Niche Partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the Same Tick Vector and Mammalian Reservoir Species

Alan G. Barbour Departments of Microbiology and Molecular Genetics and Medicine, University of California Irvine, Irvine, California; Department of Epidemiology and Public Health, Yale University School of Public Health, New Haven, Connecticut; Departments of Fisheries and Wildlife and Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan

Search for other papers by Alan G. Barbour in
Current site
Google Scholar
PubMed
Close
,
Jonas Bunikis Departments of Microbiology and Molecular Genetics and Medicine, University of California Irvine, Irvine, California; Department of Epidemiology and Public Health, Yale University School of Public Health, New Haven, Connecticut; Departments of Fisheries and Wildlife and Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan

Search for other papers by Jonas Bunikis in
Current site
Google Scholar
PubMed
Close
,
Bridgit Travinsky Departments of Microbiology and Molecular Genetics and Medicine, University of California Irvine, Irvine, California; Department of Epidemiology and Public Health, Yale University School of Public Health, New Haven, Connecticut; Departments of Fisheries and Wildlife and Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan

Search for other papers by Bridgit Travinsky in
Current site
Google Scholar
PubMed
Close
,
Anne Gatewood Hoen Departments of Microbiology and Molecular Genetics and Medicine, University of California Irvine, Irvine, California; Department of Epidemiology and Public Health, Yale University School of Public Health, New Haven, Connecticut; Departments of Fisheries and Wildlife and Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan

Search for other papers by Anne Gatewood Hoen in
Current site
Google Scholar
PubMed
Close
,
Maria A. Diuk-Wasser Departments of Microbiology and Molecular Genetics and Medicine, University of California Irvine, Irvine, California; Department of Epidemiology and Public Health, Yale University School of Public Health, New Haven, Connecticut; Departments of Fisheries and Wildlife and Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan

Search for other papers by Maria A. Diuk-Wasser in
Current site
Google Scholar
PubMed
Close
,
Durland Fish Departments of Microbiology and Molecular Genetics and Medicine, University of California Irvine, Irvine, California; Department of Epidemiology and Public Health, Yale University School of Public Health, New Haven, Connecticut; Departments of Fisheries and Wildlife and Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan

Search for other papers by Durland Fish in
Current site
Google Scholar
PubMed
Close
, and
Jean I. Tsao Departments of Microbiology and Molecular Genetics and Medicine, University of California Irvine, Irvine, California; Department of Epidemiology and Public Health, Yale University School of Public Health, New Haven, Connecticut; Departments of Fisheries and Wildlife and Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan

Search for other papers by Jean I. Tsao in
Current site
Google Scholar
PubMed
Close
Restricted access

The Lyme borreliosis agent Borrelia burgdorferi and the relapsing fever group species Borrelia miyamotoi co-occur in the United States. We used species-specific, quantitative polymerase chain reaction to study both species in the blood and skin of Peromyscus leucopus mice and host-seeking Ixodes scapularis nymphs at a Connecticut site. Bacteremias with B. burgdorferi or B. miyamotoi were most prevalent during periods of greatest activity for nymphs or larvae, respectively. Whereas B. burgdorferi was 30-fold more frequent than B. miyamotoi in skin biopsies and mice had higher densities of B. burgdorferi densities in the skin than in the blood, B. miyamotoi densities were higher in blood than skin. In a survey of host-seeking nymphs in 11 northern states, infection prevalences for B. burgdorferi and B. miyamotoi averaged ~0.20 and ~0.02, respectively. Co-infections of P. leucopus or I. scapularis with both B. burgdorferi and B. miyamotoi were neither more nor less common than random expectations.

Author Notes

Reprint requests: Alan Barbour, University of California Irvine, 3012 Hewitt, Irvine, CA 92697-4028.
  • 1

    Barbour AG, 2001. Borrelia: a diverse and ubiquitous genus of tick-borne pathogens. Scheld WM, Craig WA, Hughes JM, eds. Emerging Infections 5. Washington, DC: American Society for Microbiology Press, 153–174.

    • PubMed
    • Export Citation
  • 2

    Barbour AG, 2005. Relapsing fever. Goodman JL, Dennis D, Sonenshine DE, eds. Tick-Borne Diseases of Humans. Washington, DC: ASM Press, 268–291.

    • PubMed
    • Export Citation
  • 3

    Steere AC, Coburn J, Glickstein L, 2005. Lyme borreliosis. Goodman JL, Dennis D, Sonenshine DE, eds. Tick-Borne Diseases of Humans. Washington, DC: ASM Press, 176–206.

