Variation among strains of Borrelia burgdorferi in host tissue abundance and lifetime transmission determine the population strain structure in nature.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
08 2023
Historique:
received: 07 04 2023
accepted: 23 07 2023
revised: 01 09 2023
medline: 4 9 2023
pubmed: 22 8 2023
entrez: 22 8 2023
Statut: epublish

Résumé

Pathogen life history theory assumes a positive relationship between pathogen load in host tissues and pathogen transmission. Empirical evidence for this relationship is surprisingly rare due to the difficulty of measuring transmission for many pathogens. The comparative method, where a common host is experimentally infected with a set of pathogen strains, is a powerful approach for investigating the relationships between pathogen load and transmission. The validity of such experimental estimates of strain-specific transmission is greatly enhanced if they can predict the pathogen population strain structure in nature. Borrelia burgdorferi is a multi-strain, tick-borne spirochete that causes Lyme disease in North America. This study used 11 field-collected strains of B. burgdorferi, a rodent host (Mus musculus, C3H/HeJ) and its tick vector (Ixodes scapularis) to determine the relationship between pathogen load in host tissues and lifetime host-to-tick transmission (HTT). Mice were experimentally infected via tick bite with 1 of 11 strains. Lifetime HTT was measured by infesting mice with I. scapularis larval ticks on 3 separate occasions. The prevalence and abundance of the strains in the mouse tissues and the ticks were determined by qPCR. We used published databases to obtain estimates of the frequencies of these strains in wild I. scapularis tick populations. Spirochete loads in ticks and lifetime HTT varied significantly among the 11 strains of B. burgdorferi. Strains with higher spirochete loads in the host tissues were more likely to infect feeding larval ticks, which molted into nymphal ticks that had a higher probability of B. burgdorferi infection (i.e., higher HTT). Our laboratory-based estimates of lifetime HTT were predictive of the frequencies of these strains in wild I. scapularis populations. For B. burgdorferi, the strains that establish high abundance in host tissues and that have high lifetime transmission are the strains that are most common in nature.

Identifiants

pubmed: 37607182
doi: 10.1371/journal.ppat.1011572
pii: PPATHOGENS-D-23-00607
pmc: PMC10473547
doi:

Banques de données

Dryad
['10.5061/dryad.3r2280gnh']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011572

Informations de copyright

Copyright: © 2023 Zinck et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors declare that they have no competing interests.

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Auteurs

Christopher B Zinck (CB)

Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

Prasobh Raveendram Thampy (P)

Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

Eva-Maria E Uhlemann (EE)

Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

Hesham Adam (H)

Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

Jenny Wachter (J)

Vaccine and Infectious Disease Organization, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

Danae Suchan (D)

Institute for Microbial Systems and Society, Faculty of Science, University of Regina, Regina, Saskatchewan, Canada.
Department of Biology, University of Regina, Regina, Saskatchewan, Canada.

Andrew D S Cameron (ADS)

Institute for Microbial Systems and Society, Faculty of Science, University of Regina, Regina, Saskatchewan, Canada.
Department of Biology, University of Regina, Regina, Saskatchewan, Canada.

Ryan O M Rego (ROM)

Biology Centre, Institute of Parasitology, Czech Academy of Sciences, České Budějovice, Czech Republic.
Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic.

Dustin Brisson (D)

Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Catherine Bouchard (C)

Public Health Risk Sciences, National Microbiology Laboratory, Public Health Agency of Canada, St Hyacinthe, Quebec, Canada.
Groupe de recherche en épidémiologie des zoonoses et santé publique (GREZOSP), Faculté de Médecine Vétérinaire, Université de Montréal, Montreal, Canada.

Nicholas H Ogden (NH)

Public Health Risk Sciences, National Microbiology Laboratory, Public Health Agency of Canada, St Hyacinthe, Quebec, Canada.
Groupe de recherche en épidémiologie des zoonoses et santé publique (GREZOSP), Faculté de Médecine Vétérinaire, Université de Montréal, Montreal, Canada.
Centre de recherche en santé publique (CReSP), Université de Montréal, Montreal, QC, Canada.

Maarten J Voordouw (MJ)

Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

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