Vector microbiota manipulation by host antibodies: the forgotten strategy to develop transmission-blocking vaccines

Human and animal pathogens that are transmitted by arthropods are a global concern, particularly those vectored by ticks (e.g. Borrelia burgdorferi and tick-borne encephalitis virus) and mosquitoes (e.g. malaria and dengue virus). Breaking the circulation of pathogens in permanent foci by controlling vectors using acaricide-based approaches is threatened by the selection of acaricide resistance in vector populations, poor management practices and relaxing of control measures. Alternative strategies that can reduce vector populations and/or vector-mediated transmission are encouraged worldwide. In recent years, it has become clear that arthropod-associated microbiota are involved in many aspects of host physiology and vector competence, prompting research into vector microbiota manipulation. Here, we review how increased knowledge of microbial ecology and vector-host interactions is driving the emergence of new concepts and tools for vector and pathogen control. We focus on the immune functions of host antibodies taken in the blood meal as they can target pathogens and microbiota bacteria within hematophagous arthropods. Anti-microbiota vaccines are presented as a tool to manipulate the vector microbiota and interfere with the development of pathogens within their vectors. Since the importance of some bacterial taxa for colonization of vector-borne pathogens is well known, the disruption of the vector microbiota by host antibodies opens the possibility to develop novel transmission-blocking vaccines.

Artificial feeding of Ornithodoros fonsecai (Acari: Argasidae) with the anticoagulant Alsever

Ornithodoros fonsecai is a species of argasid tick endemic to Brazil, described in the “São Miguel” cave located in the municipality of Bonito, state of Mato Grosso do Sul, central-western region of Brazil. The artificial feeding technique makes it possible to study the biology of hematophagous arthropods using artificial or natural membranes, as well as different types of blood and anticoagulants. Thus, the aim of the present study was to feed artificially O. fonsecai second instar (N2) nymphs with rabbit blood using parafilm membrane and the anticoagulant Alsever. Ninety percent of the total N2 nymphs engorged and molted to N3 nymphs between 27 and 30 days after feeding, indicating that the use of this anticoagulant is efficient for artificially feeding O. fonsecai N2 nymphs under laboratory conditions.

Epidemiology of Shuni Virus in Horses in South Africa

The Orthobunyavirus genus, family Peribunyaviridae, contains several important emerging and re-emerging arboviruses of veterinary and medical importance. These viruses may cause mild febrile illness, to severe encephalitis, fetal deformity, abortion, hemorrhagic fever and death in humans and/or animals. Shuni virus (SHUV) is a zoonotic arbovirus thought to be transmitted by hematophagous arthropods. It was previously reported in a child in Nigeria in 1966 and horses in Southern Africa in the 1970s and again in 2009, and in humans with neurological signs in 2017. Here we investigated the epidemiology and phylogenetic relationship of SHUV strains detected in horses presenting with febrile and neurological signs in South Africa. In total, 24/1820 (1.3%) horses submitted to the zoonotic arbovirus surveillance program tested positive by real-time reverse transcription (RTPCR) between 2009 and 2019. Cases were detected in all provinces with most occurring in Gauteng (9/24, 37.5%). Neurological signs occurred in 21/24 (87.5%) with a fatality rate of 45.8%. Partial sequencing of the nucleocapsid gene clustered the identified strains with SHUV strains previously identified in South Africa (SA). Full genome sequencing of a neurological case detected in 2016 showed 97.8% similarity to the SHUV SA strain (SAE18/09) and 97.5% with the Nigerian strain and 97.1% to the 2014 Israeli strain. Our findings suggest that SHUV is circulating annually in SA and despite it being relatively rare, it causes severe neurological disease and death in horses.

Genetic Manipulation of Ticks: A Paradigm Shift in Tick and Tick-Borne Diseases Research

Ticks are obligate hematophagous arthropods that are distributed worldwide and are one of the most important vectors of pathogens affecting humans and animals. Despite the growing burden of tick-borne diseases, research on ticks has lagged behind other arthropod vectors, such as mosquitoes. This is largely because of challenges in applying functional genomics and genetic tools to the idiosyncrasies unique to tick biology, particularly techniques for stable genetic transformations. CRISPR-Cas9 is transforming non-model organism research; however, successful germline editing has yet to be accomplished in ticks. Here, we review the ancillary methods needed for transgenic tick development and the use of CRISPR/Cas9, the most promising gene-editing approach, for tick genetic transformation.

The Efficacy of Ultrasonic Pest Repellent Devices against the Australian Paralysis Tick, Ixodes holocyclus (Acari: Ixodidae)

Ultrasonic pest repellers are often promoted as a means of protecting people and pets from the bites of hematophagous arthropods, such as ticks. However, to date, there has been no published research on the effectiveness of these devices against the Australian paralysis tick, Ixodes holocyclus Neumann. The purpose of this study was to test the effectiveness of nine ultrasonic devices against female I. holocyclus. Two arenas were constructed, one for the test (with the ultrasonic device) and one for the control (no device). Each arena had a test and an escape chamber, connected by a corridor. Twenty ticks were placed in each test chamber. After the ultrasonic device was operated for 1 h, the number of ticks in both chambers was recorded. Ten replicates were conducted for each device. The average number of ticks that moved from the test to the escape chamber was greater in all the test arenas, with three devices being statistically different from the control. However, the highest percent of ticks that escaped was only 19.5%. This amount is insufficient to offer adequate protection against tick bites and this study adds further weight to previous investigations that ultrasonic devices should not be employed in pest management.

