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Anne Geiger - One of the best experts on this subject based on the ideXlab platform.
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Prevalence of symbionts and trypanosome infections in tsetse flies of two villages of the “Faro and Déo” division of the Adamawa region of Cameroon
BMC Microbiology, 2018Co-Authors: Ginette Irma Kame-ngasse, Flobert Njiokou, Oumarou Farikou, Gustave Simo, Tito Trésor Melachio-tanekou, Anne GeigerAbstract:Background Tsetse flies are vectors of human and animal African trypanosomiasis. In spite of many decades of chemotherapy and vector control, the disease has not been eradicated. Other methods like the transformation of tsetse fly symbionts to render the fly refractory to trypanosome infection are being evaluated. The aim of the present study was to evaluate the association between trypanosome infections and the presence of symbionts in these tsetse species. Tsetse flies were trapped in two villages of the “Faro and Déo” Division of the Adamawa region of Cameroon. In the field, tsetse fly species were identified and their infection by trypanosomes was checked by microscopy. In the laboratory, DNA was extracted from their midguts and the presence of symbionts ( Sodalis glossinidius and Wolbachia sp.) and trypanosomes was checked by PCR. Symbionts/trypanosomes association tests were performed. Results Three tsetse fly species including Glossina tachinoides (90.1%), Glossina morsitans submorsitans (9.4%) and Glossina fuscipes fuscipes (0.5%) were caught. In all the population we obtained an occurrence rate of 37.2% for Sodalis glossinidius and 67.6% for Wolbachia irrespective to tsetse flies species. S. glossinidius and Wolbachia sp. occurrence rates were respectively 37 and 68% for G. tachinoides and 28.6 and 59.5% for G. m. submorsitans . Between Golde Bourle and Mayo Dagoum significant differences were observed in the prevalence of symbionts. Prevalence of trypanosomes were 34.8% for Glossina tachinoides and 40.5% for Glossina morsitans submorsitans. In G. tachinoides, the trypanosome infection rates were 11, 2.6 and 13.7%, respectively, for T. brucei s.l., T. congolense forest type and T. congolense savannah type. In G. m. submorsitans, these infection rates were 16.7, 9.5 and, 2.4% respectively, for T. brucei s.l. , T. congolense forest type and T. congolense savannah type. Conclusions The rate of tsetse fly infection by trypanosomes was low compared to those obtained in HAT foci of south Cameroon, and this rate was not statistically linked to the rate of symbiont occurrence. This study allowed to show for the first time the presence of Wolbachia sp. in the tsetse fly sub-species Glossina morsitans submorsitans and Glossina tachinoides .
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Prevalence of symbionts and trypanosome infections in tsetse flies of two villages of the "Faro and Déo" division of the Adamawa region of Cameroon.
BMC microbiology, 2018Co-Authors: Ginette Irma Kame-ngasse, Flobert Njiokou, Oumarou Farikou, Gustave Simo, Tito Trésor Melachio-tanekou, Anne GeigerAbstract:Tsetse flies are vectors of human and animal African trypanosomiasis. In spite of many decades of chemotherapy and vector control, the disease has not been eradicated. Other methods like the transformation of tsetse fly symbionts to render the fly refractory to trypanosome infection are being evaluated. The aim of the present study was to evaluate the association between trypanosome infections and the presence of symbionts in these tsetse species. Tsetse flies were trapped in two villages of the "Faro and Déo" Division of the Adamawa region of Cameroon. In the field, tsetse fly species were identified and their infection by trypanosomes was checked by microscopy. In the laboratory, DNA was extracted from their midguts and the presence of symbionts (Sodalis glossinidius and Wolbachia sp.) and trypanosomes was checked by PCR. Symbionts/trypanosomes association tests were performed. Three tsetse fly species including Glossina tachinoides (90.1%), Glossina morsitans submorsitans (9.4%) and Glossina fuscipes fuscipes (0.5%) were caught. In all the population we obtained an occurrence rate of 37.2% for Sodalis glossinidius and 67.6% for Wolbachia irrespective to tsetse flies species. S. glossinidius and Wolbachia sp. occurrence rates were respectively 37 and 68% for G. tachinoides and 28.6 and 59.5% for G. m. submorsitans. Between Golde Bourle and Mayo Dagoum significant differences were observed in the prevalence of symbionts. Prevalence of trypanosomes were 34.8% for Glossina tachinoides and 40.5% for Glossina morsitans submorsitans. In G. tachinoides, the trypanosome infection rates were 11, 2.6 and 13.7%, respectively, for T. brucei s.l., T. congolense forest type and T. congolense savannah type. In G. m. submorsitans, these infection rates were 16.7, 9.5 and, 2.4% respectively, for T. brucei s.l., T. congolense forest type and T. congolense savannah type. The rate of tsetse fly infection by trypanosomes was low compared to those obtained in HAT foci of south Cameroon, and this rate was not statistically linked to the rate of symbiont occurrence. This study allowed to show for the first time the presence of Wolbachia sp. in the tsetse fly sub-species Glossina morsitans submorsitans and Glossina tachinoides.
