissettiae (PGeb) was obtained from a German patient without a history of travel, providing direct evidence that B. bissettiae occurs in Europe (Fingerle et al., 2008) (Fig. 1).

Fig. 1.

Fig. 1.

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Molecular phylogenetic analysis of Borrelia bissettiae sp. nov. (dark grey dots) and Borrelia californiensis sp. nov. (light grey dot) strains. The evolutionary history was inferred by using the maximum-likelihood method based on the Tamura–Nei model (Tamura & Nei, 1993). The tree with the highest log-likelihood ( − 21015.8975) is shown. Bootstrap values (500 replications) are shown next to nodes. Initial tree(s) for the heuristic search were obtained by applying the neighbour-joining method to a matrix of pairwise distances estimated using the maximum composite likelihood (MCL) approach. A discrete Gamma distribution was used to model evolutionary rate differences among sites [5 categories (+G, parameter = 0.2602)]. All positions containing gaps and missing data were eliminated. There were a total of 4779 positions in the final dataset. Evolutionary analyses were conducted in mega6 (Tamura et al., 2013). Bar, 0.001 substitutions per site.

In phylogenetic analyses of the rrf-rrl intergenic spacer (IGS) region of B. burgdorferi sensu lato, strains CA443 and CA446 from northern California fell into a clade well separated from all other known genomospecies, a finding consistent with them representing a distinct genomospecies for which the name Borrelia californiensis sp. nov. was proposed (Postic et al., 2007). Twenty-three Borrelia strains mainly isolated from the California kangaroo rat (Dipodomys californicus) clustered together with strains CA404, CA443 and CA446 (Postic et al., 2007). Those data suggest that all such strains belong to the genomospecies B. californiensis sp. nov., and that D. californicus is a primary reservoir host of this genomospecies. Strains CA443 and CA446 investigated by multilocus sequence analysis (MLSA) with eight housekeeping genes formed a distinct clade that differed from all other species of the genus Borrelia (Margos et al., 2010) (Fig. 1). Genetic-distance analysis confirmed the distinctness of these strains from other described species of the genus Borrelia (Margos et al., 2010).

The samples used for studies of the two genomospecies are listed in Table 1.

Table 1.

Borrelia bissettiae sp. nov. and B. californiensis sp. nov. isolates from California and Colorado, USA, evaluated in previous studies

ST* Strain ID Country of origin Region Genomospecies Biological source of isolate Year of collection Typed with: pubMLST ID/GenBank accession no.
156 CA128 USA Mendocino County, CA B. bissettiae I. neotomae (now I. spinipalpis) ex N. fuscipes 1991 MLSA 1002
282 CA370 USA Alameda County, CA B. bissettiae N. fuscipes ear biopsy 1992 MLSA 1003
283 CA371 USA Alameda County, CA B. bissettiae N. fuscipes ear biopsy 1992 MLSA 1004
270 CA389 USA Alameda County, CA B. bissettiae I. pacificus 1993 MLSA 1005
272 DN127-Cl9-2/p7 USA Del Norte County, CA B. bissettiae I. pacificus 1985 MLSA 1006
273 gom93-268 USA Larimer County, CO B. bissettiae I. spinipalpis ex Neotoma mexicana 1993 MLSA 1007
273 gom93-274 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1008
273 gom93-275 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1009
273 gom93-278 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1010
160 gom93-283 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1011
273 gom93-284 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1012
274 gom93-286 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1013
273 gom93-287 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1014
271 gom93-296 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1015
273 gom93-297 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1016
158 gom93-299 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1017
275 gom93-305 USA Larimer County, CO B. bissettiae I. spinipalpis ex Peromyscus difficilis 1993 MLSA 1018
276 gom93-310 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1019
277 gom93-501 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1020
277 gom93-543 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1021
277 gom93-544 USA Larimer County, CO B. bissettiae I. spinipalpis ex N. mexicana 1993 MLSA 1022
667 PGeb Germany Baden-Württemberg B. bissettiae Human 1996 MLSA 1874
447 CA443 USA Mendocino County, CA B. californiensis D. californicus ear biopsy 1995 MLSA 1450
447 CA446 USA Mendocino County, CA B. californiensis D. californicus ear biopsy 1995 MLSA 1277
na CA552 USA Mendocino County, CA B. californiensis Ixodes jellisoni ex D. californicus 1998 rrf-rrl IGS AY182059
na CA507 USA Mendocino County, CA B. californiensis D. californicus 1997 rrf-rrl IGS AY182056
na CA504 USA Mendocino County, CA B. californiensis D. californicus 1997 rrf-rrl IGS AY182055
na CA502 USA Mendocino County, CA B. californiensis D. californicus 1997 rrf-rrl IGS AY182054
na CA462 USA Mendocino County, CA B. californiensis D. californicus 1996 rrf-rrl IGS AY182053
na CA448 USA Mendocino County, CA B. californiensis D. californicus 1995 rrf-rrl IGS AY182052
na CA442 USA Mendocino County, CA B. californiensis D. californicus 1995 rrf-rrl IGS AF073254
na CA411 USA Mendocino County, CA B. californiensis D. californicus 1994 rrf-rrl IGS AY182048
na CA31 USA Mendocino County, CA B. californiensis D. californicus 1990 rrf-rrl IGS AJ006372
na CA22 USA Mendocino County, CA B. californiensis D. californicus 1990 rrf-rrl IGS AY177631
na CA134 USA Mendocino County, CA B. californiensis I. pacificus ex D. californicus 1991 rrf-rrl IGS AY182042
na CA468 USA Mendocino County, CA B. californiensis D. californicus 1996 rrf-rrl IGS AY177641
na CA404 USA Mendocino County, CA B. californiensis D. californicus 1993 rrf-rrl IGS AJ006371
na CA33 USA Mendocino County, CA B. californiensis D. californicus 1990 rrf-rrl IGS AY177632
na CA20 USA Mendocino County, CA B. californiensis D. californicus 1990 rrf-rrl IGS AY180239
na CA142 USA Mendocino County, CA B. californiensis D. californicus 1991 rrf-rrl IGS AY182043
na CA409 USA Mendocino County, CA B. californiensis D. californicus 1993 rrf-rrl IGS AF073255
na CA547 USA Mendocino County, CA B. californiensis D. californicus 1998 rrf-rrl IGS AY177642
na CA445 USA Mendocino County, CA B. californiensis D. californicus 1995 rrf-rrl IGS AF073256
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na, Not applicable.

