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Serap Aksoy - One of the best experts on this subject based on the ideXlab platform.
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unravelling the relationship between the tsetse fly and its obligate symbiont Wigglesworthia transcriptomic and metabolomic landscapes reveal highly integrated physiological networks
Proceedings of The Royal Society B: Biological Sciences, 2017Co-Authors: Xiaoli Bing, Emre Aksoy, Aurélien Vigneron, Brian L Weiss, Geoffrey M Attardo, Anna R Malacrida, Serap AksoyAbstract:Insects with restricted diets rely on obligate microbes to fulfil nutritional requirements essential for biological function. Tsetse flies, vectors of African trypanosome parasites, feed exclusively on vertebrate blood and harbour the obligate endosymbiont Wigglesworthia glossinidia. Without Wigglesworthia, tsetse are unable to reproduce. These symbionts are sheltered within specialized cells (bacteriocytes) that form the midgut-associated bacteriome organ. To decipher the core functions of this symbiosis essential for tsetse's survival, we performed dual-RNA-seq analysis of the bacteriome, coupled with metabolomic analysis of bacteriome and haemolymph collected from normal and symbiont-cured (sterile) females. Bacteriocytes produce immune regulatory peptidoglycan recognition protein (pgrp-lb) that protects Wigglesworthia, and a multivitamin transporter (smvt) that can aid in nutrient dissemination. Wigglesworthia overexpress a molecular chaperone (GroEL) to augment their translational/transport machinery and biosynthesize an abundance of B vitamins (specifically B1-, B2-, B3- and B6-associated metabolites) to supplement the host's nutritionally deficient diet. The absence of Wigglesworthia's contributions disrupts multiple metabolic pathways impacting carbohydrate and amino acid metabolism. These disruptions affect the dependent downstream processes of nucleotide biosynthesis and metabolism and biosynthesis of S-adenosyl methionine (SAM), an essential cofactor. This holistic fundamental knowledge of the symbiotic dialogue highlights new biological targets for the development of innovative vector control methods.
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Materials and Methods from Unravelling the relationship between the tsetse fly and its obligate symbiont Wigglesworthia: transcriptomic and metabolomic landscapes reveals highly integrated physiological networks
2017Co-Authors: Xiaoli Bing, Emre Aksoy, Aurélien Vigneron, Brian L Weiss, Geoffrey M Attardo, Anna R Malacrida, Serap AksoyAbstract:Insects with restricted diets rely on obligate microbes to fulfil nutritional requirements essential for biological function. Tsetse flies, vectors of African trypanosome parasites, feed exclusively on vertebrate blood and harbour the obligate endosymbiont Wigglesworthia glossinidia. Without Wigglesworthia, tsetse are unable to reproduce. These symbionts are sheltered within specialized cells (bacteriocytes) that form the midgut-associated bacteriome organ. To decipher the core functions of this symbiosis essential for tsetse's survival, we performed Dual-RNA-Seq analysis of the bacteriome, coupled with metabolomic analysis of bacteriome and haemolymph collected from normal and symbiont-cured (sterile) females. Bacteriocytes produce immune regulatory Peptidoglycan Recognition Protein (pgrp-lb) that protects Wigglesworthia, and a multivitamin transporter (smvt) that can aid in nutrient dissemination. Wigglesworthia overexpress a molecular chaperone (GroEL) to augment their translational/transport machinery and biosynthesize an abundance of B-vitamins (specifically B1-, B2-, B3- and B6-associated metabolites) to supplement the host's nutritionally deficient diet. The absence of Wigglesworthia's contributions disrupts multiple metabolic pathways impacting carbohydrate and amino acid metabolism. These disruptions affect the dependent downstream processes of nucleotide biosynthesis and metabolism and biosynthesis of S-adenosyl methionine (SAM), an essential cofactor. This holistic fundamental knowledge of the symbiotic dialogue highlights new biological targets for development of innovative vector control methods
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vitamin b6 generated by obligate symbionts is critical for maintaining proline homeostasis and fecundity in tsetse flies
Applied and Environmental Microbiology, 2014Co-Authors: Brian L Weiss, Veronika Michalkova, Geoffrey M Attardo, Serap AksoyAbstract:The viviparous tsetse fly utilizes proline as a hemolymph-borne energy source. In tsetse, biosynthesis of proline from alanine involves the enzyme alanine-glyoxylate aminotransferase (AGAT), which requires pyridoxal phosphate (vitamin B6) as a cofactor. This vitamin can be synthesized by tsetse's obligate symbiont, Wigglesworthia glossinidia. In this study, we examined the role of Wigglesworthia-produced vitamin B6 for maintenance of proline homeostasis, specifically during the energetically expensive lactation period of the tsetse's reproductive cycle. We found that expression of agat, as well as genes involved in vitamin B6 metabolism in both host and symbiont, increases in lactating flies. Removal of symbionts via antibiotic treatment of flies (aposymbiotic) led to hypoprolinemia, reduced levels of vitamin B6 in lactating females, and decreased fecundity. Proline homeostasis and fecundity recovered partially when aposymbiotic tsetse were fed a diet supplemented with either yeast or Wigglesworthia extracts. RNA interference-mediated knockdown of agat in wild-type flies reduced hemolymph proline levels to that of aposymbiotic females. Aposymbiotic flies treated with agat short interfering RNA (siRNA) remained hypoprolinemic even upon dietary supplementation with microbial extracts or B vitamins. Flies infected with parasitic African trypanosomes display lower hemolymph proline levels, suggesting that the reduced fecundity observed in parasitized flies could result from parasite interference with proline homeostasis. This interference could be manifested by competition between tsetse and trypanosomes for vitamins, proline, or other factors involved in their synthesis. Collectively, these results indicate that the presence of Wigglesworthia in tsetse is critical for the maintenance of proline homeostasis through vitamin B6 production.
