Colonization of the tsetse fly midgut with commensal Enterobacter inhibits trypanosome infection establishment

AbstractTsetse flies (Glossina spp.) vector pathogenic trypanosomes (Trypanosoma spp.) in sub-Saharan Africa. These parasites cause human and animal African trypanosomiases, which are debilitating diseases that inflict an enormous socio-economic burden on inhabitants of endemic regions. Current disease control strategies rely primarily on treating infected animals and reducing tsetse population densities. However, relevant programs are costly, labor intensive and difficult to sustain. As such, novel strategies aimed at reducing tsetse vector competence require development. Herein we investigated whether an Enterobacter bacterium (Esp_Z), which confers Anopheles gambiae with resistance to Plasmodium, is able to colonize tsetse and induce a trypanosome refractory phenotype in the fly. Esp_Z established stable infections in tsetse’s gut, and exhibited no adverse effect on the survival of individuals from either group. Flies with established Esp_Z infections in their gut were significantly more refractory to infection with two distinct trypanosome species (T. congolense, 6% infection; T. brucei, 32% infection) than were age-matched flies that did not house the exogenous bacterium (T. congolense, 36% infected; T. brucei, 70% infected). Additionally, 52% of Esp_Z colonized tsetse survived infection with entomopathogenic Serratia marcescens, compared with only 9% of their wild-type counterparts. These parasite and pathogen refractory phenotypes result from the fact that Esp_Z acidifies tsetse’s midgut environment, which inhibits trypanosome and Serratia growth and thus infection establishment. Finally, we determined that Esp_Z infection does not impact the fecundity of male or female tsetse, nor the ability of male flies to compete with their wild-type counterparts for mates. We propose that Esp_Z could be used as one component of an integrated strategy aimed at reducing the ability of tsetse to transmit pathogenic trypanosomes.Author SummaryTsetse flies transmit pathogenic African trypanosomes, which are the causative agents of socio-economically devastating human and animal African trypanosomiases. These diseases are currently controlled in large part by reducing the population size of tsetse vectors through the use of insecticides, traps and sterile insect technique. However, logistic and monetary hurdles often preclude the prolonged application of procedures necessary to maintain these control programs. Thus, novel strategies, including those aimed at sustainably reducing the ability of tsetse to transmit trypanosomes, are presently under development. Herein we stably colonize tsetse flies with a bacterium (Enterobacter sp. Z, Esp_Z) that acidifies their midgut, thus rendering the environment inhospitable to infection with two distinct, epidemiologically important trypanosome strains as well as an entomopathogenic bacteria. In addition to inducing a trypanosome refractory phenotype, colonization of tsetse with Esp_Z exerts only a modest fitness cost on the fly. Taken together, these findings suggest that Esp_Z could be applied to enhance the effectiveness of currently employed tsetse control programs.

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The holobiont transcriptome of teneral tsetse fly species of varying vector competence

BMC Genomics ◽

10.1186/s12864-021-07729-5 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Miguel Medina Munoz ◽

Caitlyn Brenner ◽

Dylan Richmond ◽

Noah Spencer ◽

Rita V. M. Rio

Keyword(s):