    • PubMed
    • Export Citation
  • 4

    Rich SM, Armstrong PM, Smith RD, Telford SR 3rd, 2001. Lone star tick-infecting borreliae are most closely related to the agent of bovine borreliosis. J Clin Microbiol 39 :494–497.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Barbour AG, Maupin GO, Teltow GJ, Carter CJ, Piesman J, 1996. Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: possible agent of a Lyme disease-like illness. J Infect Dis 173 :403–409.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Armstrong PM, Rich SM, Smith RD, Hartl DL, Spielman A, Telford SR 3rd, 1996. A new Borrelia infecting Lone Star ticks. Lancet 347 :67–68.

  • 7

    Varela-Stokes AS, 2007. Transmission of bacterial agents from lone star ticks to white-tailed deer. J Med Entomol 44 :478–483.

  • 8

    Bunikis J, Tsao J, Garpmo U, Berglund J, Fish D, Barbour AG, 2004. Typing of Borrelia relapsing fever group strains. Emerg Infect Dis 10 :1661–1664.

  • 9

    Fraenkel CJ, Garpmo U, Berglund J, 2002. Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J Clin Microbiol 40 :3308–3312.

  • 10

    Fukunaga M, Takahashi Y, Tsuruta Y, Matsushita O, Ralph D, McClelland M, Nakao M, 1995. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int J Syst Bacteriol 45 :804–810.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Mun J, Eisen RJ, Eisen L, Lane RS, 2006. Detection of a Borrelia miyamotoi sensu lato relapsing-fever group spirochete from Ixodes pacificus in California. J Med Entomol 43 :120–123.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Scoles GA, Papero M, Beati L, Fish D, 2001. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonotic Dis 1 :21–34.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Varela AS, Luttrell MP, Howerth EW, Moore VA, Davidson WR, Stallknecht DE, Little SE, 2004. First culture isolation of Borrelia lonestari, putative agent of southern tick-associated rash illness. J Clin Microbiol 42 :1163–1169.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Bunikis J, Barbour AG, 2005. Third Borrelia species in white-footed mice. Emerg Infect Dis 11 :1150–1151.

  • 15

    Tsao JI, Wootton JT, Bunikis J, Luna MG, Fish D, Barbour AG, 2004. An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proc Natl Acad Sci USA 101 :18159–18164.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Gatewood AG, Liebman KA, Vourc’h G, Bunikis J, Hamer SA, Cortinas R, Melton F, Cislo P, Kitron U, Tsao J, Barbour AG, Fish D, Diuk-Wasser MA, 2009. Climate and tick seasonality predict Borrelia burgdorferi genotype distribution. Appl Environ Microbiol 75 :2476–2483.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Zhioua E, Aeschlimann A, Gern L, 1994. Infection of field-collected Ixodes ricinus (Acari: Ixodidae) larvae with Borrelia burgdorferi in Switzerland. J Med Entomol 31 :763–766.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Patrican LA, 1997. Absence of Lyme disease spirochetes in larval progeny of naturally infected Ixodes scapularis (Acari:Ixodidae) fed on dogs. J Med Entomol 34 :52–55.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Nefedova VV, Korenberg EI, Gorelova NB, Kovalevskii YV, 2004. Studies on the transovarial transmission of Borrelia burgdorferi sensu lato in the taiga tick Ixodes persulcatus. Folia Parasitol (Praha) 51 :67–71.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Schwan TG, Battisti JM, Porcella SF, Raffel SJ, Schrumpf ME, Fischer ER, Carroll JA, Stewart PE, Rosa P, Somerville GA, 2003. Glycerol-3-phosphate acquisition in spirochetes: distribution and biological activity of glycerophosphodiester phosphodiesterase (GlpQ) among Borrelia species. J Bacteriol 185 :1346–1356.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Ramakrishnan U, 2001. Methods of controlling white-tailed deer. Front Plant Sci 53 :7.

  • 22

    Tsao J, Barbour AG, Luke CJ, Fikrig E, Fish D, 2001. OspA immunization decreases transmission of Borrelia burgdorferi spirochetes from infected Peromyscus leucopus mice to larval Ixodes scapularis ticks. Vector Borne Zoonotic Dis 1 :65–74.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Sinsky RJ, Piesman J, 1989. Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents. J Clin Microbiol 27 :1723–1727.

