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

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.

SUBMITTER: Rolandelli A

PROVIDER: S-EPMC10923820 | biostudies-literature | 2024 Mar

REPOSITORIES: biostudies-literature

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

Rolandelli Agustin A Laukaitis-Yousey Hanna J HJ Bogale Haikel N HN Singh Nisha N Samaddar Sourabh S O'Neal Anya J AJ Ferraz Camila R CR Butnaru Matthew M Mameli Enzo E Xia Baolong B Mendes M Tays MT Butler L Rainer LR Marnin Liron L Cabrera Paz Francy E FE Valencia Luisa M LM Rana Vipin S VS Skerry Ciaran C Pal Utpal U Mohr Stephanie E SE Perrimon Norbert N Serre David D Pedra Joao H F JHF

Nature communications 20240308 1

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 dise ...[more]

PMID: 38459063

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Project description:BackgroundThe emergence of vector-borne pathogens in novel geographic areas is regulated by the migration of their arthropod vectors. Blacklegged ticks (Ixodes scapularis) and the pathogens they vector, including the causative agents of Lyme disease, babesiosis and anaplasmosis, continue to grow in their population sizes and to expand in geographic range. Migration of this vector over the previous decades has been implicated as the cause of the re-emergence of the most prevalent infectious diseases in North America.MethodsWe systematically collected ticks from across New York State (hereafter referred to as New York) from 2004 to 2017 as part of routine tick-borne pathogen surveillance in the state. This time frame corresponds with an increase in range and incidence of tick-borne diseases within New York. We randomly sampled ticks from this collection to explore the evolutionary history and population dynamics of I. scapularis. We sequenced the mitochondrial genomes of each tick to characterize their current and historical spatial genetic structure and population growth using phylogeographic methods.ResultsWe sequenced whole mitochondrial genomes from 277 ticks collected across New York between 2004 and 2017. We found evidence of population genetic structure at a broad geographic scale due to differences in the relative abundance, but not the composition, of haplotypes among sampled ticks. Ticks were often most closely related to ticks from the same and nearby collection sites. The data indicate that both short- and long-range migration events shape the population dynamics of blacklegged ticks in New York.ConclusionsWe detailed the population dynamics of the blacklegged tick (Ixodes scapularis) in New York during a time frame in which tick-borne diseases were increasing in range and incidence. Migration of ticks occurred at both coarse and fine scales in the recent past despite evidence of limits to gene flow. Past and current tick population dynamics have implications for further range expansion as habitat suitability for ticks changes due to global climate change. Analyses of mitochondrial genome sequencing data will expound upon previously identified drivers of tick presence and abundance as well as identify additional drivers. These data provide a foundation on which to generate testable hypotheses on the drivers of tick population dynamics occurring at finer scales.

Dataset Information

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

Publications

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

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