Vertebrate Responses against Arthropod Salivary Proteins and Their Therapeutic Potential

The saliva of hematophagous arthropods contains a group of active proteins to counteract host responses against injury and to facilitate the success of a bloodmeal. These salivary proteins have significant impacts on modulating pathogen transmission, immunogenicity expression, the establishment of infection, and even disease severity. Recent studies have shown that several salivary proteins are immunogenic and antibodies against them may block infection, thereby suggesting potential vaccine candidates. Here, we discuss the most relevant salivary proteins currently studied for their therapeutic potential as vaccine candidates or to control the transmission of human vector-borne pathogens and immune responses against different arthropod salivary proteins.

High-Throughput Microfluidic Real-Time PCR for the Detection of Multiple Microorganisms in Ixodid Cattle Ticks in Northeast Algeria

Ixodid ticks are hematophagous arthropods considered to be prominent ectoparasite vectors that have a negative impact on cattle, either through direct injury or via the transmission of several pathogens. In this study, we investigated the molecular infection rates of numerous tick-borne pathogens in ticks sampled on cattle from the Kabylia region, northeastern Algeria, using a high-throughput microfluidic real-time PCR system. A total of 235 ticks belonging to seven species of the genera Rhipicephalus, Hyalomma, and Ixodes were sampled on cattle and then screened for the presence of 36 different species of bacteria and protozoans. The most prevalent tick-borne microorganisms were Rickettsia spp. at 79.1%, followed by Francisella-like endosymbionts (62.9%), Theileria spp. (17.8%), Anaplasma spp. (14.4%), Bartonella spp. (6.8%), Borrelia spp. (6.8%), and Babesia spp. (2.5%). Among the 80.4% of ticks bearing microorganisms, 20%, 36.6%, 21.7%, and 2.1% were positive for one, two, three, and four different microorganisms, respectively. Rickettsia aeschlimannii was detected in Hyalomma marginatum, Hyalomma detritum, and Rhipicephalus bursa ticks. Rickettsia massiliae was found in Rhipicephalus sanguineus, and Rickettsiamonacensis and Rickettsia helvetica were detected in Ixodesricinus. Anaplasma marginale was found in all identified tick genera, but Anaplasma centrale was detected exclusively in Rhipicephalus spp. ticks. The DNA of Borrelia spp. and Bartonella spp. was identified in several tick species. Theileria orientalis was found in R. bursa, R. sanguineus, H. detritum, H. marginatum, and I. ricinus and Babesia bigemina was found in Rhipicephalus annulatus and R. sanguineus. Our study highlights the importance of tick-borne pathogens in cattle in Algeria.

Molecular Investigation on Tick-Borne Hemoparasites and Coxiella burnetii in Dromedary Camels (Camelusdromedarius) in Al Dhafra Region of Abu Dhabi, UAE

Camels represent an important resource for inhabitants of the most arid regions of the world and their survival is mainly related to environment conditions including the risk of parasitic diseases, which may represent a significant cause of losses in livestock production of these areas. Camels may be parasitized by several hematophagous arthropods, which can be vectors of several diseases including zoonosis. This study aimed to investigate in dromedary camels and their ticks the importance of tick-borne hemoparasites that might be responsible for a recent and obscure morbidity of camels in Al Dhafra region of Abu Dhabi, UAE. Blood samples and ticks from 93 naturally infected camels belonging to 36 herds, affected by variable acute clinical syndromes lasting from 3 to 5 days, were analyzed through molecular techniques for specific DNA presence of different blood pathogens: Anaplasmamarginale/Anaplasmaovis, Anaplasma phagocytophilum, Coxiella burnetii,Babesia spp., and Theileria spp. DNA. All the 72 ticks collected belonged to the Hyalomma dromedarii species and were negative for blood pathogens. n = 15 camels (16.1%) were found positive to the following tick-borne hemoparasites: A. phagocytophilum 11 (11.8%), Coxiella burnetii 3 (3.2%), and Babesia/Theileria spp. 2 (2.1%). One singular camel showed coinfection of C. burnetii and A. phagocytophiulm. Genetic profile of C. burnetii showed a high phylogenetic relatedness to European, Asian and African C. burnetii strains. This is the first laboratory investigation on tick-borne pathogens in camels in UAE, and the first report of A. phagocytophilum and C. burnetii. Moreover, since the detected pathogens are recognized pathogens for humans, this study highlights the zoonotic risk for humans working in camel husbandry.