Immune factor of bacterial origin protects ticks against host skin microbes

SummaryHard ticks are blood-feeding arthropods that carry and transmit microbes to their vertebrate hosts1. Tick-borne disease cases have been on the rise over the last several decades, drawing much-needed attention to the molecular interplay between transmitted pathogens and their human hosts. However, far less is known about how ticks control their own microbes, which is critical for understanding how zoonotic transmission cycles persist. We previously found that ticks horizontally acquired an antimicrobial toxin gene from bacteria known as domesticated amidase effector 2 (dae2)2. Here we show that this effector from the tick vector Ixodes scapularis (Dae2Is) has structurally and biochemically diverged from ancestral bacterial representatives, expanding its antibacterial targeting range to include host skin microbes. Disruption of dae2Is increases the burden of skin-associated staphylococci within I. scapularis and adversely affects tick fitness, suggesting resistance of host microbes may be important for the parasitic blood-feeding lifestyle. In contrast, Dae2Is has no intrinsic ability to kill Borrelia burgdorferi, the tick-borne bacterium of Lyme disease. Our observations suggest that ticks have evolved to tolerate their own symbionts while resisting host skin commensals, which we discover are natural opportunistic pathogens of ticks. This work moves our understanding of vector biology beyond a human-centric view: just as tick commensals are pathogenic to humans, so too do our commensals pose a threat to ticks. These observations illuminate how a complex and mirrored set of interkingdom interactions between blood-feeding vectors, their hosts, and associated microbes can ultimately lead to disease.

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Human Coinfection withBorrelia burgdorferiandBabesia microtiin the United States

Journal of Parasitology Research ◽

10.1155/2015/587131 ◽

2015 ◽

Vol 2015 ◽

pp. 1-11 ◽

Cited By ~ 21

Author(s):

Kristen L. Knapp ◽

Nancy A. Rice

Keyword(s):

United States ◽

Lyme Disease ◽

Causative Agent ◽

Ixodes Scapularis ◽

Immunological Response ◽

The United States ◽

Babesia Microti ◽

Current State ◽

Tick Borne Disease ◽

Multiple Pathogens

Borrelia burgdorferi, the causative agent of Lyme disease, andBabesia microti, a causative agent of babesiosis, are increasingly implicated in the growing tick-borne disease burden in the northeastern United States. These pathogens are transmitted via the bite of an infected tick vector,Ixodes scapularis, which is capable of harboring and inoculating a host with multiple pathogens simultaneously. Clinical presentation of the diseases is heterogeneous and ranges from mild flu-like symptoms to near-fatal cardiac arrhythmias. While the reason for the variability is not known, the possibility exists that concomitant infection with bothB. burgdorferiandB. microtimay synergistically increase disease severity. In an effort to clarify the current state of understanding regarding coinfection withB. burgdorferiandB. microti, in this review, we discuss the geographical distribution and pathogenesis of Lyme disease and babesiosis in the United States, the immunological response of humans toB. burgdorferiorB. microtiinfection, the existing knowledge regarding coinfection disease pathology, and critical factors that have led to ambiguity in the literature regarding coinfection, in order to eliminate confusion in future experimental design and investigation.

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Blood Digestion by Trypsin-Like Serine Proteases in the Replete Lyme Disease Vector Tick, Ixodes scapularis

Insects ◽

10.3390/insects11030201 ◽

2020 ◽

Vol 11 (3) ◽

pp. 201

Author(s):

Jeremiah Reyes ◽

Cuauhtemoc Ayala-Chavez ◽

Arvind Sharma ◽

Michael Pham ◽

Andrew B. Nuss ◽

...

