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Getting under the birds’ skin: tissue tropism of Borrelia burgdorferi s.l. in naturally and experimentally infected avian hosts

  • Host Microbe Interactions
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Abstract

Wild birds are frequently exposed to the zoonotic tick-borne bacteria Borrelia burgdorferi sensu lato (s.l.), and some bird species act as reservoirs for some Borrelia genospecies. Studying the tropism of Borrelia in the host, how it is sequestered in different organs, and whether it is maintained in circulation and/or in the host’s skin is important to understand pathogenicity, infectivity to vector ticks and reservoir competency.

We evaluated tissue dissemination of Borrelia in blackbirds (Turdus merula) and great tits (Parus major), naturally and experimentally infected with Borrelia genospecies from enzootic foci. We collected both minimally invasive biological samples (feathers, skin biopsies and blood) and skin, joint, brain and visceral tissues from necropsied birds. Infectiousness of the host was evaluated through xenodiagnoses and infection rates in fed and moulted ticks. Skin biopsies were the most reliable method for assessing avian hosts’ Borrelia infectiousness, which was supported by the agreement of infection status results obtained from the analysis of chin and lore skin samples from necropsied birds and of their xenodiagnostic ticks, including a significant correlation between the estimated concentration of Borrelia genome copies in the skin and the Borrelia infection rate in the xenodiagnostic ticks. This confirms a dermatropism of Borrelia garinii, B. valaisiana and B. turdi in its avian hosts. However, time elapsed from exposure to Borrelia and interaction between host species and Borrelia genospecies may affect the reliability of skin biopsies. The blood was not useful to assess infectiousness of birds, even during the period of expected maximum spirochetaemia. From the tissues sampled (foot joint, liver, spleen, heart, kidney, gut and brain), Borrelia was detected only in the gut, which could be related with infection mode, genospecies competition, genospecies-specific seasonality and/or excretion processes.

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Data Availability Statement

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We gratefully acknowledge Joris Elst and Sophie Philtjes for technical support and Maria Salomé Gomes, Lara Augusto, Natalie Van Houtte, Aleksandra Krawczyk and Manoj Fonville for help with the laboratory analyses.

Funding

This study received financial support from Fundação para a Ciência e a Tecnologia by the strategic program of MARE (MARE - UID/MAR/04292/2019), the fellowship to Ana Cláudia Norte (SFRH/BPD/108197/2015) and from the Portuguese National Institute of Health Doutor Ricardo Jorge. Dieter Heylen is funded by the Marie Sklodowska-Curie Actions (EU-Horizon 2020, Individual Global Fellowship, project no. 799609), the Fund for Scientific Research – Flanders (FWO) and the Bill & Melinda Gates Foundation.

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Authors and Affiliations

  1. Marine and Environmental Sciences Centre, Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Largo Marquês de Pombal, 3004-517, Coimbra, Portugal

    Ana Cláudia Norte, Pedro Miguel Araújo & Jaime Albino Ramos

  2. Centre for Vectors and Infectious Diseases Dr. Francisco Cambournac, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal

    Ana Cláudia Norte, Isabel Lopes de Carvalho & Maria Sofia Núncio

  3. Evolutionary Ecology Group, Department of Biology, University of Antwerp, Universiteitsplein 1, 2610, Wilrijk, Belgium

    Erik Matthysen

  4. Centre for Infectious Disease Control (CIb), vhNational Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands

    Hein Sprong

  5. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

    Dieter Heylen

  6. Interuniversity Institute for Biostatistics and Statistical Bioinformatics, Hasselt University, Diepenbeek, Belgium

    Dieter Heylen

Authors
  1. Ana Cláudia Norte
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  2. Isabel Lopes de Carvalho
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  3. Maria Sofia Núncio
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  4. Pedro Miguel Araújo
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  5. Erik Matthysen
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  6. Jaime Albino Ramos
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  7. Hein Sprong
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  8. Dieter Heylen
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Corresponding author

Correspondence to Ana Cláudia Norte.

Ethics declarations

All bird captures were performed under licences of the Agency for Nature and Forests (Flemish Government, Belgium) and experimental setups were approved by the Ethics Committee for Animal Experiments of the University of Antwerp (2009-32 and 2014-49).

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The authors declare that they have no conflict of interest.

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Norte, A.C., Lopes de Carvalho, I., Núncio, M.S. et al. Getting under the birds’ skin: tissue tropism of Borrelia burgdorferi s.l. in naturally and experimentally infected avian hosts. Microb Ecol 79, 756–769 (2020). https://doi.org/10.1007/s00248-019-01442-3

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  • DOI: https://doi.org/10.1007/s00248-019-01442-3

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