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Blood feeding tsetse flies as hosts and vectors of mammals-pre-adapted African Trypanosoma: current and expected research directions
BMC Microbiology, 2018Co-Authors: Anne Geiger, Imna Malele, Adly M Abd-alla, Flobert NjiokouAbstract:Research on the zoo-anthropophilic blood feeding tsetse flies’ biology conducted, by different teams, in laboratory settings and at the level of the ecosystems- where also co-perpetuate African Trypanosoma- has allowed to unveil and characterize key features of tsetse flies’ bacterial symbionts on which rely both (a) the perpetuation of the tsetse fly populations and (b) the completion of the developmental program of the African Trypanosoma . Transcriptomic analyses have already provided much information on tsetse fly genes as well as on genes of the fly symbiotic partners Sodalis glossinidius and Wigglesworthia, which account for the successful onset or not of the African Trypanosoma developmental program. In parallel, identification of the non- symbiotic bacterial communities hosted in the tsetse fly gut has recently been initiated: are briefly introduced those bacteria genera and species common to tsetse flies collected from distinct ecosystems, that could be further studied as potential biologicals preventing the onset of the African Trypanosoma developmental program. Finally, future work will need to concentrate on how to render tsetse flies refractory, and the best means to disseminate them in the field in order to establish an overall refractory fly population.
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Technical data of the transcriptomic analysis performed on tsetse fly symbionts, Sodalis glossinidius and Wigglesworthia glossinidia, harbored, respectively by non-infected, Trypanosoma brucei gambiense infected and self-cured Glossina palpalis gambi
Genomics data, 2015Co-Authors: Anne Geiger, Bernadette Tchicaya, Pascal RihetAbstract:Microarray is a powerful and cheap method to identify and quantify gene expression in particular in a mix of total RNA extracted from biological samples such as the tsetse fly gut, including several organisms (here, the fly tissue and the intestinal microorganisms). Besides, biostatistics and bioinformatics allow comparing the transcriptomes from samples collected from differently treated flies, and thus to identify and quantify differential expressed genes. Here, we describe in details a whole microarray transcriptome dataset produced from tsetse flies symbionts, Sodalis glossinidius and Wigglesworthia glossinidia. The tsetse fly midguts were sampled at key steps of tsetse fly infection by trypanosomes, 3-day and 10-day sampling times to target differentially expressed genes involved, respectively, in early events associated with trypanosome entry into the midgut and with the establishment of infection; 20 days to target the genes involved in events occurring later in the infection process. We describe in detail the methodology applied for analyzing the microarray data including differential expression as well as functional annotation of the identified symbiont genes. Both the microarray data and design are available at http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE48360;http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE48361;http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE55931.
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the transcriptional signatures of Sodalis glossinidius in the glossina palpalis gambiensis flies negative for trypanosoma brucei gambiense contrast with those of this symbiont in tsetse flies positive for the parasite possible involvement of a sodali
Infection Genetics and Evolution, 2014Co-Authors: Illiassou Hamidou Soumana, Sophie Ravel, Bernadette Tchicaya, Pascal Rihet, Beatrice Loriod, Gustave Simo, Anne GeigerAbstract:Abstract Tsetse flies, such as Glossina palpalis gambiensis , are blood-feeding insects that could be subverted as hosts of the parasite Trypanosoma brucei gambiense : initiated in the tsetse fly mid gut, the developmental program of this parasite further proceeds in the salivary glands. The flies act as vectors of this human-invasive parasite when their salivary glands sustain the generation of metacyclic trypomastigotes, the exclusive morphotypes pre-programmed to further develop in the human individuals. Briefly, once the metacyclic trypomastigotes have been deposited in the skin of humans from whom the parasite-hosting tsetse flies are taking their blood meals, the complex developmental program of this Trypanosoma brucei subspecies can result in a severe disease named sleeping sickness. Unveiling the processes that could prevent, in tsetse flies, the developmental program of T. b. gambiense could contribute reducing the prevalence of the disease. Using a global approach, we were curious to extract transcriptional signatures of Sodalis glossinidius , a symbiont hosted by three distinct groups of tsetse flies. To meet this objective, the transcriptome of S. glossinidius from susceptible and refractory tsetse flies was analyzed at 3, 10 and 20 days after flies blood feed on T. b. gambiense -hosting mice. Within this temporal window, 176 trypanosome responsive genes were shown to interact in well-defined patterns making it possible to distinguish flies susceptible to the parasite infection from refractory flies. Among the modulated transcripts in the symbiont population of flies refractory to trypanosome infection many were shown to cluster within the following networks: “lysozyme activity, bacteriolytic enzyme, bacterial cytolysis, cell wall macromolecule catabolic process”. These novel data are further delineated in the following questions: could the activation of prophage hosted by S. glossinidius lead to the release of bacterial agonists that trigger the tsetse fly immune system along a profile that no more allows the parasite developmental program?
Jan Van Den Abbeele - One of the best experts on this subject based on the ideXlab platform.
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The Tsetse Fly Displays an Attenuated Immune Response to Its Secondary Symbiont, Sodalis glossinidius.
Frontiers in microbiology, 2019Co-Authors: Katrien Trappeniers, Jan Van Den Abbeele, Irina Matetovici, Linda De VooghtAbstract:Sodalis glossinidius, a vertically transmitted facultative symbiont of the tsetse fly, is a bacterium in the early/intermediate state of its transition toward symbiosis, representing an important model for investigating how the insect host immune defense response is regulated to allow endosymbionts to establish a chronic infection within their hosts without being eliminated. In this study, we report on the establishment of a tsetse fly line devoid of S. glossinidius only, allowing us to experimentally investigate i) the complex immunological interactions between a single bacterial species and its host, ii) how the symbiont population is kept under control, and iii) the impact of the symbiont on the vector competence of the tsetse fly to transmit the sleeping sickness parasite. Comparative transcriptome analysis showed no difference in the expression of genes involved in innate immune processes between symbiont-harbouring (GmmSod+) and S. glossinidius-free (GmmSod-) flies. Re-exposure of (GmmSod-) flies to the endosymbiotic bacterium resulted in a moderate immune response, whereas exposure to pathogenic E. coli or to a close non-insect associated relative of S. glossinidius, i.e. S. praecaptivus, resulted in full immune activation. We also showed that S. glossinidius densities are not affected by experimental activation or suppression of the host immune system, indicating that S. glossinidius is resistant to mounted immune attacks and that the host immune system does not play a major role in controlling S. glossinidius proliferation. Finally, we demonstrate that the absence or presence of S. glossinidius in the tsetse fly does not alter its capacity to mount an immune response to pathogens nor does it affect the fly’s susceptibility towards trypanosome infection.
