Document Type

Article

Publication Date

2022

DOI

10.1186/s40168-022-01378-w

Publication Title

Microbiome

Volume

10

Issue

1

Pages

173 (1-17)

Abstract

Background

Ixodes scapularis is the predominant tick vector of Borrelia burgdorferi, the agent of Lyme disease, in the USA. Molecular interactions between the tick and B. burgdorferi orchestrate the migration of spirochetes from the midgut to the salivary glands—critical steps that precede transmission to the vertebrate host. Over the last decade, research efforts have invoked a potential role for the tick microbiome in modulating tick-pathogen interactions.

Results

Using multiple strategies to perturb the microbiome composition of B. burgdorferi-infected nymphal ticks, we observe that changes in the microbiome composition do not significantly influence B. burgdorferi migration from the midgut, invasion of salivary glands, or transmission to the murine host. We also show that within 24 and 48 h of the onset of tick feeding, B. burgdorferi spirochetes are within the peritrophic matrix and epithelial cells of the midgut in preparation for exit from the midgut.

Conclusions

This study highlights two aspects of tick-spirochete interactions: (1) environmental bacteria associated with the tick do not influence spirochete transmission to the mammalian host and (2) the spirochete may utilize an intracellular exit route during migration from the midgut to the salivary glands, a strategy that may allow the spirochete to distance itself from microbiota in the midgut lumen effectively. This may explain in part, the inability of environment-acquired midgut microbiota to significantly influence spirochete transmission. Unraveling a molecular understanding of this exit strategy will be critical to gain new insights into the biology of the spirochete and the tick.

Rights

This article is licensed under a Creative Commons Attribution 4.0 International (CC BY 4.0) License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

The Creative Commons Public Domain Dedication (CC0 1.0) waiver applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Data Availability

Article States: "All data generated in this work will be readily shared and available upon request. The sequence data has been deposited in the NCBI Biorepository database. The accession number for the BioProject is PRJNA232504."

Corresponding author: Sukanya Narasimhan

Link to BioProject accession number PRJNA232504 as referenced in the article is: https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA232504

Original Publication Citation

Narasimhan, S., Rajeevan, N., Graham, M., Wu, M.-J., DePonte, K., Marion, S., Masson, O., O’Neal, A. J., Pedra, J. H. F., Sonenshine, D. E., & Fikrig, E. (2022). Tick transmission of Borrelia burgdorferi to the murine host is not influenced by environmentally acquired midgut microbiota. Microbiome, 10(1), 1-17, Article 173. https://doi.org/10.1186/s40168-022-01378-w

ORCID

0000-0001-9370-918X (Sonenshine)

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