Keyword(s):

Lyme Disease ◽

Blood Meal ◽

Serine Proteases ◽

Ixodes Scapularis ◽

Life Stage ◽

Blood Feeding ◽

Eastern United States ◽

Blood Digestion ◽

Hemoglobin Degradation

Ixodes scapularis is the major vector of Lyme disease in the Eastern United States. Each active life stage (larva, nymph, and adult) takes a blood meal either for developing and molting to the next stage (larvae and nymphs) or for oviposition (adult females). This protein-rich blood meal is the only food taken by Ixodes ticks and therefore efficient blood digestion is critical for survival. Studies in partially engorged ticks have shown that the initial stages of digestion are carried out by cathepsin proteases within acidic digestive cells. In this study, we investigated the potential role of serine proteases in blood digestion in replete ticks. RNA interference was used for functional analysis and a trypsin-benzoyl-D, L-arginine 4-nitoanilide assay was used to measure active trypsin levels. Hemoglobinolytic activity was determined in vitro, with or without a serine protease inhibitor. Our data suggest that trypsin levels increase significantly after repletion. Knockdown of serine proteases negatively impacted blood feeding, survival, fecundity, levels of active trypsin in the midgut, and resulted in lower hemoglobin degradation. Incubation of midgut extract with a trypsin inhibitor resulted in 65% lower hemoglobin degradation. We provide evidence of the serine proteases as digestive enzymes in fully engorged, replete females. Understanding the digestive profile of trypsin during blood meal digestion in I. scapularis improves our understanding of the basic biology of ticks and may lead to new methods for tick control.

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Recent and rapid population growth and range expansion of the Lyme disease tick vector,Ixodes scapularis, in North America

Evolution ◽

10.1111/evo.12690 ◽

2015 ◽

Vol 69 (7) ◽

pp. 1678-1689 ◽

Cited By ~ 25

Author(s):

Camilo E. Khatchikian ◽

Melissa A. Prusinski ◽

Melissa Stone ◽

Peter Bryon Backenson ◽

Ing-Nang Wang ◽

...

Keyword(s):

North America ◽

Lyme Disease ◽

Population Growth ◽

Range Expansion ◽

Ixodes Scapularis ◽

Rapid Population Growth ◽

Tick Vector

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Gut Microbiota of the Tick Vector Ixodes scapularis Modulate Colonization of the Lyme Disease Spirochete

Cell Host & Microbe ◽

10.1016/j.chom.2013.12.001 ◽

2014 ◽

Vol 15 (1) ◽

pp. 58-71 ◽

Cited By ~ 144

Author(s):

Sukanya Narasimhan ◽

Nallakkandi Rajeevan ◽

Lei Liu ◽

Yang O. Zhao ◽

Julia Heisig ◽

...

Keyword(s):

Lyme Disease ◽

Gut Microbiota ◽

Ixodes Scapularis ◽

Tick Vector

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Implications of climate change on the distribution of the tick vector Ixodes scapularis and risk for Lyme disease in the Texas-Mexico transboundary region

Parasites & Vectors ◽

10.1186/1756-3305-7-199 ◽

2014 ◽

Vol 7 (1) ◽

pp. 199 ◽

Cited By ~ 47

Author(s):

Teresa P Feria-Arroyo ◽

Ivan Castro-Arellano ◽

Guadalupe Gordillo-Perez ◽

Ana L Cavazos ◽

Margarita Vargas-Sandoval ◽

...

Keyword(s):

Climate Change ◽

Lyme Disease ◽

Ixodes Scapularis ◽

Tick Vector

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The effect of infection with Lyme disease spirochetes (Borrelia burgdorferi) on the phototaxis, activity, and questing height of the tick vector Ixodes scapularis

Parasitology ◽

10.1017/s0031182000066336 ◽

1996 ◽

Vol 113 (2) ◽

pp. 97-103 ◽

Cited By ~ 33

Author(s):

H. Lefcort ◽

L. A. Durden

Keyword(s):

Lyme Disease ◽

Borrelia Burgdorferi ◽

Kin Selection ◽

Ixodes Scapularis ◽

Bacterial Pathogen ◽

Pathogen Transmission ◽

Ecological Effects ◽

Infected Tick ◽

Tick Vector ◽

Tick Vectors

SUMMARYLittle is known about the effects of infection with Borrelia burgdorferi, the bacterium that causes Lyme disease, on its tick vectors. The purpose of this study was to determine the behavioural and ecological effects of infection by the bacterium in nymphal and adult black-legged (Ixodes scapularis) ticks. We found that the effects of infection were more pronounced in adults than in nymphs. Compared to uninfected adults, infected adults were less able to overcome physical obstacles, avoided vertical surfaces, were less active and quested at lower heights. Infected nymphs showed increased phototaxis and attraction to vertical surfaces. Infected nymphs also showed trends toward increased questing height and a greater tendency to overcome physical obstacles although these trends were not statistically significant. These altered behaviours in an infected tick may affect survival or pathogen transmission and may reflect kin selection in the bacterial pathogen.