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Combining paratransgenesis with SIT: impact of ionizing radiation on the DNA copy number of Sodalis glossinidius in tsetse flies
BMC Microbiology, 2018Co-Authors: Güler Demirbas-uzel, Jan Van Den Abbeele, Linda De Vooght, Andrew G. Parker, Marc J. B. Vreysen, Robert L. Mach, Adly M. M. Abd-allaAbstract:Background Tsetse flies (Diptera: Glossinidae) are the cyclical vectors of the causative agents of African Trypanosomosis, which has been identified as a neglected tropical disease in both humans and animals in many regions of sub-Saharan Africa. The sterile insect technique (SIT) has shown to be a powerful method to manage tsetse fly populations when used in the frame of an area-wide integrated pest management (AW-IPM) program. To date, the release of sterile males to manage tsetse fly populations has only been implemented in areas to reduce transmission of animal African Trypanosomosis (AAT). The implementation of the SIT in areas with Human African Trypanosomosis (HAT) would require additional measures to eliminate the potential risk associated with the release of sterile males that require blood meals to survive and hence, might contribute to disease transmission. Paratransgenesis offers the potential to develop tsetse flies that are refractory to trypanosome infection by modifying their associated bacteria (Sodalis glossinidius) here after referred to as Sodalis. Here we assessed the feasibility of combining the paratransgenesis approach with SIT by analyzing the impact of ionizing radiation on the copy number of Sodalis and the vectorial capacity of sterilized tsetse males.
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Combining paratransgenesis with SIT: impact of ionizing radiation on the DNA copy number of Sodalis glossinidius in tsetse flies.
BMC microbiology, 2018Co-Authors: Güler Demirbas-uzel, Jan Van Den Abbeele, Linda De Vooght, Andrew G. Parker, Marc J. B. Vreysen, Robert L. Mach, Adly M. M. Abd-allaAbstract:Tsetse flies (Diptera: Glossinidae) are the cyclical vectors of the causative agents of African Trypanosomosis, which has been identified as a neglected tropical disease in both humans and animals in many regions of sub-Saharan Africa. The sterile insect technique (SIT) has shown to be a powerful method to manage tsetse fly populations when used in the frame of an area-wide integrated pest management (AW-IPM) program. To date, the release of sterile males to manage tsetse fly populations has only been implemented in areas to reduce transmission of animal African Trypanosomosis (AAT). The implementation of the SIT in areas with Human African Trypanosomosis (HAT) would require additional measures to eliminate the potential risk associated with the release of sterile males that require blood meals to survive and hence, might contribute to disease transmission. Paratransgenesis offers the potential to develop tsetse flies that are refractory to trypanosome infection by modifying their associated bacteria (Sodalis glossinidius) here after referred to as Sodalis. Here we assessed the feasibility of combining the paratransgenesis approach with SIT by analyzing the impact of ionizing radiation on the copy number of Sodalis and the vectorial capacity of sterilized tsetse males. Adult Glossina morsitans morsitans that emerged from puparia irradiated on day 22 post larviposition did not show a significant decline in Sodalis copy number as compared with non-irradiated flies. Conversely, the Sodalis copy number was significantly reduced in adults that emerged from puparia irradiated on day 29 post larviposition and in adults irradiated on day 7 post emergence. Moreover, irradiating 22-day old puparia reduced the copy number of Wolbachia and Wigglesworthia in emerged adults as compared with non-irradiated controls, but the radiation treatment had no significant impact on the vectorial competence of the flies. Although the radiation treatment significantly reduced the copy number of some tsetse fly symbionts, the copy number of Sodalis recovered with time in flies irradiated as 22-day old puparia. This recovery offers the opportunity to combine a paratransgenesis approach - using modified Sodalis to produce males refractory to trypanosome infection - with the release of sterile males to minimize the risk of disease transmission, especially in HAT endemic areas. Moreover, irradiation did not increase the vector competence of the flies for trypanosomes.
