Tick hemocytes have a pleiotropic role in microbial infection and arthropod fitness

Agustin Rolandelli, Hanna J. Laukaitis-Yousey, Haikel N. Bogale, Nisha Singh, Sourabh Samaddar, Anya J. O’Neal, Camila R. Ferraz, Matthew Butnaru, Enzo Mameli, Baolong Xia, M. Tays Mendes, L. Rainer Butler, Liron Marnin, Francy E. Cabrera Paz, Luisa M. Valencia, Vipin S. Rana, Ciaran Skerry, Utpal Pal, Stephanie E. Mohr, Norbert Perrimon, David Serre and Joao H. F. Pedra ()
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Agustin Rolandelli: University of Maryland School of Medicine
Hanna J. Laukaitis-Yousey: University of Maryland School of Medicine
Haikel N. Bogale: University of Maryland School of Medicine
Nisha Singh: University of Maryland School of Medicine
Sourabh Samaddar: University of Maryland School of Medicine
Anya J. O’Neal: University of Maryland School of Medicine
Camila R. Ferraz: University of Maryland School of Medicine
Matthew Butnaru: Blavatnik Institute, Harvard Medical School
Enzo Mameli: Blavatnik Institute, Harvard Medical School
Baolong Xia: Blavatnik Institute, Harvard Medical School
M. Tays Mendes: University of Maryland School of Medicine
L. Rainer Butler: University of Maryland School of Medicine
Liron Marnin: University of Maryland School of Medicine
Francy E. Cabrera Paz: University of Maryland School of Medicine
Luisa M. Valencia: University of Maryland School of Medicine
Vipin S. Rana: University of Maryland
Ciaran Skerry: University of Maryland School of Medicine
Utpal Pal: University of Maryland
Stephanie E. Mohr: Blavatnik Institute, Harvard Medical School
Norbert Perrimon: Blavatnik Institute, Harvard Medical School
David Serre: University of Maryland School of Medicine
Joao H. F. Pedra: University of Maryland School of Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Uncovering the complexity of systems in non-model organisms is critical for understanding arthropod immunology. Prior efforts have mostly focused on Dipteran insects, which only account for a subset of existing arthropod species in nature. Here we use and develop advanced techniques to describe immune cells (hemocytes) from the clinically relevant tick Ixodes scapularis at a single-cell resolution. We observe molecular alterations in hemocytes upon feeding and infection with either the Lyme disease spirochete Borrelia burgdorferi or the rickettsial agent Anaplasma phagocytophilum. We reveal hemocyte clusters exhibiting defined signatures related to immunity, metabolism, and proliferation. Depletion of phagocytic hemocytes affects hemocytin and astakine levels, two I. scapularis hemocyte markers, impacting blood-feeding, molting behavior, and bacterial acquisition. Mechanistically, astakine alters hemocyte proliferation, whereas hemocytin affects the c-Jun N-terminal kinase (JNK) signaling pathway in I. scapularis. Altogether, we discover a role for tick hemocytes in immunophysiology and provide a valuable resource for comparative biology in arthropods.

Date: 2024
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DOI: 10.1038/s41467-024-46494-3

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