Control Strategies ◽

Vector Competence ◽

Tsetse Fly ◽

Tsetse Flies ◽

Protein Coding ◽

African Trypanosomes ◽

Animal African Trypanosomiasis ◽

Protein Coding Genes ◽

Sodalis Glossinidius ◽

Immunological Protection

Abstract Background Tsetse flies are the obligate vectors of African trypanosomes, which cause Human and Animal African Trypanosomiasis. Teneral flies (newly eclosed adults) are especially susceptible to parasite establishment and development, yet our understanding of why remains fragmentary. The tsetse gut microbiome is dominated by two Gammaproteobacteria, an essential and ancient mutualist Wigglesworthia glossinidia and a commensal Sodalis glossinidius. Here, we characterize and compare the metatranscriptome of teneral Glossina morsitans to that of G. brevipalpis and describe unique immunological, physiological, and metabolic landscapes that may impact vector competence differences between these two species. Results An active expression profile was observed for Wigglesworthia immediately following host adult metamorphosis. Specifically, ‘translation, ribosomal structure and biogenesis’ followed by ‘coenzyme transport and metabolism’ were the most enriched clusters of orthologous genes (COGs), highlighting the importance of nutrient transport and metabolism even following host species diversification. Despite the significantly smaller Wigglesworthia genome more differentially expressed genes (DEGs) were identified between interspecific isolates (n = 326, ~ 55% of protein coding genes) than between the corresponding Sodalis isolates (n = 235, ~ 5% of protein coding genes) likely reflecting distinctions in host co-evolution and adaptation. DEGs between Sodalis isolates included genes involved in chitin degradation that may contribute towards trypanosome susceptibility by compromising the immunological protection provided by the peritrophic matrix. Lastly, G. brevipalpis tenerals demonstrate a more immunologically robust background with significant upregulation of IMD and melanization pathways. Conclusions These transcriptomic differences may collectively contribute to vector competence differences between tsetse species and offers translational relevance towards the design of novel vector control strategies.

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Positional Dynamics and Glycosomal Recruitment of Developmental Regulators during Trypanosome Differentiation

mBio ◽

10.1128/mbio.00875-19 ◽

2019 ◽

Vol 10 (4) ◽

Cited By ~ 2

Author(s):

Balázs Szöőr ◽

Dorina V. Simon ◽

Federico Rojas ◽

Julie Young ◽

Derrick R. Robinson ◽

...

Keyword(s):

Life Cycle ◽

Trypanosoma Brucei ◽

Tyrosine Phosphatase ◽

Tsetse Fly ◽

Sub Saharan Africa ◽

Metabolic Adaptation ◽

Tsetse Flies ◽

Content Type ◽

African Trypanosomes ◽

Sub Saharan

ABSTRACT Glycosomes are peroxisome-related organelles that compartmentalize the glycolytic enzymes in kinetoplastid parasites. These organelles are developmentally regulated in their number and composition, allowing metabolic adaptation to the parasite’s needs in the blood of mammalian hosts or within their arthropod vector. A protein phosphatase cascade regulates differentiation between parasite developmental forms, comprising a tyrosine phosphatase, Trypanosoma brucei PTP1 (TbPTP1), which dephosphorylates and inhibits a serine threonine phosphatase, TbPIP39, which promotes differentiation. When TbPTP1 is inactivated, TbPIP39 is activated and during differentiation becomes located in glycosomes. Here we have tracked TbPIP39 recruitment to glycosomes during differentiation from bloodstream “stumpy” forms to procyclic forms. Detailed microscopy and live-cell imaging during the synchronous transition between life cycle stages revealed that in stumpy forms, TbPIP39 is located at a periflagellar pocket site closely associated with TbVAP, which defines the flagellar pocket endoplasmic reticulum. TbPTP1 is also located at the same site in stumpy forms, as is REG9.1, a regulator of stumpy-enriched mRNAs. This site provides a molecular node for the interaction between TbPTP1 and TbPIP39. Within 30 min of the initiation of differentiation, TbPIP39 relocates to glycosomes, whereas TbPTP1 disperses to the cytosol. Overall, the study identifies a “stumpy regulatory nexus” (STuRN) that coordinates the molecular components of life cycle signaling and glycosomal development during transmission of Trypanosoma brucei. IMPORTANCE African trypanosomes are parasites of sub-Saharan Africa responsible for both human and animal disease. The parasites are transmitted by tsetse flies, and completion of their life cycle involves progression through several development steps. The initiation of differentiation between blood and tsetse fly forms is signaled by a phosphatase cascade, ultimately trafficked into peroxisome-related organelles called glycosomes that are unique to this group of organisms. Glycosomes undergo substantial remodeling of their composition and function during the differentiation step, but how this is regulated is not understood. Here we identify a cytological site where the signaling molecules controlling differentiation converge before the dispersal of one of them into glycosomes. In combination, the study provides the first insight into the spatial coordination of signaling pathway components in trypanosomes as they undergo cell-type differentiation.