  • 24

    Pennington PM, Allred CD, West CS, Alvarez R, Barbour AG, 1997. Arthritis severity and spirochete burden are determined by serotype in the Borrelia turicatae-mouse model of Lyme disease. Infect Immun 65 :285–292.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Falco RC, Fish D, 1992. A comparison of methods for sampling the deer tick, Ixodes dammini, in a Lyme disease endemic area. Exp Appl Acarol 14 :165–173.

  • 26

    Diuk-Wasser MA, GatewoodAG, Cortinas MR,Yaremych-Hamer S, Tsao J, Kitron U, Hickling G, Brownstein JS, Walker E, Piesman J, Fish D, 2006. Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. J Med Entomol 43 :166–176.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Bunikis J, Tsao J, Luke CJ, Luna MG, Fish D, Barbour AG, 2004. Borrelia burgdorferi infection in a natural population of Peromyscus leucopus mice: a longitudinal study in an area where Lyme borreliosis is highly endemic. J Infect Dis 189 :1515–1523.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Beati L, Keirans JE, 2001. Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters. J Parasitol 87 :32–48.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Hanincova K, Kurtenbach K, Diuk-Wasser M, Brei B, Fish D, 2006. Epidemic spread of Lyme borreliosis, northeastern United States. Emerg Infect Dis 12 :604–611.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Comstedt P, Bergstrom S, Olsen B, Garpmo U, Marjavaara L, Mejlon H, Barbour AG, Bunikis J, 2006. Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerg Infect Dis 12 :1087–1095.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Barbour AG, 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57 :521–525.

  • 32

    Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG, 2004. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 150 :1741–1755.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Hutchinson G, 1959. Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93 :145–159.

  • 34

    Anderson JF, Flavell RA, Magnarelli LA, Barthold SW, Kantor FS, Wallich R, Persing DH, Mathiesen D, Fikrig E, 1996. Novel Borrelia burgdorferi isolates from Ixodes scapularis and Ixodes dentatus ticks feeding on humans. J Clin Microbiol 34 :524–529.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Goethert HK, Telford SR 3rd, 2003. Enzootic transmission of Babesia divergens among cottontail rabbits on Nantucket Island, Massachusetts. Am J Trop Med Hyg 69 :455–460.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Schneider BS, Zeidner NS, Burkot TR, Maupin GO, Piesman J, 2000. Borrelia isolates in Northern Colorado identified as Borrelia bissettii. J Clin Microbiol 38 :3103–3105.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Rijpkema S, Golubic D, Molkenboer M, Verbeek-De Kruif N, Schellekens J, 1996. Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Exp Appl Acarol 20 :23–30.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Kurtenbach K, De Michelis S, Sewell HS, Etti S, Schafer SM, Hails R, Collares-Pereira M, Santos-Reis M, Hanincova K, Labuda M, Bormane A, Donaghy M, 2001. Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl Environ Microbiol 67 :4926–4929.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Vennestrom J, Egholm H, Jensen PM, 2008. Occurrence of multiple infections with different Borrelia burgdorferi genospecies in Danish Ixodes ricinus nymphs. Parasitol Int 57 :32–37.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Kurtenbach K, Hanincova K, Tsao JI, Margos G, Fish D, Ogden NH, 2006. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat Rev Microbiol 4 :660–669.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Donahue JG, Piesman J, Spielman A, 1987. Reservoir competence of white-footed mice for Lyme disease spirochetes. Am J Trop Med Hyg 36 :92–96.

  • 42

    Richter D, Klug B, Spielman A, Matuschka FR, 2004. Adaptation of diverse lyme disease spirochetes in a natural rodent reservoir host. Infect Immun 72 :2442–2444.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Hanincova K, Ogden NH, Diuk-Wasser M, Pappas CJ, Iyer R, Fish D, Schwartz I, Kurtenbach K, 2008. Fitness variation of Borrelia burgdorferi sensu stricto strains in mice. Appl Environ Microbiol 74 :153–157.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Piesman J, Gern L, 2004. Lyme borreliosis in Europe and North America. Parasitology 129 (Suppl):S191–S220.

  • 45

    Woolhouse ME, Taylor LH, Haydon DT, 2001. Population biology of multihost pathogens. Science 292 :1109–1112.

