The ecologic, epidemiologic and molecular aspects of Borrelia burgdorferi sensu lato: consequence of

diversity, distribution and genome variations of Lyme borreliosis spirochetes.

Biology Centre CAS, Institute of Parasitology,

Laboratory of Molecular Ecology of Vectors and PathogensBranisovska 31, 37005, Ceske Budejovice, Czech Republic

natasha@paru.cas.cz

Natasha Rudenko

Susan Oliver

vector host

pathogen

What factors make the Lyme borreliosis system so successful?

Diverse interaction that occurs between spirochete, thetick vector and the host makes Borrelia an elusive pathogen!!!

TICK FACTOIDS

Approximately 900 tick species exists; 10% are of concern to humans.

All ticks are obligate, nonpermanent blood feeders; hosts include all terrestrial vertebrates.

Ticks are vectors of more kinds of microorganisms than any other arthropod taxon.

Worldwide distribution from arctic to antarctic.

The most important genera of hard ticks are:Amblyomma, Boophilus, Dermacentor,

Haemaphysalis, Hyalomma, Ixodes and Rhipicephalus.

The worldwide distribution of major Ixodes tick species

of medical and veterinary importance(“bridge” vectors)

I.pacificus

I.scapularis I.ricinus

I.persulcatus

adapted from B. Rosner 2006; www.lymebook.com

Ticks, important as “maintenance” vectors of Borrelia burgdorferi

(usually non-human biting)

I. hexagonus, I. trianguliceps, I. uriae, H. concinna, –Europe

I. minor, I. affinis, I. dentatus, I. spinipalpis - USA

I. turdus, I. ovatus, I. columnae, I. tanuki – Japan

I. nipponensis –Korea, Japan

I. granulatus, I. monospinosus – China, Korea

I. moschiferi, H. concinna, H. longicornis, H. bispinosa - China

In some areas maintenance vectors appear to be more important in the enzootic cycle of B. burgdorferi s.l. than the ‘bridge’ vectors that feed on the same hosts and bite humans

(Oliver, 1996).

Tick species experimentally confirmed as vectors of Borrelia burgdorferi sensu lato (Eisen&Lane)

Tick specie Bb SL Bb ss B. afzelii B. garinii B. bissettii

I. affinis ☺

I. angustus ☺ ☺

I. dentatus ☺

I. hexagonus ☺

I. jellisoni ☺

I. minor ☺ ☺

I. muris ☺

I. pacificus ☺ ☺

I. persulcatus ☺

I. ricinus ☺ ☺ ☺ ☺ ☺

I. scapularis ☺ ☺ ☺ ☺ ☺

I. spinipalpis ☺ ☺

I. sinensis ☺

Tick species experimentally confirmed as vectors of Borrelia burgdorferi sensu lato (Eisen&Lane)

Tick specie Bb SL Bb ss B. afzelii B. garinii B. bissettii

I. affinis ☺

I. angustus ☺ ☺

I. dentatus ☺

I. hexagonus ☺

I. jellisoni ☺

I. minor ☺ ☺

I. muris ☺

I. pacificus ☺ ☺

I. persulcatus ☺

I. ricinus ☺ ☺ ☺ ☺ ☺

I. scapularis ☺ ☺ ☺ ☺ ☺

I. spinipalpis ☺ ☺

I. sinensis ☺

Reservoir hosts of Borrelia burgdorferi sensu lato

Efficient reservoir hosts of B. burgdorferi s.l. share several characteristics.

They are abundant, large number of them is naturally infected and serves as hosts to numerous vector competent ticks.

They do not usually become resistant to repeated tick feeding.

They are readily infected and remain infected and infective to competent tick vectors for long periods of time, often for life.

Lyme disease spirochetes infect diverse animal species, but not all of them serve as competent hosts.

Reservoir Hosts- mammals; -rodents; -birds; -lizards;

Pattern of response of vertebrate serum complement to

B. burgdorferi s.l. spirochetes.

Ticha et al., 2016

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Expanding complex of Borrelia burgdorferi sensu lato spirochetes

Currently known spirochete species from the Borrelia burgdorferi sensu lato complex

Spirochete species from the B. burgdorferi sensu lato complex involved in LB worldwide

Altering the level of gene expression in response to changes in temperature, pH, salts, nutrient

content, host and vector dependent factors spirochetes developed strategies to sense and

survive in these diverse environments, often changing their phenotypes….