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Combining paratransgenesis with SIT: impact of ionizing radiation on the DNA copy number of Sodalis glossinidius in tsetse flies
BMC Microbiology, 2018Co-Authors: Güler Demirbas-uzel, Jan Van Den Abbeele, Linda De Vooght, Andrew G. Parker, Marc J. B. Vreysen, Robert L. Mach, Adly M. M. Abd-allaAbstract:Background Tsetse flies (Diptera: Glossinidae) are the cyclical vectors of the causative agents of African Trypanosomosis, which has been identified as a neglected tropical disease in both humans and animals in many regions of sub-Saharan Africa. The sterile insect technique (SIT) has shown to be a powerful method to manage tsetse fly populations when used in the frame of an area-wide integrated pest management (AW-IPM) program. To date, the release of sterile males to manage tsetse fly populations has only been implemented in areas to reduce transmission of animal African Trypanosomosis (AAT). The implementation of the SIT in areas with Human African Trypanosomosis (HAT) would require additional measures to eliminate the potential risk associated with the release of sterile males that require blood meals to survive and hence, might contribute to disease transmission. Paratransgenesis offers the potential to develop tsetse flies that are refractory to trypanosome infection by modifying their associated bacteria ( Sodalis glossinidius ) here after referred to as Sodalis . Here we assessed the feasibility of combining the paratransgenesis approach with SIT by analyzing the impact of ionizing radiation on the copy number of Sodalis and the vectorial capacity of sterilized tsetse males. Results Adult Glossina morsitans morsitans that emerged from puparia irradiated on day 22 post larviposition did not show a significant decline in Sodalis copy number as compared with non-irradiated flies. Conversely, the Sodalis copy number was significantly reduced in adults that emerged from puparia irradiated on day 29 post larviposition and in adults irradiated on day 7 post emergence. Moreover, irradiating 22-day old puparia reduced the copy number of Wolbachia and Wigglesworthia in emerged adults as compared with non-irradiated controls, but the radiation treatment had no significant impact on the vectorial competence of the flies. Conclusion Although the radiation treatment significantly reduced the copy number of some tsetse fly symbionts, the copy number of Sodalis recovered with time in flies irradiated as 22-day old puparia. This recovery offers the opportunity to combine a paratransgenesis approach – using modified Sodalis to produce males refractory to trypanosome infection – with the release of sterile males to minimize the risk of disease transmission, especially in HAT endemic areas. Moreover, irradiation did not increase the vector competence of the flies for trypanosomes.
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paternal transmission of a secondary symbiont during mating in the viviparous tsetse fly
Molecular Biology and Evolution, 2015Co-Authors: Linda De Vooght, Guy Caljon, Jan Van Den Abbeele, Jos Van HeesAbstract:Sodalis glossinidius, a maternally inherited secondary symbiont of the tsetse fly, is a bacterium in the early/intermediate state of the transition toward symbiosis, representing an important model for investigating establishment and evolution of insect-bacteria symbiosis. The absence of phylogenetic congruence in tsetse-Sodalis coevolution and the existence of Sodalis genotypic diversity in field flies are suggestive for a horizontal transmission route. However, to date no natural mechanism for the horizontal transfer of this symbiont has been identified. Using novel methodologies for the stable fluorescent-labeling and introduction of modified Sodalis in tsetse flies, we unambiguously show that male-borne Sodalis is 1) horizontally transferred to females during mating and 2) subsequently vertically transmitted to the progeny, that is, paternal transmission. This mixed mode of transmission has major consequences regarding Sodalis' genome evolution as it can lead to coinfections creating opportunities for lateral gene transfer which in turn could affect the interaction with the tsetse host.
Linda De Vooght - One of the best experts on this subject based on the ideXlab platform.
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The Tsetse Fly Displays an Attenuated Immune Response to Its Secondary Symbiont, Sodalis glossinidius.
Frontiers in microbiology, 2019Co-Authors: Katrien Trappeniers, Jan Van Den Abbeele, Irina Matetovici, Linda De VooghtAbstract:Sodalis glossinidius, a vertically transmitted facultative symbiont of the tsetse fly, is a bacterium in the early/intermediate state of its transition toward symbiosis, representing an important model for investigating how the insect host immune defense response is regulated to allow endosymbionts to establish a chronic infection within their hosts without being eliminated. In this study, we report on the establishment of a tsetse fly line devoid of S. glossinidius only, allowing us to experimentally investigate i) the complex immunological interactions between a single bacterial species and its host, ii) how the symbiont population is kept under control, and iii) the impact of the symbiont on the vector competence of the tsetse fly to transmit the sleeping sickness parasite. Comparative transcriptome analysis showed no difference in the expression of genes involved in innate immune processes between symbiont-harbouring (GmmSod+) and S. glossinidius-free (GmmSod-) flies. Re-exposure of (GmmSod-) flies to the endosymbiotic bacterium resulted in a moderate immune response, whereas exposure to pathogenic E. coli or to a close non-insect associated relative of S. glossinidius, i.e. S. praecaptivus, resulted in full immune activation. We also showed that S. glossinidius densities are not affected by experimental activation or suppression of the host immune system, indicating that S. glossinidius is resistant to mounted immune attacks and that the host immune system does not play a major role in controlling S. glossinidius proliferation. Finally, we demonstrate that the absence or presence of S. glossinidius in the tsetse fly does not alter its capacity to mount an immune response to pathogens nor does it affect the fly’s susceptibility towards trypanosome infection.
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Combining paratransgenesis with SIT: impact of ionizing radiation on the DNA copy number of Sodalis glossinidius in tsetse flies
BMC Microbiology, 2018Co-Authors: Güler Demirbas-uzel, Jan Van Den Abbeele, Linda De Vooght, Andrew G. Parker, Marc J. B. Vreysen, Robert L. Mach, Adly M. M. Abd-allaAbstract:Background Tsetse flies (Diptera: Glossinidae) are the cyclical vectors of the causative agents of African Trypanosomosis, which has been identified as a neglected tropical disease in both humans and animals in many regions of sub-Saharan Africa. The sterile insect technique (SIT) has shown to be a powerful method to manage tsetse fly populations when used in the frame of an area-wide integrated pest management (AW-IPM) program. To date, the release of sterile males to manage tsetse fly populations has only been implemented in areas to reduce transmission of animal African Trypanosomosis (AAT). The implementation of the SIT in areas with Human African Trypanosomosis (HAT) would require additional measures to eliminate the potential risk associated with the release of sterile males that require blood meals to survive and hence, might contribute to disease transmission. Paratransgenesis offers the potential to develop tsetse flies that are refractory to trypanosome infection by modifying their associated bacteria (Sodalis glossinidius) here after referred to as Sodalis. Here we assessed the feasibility of combining the paratransgenesis approach with SIT by analyzing the impact of ionizing radiation on the copy number of Sodalis and the vectorial capacity of sterilized tsetse males.