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Blood Digestion by Trypsin-Like Serine Protease in the Replete Lyme Disease Vector Tick, Ixodes scapularis

10.20944/preprints201910.0026.v2 ◽

2020 ◽

Author(s):

Jeremiah Reyes ◽

Cuauhtemoc Ayala-Chavez ◽

Michael Pham ◽

Arvind Sharma ◽

Andrew Nuss ◽

...

Keyword(s):

Lyme Disease ◽

Serine Protease ◽

Blood Meal ◽

Serine Proteases ◽

Ixodes Scapularis ◽

Life Stage ◽

Blood Feeding ◽

Blood Digestion ◽

Hemoglobin Degradation

Ixodes scapularis is the major vector of Lyme disease in the eastern United States. Each active life stage (larva, nymph, and adult) takes a blood meal either for developing and molting to the next stage (larvae and nymphs) or for oviposition (adult females). This protein-rich blood meal is the only food taken by Ixodes ticks and therefore blood digestion is very important for tick survival. Most studies on blood digestion in ticks have shown that the initial stages of digestion are carried out by cathepsin proteases within acidic digestive cells. However, most of these studies have focused on partially engorged ticks. In other hematophagous arthropods, the serine proteases play an important role in blood protein degradation. In this study, we determined transcript expression of four I. scapularis serine proteases with previously characterized roles in blood digestion. RNA interference was used for functional analysis and a trypsin-benzoyl-D, L-arginine 4-nitoanilide assay was used to measure active trypsin levels. An in vitro hemoglobinolytic assay was performed with or without serine protease inhibitor. Our data suggest that trypsin levels increase significantly after blood feeding and peaked in larvae, nymphs, and adults at 3, 1, and 1 day post host detachment, respectively. The knockdown of three previously identified serine proteases by RNAi negatively impacted blood intake, survival, fecundity, levels of active trypsin in the gut and resulted in lower hemoglobin degradation in vitro. A trypsin inhibitor, PMSF, blocked the action of trypsin in the gut extract resulting in 65% lower hemoglobin degradation. We provide evidence of the serine proteases as digestive enzymes in fully engorged, replete females. Our data also demonstrated that in addition to blood digestion, these serine proteases might have a role in blood feeding success in I. scapularis.

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Identification ofBorrelia bissettiiinIxodes scapularisticks from New Brunswick, Canada

Canadian Journal of Microbiology ◽

10.1139/cjm-2018-0376 ◽

2019 ◽

Vol 65 (2) ◽

pp. 155-161

Author(s):

Julie Lewis ◽

Vett K. Lloyd

Keyword(s):

Lyme Disease ◽

New Brunswick ◽

Diagnostic Tests ◽

Disease Risk ◽

Ixodes Scapularis ◽

Clinical Manifestations ◽

Sensu Stricto ◽

Tick Borne Disease ◽

Borrelia Burgdorferi Sensu Stricto ◽

Lyme Disease Risk

Lyme disease is a tick-borne disease that is emerging in Canada. The disease is caused by spirochetes of the Lyme borreliosis group, which is expanding as new species are discovered. In Canada, Lyme disease risk has so far been assessed primarily by detection of Borrelia burgdorferi sensu stricto. Of Ixodes scapularis ticks collected between 2014 and 2016 in New Brunswick, Canada, 7 were shown to be infected with Borrelia bissettii by nested PCR and sequencing of 5 B. bissettii genes. Since different Borrelia species are associated with different clinical manifestations and are not detected with the same diagnostic tests, the identification of a previously undocumented or underreported pathogenic Borrelia species has important implications for public and veterinary medicine.

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