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Viviparity and habitat restrictions may influence the evolution of male reproductive genes in tsetse fly (Glossina) species

BMC Biology ◽

10.1186/s12915-021-01148-4 ◽

2021 ◽

Vol 19 (1) ◽

Author(s):

Grazia Savini ◽

Francesca Scolari ◽

Lino Ometto ◽

Omar Rota-Stabelli ◽

Davide Carraretto ◽

...

Keyword(s):

Reproductive Behavior ◽

Selective Pressure ◽

Demographic History ◽

Reproductive Rate ◽

Tsetse Fly ◽

Sub Saharan Africa ◽

Comparative Genomic ◽

Tsetse Flies ◽

African Trypanosomes ◽

Reproductive Genes

Abstract Background Glossina species (tsetse flies), the sole vectors of African trypanosomes, maintained along their long evolutionary history a unique reproductive strategy, adenotrophic viviparity. Viviparity reduces their reproductive rate and, as such, imposes strong selective pressures on males for reproductive success. These species live in sub-Saharan Africa, where the distributions of the main sub-genera Fusca, Morsitans, and Palpalis are restricted to forest, savannah, and riverine habitats, respectively. Here we aim at identifying the evolutionary patterns of the male reproductive genes of six species belonging to these three main sub-genera. We then interpreted the different patterns we found across the species in the light of viviparity and the specific habitat restrictions, which are known to shape reproductive behavior. Results We used a comparative genomic approach to build consensus evolutionary trees that portray the selective pressure acting on the male reproductive genes in these lineages. Such trees reflect the long and divergent demographic history that led to an allopatric distribution of the Fusca, Morsitans, and Palpalis species groups. A dataset of over 1700 male reproductive genes remained conserved over the long evolutionary time scale (estimated at 26.7 million years) across the genomes of the six species. We suggest that this conservation may result from strong functional selective pressure on the male imposed by viviparity. It is noteworthy that more than half of these conserved genes are novel sequences that are unique to the Glossina genus and are candidates for selection in the different lineages. Conclusions Tsetse flies represent a model to interpret the evolution and differentiation of male reproductive biology under different, but complementary, perspectives. In the light of viviparity, we must take into account that these genes are constrained by a post-fertilization arena for genomic conflicts created by viviparity and absent in ovipositing species. This constraint implies a continuous antagonistic co-evolution between the parental genomes, thus accelerating inter-population post-zygotic isolation and, ultimately, favoring speciation. Ecological restrictions that affect reproductive behavior may further shape such antagonistic co-evolution.

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African trypanosomes: the genome and adaptations for immune evasion

Essays in Biochemistry ◽

10.1042/bse0510047 ◽

2011 ◽

Vol 51 ◽

pp. 47-62 ◽

Cited By ~ 43

Author(s):

Gloria Rudenko

Keyword(s):

Immune Evasion ◽

Cell Biology ◽

Antigenic Variation ◽

Critical Role ◽

Sub Saharan Africa ◽

Surface Glycoprotein ◽

Tsetse Flies ◽

African Trypanosomes ◽

Genes Encoding ◽

Sub Saharan

The African trypanosome Trypanosoma brucei is a flagellated unicellular parasite transmitted by tsetse flies that causes African sleeping sickness in sub-Saharan Africa. Trypanosomes are highly adapted for life in the hostile environment of the mammalian bloodstream, and have various adaptations to their cell biology that facilitate immune evasion. These include a specialized morphology, with most nutrient uptake occurring in the privileged location of the flagellar pocket. In addition, trypanosomes show extremely high rates of recycling of a protective VSG (variant surface glycoprotein) coat, whereby host antibodies are stripped off of the VSG before it is re-used. VSG recycling therefore functions as a mechanism for cleaning the VSG coat, allowing trypanosomes to survive in low titres of anti-VSG antibodies. Lastly, T. brucei has developed an extremely sophisticated strategy of antigenic variation of its VSG coat allowing it to evade host antibodies. A single trypanosome has more than 1500 VSG genes, most of which are located in extensive silent arrays. Strikingly, most of these silent VSGs are pseudogenes, and we are still in the process of trying to understand how non-intact VSGs are recombined to produce genes encoding functional coats. Only one VSG is expressed at a time from one of approximately 15 telomeric VSG ES (expression site) transcription units. It is becoming increasingly clear that chromatin remodelling must play a critical role in ES control. Hopefully, a better understanding of these unique trypanosome adaptations will eventually allow us to disrupt their ability to multiply in the mammalian bloodstream.

