Phylogeography of
 Borrelia burgdorferi
 in the eastern United States reflects multiple independent Lyme disease emergence events

Hoen, Anne G.; Margos, Gabriele; Bent, Stephen J.; Diuk‐Wasser, Maria A.; Barbour, Alan G.; Kurtenbach, Klaus; Fish, Durland

doi:10.1073/pnas.0903810106

Cited by 152 publications

(195 citation statements)

References 60 publications

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“…While the significance of these foci is uncertain, it is interesting that the distribution of Lyme disease follows the same profile (http://www.cdc.gov/lyme/stats/maps/map2010.html). The phylogeography of Borrelia burgdorferi suggests a wide prehistoric distribution that was reduced to localized refugia in the 19th and early 20th century by deforestation and unregulated deer hunting (28). The earliest records of I. scapularis in North America come from the 1920s for Naushon Island, MA (34), and the 1960s for Wisconsin (30); these areas may represent refugial foci from which deer, ticks, and tick-borne disease are expanding into the United States.…”

Section: Resultsmentioning

confidence: 99%

Revisiting the Clinal Concept of Evolution and Dispersal for the Tick-Borne Flaviviruses by Using Phylogenetic and Biogeographic Analyses

Heinze

Gould

Forrester

2012

J Virol

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b Tick-borne flaviviruses (TBF) are widely dispersed across Africa, Europe, Asia, Oceania, and North America, and some present a significant threat to human health. Seminal studies on tick-borne encephalitis viruses (TBEV), based on partial envelope gene sequences, predicted a westward clinal pattern of evolution and dispersal across northern Eurasia, terminating in the British Isles. We tested this hypothesis using all available full-length open reading frame (ORF) TBF sequences. Phylogenetic analysis was consistent with current reports. However, linear and nonlinear regression analysis of genetic versus geographic distance combined with BEAST analysis identified two separate clines, suggesting that TBEV spread both east and west from a central point. In addition, BEAST analysis suggested that TBF emerged and dispersed more than 16,000 years ago, significantly earlier than previously predicted. Thus, climatic and ecological changes may have played a greater role in TBF dispersal than humans.

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Section: Resultsmentioning

confidence: 99%

Revisiting the Clinal Concept of Evolution and Dispersal for the Tick-Borne Flaviviruses by Using Phylogenetic and Biogeographic Analyses

Heinze

Gould

Forrester

2012

J Virol

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“…Although being members of a single genospecies, the European and North American B. burgdorferi s.s. populations have diverged and share only a few genomic groups due to recent trans-Atlantic migrations (Margos et al 2008;Qiu et al 2008). In the United States, the northeastern and midwestern B. burgdorferi s.s. populations have differentiated significantly (Qiu et al 2008;Hoen et al 2009;Brisson et al 2010). Population divergence in B. burgdorferi s.l.…”

Section: Maintenance Of Genome Clusters By Frequency-dependent Selectionmentioning

confidence: 99%

“…Second, consistent with the FDS model and less compatible with the host-specialization model, a number of recently dispersed B. burgdorferi s.s. genomic groups flourish in two separate transmission cycles (Europe and North America), which differ in tick-vector species and presumably in host-species composition as well (Qiu et al 2008). Third, the severe human virulence of B. burgdorferi s.s. is itself evidence for it being a generalist parasite of mammalian hosts, since despite the fact that humans are not its natural reservoir hosts, B. burgdorferi s.s. is capable of (Qiu et al 2008;Hoen et al 2009;Brisson et al 2010). Population divergence in B. burgdorferi s.l.…”

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confidence: 99%

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Pervasive Recombination and Sympatric Genome Diversification Driven by Frequency-Dependent Selection in Borrelia burgdorferi, the Lyme Disease Bacterium

