Infection With the Secondary Tsetse-Endosymbiont Sodalis glossinidius (Enterobacteriales: Enterobacteriaceae) Influences Parasitism in Glossina pallidipes (Diptera: Glossinidae)

Wamwiri, Florence N.; Ndung’u, Kariuki; Thande, Paul C.; Thungu, Daniel; Auma, Joanna E.; Ngure, R. M.

doi:10.1093/jisesa/ieu134

Cited by 16 publications

(18 citation statements)

References 28 publications

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“…Our finding that higher proportions of tsetse flies infected with the endosymbiont S. glossinidus were infected with trypanosomes than those without S. glossinidius corroborates previous studies that suggest that S. glossinidius infection may have the potential to increase the ability of both wild caught [40,41] and lab reared [42,75] tsetse flies to acquire trypanosomes. Further, this finding implies that S. glossinidius infection in tsetse populations may be used as a positive indicator of trypanosomiasis risk.…”

Section: Discussionsupporting

confidence: 91%

“…Our findings revealed that humans, hippopotamus, and African buffaloes were the most frequent blood-meal sources of tsetse flies in the MMNR. We also found that the endosymbiont, S. glossinidius , was positively correlated with trypanosome infection in wild-caught G. pallidipes tsetse flies in the MMNR, supporting the hypothesis that Sodalis potentiates AAT transmission in tsetse flies [40–42]. However, we found no correlation between Wolbachia and trypanosome infections, and no evidence of SGHV endosymbionts in the tsetse populations analyzed.…”

Section: Discussionsupporting

confidence: 81%

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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

Makhulu

Villinger

Adung’a

et al. 2020

Preprint

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36 Background: African trypanosomiasis (AT) is a neglected disease of both humans and animals 37 caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies 38 (Glossina spp.). Understanding of AT transmission is hampered by limited knowledge on 39 interactions of tsetse flies with their vertebrate hosts and the influence of endosymbionts on 40 vector competence, especially in wildlife-human-livestock interfaces. We identified the tsetse 41 species, their blood-meal sources, and the correlation between endosymbiont and trypanosome 42 infection status in the trypanosome-endemic Maasai Mara National Reserve (MMNR) of Kenya.3 43 Methodology/Principal Findings: Among 1167 tsetse flies (1136 Glossina pallidipes, 31 44 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for 45 trypanosomes, majority (17/28) being Trypanosoma vivax. Blood-meal analyses based on high-46 resolution melting analysis of mitochondrial cytochrome c oxidase 1 and cytochrome b gene 47 PCR products (n = 345) identified humans as the most common vertebrate host (37%), followed 48 by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%) , and giraffe (0.84%).49 Trypanosome-infected flies had fed on hippopotamus and buffalo. Additionally, PCR analysis 50 revealed that tsetse flies were more likely to be infected with trypanosomes if they were infected 51 with the Sodalis glossinidius endosymbiont (P = 0.0022 Fisher's exact test).52 Conclusions/Significance: Diverse species of wildlife hosts may contribute to the maintenance 53 of tsetse populations and/or persistent circulation of African trypanosomes in the MMNR.54 Although the African buffalo is known to be a key reservoir of AT, the higher proportion of 55 hippopotamus blood-meals in trypanosomes-infected flies identified here indicates that other 56 wildlife species may also be important to transmission cycles. No trypanosomes associated with 57 human disease were identified, but the high proportion of human blood-meals identified are 58 indicative of human African trypanosomiasis transmission risk. Furthermore, this work provides 59 data showing that Sodalis endosymbionts can is associated with increased trypanosome infection 60 rates in endemic ecologies. 61Author summary 62 Human and animal African trypanosomiasis are neglected tropical diseases with potential to 63 spread to new areas. Wild animals are important reservoirs for African trypanosomes and crucial 64 in the emergence and re-emergence of AT. Vertebrate host-vector-parasite interactions are 65 integral to trypanosome transmission. We investigated the vertebrate blood-meals and 4 66 trypanosomes-endosymbionts co-infections in tsetse flies, which have been associated with 67 reservoirs and vector competence, respectively, on AT transmission in Kenya's Maasai Mara 68 National Reserve. We identified tsetse fly diversity, trypanosome and endosymbiont infection 69 status, and vertebrate blood-meal hosts to infer potential transmission dynamics. We found 70...