The geographical distribution of Borrelia burgdorferi sensu lato 10 years ago

(K. Kurtenbach et al., 2006)

The geographical distribution of Borrelia burgdorferi sensu lato 5 years ago

(G. Margos et al., 2011)

Map showing the updated distribution of the LB species based on published and unpublished results (2016)

The present geographical distribution of Borrelia burgdorferi sensu lato -updates

Map showing the updated distribution of the LB species based on published and unpublished results (2016)

The present geographical distribution of Borrelia burgdorferi sensu lato -updates

Borrelia finlandensis, 2011

Borrelia chilensis, 2014

Borrelia mayoni, 2016

New species from B. burgdorferi sensu lato complex

"The spread of Lyme disease is driven, in part, by climate change, as the tick vector spreadsnorthwards from endemic areas of the United States" (Steven Sternthal)

Main migration flyways

The Atlantic Flyway is a bird migration route that generally follows the Atlantic Coast of North America and the Appalachian Mountains.

The migration route tends to narrow considerably in the southern U.S.A. in the states of Virginia, North Carolina, South Carolina, Georgia, and Florida. It serves as avian superhighway’s for 500 +

bird species and millions of individual birds.

The diversity of spirochetes from B. burgdorferi sensu lato in the United States

(adapted from G. Margos et al., 2010)

B. garinii

B. afzelii

B. kurtenbachii

B. mayonii

Worldwide frequency of B. burgdorferi ospC types

B. burgdorferi ospC allelesdetected in southeastern USA

Rudenko et al., 2013

B. burgdorferi ospC alleles detected in Canada

Ogden et al., 2011

Rudenko et al., 2013

Some spirochete complexes were believed to be restricted:

exclusively to North America - B1, C, D, F, G, H, I, J, N, and U –

OR

exclusively to Europe:- B2, S, L, Q, and V-

three ospC types - A, E, and K- were previously detected on both continents

Geographic distribution of rare ospC allele in N. America

A significant spatial cluster of ticks infected with B. burgdorferi carrying rare allele L was detected in Canada and in the southeastern USA (indicated by the black ellipses)

MLST

locus

sample

uvrA rplB pepX clpX ospC

allele

Bb316

PubMLST

Allele

distribution

GenBank

best match

(strains)

KU577579

allele 19

USA(CT,NY,

PA), Canada

M11p†,

CA382, B31

KU577578

allele 1

USA(CT,NY,

MA,MD,IL,

MN,MI,WI, CA),

Canada, Europe

M6p†, M11p†

KU577577

allele1

USA(CT,NY,

PA,VT,WI,

MA,ME,MN,

CA), Canada,

Europe

M11p†, M6p†

CA382, B31

KU577576

allele1

USA(CT,NY,

PA,WI, MI,

ME,MN,IN,

VT,MA,CA)

Canada,

Europe

M11p†, B31,

M6p†,CA382

A

Bb324

PubMLST

Allele

distribution

GenBank

best match

(strains)

KU598201

allele 1

USA(NY,CT,

ME, VT, PA,

MA, MD),

Canada,

Europe§

M11p†,

B31, CA382

KT598395

allele 1

as Bb316

M11p†,

CA382, B31

N/A N/A M

Bb327

PubMLST

Allele

distribution

GenBank

best match

(strains)

KU598202

allele 19

as Bb316

M11p†,

CA382, B31

KT598396

allele 1

as Bb316

as Bb324

M11p†,

CA382, B31

N/A N/A A

B. burgdorferi sensu stricto detected in A. americanum ticksin the southeastern United States

A hypothesis for the migration route of Borrelia between the continents was proposed and the first evidences of trans-oceanic dispersals of B. burgdorferi sensu stricto were presented almost 15 years ago.

(Foretz et al., 1997; Ras et al., 1997; Postic et al., 1999; Marti et al., 1997; Qiu et al., 2008).

The worldwide distribution of Borrelia is supported by long-distance transmission of infected ticks by migrating hosts.

Marie Vancová

Libor Grubhoffer and James H. Oliver Jr.

Marina Golovchenko

ACKNOWLEDGEMENTS

Where Lyme disease is absent:Is it the tick,

the vertebrate host, or just a matter of time?

ESA, 2004

"Absence of proof is not proof of absence."

- Dr. Edwin J. Masters, M.D.

THANK YOU FOR YOUR ATTENTION!

natasha@paru.cas.cz