Characterization of Transstadial Transmission of Rickettsia Amblyommatis in Haemaphysalis Longicornis Using Optimized Artificial Membrane Feeding System

Justin Le Center for Infectious Diseases, Stony Brook University, Stony Brook, New York;
Department of Microbiology and Immunology, Stony Brook University, Stony Brook, New York;

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Molly B. Thompson Center for Infectious Diseases, Stony Brook University, Stony Brook, New York;
Department of Microbiology and Immunology, Stony Brook University, Stony Brook, New York;

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Wan-Yi Yen Center for Infectious Diseases, Stony Brook University, Stony Brook, New York;
Department of Microbiology and Immunology, Stony Brook University, Stony Brook, New York;

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Smruti Mishra Center for Infectious Diseases, Stony Brook University, Stony Brook, New York;
Department of Microbiology and Immunology, Stony Brook University, Stony Brook, New York;

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David Carlson Institute for Advanced Computational Science, Stony Brook University, Stony Brook, New York;

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Andrew S. Handel Department of Pediatrics, Stony Brook University, Stony Brook, New York

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Erich R. Mackow Center for Infectious Diseases, Stony Brook University, Stony Brook, New York;
Department of Microbiology and Immunology, Stony Brook University, Stony Brook, New York;

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Jorge L. Benach Center for Infectious Diseases, Stony Brook University, Stony Brook, New York;
Department of Microbiology and Immunology, Stony Brook University, Stony Brook, New York;

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Ilia Rochlin Center for Infectious Diseases, Stony Brook University, Stony Brook, New York;
Department of Microbiology and Immunology, Stony Brook University, Stony Brook, New York;

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Hwan Keun Kim Center for Infectious Diseases, Stony Brook University, Stony Brook, New York;
Department of Microbiology and Immunology, Stony Brook University, Stony Brook, New York;

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Ticks are blood-feeding arthropods and serve as vectors and reservoirs for diverse pathogens. Recent environmental changes have triggered the invasion of ticks into new geographical areas, prompting a public health alert for increased risk of tick-borne diseases. Amblyomma (A.) americanum (lone star tick) has emerged as the most common human-biting tick species in the eastern United States. Amblyomma americanum transmits multiple pathogens, including Rickettsia (R.) amblyommatis, the suspected cause of mild spotted fever rickettsiosis. As an invasive tick species, Haemaphysalis (H.) longicornis (longhorned tick) has rapidly invaded and expanded to high densities in the eastern United States. Haemaphysalis longicornis and A. americanum often share the habitat with preferential feeding on mid- to large-sized animals, such as white-tailed deer. This sympatric association of H. longicornis with A. americanum raises the potential for H. longicornis to acquire pathogens native to A. americanum during blood-feeding on the same host. In its native ranges, H. longicornis transmits R. japonica and R. heilongjiangensis. However, it remains unclear whether H. longicornis can transmit R. amblyommatis abundantly present in A. americanum in the United States. Using artificial membrane feeding, we establish that R. amblyommatis can stably colonize H. longicornis without altering feeding and molting behaviors. Transovarial transmission of R. amblyommatis did not occur in parthenogenetic H. longicornis. However, R. amblyommatis successfully invaded the midgut and salivary glands of H. longicornis, key organ tissues of rickettsial replication and horizontal transmission. Our results suggest that H. longicornis may serve as a vector, but not as a reservoir, for R. amblyommatis transmission.

Author Notes

Financial support: This article received support from the National Institute of Allergy and Infectious Diseases (AI152208 and AI169287 to H. K. Kim) of the NIH and funding from the Office of the Vice President for Research Seed Grant Program (to H. K. Kim) and Biomedical Sciences Innovation Fund (to H. K. Kim, J. L. Benach, E. R. Mackow, and A. S. Handel), Stony Brook University.

Disclosure: The authors declare no competing interests.

Data availability: The data and unique materials that support the findings of this study are available from the corresponding authors upon request.

Current contact information: Justin Le, Molly B. Thompson, Wan-Yi Yen, Smruti Mishra, Erich R. Mackow, and Jorge L. Benach, Center for Infectious Diseases, Stony Brook University, Stony Brook, NY, E-mails: thanh.le.justin@gmail.com, thompson.molly@gmail.com, wanyi0529@gmail.com, smruti.mishra@stonybrook.edu, erich.mackow@stonybrook.edu, and jorge.benach@stonybrook.edu. David Carlson, Institute for Advanced Computational Science, Stony Brook University, Stony Brook, NY, E-mail: david.carlson@stonybrook.edu. Andrew S. Handel, Department of Pediatrics, Stony Brook University, Stony Brook, NY, E-mail: andrew.handel@stonybrookmedicine.edu. Ilia Rochlin and Hwan Keun Kim, Centers for Molecular Medicine, Stony Brook University, Stony Brook, NY, E-mails: ilia.rochlin@stonybrook.edu and hwan.kim@stonybrook.edu.

Address correspondence to Ilia Rochlin or Hwan Keun Kim, 238 Centers for Molecular Medicine, Stony Brook University, Stony Brook, NY 11794. E-mails: ilia.rochlin@stonybrook.edu and hwan.kim@stonybrook.edu
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