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 81%

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

Makhulu

Villinger

Adung’a

et al. 2020

Preprint

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“…Other experimental studies revealed that the correlation between S. glossinidius and the ability of trypanosome to infect tsetse flies is trypanosome species-specific. For example, Wamwiri et al [ 25 ] demonstrated that teneral male G. pallidipes were about 6 times more likely to become infected by T. b. rhodesiense if they were infected with S. glossinidius while infection by T. b. brucei was not correlated with the presence of the endosymbiont. Wamwiri et al [ 25 ] also showed that T. congolense infection was 1.3 times more likely in flies not showing the presence of S. glossinidius .…”

Section: Introductionmentioning

confidence: 99%

Sodalis glossinidius presence in wild tsetse is only associated with presence of trypanosomes in complex interactions with other tsetse-specific factors

et al. 2018

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BackgroundSusceptibility of tsetse flies (Glossina spp.) to trypanosomes of both humans and animals has been associated with the presence of the endosymbiont Sodalis glossinidius. However, intrinsic biological characteristics of the flies and environmental factors can influence the presence of both S. glossinidius and the parasites. It thus remains unclear whether it is the S. glossinidius or other attributes of the flies that explains the apparent association. The objective of this study was to test whether the presence of Trypanosoma vivax, T. congolense and T. brucei are related to the presence of S. glossinidius in tsetse flies when other factors are accounted for: geographic location, species of Glossina, sex or age of the host flies.ResultsFlies (n = 1090) were trapped from four sites in the Shimba Hills and Nguruman regions in Kenya. Sex and species of tsetse (G. austeni, G. brevipalpis, G. longipennis and G. pallidipes) were determined based on external morphological characters and age was estimated by a wing fray score method. The presence of trypanosomes and S. glossinidius was detected using PCR targeting the internal transcribed spacer region 1 and the haemolysin gene, respectively. Sequencing was used to confirm species identification. Generalised Linear Models (GLMs) and Multiple Correspondence Analysis (MCA) were applied to investigate multivariable associations. The overall prevalence of trypanosomes was 42.1%, but GLMs revealed complex patterns of associations: the presence of S. glossinidius was associated with trypanosome presence but only in interactions with other factors and only in some species of trypanosomes. The strongest association was found for T. congolense, and no association was found for T. vivax. The MCA also suggested only a weak association between the presence of trypanosomes and S. glossinidius. Trypanosome-positive status showed strong associations with sex and age while S. glossinidius-positive status showed a strong association with geographic location and species of fly.ConclusionsWe suggest that previous conclusions about the presence of endosymbionts increasing probability of trypanosome presence in tsetse flies may have been confounded by other factors, such as community composition of the tsetse flies and the specific trypanosomes found in different regions.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1285-6) contains supplementary material, which is available to authorized users.

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“…Moreover, it will also be critical to ensure that the recombinant Sodalis strain is transmitted from mother to offspring with a nearly 100% probability, and that it imposes only minor fecundity or mortality penalties. There is evidence that unmodified Sodalis alone may affect the fecundity or mortality of some tsetse species [ 14 , 26 , 27 ]. Of particular importance is the engineering of recombinant Sodalis to produce a molecule that effectively targets trypanosomes without simultaneously reducing the fitness of Sodalis .…”

Section: Discussionmentioning

confidence: 99%

Determinants of Human African Trypanosomiasis Elimination via Paratransgenesis

et al. 2016

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Human African trypanosomiasis (HAT), transmitted by tsetse flies, has historically infected hundreds of thousands of individuals annually in sub-Saharan Africa. Over the last decade, concerted control efforts have reduced reported cases to below 10,000 annually, bringing complete elimination within reach. A potential technology to eliminate HAT involves rendering the flies resistant to trypanosome infection. This approach can be achieved through the introduction of transgenic Sodalis symbiotic bacteria that have been modified to produce a trypanocide, and propagated via Wolbachia symbionts, which confer a reproductive advantage to the paratransgenic tsetse. However, the population dynamics of these symbionts within tsetse flies have not yet been evaluated. Specifically, the key factors that determine the effectiveness of paratransgenesis have yet to be quantified. To identify the impact of these determinants on T.b. gambiense and T.b. rhodesiense transmission, we developed a mathematical model of trypanosome transmission that incorporates tsetse and symbiont population dynamics. We found that fecundity and mortality penalties associated with Wolbachia or recombinant Sodalis colonization, probabilities of vertical transmission, and tsetse migration rates are fundamental to the feasibility of HAT elimination. For example, we determined that HAT elimination could be sustained over 25 years when Wolbachia colonization minimally impacted fecundity or mortality, and when the probability of recombinant Sodalis vertical transmission exceeded 99.9%. We also found that for a narrow range of recombinant Sodalis vertical transmission probability (99.9–90.6% for T.b. gambiense and 99.9–85.8% for T.b. rhodesiense), cumulative HAT incidence was reduced between 30% and 1% for T.b. gambiense and between 21% and 3% for T.b. rhodesiense, although elimination was not predicted. Our findings indicate that fitness and mortality penalties associated with paratransgenic symbionts, as well as tsetse migration rates, are instrumental to HAT elimination, and should be a key focus in the development of paratransgenic symbionts.

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Infection With the Secondary Tsetse-Endosymbiont Sodalis glossinidius (Enterobacteriales: Enterobacteriaceae) Influences Parasitism in Glossina pallidipes (Diptera: Glossinidae)

Cited by 16 publications

References 28 publications

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

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

Sodalis glossinidius presence in wild tsetse is only associated with presence of trypanosomes in complex interactions with other tsetse-specific factors

Determinants of Human African Trypanosomiasis Elimination via Paratransgenesis

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