Vargas²,

et al. 2011

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How genomic diversity within bacterial populations originates and is maintained in the presence of frequent recombination is a central problem in understanding bacterial evolution. Natural populations of Borrelia burgdorferi, the bacterial agent of Lyme disease, consist of diverse genomic groups co-infecting single individual vertebrate hosts and tick vectors. To understand mechanisms of sympatric genome differentiation in B. burgdorferi, we sequenced and compared 23 genomes representing major genomic groups in North America and Europe. Linkage analysis of .13,500 single-nucleotide polymorphisms revealed pervasive horizontal DNA exchanges. Although three times more frequent than point mutation, recombination is localized and weakly affects genome-wide linkage disequilibrium. We show by computer simulations that, while enhancing population fitness, recombination constrains neutral and adaptive divergence among sympatric genomes through periodic selective sweeps. In contrast, simulations of frequency-dependent selection with recombination produced the observed pattern of a large number of sympatric genomic groups associated with major sequence variations at the selected locus. We conclude that negative frequency-dependent selection targeting a small number of surface-antigen loci (ospC in particular) sufficiently explains the maintenance of sympatric genome diversity in B. burgdorferi without adaptive divergence. We suggest that pervasive recombination makes it less likely for local B. burgdorferi genomic groups to achieve host specialization. B. burgdorferi genomic groups in the northeastern United States are thus best viewed as constituting a single bacterial species, whose generalist nature is a key to its rapid spread and human virulence. G ENETIC discontinuity, the basis of biodiversity, is ubiquitous in prokaryotes as well as in eukaryotes. Most bacterial populations display a highly clonal genetic structure, in which the observable number of multilocus genotypes is far fewer than the number expected under the assumption of free recombination (Maynard Smith et al. 1993). Bacterial clonality was originally thought of as a result of a lack or rarity of recombination among asexually reproducing and independently evolving clones (Ochman and Selander 1984). Since then, molecular surveys of natural bacterial populations using protein electrophoresis, multilocus sequencing typing (MLST), and whole-genome PRJNA3, PRJNA28633, PRJNA19839, PRJNA29359, PRJNA28629, PRJNA29357, PRJNA21003, PRJNA19835, PRJNA28627, PRJNA21001, PRJNA29361, PRJNA28621, PRJNA19837, PRJNA20999, PRJNA28631, PRJNA29363, PRJNA17057, PRJNA19841, PRJNA12554, PRJNA28625, PRJNA29573, PRJNA19843, and PRJNA28635. 1 Present address: Odum School of Ecology, University of Georgia, Athens, GA 30602. sequencing revealed that horizontal genetic exchange is in fact often more frequent than point mutations in bacteria, including species known as strongly clonal (Maynard Smith et al. 1993;Feil and Spratt 2001;Didelot and Maiden 2010;Retc...

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“…MLST: MLST was originally proposed as a tool for epidemiological study of infectious diseases [13,17]. MLST is now being advocated as an alternative method for determining Borrelia sp.…”

Section: Identification Of Borrelia Isolatesmentioning

confidence: 99%

Multilocus Sequence Typing and DNA Similarity Analysis Implicates that a Borrelia valaisiana–related sp. Isolated in Japan is Distinguishable from European B. valaisiana

et al. 2013

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ABSTRACT. Lyme disease Borrelia spp. are transmitted by Ixodes ticks, and more than 10 species of borreliae have been identified around the world. Recently, another Borrelia sp. has been reported in Asia (Japan, Korea, China, Taiwan and Thailand) as Borrelia valaisiana-related sp. In the present study, we obtained and genetically characterized 19 B. valaisiana-related sp. strains from mammals and ticks. Genetic analyses showed that the Borrelia strains were distinct from B. valaisiana found in Europe. Multilocus sequence typing revealed that these Borrelia isolates formed a monophyletic group with B. yangtze strains in China. Some of the strains were isolated from the bladders of small mammals, and also two strains were experimentally confirmed to be infectious in C3H/HeN mice. We observed that the Borrelia sp. was maintained in the Ixodes granulatus tick after molting. These results suggested that small mammals and I. granulatus were possible reservoir hosts and the vector tick for the Borrelia sp., respectively. B. valaisiana, originally found in Europe, was transmitted mainly by I. ricinus, and birds were mainly thought to be reservoir hosts. Our results suggested that Japanese isolates of B. yangtze (formerly B. valaisiana-related sp.) were distinguishable from B. valaisiana according to the reservoir host and its vector tick. In this study, we also deposited borrelia strain Okinawa-CW62 into bioresource centers as a reference strain of B. yangtze (=DSM 24625, JCM 17189).

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Phylogeography of Borrelia burgdorferi in the eastern United States reflects multiple independent Lyme disease emergence events

Cited by 152 publications

References 60 publications

Revisiting the Clinal Concept of Evolution and Dispersal for the Tick-Borne Flaviviruses by Using Phylogenetic and Biogeographic Analyses

Revisiting the Clinal Concept of Evolution and Dispersal for the Tick-Borne Flaviviruses by Using Phylogenetic and Biogeographic Analyses

Pervasive Recombination and Sympatric Genome Diversification Driven by Frequency-Dependent Selection in Borrelia burgdorferi, the Lyme Disease Bacterium

Multilocus Sequence Typing and DNA Similarity Analysis Implicates that a <i>Borrelia valaisiana</i>–related sp. Isolated in Japan is Distinguishable from European <i>B. valaisiana</i>

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