Tick gut barriers impacting tick–microbe interactions and pathogen persistence

Abstract

Ticks represent a major group of arthropod vectors that are present worldwide and transmit a number of serious infections (Parola & Raoult, 2001). They exhibit a high degree of heterogeneity in terms of their habitat, biology, and genome, which possibly dictates their remarkable vectorial competence, as evidenced by their ability to harbor a diverse range of pathogenic agents, including viruses, bacteria, protozoa, and nematodes (Jia et al., 2020). The hematophagous and ectoparasitic behavior of ticks facilitates the acquisition and transmission of certain pathogens between reservoir hosts and ticks, as well as frequent transmission from ticks to incidental hosts. Many human and animal diseases are caused by tick-borne pathogens. For example, tick-borne encephalitis (TBE) (Beaute et al., 2018) is elicited by a virus of the family Flaviviridae, the TBE virus (Mansfield et al., 2009), which occurs in many European countries, northern China, Mongolia, and the Russian Federation, while Lyme disease, or Lyme borreliosis, is caused by the bacteria Borrelia burgdorferi sensu lato, which is prevalent in North America and Eurasia (Radolf et al., 2012). The latest estimate from the United States Center for Disease Control and Prevention (CDC) suggests that, in recent years, there were likely over 400,000 new cases of Lyme disease annually in the United States alone (Kugeler et al., 2021). This infection is predominantly transmitted by Ixodes scapularis ticks, in addition to closely related species, such as I. pacificus, I. ricinus, and I. persulcatus, that are found across specific geographical regions of North America, Eurasia, and Asia. While many distinct tick species transmit various human diseases, Ixodes ticks are considered as one of the most prolific vectors; besides Lyme disease and TBE, they also transmit numerous other human infections, such as anaplasmosis,

De novo assembly and annotation of the Amblyomma hebraeum tick midgut transcriptome response to Ehrlichia ruminantium infection

“…Serine proteases and protease inhibitors (Kunitz) have been shown modulate immune cascades involved in pathogen recognition and control [ 81 ]. Mucin and peritrophin are important innate immunity barriers with a direct impact on pathogen colonization of the midgut [ 82 , 83 ]. Serine protease inhibitors have been investigated in several recent studies focused on uncovering their role in the regulation of inflammation and complement activation in mammals [ 84 ].…”

Insect–microbe interactions and their influence on organisms and ecosystems

“…These interactions can be visualized as feedback loops where environmental microbes affect other living organisms, such as insects and plants, which in turn transport or share microbial organisms back to the surrounding environment (Figure 1). Noninsect arthropods such as ticks in the order Ixodida are also infected with a wide diversity of both pathogenic and nonpathogenic microbes, including intracellular bacteria, which together impact tick biology as well as pathogen establishment and transmission (Abraham et al, 2017;Bonnet et al, 2017;Buysse et al, 2021;Cull et al, 2021;Kitsou et al, 2021;Maitre et al, 2022). For instance, sheep ticks (Ixodes ricinus L.) harbored co-infections with B. burgdorferi and other animal pathogens (i.e., Lariskella, Rickettsia, Rickettsiella, and Spiroplasma), a composition that can be shaped by the host tick genotype, elevational cline or geographic location, and potentially through ecological facilitation via other microbes (Aivelo et al, 2019).…”

Changing Geographic Ranges of Human Biting Ticks and Implications for Tick-Borne Zoonoses in North America

“…Borrelia burgdorferi spirochete molecular adaptations are determinants of tick vector colonization that include midgut binding, microbiome modulation upon infection, translocation across the gut to the hemolymph, adapting to tick defenses, salivary gland infection, and adaptations associated with the transition from the tick to the mammalian host tissue environments [85][86][87][88]. Changes occur in Borrelia burgdorferi numbers in tick tissues when an infected nymph begins to blood feed.…”