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Combining paratransgenesis with SIT: impact of ionizing radiation on the DNA copy number of Sodalis glossinidius in tsetse flies.
BMC microbiology, 2018Co-Authors: Güler Demirbas-uzel, Jan Van Den Abbeele, Linda De Vooght, Andrew G. Parker, Marc J. B. Vreysen, Robert L. Mach, Adly M. M. Abd-allaAbstract:Tsetse flies (Diptera: Glossinidae) are the cyclical vectors of the causative agents of African Trypanosomosis, which has been identified as a neglected tropical disease in both humans and animals in many regions of sub-Saharan Africa. The sterile insect technique (SIT) has shown to be a powerful method to manage tsetse fly populations when used in the frame of an area-wide integrated pest management (AW-IPM) program. To date, the release of sterile males to manage tsetse fly populations has only been implemented in areas to reduce transmission of animal African Trypanosomosis (AAT). The implementation of the SIT in areas with Human African Trypanosomosis (HAT) would require additional measures to eliminate the potential risk associated with the release of sterile males that require blood meals to survive and hence, might contribute to disease transmission. Paratransgenesis offers the potential to develop tsetse flies that are refractory to trypanosome infection by modifying their associated bacteria (Sodalis glossinidius) here after referred to as Sodalis. Here we assessed the feasibility of combining the paratransgenesis approach with SIT by analyzing the impact of ionizing radiation on the copy number of Sodalis and the vectorial capacity of sterilized tsetse males. Adult Glossina morsitans morsitans that emerged from puparia irradiated on day 22 post larviposition did not show a significant decline in Sodalis copy number as compared with non-irradiated flies. Conversely, the Sodalis copy number was significantly reduced in adults that emerged from puparia irradiated on day 29 post larviposition and in adults irradiated on day 7 post emergence. Moreover, irradiating 22-day old puparia reduced the copy number of Wolbachia and Wigglesworthia in emerged adults as compared with non-irradiated controls, but the radiation treatment had no significant impact on the vectorial competence of the flies. Although the radiation treatment significantly reduced the copy number of some tsetse fly symbionts, the copy number of Sodalis recovered with time in flies irradiated as 22-day old puparia. This recovery offers the opportunity to combine a paratransgenesis approach - using modified Sodalis to produce males refractory to trypanosome infection - with the release of sterile males to minimize the risk of disease transmission, especially in HAT endemic areas. Moreover, irradiation did not increase the vector competence of the flies for trypanosomes.
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Combining paratransgenesis with SIT: impact of ionizing radiation on the DNA copy number of Sodalis glossinidius in tsetse flies
BMC Microbiology, 2018Co-Authors: Güler Demirbas-uzel, Jan Van Den Abbeele, Linda De Vooght, Andrew G. Parker, Marc J. B. Vreysen, Robert L. Mach, Adly M. M. Abd-allaAbstract:Background Tsetse flies (Diptera: Glossinidae) are the cyclical vectors of the causative agents of African Trypanosomosis, which has been identified as a neglected tropical disease in both humans and animals in many regions of sub-Saharan Africa. The sterile insect technique (SIT) has shown to be a powerful method to manage tsetse fly populations when used in the frame of an area-wide integrated pest management (AW-IPM) program. To date, the release of sterile males to manage tsetse fly populations has only been implemented in areas to reduce transmission of animal African Trypanosomosis (AAT). The implementation of the SIT in areas with Human African Trypanosomosis (HAT) would require additional measures to eliminate the potential risk associated with the release of sterile males that require blood meals to survive and hence, might contribute to disease transmission. Paratransgenesis offers the potential to develop tsetse flies that are refractory to trypanosome infection by modifying their associated bacteria ( Sodalis glossinidius ) here after referred to as Sodalis . Here we assessed the feasibility of combining the paratransgenesis approach with SIT by analyzing the impact of ionizing radiation on the copy number of Sodalis and the vectorial capacity of sterilized tsetse males. Results Adult Glossina morsitans morsitans that emerged from puparia irradiated on day 22 post larviposition did not show a significant decline in Sodalis copy number as compared with non-irradiated flies. Conversely, the Sodalis copy number was significantly reduced in adults that emerged from puparia irradiated on day 29 post larviposition and in adults irradiated on day 7 post emergence. Moreover, irradiating 22-day old puparia reduced the copy number of Wolbachia and Wigglesworthia in emerged adults as compared with non-irradiated controls, but the radiation treatment had no significant impact on the vectorial competence of the flies. Conclusion Although the radiation treatment significantly reduced the copy number of some tsetse fly symbionts, the copy number of Sodalis recovered with time in flies irradiated as 22-day old puparia. This recovery offers the opportunity to combine a paratransgenesis approach – using modified Sodalis to produce males refractory to trypanosome infection – with the release of sterile males to minimize the risk of disease transmission, especially in HAT endemic areas. Moreover, irradiation did not increase the vector competence of the flies for trypanosomes.