  • 46

    Krampitz HE, 1986. In vivo isolation and maintenance of some wild strains of European hard tick spirochetes in mammalian and arthropod hosts. A parasitologist’s view. Zentralbl Bakteriol Mikrobiol Hyg [A] 263 :21–28.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Stanek G, Burger I, Hirschl A, Wewalka G, Radda A, 1986. Borrelia transfer by ticks during their life cycle. Studies on laboratory animals. Zentralbl Bakteriol Mikrobiol Hyg [A] 263 :29–33.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48

    Richter D, Matuschka FR, 2006. Modulatory effect of cattle on risk for Lyme disease. Emerg Infect Dis 12 :1919–1923.

  • 49

    Wodecka B, 2007. [Significance of red deer (Cervus elaphus) in the ecology of Borrelia burgdorferi sensu lato]. Wiad Parazytol 53 :231–237.

  • 50

    Burgdorfer W, Gage KL, 1987. Susceptibility of the hispid cotton rat (Sigmodon hispidus) to the Lyme disease spirochete (Borrelia burgdorferi). Am J Trop Med Hyg 37 :624–628.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51

    Ullmann AJ, Gabitzsch ES, Schulze TL, Zeidner NS, Piesman J, 2005. Three multiplex assays for detection of Borrelia burgdorferi sensu lato and Borrelia miyamotoi sensu lato in field-collected Ixodes nymphs in North America. J Med Entomol 42 :1057–1062.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52

    Richter D, Schlee DB, Matuschka FR, 2003. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerg Infect Dis 9 :697–701.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53

    Hulinska D, Votypka J, Kriz B, Holinkova N, Novakova J, Hulinsky V, 2007. Phenotypic and genotypic analysis of Borrelia spp. isolated from Ixodes ricinus ticks by using electrophoretic chips and real-time polymerase chain reaction. Folia Microbiol (Praha) 52 :315–324.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54

    Anderson JF, Magnarelli LA, Burgdorfer W, Barbour AG, 1983. Spirochetes in Ixodes dammini and mammals from Connecticut. Am J Trop Med Hyg 32 :818–824.

  • 55

    Walker ED, Smith TW, DeWitt J, Beaudo DC, McLean RG, 1994. Prevalence of Borrelia burgdorferi in host-seeking ticks (Acari: Ixodidae) from a Lyme disease endemic area in northern Michigan. J Med Entomol 31 :524–528.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56

    Wang G, Liveris D, Brei B, Wu H, Falco RC, Fish D, Schwartz I, 2003. Real-time PCR for simultaneous detection and quantification of Borrelia burgdorferi in field-collected Ixodes scapularis ticks from the Northeastern United States. Appl Environ Microbiol 69 :4561–4565.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57

    Ornstein K, Barbour AG, 2006. A reverse transcriptase-polymerase chain reaction assay of Borrelia burgdorferi 16S rRNA for highly sensitive quantification of pathogen load in a vector. Vector Borne Zoonotic Dis 6 :103–112.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 58

    Brunet LR, Spielman A, Telford SR 3rd, 1995. Short report: density of Lyme disease spirochetes within deer ticks collected from zoonotic sites. Am J Trop Med Hyg 53 :300–302.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 59

    Burkot TR, Patrican L, Piesman J, 1994. Field trial of an outer surface protein A (OspA) antigen-capture enzyme-linked immunosorbent assay (ELISA) to detect Borrelia burgdorferi in Ixodes scapularis. Am J Trop Med Hyg 50 :354–358.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 60

    Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP, 1982. Lyme disease—a tick-borne spirochetosis? Science 216 :1317–1319.

  • 61

    De Silva AM, Fikrig E, 1995. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am J Trop Med Hyg 53 :397–404.

  • 62

    Lane RS, Burgdorfer W, 1987. Transovarial and transstadial passage of Borrelia burgdorferi in the western black-legged tick, Ixodes pacificus (Acari: Ixodidae). Am J Trop Med Hyg 37 :188–192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 63

    Burgdorfer W, Lane RS, Barbour AG, Gresbrink RA, Anderson JR, 1985. The western black-legged tick, Ixodes pacificus: a vector of Borrelia burgdorferi. Am J Trop Med Hyg 34 :925–930.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 64

    Fine PE, 1975. Vectors and vertical transmission: an epidemiologic perspective. Ann N Y Acad Sci 266 :173–194.

Past two years Past Year Past 30 Days
Abstract Views 1271 940 30
Full Text Views 1162 33 6
PDF Downloads 565 39 6
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save