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Mammalian African trypanosome VSG coat enhances tsetse’s vector competence

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1600304113 ◽

2016 ◽

Vol 113 (25) ◽

pp. 6961-6966 ◽

Cited By ~ 28

Author(s):

Emre Aksoy ◽

Aurélien Vigneron ◽

XiaoLi Bing ◽

Xin Zhao ◽

Michelle O’Neill ◽

...

Keyword(s):

Disease Transmission ◽

Vector Competence ◽

Wnt Signaling Pathway ◽

Sub Saharan Africa ◽

Parasite Development ◽

Mammalian Host ◽

Tsetse Flies ◽

Insect Vector ◽

Coat Proteins ◽

African Trypanosomes

Tsetse flies are biological vectors of African trypanosomes, the protozoan parasites responsible for causing human and animal trypanosomiases across sub-Saharan Africa. Currently, no vaccines are available for disease prevention due to antigenic variation of the Variant Surface Glycoproteins (VSG) that coat parasites while they reside within mammalian hosts. As a result, interference with parasite development in the tsetse vector is being explored to reduce disease transmission. A major bottleneck to infection occurs as parasites attempt to colonize tsetse’s midgut. One critical factor influencing this bottleneck is the fly’s peritrophic matrix (PM), a semipermeable, chitinous barrier that lines the midgut. The mechanisms that enable trypanosomes to cross this barrier are currently unknown. Here, we determined that as parasites enter the tsetse’s gut, VSG molecules released from trypanosomes are internalized by cells of the cardia—the tissue responsible for producing the PM. VSG internalization results in decreased expression of a tsetse microRNA (mir-275) and interferes with the Wnt-signaling pathway and the Iroquois/IRX transcription factor family. This interference reduces the function of the PM barrier and promotes parasite colonization of the gut early in the infection process. Manipulation of the insect midgut homeostasis by the mammalian parasite coat proteins is a novel function and indicates that VSG serves a dual role in trypanosome biology—that of facilitating transmission through its mammalian host and insect vector. We detail critical steps in the course of trypanosome infection establishment that can serve as novel targets to reduce the tsetse’s vector competence and disease transmission.

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Tsetse fly distribution and occurrence of Trypanosoma species among cattle and goats around Queen Elizabeth National park, Uganda

10.21203/rs.3.rs-32266/v2 ◽

2020 ◽

Author(s):

Mallion Kangume ◽

Denis Muhangi ◽

Joseph Byaruhanga ◽

Aggrey Agaba ◽

Joachim Sserunkuma ◽

...

Keyword(s):

National Park ◽

Glossina Pallidipes ◽

Dual Infection ◽

Tsetse Fly ◽

Sub Saharan Africa ◽

Tsetse Flies ◽

Baseline Information ◽

Veterinary Importance ◽

Sub Saharan ◽

Animal Trypanosomiasis

Abstract Background: African Animal Trypanosomiasis (AAT) is an infectious disease of economic and veterinary importance in Sub-Saharan Africa. The current study aimed at providing baseline information on tsetse fly distribution and occurrence of Trypanosoma species in cattle and goats within and around Queen Elizabeth National Park (QENP), in western Uganda. A minimal entomological survey was conducted in April 2017 while blood samples collected from cattle (n = 576) and goats (n = 319) in June 2015 and May 2017 were subjected to Polymerase Chain Reaction (PCR) to determine the occurrence of Trypanosoma species.Results: Glossina pallidipes and G. fuscipes were the only tsetse fly species trapped in the study area with apparent density of 20.6. The overall prevalence of Trypanosoma spp. was 27% for goats and approximately 38% for cattle. The most prevalent Trypanosoma spp. in goats was T. brucei (n = 60, 18.8%) while the most prevalent in cattle was T. congolense (n = 102, 27.1%). In both cattle and goats, a dual infection of T. brucei + T. congolense was most encountered. In goats a triple infection of T. brucei + T. congolense + T. vivax was higher than that in cattle. Conclusions: Current findings show that there are two species of tsetse flies, and three species of Trypanosoma, important in transmission of AAT in both cattle and goats. Control efforts of AAT have mainly focused on cattle and this study proves that prevention and control efforts should also involve goat farmers.