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paternal transmission of a secondary symbiont during mating in the viviparous tsetse fly
Molecular Biology and Evolution, 2015Co-Authors: Linda De Vooght, Guy Caljon, Jan Van Den Abbeele, Jos Van HeesAbstract:Sodalis glossinidius, a maternally inherited secondary symbiont of the tsetse fly, is a bacterium in the early/intermediate state of the transition toward symbiosis, representing an important model for investigating establishment and evolution of insect-bacteria symbiosis. The absence of phylogenetic congruence in tsetse-Sodalis coevolution and the existence of Sodalis genotypic diversity in field flies are suggestive for a horizontal transmission route. However, to date no natural mechanism for the horizontal transfer of this symbiont has been identified. Using novel methodologies for the stable fluorescent-labeling and introduction of modified Sodalis in tsetse flies, we unambiguously show that male-borne Sodalis is 1) horizontally transferred to females during mating and 2) subsequently vertically transmitted to the progeny, that is, paternal transmission. This mixed mode of transmission has major consequences regarding Sodalis' genome evolution as it can lead to coinfections creating opportunities for lateral gene transfer which in turn could affect the interaction with the tsetse host.
Serap Aksoy - One of the best experts on this subject based on the ideXlab platform.
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Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.
PLoS neglected tropical diseases, 2019Co-Authors: Jose Santinni Roma, Serap Aksoy, Laura Runyen-janecky, Shaina D’souza, Patrick J. Somers, Leah F. Cabo, Ruhan Farsin, Brian L. WeissAbstract:Tsetse flies (Diptera: Glossinidae) house a taxonomically diverse microbiota that includes environmentally acquired bacteria, maternally transmitted symbiotic bacteria, and pathogenic African trypanosomes. Sodalis glossinidius, which is a facultative symbiont that resides intra and extracellularly within multiple tsetse tissues, has been implicated as a mediator of trypanosome infection establishment in the fly’s gut. Tsetse’s gut-associated population of Sodalis are subjected to marked temperature fluctuations each time their ectothermic fly host imbibes vertebrate blood. The molecular mechanisms that Sodalis employs to deal with this heat stress are unknown. In this study, we examined the thermal tolerance and heat shock response of Sodalis. When grown on BHI agar plates, the bacterium exhibited the most prolific growth at 25oC, and did not grow at temperatures above 30oC. Growth on BHI agar plates at 31°C was dependent on either the addition of blood to the agar or reduction in oxygen levels. Sodalis was viable in liquid cultures for 24 hours at 30oC, but began to die upon further exposure. The rate of death increased with increased temperature. Similarly, Sodalis was able to survive for 48 hours within tsetse flies housed at 30oC, while a higher temperature (37oC) was lethal. Sodalis’ genome contains homologues of the heat shock chaperone protein-encoding genes dnaK, dnaJ, and grpE, and their expression was up-regulated in thermally stressed Sodalis, both in vitro and in vivo within tsetse fly midguts. Arrested growth of E. coli dnaK, dnaJ, or grpE mutants under thermal stress was reversed when the cells were transformed with a low copy plasmid that encoded the Sodalis homologues of these genes. The information contained in this study provides insight into how arthropod vector enteric commensals, many of which mediate their host’s ability to transmit pathogens, mitigate heat shock associated with the ingestion of a blood meal.
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Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies
2019Co-Authors: Jose Santinni Roma, Serap Aksoy, Laura Runyen-janecky, Shaina D’souza, Patrick J. Somers, Leah F. Cabo, Ruhan Farsin, Brian L. WeissAbstract:Tsetse flies (Diptera: Glossinidae) house a taxonomically diverse microbiota that includes environmentally acquired bacteria, maternally transmitted symbiotic bacteria, and pathogenic African trypanosomes. Sodalis glossinidius, which is a facultative symbiont that resides intra and extracellularly within multiple tsetse tissues, has been implicated as a mediator of trypanosome infection establishment in the flys gut. Tsetses gut-associated population of Sodalis are subjected to marked temperature fluctuations each time their ectothermic fly host imbibes vertebrate blood. The molecular mechanisms that Sodalis employs to deal with this heat stress are unknown. In this study, we examined the thermal tolerance and heat shock response of Sodalis. When grown on BHI agar plates, the bacterium exhibited the most prolific growth at 25{degrees}C, and did not grow at temperatures above 30{degrees}C. Growth on BHI agar plates at 31{degrees}C was dependent on either the addition of blood to the agar or reduction in oxygen levels. Sodalis was viable in liquid cultures for 24 hours at 30{degrees}C, but began to die upon further exposure. The rate of death increased with increased temperature. Similarly, Sodalis was able to survive for 48 hours within tsetse flies housed at 30{degrees}C, while a higher temperature (37{degrees}C) was lethal. Sodalis genome contains homologues of the heat shock chaperone protein-encoding genes dnaK, dnaJ, and grpE, and their expression was up-regulated in thermally stressed Sodalis, both in vitro and in vivo within tsetse flies. Arrested growth of E. coli dnaK, dnaJ, or grpE mutants under thermal stress was reversed when the cells were transformed with a low copy plasmid that encoded the Sodalis homologues of these genes. The information contained in this study provides insight into how arthropod vector enteric commensals, many of which mediate their hosts ability to transmit pathogens, mitigate heat shock associated with the ingestion of a blood meal.nnAUTHOR SUMMARYMicroorganisms associated with insects must cope with fluctuating temperatures. Because symbiotic bacteria influence the biology of their host, how they respond to temperature changes will have an impact on the host and other microorganisms in the host. The tsetse fly and its symbionts represent an important model system for studying thermal tolerance because the fly feeds exclusively on vertebrate blood and is thus exposed to dramatic temperature shifts. Tsetse flies house a microbial community that can consist of symbiotic and environmentally acquired bacteria, viruses, and parasitic African trypanosomes. This work, which makes use of tsetses commensal symbiont, Sodalis glossinidius, is significance because it represents the only examination of thermal tolerance mechanisms in a bacterium that resides indigenously within an arthropod disease vector. A better understanding of the biology of thermal tolerance in Sodalis provides insight into thermal stress survival in other insect symbionts and may yield information to help control vector-borne disease.