*

st, sequence type.

Description of Borrelia bissettiae sp. nov.

Borrelia bissettiae [bis.set′ti.ae. N.L. gen. n. bissettiae of Bissett, proposed in honour of Dr Marjorie L. Bissett, who isolated and described this spirochaete along with her co-worker Warren Hill (Bissett & Hill, 1987)].

Cells are helical, approximately 0.2 μm by 20 μm, and stain well with Giemsa stain. Unstained cells can be visualized by dark-field microscopy. Flexible and motile with rotational and forward/backwards movement. Cells can be cultured in vitro under microaerophilic conditions (Johnson et al., 1984b) using liquid media such as Barbour–Stoenner–Kelly (BSK) medium. Optimal growth occurs at 33–34 °C.

The type strain, DN127T, was isolated from a questing I. pacificus tick in the late 1980s. It has been deposited in the German Microbial Strain Collection ( = DSM 17990T) and at the Institut Pasteur, Paris, France ( = CIP 109136T). B. bissettiae can be distinguished from other genomospecies of the genus Borrelia via sequences of the 5S–23S IGS, the rrs locus and by MLSA (Margos et al., 2010; Postic et al., 1998). The B. bissettiae group is heterogeneous as shown by 5S–23S rRNA IGS (Postic et al., 1998), MLSA analyses and by the size of the 16S–23S rRNA IGS fragment (Bunikis et al., 2004) that approximates 1000 or 1100 bp (unpublished data). This bacterium is maintained in nature in diverse transmission cycles involving various rodent reservoir hosts and certain tick species of the genus Ixodes. Strains of this species have been found in the USA and Europe. The mean DNA G+C content of the type strain is 27 mol%.

Description of Borrelia californiensis sp. nov.

Borrelia californiensis (ca.li.for.ni.en′sis N.L. fem. adj. californiensis belonging to California, from where the type strain was isolated) was proposed by Postic et al. (2007).

Cells are helical, approximately 0.2 μm by 20 μm, and stain well with Giemsa stain. Unstained cells can be visualized by dark-field microscopy. Flexible and motile with rotational and forward/backwards movement. Cells can be cultured in vitro under microaerophilic conditions (Johnson et al., 1984a) using liquid media such as BSK medium. Optimal growth occurs at 33–34 °C.

The type strain, CA446T, was isolated from an ear-punch biopsy excised from a male D. californicus captured in November 1995 by Kerry A. Padgett at the University of California Hopland Research and Extension Center in Mendocino County, California. It has been deposited in the American Type Culture Collection ( = ATCC BAA-2689T) and the German Microbial strain collection ( = DSM 17989T). Sequence analysis of the rrf-rrl intergenic spacer and the rrs and flagellin genes differentiates B. californiensis from B. bissettiae (Postic et al., 1998). B. californiensis strains are also distinguishable from all other LB species by using two different MLSA schemes (Margos et al., 2010; Postic et al., 2007). B. californiensis seems a rather homogeneous species. So far, it is restricted in distribution to northern California where its primary vertebrate host is the California kangaroo rat, Dipodomys californicus (Brown & Lane, 1992, 1996; Lane & Brown, 1991). Known vectors include Ixodes jellisoni, I. pacificus and I. spinipalpis. The mean DNA G+C content of the type strain is 27 mol%.

Acknowledgements

The authors gratefully acknowledge Richard N. Brown, Kerry A. Padgett and Joyce E. Kleinjan who conducted ecologic studies at the University of California Hopland Research and Extension Center (formerly the Hopland Field Station) in Mendocino County that resulted in the detection and isolation of both spirochaetes at that facility. Those studies were supported in large part by funding to R. S. L. from the US National Institutes of Health (grant AI22501) and the Centers for Disease Control and Prevention (cooperative agreement U50/CCU906594).

Footnotes

Abbreviations: IGS, intergenic spacer; LB, Lyme borreliosis; MLSA, multilocus sequence analysis.

The GenBank/EMBL/DDBJ accession numbers for the sequences obtained in this study are KT709291–KT709458 and KT709517–KT709532. Sequence data are also available at the Borrelia MLST website at http://www.pubMLST.org/borrelia, hosted at the University of Oxford, UK (ID numbers 1002–1022, 1277 and 1450).

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