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Slippery customers: How African trypanosomes evade mammalian defences

The Biochemist ◽

10.1042/bio03104008 ◽

2009 ◽

Vol 31 (4) ◽

pp. 8-11

Author(s):

Mark Carrington

Keyword(s):

Cell Biology ◽

Sub Saharan Africa ◽

Mammalian Host ◽

Tsetse Flies ◽

Insect Vector ◽

African Trypanosomiasis ◽

Long Distance ◽

African Trypanosomes ◽

Endemic Areas ◽

Sub Saharan

African trypanosomes are excellent parasites and can maintain an infection of a large mammalian host for months or years. In endemic areas, Human African Trypanosomiasis, also called sleeping sickness, has been largely unaffected by the advent of modern medicine, and trypanosomiasis of domestic livestock is a major restraint on productivity in endemic areas and is arguably the major contributor to the institutionalized poverty in much of rural sub-Saharan Africa1,2. A simple way of visualizing the effect of the livestock disease is to compare maps showing the distribution of livestock (www.ilri.org/InfoServ/Webpub/Fulldocs/Mappoverty/index.htm) and tsetse flies, the insect vector (www.fao.org/ag/AGAinfo/programmes/en/paat/maps.html): the lack of overlap is remarkable. Tsetse flies are only present in sub-Saharan Africa, and this probably restricted the spread of African trypanosomiasis until historical times. Livestock infections are now present in much of South Asia and South America, a product of long distance trade and adaptation of the trypanosomes to mechanical transmission3. The majority of research is on Trypanosoma brucei as this includes the human infective subspecies. This article provides a description of progress in the understanding the molecular details of how the trypanosome interacts with the mammalian immune system and how these studies have extended beyond this to fundamental aspects of eukaryotic cell biology.

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Steep Rebound of Chloroquine-Sensitive Plasmodium falciparum in Zimbabwe

The Journal of Infectious Diseases ◽

10.1093/infdis/jiaa368 ◽

2020 ◽

Cited By ~ 2

Author(s):

Sungano Mharakurwa ◽

Zvifadzo Matsena-Zingoni ◽

Nobert Mudare ◽

Charmaine Matimba ◽

Tanatswa Xuxa Gara ◽

...

Keyword(s):

Drug Resistance ◽

Plasmodium Falciparum ◽

Drug Policy ◽

Sub Saharan Africa ◽

Wild Type ◽

Control Programs ◽

Antimalarial Resistance ◽

Steep Decline ◽

Vital Component ◽

Sub Saharan

Abstract Removal of chloroquine from national malaria formularies can lead to the reversion of resistant Plasmodium falciparum to wild-type. We report a steep decline in chloroquine-resistant P falciparum within 10 years of national discontinuation of chloroquine monotherapy in Zimbabwe. Drug resistance surveillance is a vital component of malaria control programs, and the experience with chloroquine in Zimbabwe and elsewhere in sub-Saharan Africa is illustrative of the potentially rapid and dramatic impact of drug policy on antimalarial resistance.

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Molecular screening for Anaplasmataceae in ticks and tsetse flies from Ethiopia

Acta Veterinaria Hungarica ◽

10.1556/004.2016.007 ◽

2016 ◽

Vol 64 (1) ◽

pp. 65-70 ◽

Cited By ~ 3

Author(s):

Sándor Hornok ◽

Getachew Abichu ◽

Nóra Takács ◽

Miklós Gyuranecz ◽

Róbert Farkas ◽

...