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Tsetse-Wolbachia symbiosis: Comes of age and has great potential for pest and disease control
Journal of Invertebrate Pathology, 2013Co-Authors: Vangelis Doudoumis, George Tsiamis, Corey Brelsfoard, Uzma Alam, Emre Aksoy, Adly M. M. Abd-alla, Serap Aksoy, Kostas BourtzisAbstract:Tsetse flies (Diptera: Glossinidae) are the sole vectors of African trypanosomes, the causative agent of sleeping sickness in human and nagana in animals. Like most eukaryotic organisms, Glossina species have established symbiotic associations with bacteria. Three main symbiotic bacteria have been found in tsetse flies: Wigglesworthia glossinidia, an obligate symbiotic bacterium, the secondary endosymbiont Sodalis glossinidius and the reproductive symbiont Wolbachia pipientis. In the present review, we discuss recent studies on the detection and characterization of Wolbachia infections in Glossina species, the horizontal transfer of Wolbachia genes to tsetse chromosomes, the ability of this symbiont to induce cytoplasmic incompatibility in Glossina morsitans morsitans and also how new environment-friendly tools for disease control could be developed by harnessing Wolbachia symbiosis.
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Characterization of the achromobactin iron acquisition operon in Sodalis glossinidius.
Applied and environmental microbiology, 2013Co-Authors: Caitlin L. Smith, Serap Aksoy, Brian L. Weiss, Laura Runyen-janeckyAbstract:Sodalis glossinidius is a facultative, extra- and intracellular symbiont found in most tissues of the tsetse fly (Glossinia sp.). Sodalis has a putative achromobactin siderophore iron acquisition system on the pSG1 plasmid. Reverse transcription (RT)-PCR analysis revealed that the achromobactin operon is transcribed as a single polycistronic molecule and is expressed when Sodalis is within the tsetse fly. Expression of the achromobactin operon was repressed under iron-replete conditions; in a mutant that lacks the iron-responsive transcriptional repressor protein Fur, expression was aberrantly derepressed under these iron-replete conditions, indicating that the Fur protein repressed achromobactin gene expression when iron was plentiful. A putative Fur binding site within the Sodalis achromobactin promoter bound Fur in Escherichia coli Fur titration assays. Wild-type Sodalis produced detectable siderophore in vitro, but a mutation in the putative achromobactin biosynthesis gene acsD eliminated detectable siderophore production in Sodalis. Reduced growth of the siderophore synthesis mutant was reconstituted by addition of exogenous achromobactin, suggesting the strain retains a functional siderophore transport system; however, reduced growth of a Sodalis ferric-siderophore outer membrane receptor mutant with a mutation in acr was not reconstituted by exogenous siderophore due to its defective transporter. The Sodalis siderophore synthesis mutant showed reduced growth in tsetse that lacked endogenous symbionts (aposymbiotic) when the flies were inoculated with Sodalis intrathoracically, but not when inoculated per os. Our findings suggest that Sodalis siderophores play a role in iron acquisition in certain tsetse fly tissues and provide evidence for the regulation of iron acquisition mechanisms in insect symbionts.
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ompa mediated biofilm formation is essential for the commensal bacterium Sodalis glossinidius to colonize the tsetse fly gut
Applied and Environmental Microbiology, 2012Co-Authors: Michele A Maltz, Brian L. Weiss, Michelle Oneill, Serap AksoyAbstract:ABSTRACT Many bacteria successfully colonize animals by forming protective biofilms. Molecular processes that underlie the formation and function of biofilms in pathogenic bacteria are well characterized. In contrast, the relationship between biofilms and host colonization by symbiotic bacteria is less well understood. Tsetse flies (Glossina spp.) house 3 maternally transmitted symbionts, one of which is a commensal (Sodalis glossinidius) found in several host tissues, including the gut. We determined that Sodalis forms biofilms in the tsetse gut and that this process is influenced by the Sodalis outer membrane protein A (OmpA). Mutant Sodalis strains that do not produce OmpA (Sodalis ΔOmpA mutants) fail to form biofilms in vitro and are unable to colonize the tsetse gut unless endogenous symbiotic bacteria are present. Our data indicate that in the absence of biofilms, Sodalis ΔOmpA mutant cells are exposed to and eliminated by tsetse9s innate immune system, suggesting that biofilms help Sodalis evade the host immune system. Tsetse is the sole vector of pathogenic African trypanosomes, which also reside in the fly gut. Acquiring a better understanding of the dynamics that promote Sodalis colonization of the tsetse gut may enhance the development of novel disease control strategies.
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The regulation of antimicrobial peptide resistance in the transition to insect symbiosis.
Molecular microbiology, 2017Co-Authors: Adam L. Clayton, Shinichiro Enomoto, Colin DaleAbstract:Summary Many bacteria utilize two-component systems consisting of a sensor kinase and a transcriptional response regulator to detect environmental signals and modulate gene expression for adaptation. The response regulator PhoP and its cognate sensor kinase PhoQ compose a two-component system known for its role in responding to low levels of Mg2+, Ca2+, pH and to the presence of antimicrobial peptides and activating the expression of genes involved in adaptation to host association. Compared with their free-living relatives, mutualistic insect symbiotic bacteria inhabit a static environment where the requirement for sensory functions is expected to be relaxed. The insect symbiont, Sodalis glossinidius, requires PhoP to resist killing by host derived antimicrobial peptides. However, the S. glossinidius PhoQ was found to be insensitive to Mg2+, Ca2+ and pH. Here they show that Sodalis praecaptivus, a close non host-associated relative of S. glossinidius, utilizes a magnesium sensing PhoP-PhoQ and an uncharacterized MarR-like transcriptional regulator (Sant_4061) to control antimicrobial peptide resistance in vitro. While the inactivation of phoP, phoQ or Sant_4061 completely retards the growth of S. praecaptivus in the presence of an antimicrobial peptide in vitro, inactivation of both phoP and Sant_4061 is necessary to abrogate growth of this bacterium in an insect host.
