Pathogens Manipulating Tick Behavior—Through a Glass, Darkly

Benelli, Giovanni

doi:10.3390/pathogens9080664

Cited by 50 publications

(62 citation statements)

References 90 publications

(119 reference statements)

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“…In the current study, we confirmed the expression of a complete Ixodes neuropeptidome in ISE6 cells. Considering that neuropeptides are regulators of all tick physiological processes and pathogens modulate tick physiology [ 32 ], our study suggests that ISE6 cells are an effective in vitro archetype for investigating TBP interactions with vital elements (i.e., neuropeptides) of the tick synganglion. Therefore, investigating tick–pathogen interactions by enlisting parallel, yet similar, cell-types (i.e., ISE6 cells and tick synganglion) may contribute to advancing tick control strategies to prevent TBP transmission.…”

Section: Discussionmentioning

confidence: 99%

“…A. phagocytophilum induces tissue-specific transcriptional reprogramming, thereby affecting different cellular functions in infected tick [ 21 , 22 , 23 , 26 , 27 , 28 ]. A. phagocytophilum infection also alters tick physiology and behavior [ 32 ]. For example, A. phagocytophilum -infected ticks were more fitted to survive in cold temperatures [ 34 ] or desiccating conditions [ 35 ] compared to uninfected ticks.…”

Section: Discussionmentioning

confidence: 99%

“…The main cellular components and processes affecting ticks by A. phagocytophilum infection are the cytoskeleton, immunity, epigenetics, apoptosis, and metabolism [ 25 , 26 , 27 , 30 , 31 ]. Recent studies also suggest that A. phagocytophilum modulates complex behavioral responses in infected ticks [ 32 , 33 , 34 , 35 ]. Although the capacity of A. phagocytophilum to manipulate cellular processes is well established, the interaction of specific signaling molecules within the tick central nervous system, i.e., the synganglion, is overlooked.…”

Section: Introductionmentioning

confidence: 99%

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Enlisting the Ixodes scapularis Embryonic ISE6 Cell Line to Investigate the Neuronal Basis of Tick—Pathogen Interactions

et al. 2021

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Neuropeptides are small signaling molecules expressed in the tick central nervous system, i.e., the synganglion. The neuronal-like Ixodes scapularis embryonic cell line, ISE6, is an effective tool frequently used for examining tick–pathogen interactions. We detected 37 neuropeptide transcripts in the I. scapularis ISE6 cell line using in silico methods, and six of these neuropeptide genes were used for experimental validation. Among these six neuropeptide genes, the tachykinin-related peptide (TRP) of ISE6 cells varied in transcript expression depending on the infection strain of the tick-borne pathogen, Anaplasma phagocytophilum. The immunocytochemistry of TRP revealed cytoplasmic expression in a prominent ISE6 cell subpopulation. The presence of TRP was also confirmed in A. phagocytophilum-infected ISE6 cells. The in situ hybridization and immunohistochemistry of TRP of I. scapularis synganglion revealed expression in distinct neuronal cells. In addition, TRP immunoreaction was detected in axons exiting the synganglion via peripheral nerves as well as in hemal nerve-associated lateral segmental organs. The characterization of a complete Ixodes neuropeptidome in ISE6 cells may serve as an effective in vitro tool to study how tick-borne pathogens interact with synganglion components that are vital to tick physiology. Therefore, our current study is a potential stepping stone for in vivo experiments to further examine the neuronal basis of tick–pathogen interactions.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Enlisting the Ixodes scapularis Embryonic ISE6 Cell Line to Investigate the Neuronal Basis of Tick—Pathogen Interactions

et al. 2021

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“…Conversely, vector-borne pathogens can manipulate their arthropod vectors (e.g., increase the biting rate, shift resources from reproduction to survival) to increase their own transmission, and thereby increase the R 0 of the vector-borne disease [8][9][10][11] . Measuring the effects of vector-borne pathogens on the tness of their arthropod vectors is therefore important for understanding the epidemiology of vector-borne diseases.…”

Section: Introductionmentioning

confidence: 99%

“…Hard ticks of the genus Ixodes transmit a diversity of tick-borne pathogens such as the spirochete bacteria belonging to the Borrelia burgdorferi sensu lato (sl) complex, which includes the causative agents of Lyme disease 3,26,27 . Some reviews have suggested that B. burgdorferi sl can adaptively manipulate its Ixodes tick vector to enhance its own transmission, and hence the R 0 of Lyme disease 11,28 . Ixodes ticks infected with B. burgdorferi sl differ from their uninfected counterparts in a number of tick phenotypes including questing behaviour, survival rates, body weight, and energy reserves [29][30][31][32][33][34][35] .…”