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Wolbachia, Sodalis and trypanosome co-infections in natural populations of Glossina austeni and Glossina pallidipes
Parasites & vectors, 2013Co-Authors: Florence N. Wamwiri, Uzma Alam, Emre Aksoy, Serap Aksoy, Paul C. Thande, R. M. Ngure, Johnson O. Ouma, Grace MurillaAbstract:Background: Tsetse flies harbor at least three bacterial symbionts: Wigglesworthia glossinidia, Wolbachia pipientis and Sodalis glossinidius. Wigglesworthia and Sodalis reside in the gut in close association with trypanosomes and may influence establishment and development of midgut parasite infections. Wolbachia has been shown to induce reproductive effects in infected tsetse. This study was conducted to determine the prevalence of these endosymbionts in natural populations of G. austeni and G. pallidipes and to assess the degree of concurrent infections with trypanosomes. Methods: Fly samples analyzed originated from Kenyan coastal forests (trapped in 2009–2011) and South African G. austeni collected in 2008. The age structure was estimated by standard methods. G. austeni (n=298) and G. pallidipes (n= 302) were analyzed for infection with Wolbachia and Sodalis using PCR. Trypanosome infection was determined either by microscopic examination of dissected organs or by PCR amplification. Results: Overall we observed that G. pallidipes females had a longer lifespan (70 d) than G. austeni (54 d) in natural populations. Wolbachia infections were present in all G. austeni flies analysed, while in contrast, this symbiont was absent from G. pallidipes. The density of Wolbachia infections in the Kenyan G. austeni population was higher than that observed in South African flies. The infection prevalence of Sodalis ranged from 3.7% in G. austeni to about 16% in G. pallidipes. Microscopic examination of midguts revealed an overall trypanosome infection prevalence of 6% (n = 235) and 5% (n = 552), while evaluation with ITS1 primers indicated a prevalence of about 13% (n = 296) and 10% (n = 302) in G. austeni and G. pallidipes, respectively. The majority of infections (46%) were with T. congolense. Co-infection with all three organisms was observed at 1% and 3.3% in G. austeni and G. pallidipes, respectively. Eleven out of the thirteen (85%) co-infected flies harboured T. congolense and T. simiae parasites. While the association between trypanosomes and Sodalis infection was statistically significant in G. pallidipes (P = 0.0127), the number of co-infected flies was too few for a definite conclusion. Conclusions: The tsetse populations analyzed differed in the prevalence of symbionts, despite being sympatric and therefore exposed to identical environmental factors. The density of infections with Wolbachia also differed between G. austeni populations. There were too few natural co-infections detected with the Sodalis and trypanosomes to suggest extensive inter-relations between these infections in natural populations. We discuss these findings in the context of potential symbiont-mediated control interventions to reduce parasite infections and/or fly populations.