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Phenotypic characterization of Sodalis praecaptivus sp. nov., a close non-insect-associated member of the Sodalis-allied lineage of insect endosymbionts.
International journal of systematic and evolutionary microbiology, 2015Co-Authors: Abhishek Chari, Kelly Oakeson, Mark A. Fisher, Shinichiro Enomoto, D Grant Jackson, Colin DaleAbstract:A Gram-stain-negative bacterium, isolated from a human wound was previously found to share an unprecedentedly close relationship with Sodalis glossinidius and other members of the Sodalis-allied clade of insect symbionts. This relationship was inferred from sequence analysis of the 16S rRNA gene and genomic comparisons and suggested the strain belonged to a novel species. Biochemical and genetic analyses supported this suggestion and demonstrated that the organism has a wide repertoire of metabolic properties, which is consistent with the presence of a relatively large gene inventory. Among members of the Sodalis-allied clade, this is the first representative that has sufficient metabolic capabilities to sustain growth in minimal media. On the basis of the results of this study, we propose that this organism be classified as a representative of a novel species, Sodalis praecaptivus sp. nov. (type strain HS(T) = DSM 27494(T) = ATCC BAA-2554(T)).
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Quorum Sensing Primes the Oxidative Stress Response in the Insect Endosymbiont, Sodalis glossinidius
2013Co-Authors: Mauricio H. Pontes, Markus Babst, Robert Lochhead, Kelly Oakeson, Kari Smith, Colin DaleAbstract:Background: Sodalis glossinidius, a maternally transmitted bacterial endosymbiont of tsetse flies (Glossina spp.), uses an acylated homoserine lactone (AHL)-based quorum sensing system to modulate gene expression in accordance with bacterial cell density. The S. glossinidius quorum sensing system relies on the function of two regulatory proteins; SogI (a LuxI homolog) synthesizes a signaling molecule, characterized as N-(3-oxohexanoyl) homoserine lactone (OHHL), and SogR1 (a LuxR homolog) interacts with OHHL to modulate transcription of specific target genes. Methodology/Principal Findings: We used a tiling microarray to analyze the S. glossinidius transcriptome in the presence and absence of exogenous OHHL. The major finding is that OHHL increases transcription of a large number of genes that are known to be involved in the oxidative stress response. We also show that the obligate symbiont of the rice weevil, Sitophilus oryzae (SOPE), maintains copies of the quorum sensing regulatory genes that are found in S. glossinidius. Molecular evolutionary analyses indicate that these sequences are evolving under stabilizing selection, consistent with the maintenance of their functions in the SOPE symbiosis. Finally, the expression studies in S. glossinidius also reveal that quorum sensing regulates the expression of a cryptic, degenerate gene (carA) that arose from an ancient deletion in the last common ancestor of S. glossinidius and SOPE. Conclusions/Significance: This oxidative stress response is likely mandated under conditions of dense intracellula
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A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insect-bacterial symbioses.
PLoS genetics, 2012Co-Authors: Adam L. Clayton, Kelly Oakeson, Maria Gutin, Arthur Henriques Pontes, Diane M. Dunn, Andrew Von Niederhausern, Robert B. Weiss, Mark A. Fisher, Colin DaleAbstract:Despite extensive study, little is known about the origins of the mutualistic bacterial endosymbionts that inhabit approximately 10% of the world's insects. In this study, we characterized a novel opportunistic human pathogen, designated “strain HS,” and found that it is a close relative of the insect endosymbiont Sodalis glossinidius. Our results indicate that ancestral relatives of strain HS have served as progenitors for the independent descent of Sodalis-allied endosymbionts found in several insect hosts. Comparative analyses indicate that the gene inventories of the insect endosymbionts were independently derived from a common ancestral template through a combination of irreversible degenerative changes. Our results provide compelling support for the notion that mutualists evolve from pathogenic progenitors. They also elucidate the role of degenerative evolutionary processes in shaping the gene inventories of symbiotic bacteria at a very early stage in these mutualistic associations.
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A Novel Human-Infection-Derived Bacterium Provides Insights into the Evolutionary Origins of Mutualistic Insect–Bacterial Symbioses
2012Co-Authors: Adam L. Clayton, Kelly Oakeson, Maria Gutin, Diane M. Dunn, Andrew Von Niederhausern, Robert B. Weiss, Arthur Pontes, Mark Fisher, Colin DaleAbstract:Despite extensive study, little is known about the origins of the mutualistic bacterial endosymbionts that inhabit approximately 10% of the world's insects. In this study, we characterized a novel opportunistic human pathogen, designated “strain HS,” and found that it is a close relative of the insect endosymbiont Sodalis glossinidius. Our results indicate that ancestral relatives of strain HS have served as progenitors for the independent descent of Sodalis-allied endosymbionts found in several insect hosts. Comparative analyses indicate that the gene inventories of the insect endosymbionts were independently derived from a common ancestral template through a combination of irreversible degenerative changes. Our results provide compelling support for the notion that mutualists evolve from pathogenic progenitors. They also elucidate the role of degenerative evolutionary processes in shaping the gene inventories of symbiotic bacteria at a very early stage in these mutualistic associations.