Section: Introductionmentioning

confidence: 99%

Infection with Borrelia afzelii reduces moulting time of Ixodes ricinus ticks

Hurry

Maluenda

Sarr

et al. 2021

Preprint

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Arthropod vectors carry vector-borne pathogens that cause infectious disease in vertebrate hosts, and arthropod-associated non-pathogenic microorganisms. Both types of micro-organisms can influence the fitness of their arthropod vectors, and hence the epidemiology of vector-borne diseases. The bacterium Borrelia afzelii, which causes Lyme disease in Europe, is transmitted among vertebrate reservoir hosts by Ixodes ricinus ticks, which also harbour a large diversity of non-pathogenic bacteria. The purpose of this study was to test experimentally whether B. afzelii and tick-associated non-pathogenic bacteria influence the fitness of I. ricinus. Eggs obtained from field-collected adult female ticks were washed with bleach, which reduced the abundance of non-pathogenic bacteria in the hatched I. ricinus larvae by 28-fold compared to larvae that hatched from eggs washed with water. The dysbiosed and control larvae were subsequently fed on B. afzelii-infected or uninfected control mice, and the engorged larvae were allowed to moult into nymphs under laboratory conditions. I. ricinus larvae that fed on B. afzelii-infected mice had a significantly faster larva-to-nymph moulting time compared to larvae that fed on uninfected control mice. In contrast, we found no evidence that B. afzelii infection or larval dysbiosis influenced the four other life history traits of the immature I. ricinus ticks, which included engorged larval weight, unfed nymphal weight, larva-to-nymph moulting success, and immature tick survival. A power analysis found that our sampling effort had sufficient power (>80%) to detect small effects (difference of 5% – 10%) of either B. afzelii infection or larval dysbiosis. Under the laboratory conditions of our study, B. afzelii appears to be a mostly passive passenger in I. Ricinus ticks.

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Climatic stress decreases tick survival but increases rate of host‐seeking behavior

et al. 2023

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Ticks are vectors of many diseases and are expanding in geographic distribution. However, how ticks will fare in their new environments, where they may experience stressful climatic conditions at the expansion front, remains unclear. Since there is a trade-off in ticks between behaviors that promote longevity and behaviors that promote reproduction, we hypothesized that extreme climatic stress reduces the survivorship of ticks but increases the frequency of tick host-seeking behavior, or questing. Here, we used a novel method to simulate climatic stress on individual ticks of three species-Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis-to evaluate their survival, physiology, and questing behavior. The first experiment involved placing 144 adult ticks of each species in two temperature ranges (15-25 C and 25-35 C) and three relative humidity (RH) treatments (32%, 58%, and 84% RH).We assessed the ticks daily for survivorship and questing, and we measured water loss by comparing the mass of each tick when it died to when it was fully hydrated. In this first experiment, ticks in warmer and less humid conditions generally died faster than those in cooler and more humid conditions. Ticks of all three species were more likely to quest shortly before their death and consistently died after losing approximately 50%-56% of their total body water content, but Ixodes reached that threshold much faster than the other two species.The second experiment involved placing 18 ticks of each species at 35 C and 32% RH. We assessed the ticks every 3 h for survivorship, questing, and water loss. Ticks again were more likely to quest shortly before their death. With frequent checks, we were able to measure the dehydration tolerance more accurately and the rate of water loss. Ticks of all three species consistently died after losing approximately 51% of their total body water content. However, Ixodes lost water approximately 5 times faster than Amblyomma and 11 times faster than Dermacentor. These results demonstrate that severe climatic stress tilts the trade-off toward higher questing rates but not higher overall questing time because of reduced survival rates.

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Pathogens Manipulating Tick Behavior—Through a Glass, Darkly

Cited by 50 publications

References 90 publications

Enlisting the Ixodes scapularis Embryonic ISE6 Cell Line to Investigate the Neuronal Basis of Tick—Pathogen Interactions

Enlisting the Ixodes scapularis Embryonic ISE6 Cell Line to Investigate the Neuronal Basis of Tick—Pathogen Interactions

Infection with Borrelia afzelii reduces moulting time of Ixodes ricinus ticks

Climatic stress decreases tick survival but increases rate of host‐seeking behavior

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