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Tsetse Immune System Maturation Requires the Presence of Obligate Symbionts in Larvae
2013Co-Authors: Brian L Weiss, Jingwen Wang, Serap AksoyAbstract:Beneficial microbial symbionts serve important functions within their hosts, including dietary supplementation and maintenance of immune system homeostasis. Little is known about the mechanisms that enable these bacteria to induce specific host phenotypes during development and into adulthood. Here we used the tsetse fly, Glossina morsitans, and its obligate mutualist, Wigglesworthia glossinidia, to investigate the co-evolutionary adaptations that influence the development of host physiological processes. Wigglesworthia is maternally transmitted to tsetse’s intrauterine larvae through milk gland secretions. We can produce flies that lack Wigglesworthia (Gmm Wgm2) yet retain their other symbiotic microbes. Such offspring give rise to adults that exhibit a largely normal phenotype, with the exception being that they are reproductively sterile. Our results indicate that when reared under normal environmental conditions Gmm Wgm2 adults are also immuno-compromised and highly susceptible to hemocoelic E. coli infections while age-matched wild-type individuals are refractory. Adults that lack Wigglesworthia during larval development exhibit exceptionally compromised cellular and humoral immune responses following microbial challenge, including reduced expression of genes that encode antimicrobial peptides (cecropin and attacin), hemocyte-mediated processes (thioester-containing proteins 2 and 4 and prophenoloxidase), and signal-mediating molecules (inducible nitric oxide synthase). Furthermore, Gmm Wgm2 adults harbor a reduced population of sessile and circulating hemocytes, a phenomenon that likely results from a significant decrease i
Brian L Weiss - One of the best experts on this subject based on the ideXlab platform.
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unravelling the relationship between the tsetse fly and its obligate symbiont Wigglesworthia transcriptomic and metabolomic landscapes reveal highly integrated physiological networks
Proceedings of The Royal Society B: Biological Sciences, 2017Co-Authors: Xiaoli Bing, Emre Aksoy, Aurélien Vigneron, Brian L Weiss, Geoffrey M Attardo, Anna R Malacrida, Serap AksoyAbstract:Insects with restricted diets rely on obligate microbes to fulfil nutritional requirements essential for biological function. Tsetse flies, vectors of African trypanosome parasites, feed exclusively on vertebrate blood and harbour the obligate endosymbiont Wigglesworthia glossinidia. Without Wigglesworthia, tsetse are unable to reproduce. These symbionts are sheltered within specialized cells (bacteriocytes) that form the midgut-associated bacteriome organ. To decipher the core functions of this symbiosis essential for tsetse's survival, we performed dual-RNA-seq analysis of the bacteriome, coupled with metabolomic analysis of bacteriome and haemolymph collected from normal and symbiont-cured (sterile) females. Bacteriocytes produce immune regulatory peptidoglycan recognition protein (pgrp-lb) that protects Wigglesworthia, and a multivitamin transporter (smvt) that can aid in nutrient dissemination. Wigglesworthia overexpress a molecular chaperone (GroEL) to augment their translational/transport machinery and biosynthesize an abundance of B vitamins (specifically B1-, B2-, B3- and B6-associated metabolites) to supplement the host's nutritionally deficient diet. The absence of Wigglesworthia's contributions disrupts multiple metabolic pathways impacting carbohydrate and amino acid metabolism. These disruptions affect the dependent downstream processes of nucleotide biosynthesis and metabolism and biosynthesis of S-adenosyl methionine (SAM), an essential cofactor. This holistic fundamental knowledge of the symbiotic dialogue highlights new biological targets for the development of innovative vector control methods.
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Materials and Methods from Unravelling the relationship between the tsetse fly and its obligate symbiont Wigglesworthia: transcriptomic and metabolomic landscapes reveals highly integrated physiological networks
2017Co-Authors: Xiaoli Bing, Emre Aksoy, Aurélien Vigneron, Brian L Weiss, Geoffrey M Attardo, Anna R Malacrida, Serap AksoyAbstract:Insects with restricted diets rely on obligate microbes to fulfil nutritional requirements essential for biological function. Tsetse flies, vectors of African trypanosome parasites, feed exclusively on vertebrate blood and harbour the obligate endosymbiont Wigglesworthia glossinidia. Without Wigglesworthia, tsetse are unable to reproduce. These symbionts are sheltered within specialized cells (bacteriocytes) that form the midgut-associated bacteriome organ. To decipher the core functions of this symbiosis essential for tsetse's survival, we performed Dual-RNA-Seq analysis of the bacteriome, coupled with metabolomic analysis of bacteriome and haemolymph collected from normal and symbiont-cured (sterile) females. Bacteriocytes produce immune regulatory Peptidoglycan Recognition Protein (pgrp-lb) that protects Wigglesworthia, and a multivitamin transporter (smvt) that can aid in nutrient dissemination. Wigglesworthia overexpress a molecular chaperone (GroEL) to augment their translational/transport machinery and biosynthesize an abundance of B-vitamins (specifically B1-, B2-, B3- and B6-associated metabolites) to supplement the host's nutritionally deficient diet. The absence of Wigglesworthia's contributions disrupts multiple metabolic pathways impacting carbohydrate and amino acid metabolism. These disruptions affect the dependent downstream processes of nucleotide biosynthesis and metabolism and biosynthesis of S-adenosyl methionine (SAM), an essential cofactor. This holistic fundamental knowledge of the symbiotic dialogue highlights new biological targets for development of innovative vector control methods
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vitamin b6 generated by obligate symbionts is critical for maintaining proline homeostasis and fecundity in tsetse flies
Applied and Environmental Microbiology, 2014Co-Authors: Brian L Weiss, Veronika Michalkova, Geoffrey M Attardo, Serap AksoyAbstract:The viviparous tsetse fly utilizes proline as a hemolymph-borne energy source. In tsetse, biosynthesis of proline from alanine involves the enzyme alanine-glyoxylate aminotransferase (AGAT), which requires pyridoxal phosphate (vitamin B6) as a cofactor. This vitamin can be synthesized by tsetse's obligate symbiont, Wigglesworthia glossinidia. In this study, we examined the role of Wigglesworthia-produced vitamin B6 for maintenance of proline homeostasis, specifically during the energetically expensive lactation period of the tsetse's reproductive cycle. We found that expression of agat, as well as genes involved in vitamin B6 metabolism in both host and symbiont, increases in lactating flies. Removal of symbionts via antibiotic treatment of flies (aposymbiotic) led to hypoprolinemia, reduced levels of vitamin B6 in lactating females, and decreased fecundity. Proline homeostasis and fecundity recovered partially when aposymbiotic tsetse were fed a diet supplemented with either yeast or Wigglesworthia extracts. RNA interference-mediated knockdown of agat in wild-type flies reduced hemolymph proline levels to that of aposymbiotic females. Aposymbiotic flies treated with agat short interfering RNA (siRNA) remained hypoprolinemic even upon dietary supplementation with microbial extracts or B vitamins. Flies infected with parasitic African trypanosomes display lower hemolymph proline levels, suggesting that the reduced fecundity observed in parasitized flies could result from parasite interference with proline homeostasis. This interference could be manifested by competition between tsetse and trypanosomes for vitamins, proline, or other factors involved in their synthesis. Collectively, these results indicate that the presence of Wigglesworthia in tsetse is critical for the maintenance of proline homeostasis through vitamin B6 production.
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Tsetse Immune System Maturation Requires the Presence of Obligate Symbionts in Larvae
2013Co-Authors: Brian L Weiss, Jingwen Wang, Serap AksoyAbstract:Beneficial microbial symbionts serve important functions within their hosts, including dietary supplementation and maintenance of immune system homeostasis. Little is known about the mechanisms that enable these bacteria to induce specific host phenotypes during development and into adulthood. Here we used the tsetse fly, Glossina morsitans, and its obligate mutualist, Wigglesworthia glossinidia, to investigate the co-evolutionary adaptations that influence the development of host physiological processes. Wigglesworthia is maternally transmitted to tsetse’s intrauterine larvae through milk gland secretions. We can produce flies that lack Wigglesworthia (Gmm Wgm2) yet retain their other symbiotic microbes. Such offspring give rise to adults that exhibit a largely normal phenotype, with the exception being that they are reproductively sterile. Our results indicate that when reared under normal environmental conditions Gmm Wgm2 adults are also immuno-compromised and highly susceptible to hemocoelic E. coli infections while age-matched wild-type individuals are refractory. Adults that lack Wigglesworthia during larval development exhibit exceptionally compromised cellular and humoral immune responses following microbial challenge, including reduced expression of genes that encode antimicrobial peptides (cecropin and attacin), hemocyte-mediated processes (thioester-containing proteins 2 and 4 and prophenoloxidase), and signal-mediating molecules (inducible nitric oxide synthase). Furthermore, Gmm Wgm2 adults harbor a reduced population of sessile and circulating hemocytes, a phenomenon that likely results from a significant decrease i
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Tsetse immune system maturation requires the presence of obligate symbionts in larvae.
