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Ixodes scapularis does not harbor a stable midgut microbiome

The ISME Journalvolume 12pages25962607 (2018) | Download Citation

Abstract

Hard ticks of the order Ixodidae serve as vectors for numerous human pathogens, including the causative agent of Lyme Disease Borrelia burgdorferi. Tick-associated microbes can influence pathogen colonization, offering the potential to inhibit disease transmission through engineering of the tick microbiota. Here, we investigate whether B. burgdorferi encounters abundant bacteria within the midgut of wild adult Ixodes scapularis, its primary vector. Through the use of controlled sequencing methods and confocal microscopy, we find that the majority of field-collected adult I. scapularis harbor limited internal microbial communities that are dominated by endosymbionts. A minority of I. scapularis ticks harbor abundant midgut bacteria and lack B. burgdorferi. We find that the lack of a stable resident midgut microbiota is not restricted to I. scapularis since extension of our studies to I. pacificus, Amblyomma maculatum, and Dermacentor spp showed similar patterns. Finally, bioinformatic examination of the B. burgdorferi genome revealed the absence of genes encoding known interbacterial interaction pathways, a feature unique to the Borrelia genus within the phylum Spirochaetes. Our results suggest that reduced selective pressure from limited microbial populations within ticks may have facilitated the evolutionary loss of genes encoding interbacterial competition pathways from Borrelia.

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Acknowledgements

We thank the Fred Hutch Experimental Histopathology Core facility and Dan Long at Rocky Mountain Labs for tick sectioning and slide preparation. We thank Barbara Simon, Jim Ruppa, David Simon, and June Reznikoff for their indefatigable efforts in collection of ticks from the Klickitat River “Ant Ranch”, and Susan Little for collection of Amblyomma ticks. We thank the UW Keck Imaging Center for providing equipment and assistance in confocal microscopy and acknowledge its support from the NIH (S10 OD016240). We thank Mr. DNA for sequencing support. We are grateful to our colleagues for careful review of the manuscript, and members of the Mougous lab for helpful discussions. This work was supported by the National Institutes of Health grant R21AI114923 (JDM). JDM holds an Investigator in the Pathogenesis of Infectious Disease Award from the Burroughs Wellcome Fund (BWF 1010010) and is an HHMI investigator. BDR was supported by a Simons Foundation-sponsored Life Sciences Research Foundation postdoctoral fellowship. SC was supported by the Program for Breakthrough Biomedical Research, which is partially funded by the Sandler Foundation.

Author contributions

B.D.R., S.C. and J.D.M. conceived the study. B.D.R., S.C. and J.D.M. designed the study. B.D.R., S.C., B.H. and M.C.R. conducted experimental work. X.L., T.J., D.N. and J.B. collected ticks. B.D.R., S.C. and J.D.M. wrote the paper. All authors read and approved the paper.

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Affiliations

  1. Department of Microbiology, School of Medicine, University of Washington, Seattle, WA, 98195, USA

    • Benjamin D. Ross
    • , Matthew C. Radey
    •  & Joseph D. Mougous
  2. Department of Biochemistry and Biophysics, University of California, San Francisco, CA, USA

    • Beth Hayes
    •  & Seemay Chou
  3. Department of Entomology, University of Wisconsin, Madison, WI, 53706, USA

    • Xia Lee
    •  & Susan Paskewitz
  4. Department of Entomology, University of Illinois Urbana-Champaign, Urbana, IL, 61801, USA

    • Tanya Josek
  5. Vectorborne Diseases Unit, Minnesota Department of Health, St. Paul, MN, 55164, USA

    • Jenna Bjork
    •  & David Neitzel
  6. Howard Hughes Medical Institute, School of Medicine, University of Washington, Seattle, WA, 98195, USA

    • Joseph D. Mougous

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The authors declare that they have no conflict of interest.

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Correspondence to Benjamin D. Ross or Seemay Chou or Joseph D. Mougous.

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https://doi.org/10.1038/s41396-018-0161-6