Keyword(s):

Glossina Pallidipes ◽

Tsetse Fly ◽

Ixodid Ticks ◽

Sub Saharan Africa ◽

Tsetse Flies ◽

Ehrlichia Ruminantium ◽

Blood Sucking ◽

Sub Saharan ◽

Transmission Studies ◽

First Time

Hard ticks and tsetse flies are regarded as the most important vectors of disease agents in Sub-Saharan Africa. With the aim of screening these blood-sucking arthropods for vector-borne pathogens belonging to the family Anaplasmataceae in South-Western Ethiopia, four species of tsetse flies (collected by traps) and seven species of ixodid ticks (removed from cattle) were molecularly analysed. DNA was extracted from 296 individual ticks and from 162 individuals or pools of tsetse flies. Besides known vector–pathogen associations, in Amblyomma cohaerens ticks sequences of Anaplasma marginale and A. phagocytophilum were detected, the latter for the first time in any ticks from cattle in Africa. In addition, part of the gltA gene of Ehrlichia ruminantium was successfully amplified from tsetse flies (Glossina pallidipes). First-time identification of sequences of the above pathogens in certain tick or tsetse fly species may serve as the basis of further epidemiological and transmission studies.

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Tsetse blood-meal sources, endosymbionts, and trypanosome infections provide insight into African trypanosomiasis transmission in the Maasai Mara National Reserve, a wildlife-human-livestock interface

10.1101/2020.04.06.027367 ◽

2020 ◽

Cited By ~ 1

Author(s):

Edward Edmond Makhulu ◽

Jandouwe Villinger ◽

Vincent Owino Adunga ◽

Maamun M. Jeneby ◽

Edwin Murungi Kimathi ◽

...

Keyword(s):

Blood Meal ◽

Vector Competence ◽

Glossina Pallidipes ◽

Tsetse Fly ◽

Tsetse Flies ◽

African Buffalo ◽

African Trypanosomiasis ◽

Trypanosome Infection ◽

African Trypanosomes ◽

Blood Meals

AbstractBackgroundAfrican trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Understanding of AT transmission is hampered by limited knowledge on interactions of tsetse flies with their vertebrate hosts and the influence of endosymbionts on vector competence, especially in wildlife-human-livestock interfaces. We identified the tsetse species, their blood-meal sources, and the correlation between endosymbiont and trypanosome infection status in the trypanosome-endemic Maasai Mara National Reserve (MMNR) of Kenya.Methodology/Principal FindingsAmong 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosomes, majority (17/28) being Trypanosoma vivax. Blood-meal analyses based on high-resolution melting analysis of mitochondrial cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 345) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Trypanosome-infected flies had fed on hippopotamus and buffalo. Additionally, PCR analysis revealed that tsetse flies were more likely to be infected with trypanosomes if they were infected with the Sodalis glossinidius endosymbiont (P = 0.0022 Fisher’s exact test).Conclusions/SignificanceDiverse species of wildlife hosts may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes in the MMNR. Although the African buffalo is known to be a key reservoir of AT, the higher proportion of hippopotamus blood-meals in trypanosomes-infected flies identified here indicates that other wildlife species may also be important to transmission cycles. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis transmission risk. Furthermore, this work provides data showing that Sodalis endosymbionts can is associated with increased trypanosome infection rates in endemic ecologies.Author summaryHuman and animal African trypanosomiasis are neglected tropical diseases with potential to spread to new areas. Wild animals are important reservoirs for African trypanosomes and crucial in the emergence and re-emergence of AT. Vertebrate host-vector-parasite interactions are integral to trypanosome transmission. We investigated the vertebrate blood-meals and trypanosomes-endosymbionts co-infections in tsetse flies, which have been associated with reservoirs and vector competence, respectively, on AT transmission in Kenya’s Maasai Mara National Reserve. We identified tsetse fly diversity, trypanosome and endosymbiont infection status, and vertebrate blood-meal hosts to infer potential transmission dynamics. We found that Glossina pallidipes was the major tsetse fly vector and that Trypanosoma vivax was the main trypanosome species circulating in the region. Humans, hippopotamus, and buffalo were the most frequented for blood-meals. Buffalo and hippopotamus blood-meals were identified in trypanosome infected flies. Feeding of the flies on both humans and wildlife may potentiate the risk of the human trypanosomiasis in this ecology. Additionally, we found that the endosymbiont Sodalis glossinidius is associated with higher trypanosome infection rates in wild tsetse flies. These findings emphasize the importance of understanding the interaction of tsetse flies with vertebrate blood-meal sources and their endosymbionts in the transmission and control of AT.

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