PLoS biology, 2011Co-Authors: Brian L Weiss, Jingwen Wang, Serap AksoyAbstract:Beneficial microbial symbionts serve important functions within their hosts, including dietary supplementation and maintenance of immune system homeostasis. Little is known about the mechanisms that enable these bacteria to induce specific host phenotypes during development and into adulthood. Here we used the tsetse fly, Glossina morsitans, and its obligate mutualist, Wigglesworthia glossinidia, to investigate the co-evolutionary adaptations that influence the development of host physiological processes. Wigglesworthia is maternally transmitted to tsetse's intrauterine larvae through milk gland secretions. We can produce flies that lack Wigglesworthia (Gmm(Wgm-) yet retain their other symbiotic microbes. Such offspring give rise to adults that exhibit a largely normal phenotype, with the exception being that they are reproductively sterile. Our results indicate that when reared under normal environmental conditions Gmm(Wgm-) adults are also immuno-compromised and highly susceptible to hemocoelic E. coli infections while age-matched wild-type individuals are refractory. Adults that lack Wigglesworthia during larval development exhibit exceptionally compromised cellular and humoral immune responses following microbial challenge, including reduced expression of genes that encode antimicrobial peptides (cecropin and attacin), hemocyte-mediated processes (thioester-containing proteins 2 and 4 and prophenoloxidase), and signal-mediating molecules (inducible nitric oxide synthase). Furthermore, Gmm(Wgm-) adults harbor a reduced population of sessile and circulating hemocytes, a phenomenon that likely results from a significant decrease in larval expression of serpent and lozenge, both of which are associated with the process of early hemocyte differentiation. Our results demonstrate that Wigglesworthia must be present during the development of immature progeny in order for the immune system to function properly in adult tsetse. This phenomenon provides evidence of yet another important physiological adaptation that further anchors the obligate symbiosis between tsetse and Wigglesworthia.
Jingwen Wang - One of the best experts on this subject based on the ideXlab platform.
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Tsetse Immune System Maturation Requires the Presence of Obligate Symbionts in Larvae
2013Co-Authors: Brian L Weiss, Jingwen Wang, Serap AksoyAbstract:Beneficial microbial symbionts serve important functions within their hosts, including dietary supplementation and maintenance of immune system homeostasis. Little is known about the mechanisms that enable these bacteria to induce specific host phenotypes during development and into adulthood. Here we used the tsetse fly, Glossina morsitans, and its obligate mutualist, Wigglesworthia glossinidia, to investigate the co-evolutionary adaptations that influence the development of host physiological processes. Wigglesworthia is maternally transmitted to tsetse’s intrauterine larvae through milk gland secretions. We can produce flies that lack Wigglesworthia (Gmm Wgm2) yet retain their other symbiotic microbes. Such offspring give rise to adults that exhibit a largely normal phenotype, with the exception being that they are reproductively sterile. Our results indicate that when reared under normal environmental conditions Gmm Wgm2 adults are also immuno-compromised and highly susceptible to hemocoelic E. coli infections while age-matched wild-type individuals are refractory. Adults that lack Wigglesworthia during larval development exhibit exceptionally compromised cellular and humoral immune responses following microbial challenge, including reduced expression of genes that encode antimicrobial peptides (cecropin and attacin), hemocyte-mediated processes (thioester-containing proteins 2 and 4 and prophenoloxidase), and signal-mediating molecules (inducible nitric oxide synthase). Furthermore, Gmm Wgm2 adults harbor a reduced population of sessile and circulating hemocytes, a phenomenon that likely results from a significant decrease i
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Implications of microfauna-host interactions for trypanosome transmission dynamics in Glossina fuscipes fuscipes in Uganda.
Applied and environmental microbiology, 2012Co-Authors: Uzma Alam, Jingwen Wang, Rebecca E. Symula, Chaz Hyseni, Oleg Kruglov, Richard Echodu, Victor Alioni, Loyce M. OkediAbstract:Tsetse flies (Diptera: Glossinidae) are vectors for African trypanosomes (Euglenozoa: kinetoplastida), protozoan parasites that cause African trypanosomiasis in humans (HAT) and nagana in livestock. In addition to trypanosomes, two symbiotic bacteria (Wigglesworthia glossinidia and Sodalis glossinidius) and two parasitic microbes, Wolbachia and a salivary gland hypertrophy virus (SGHV), have been described in tsetse. Here we determined the prevalence of and coinfection dynamics between Wolbachia, trypanosomes, and SGHV in Glossina fuscipes fuscipes in Uganda over a large geographical scale spanning the range of host genetic and spatial diversity. Using a multivariate analysis approach, we uncovered complex coinfection dynamics between the pathogens and statistically significant associations between host genetic groups and pathogen prevalence. It is important to note that these coinfection dynamics and associations with the host were not apparent by univariate analysis. These associations between host genotype and pathogen are particularly evident for Wolbachia and SGHV where host groups are inversely correlated for Wolbachia and SGHV prevalence. On the other hand, trypanosome infection prevalence is more complex and covaries with the presence of the other two pathogens, highlighting the importance of examining multiple pathogens simultaneously before making generalizations about infection and spatial patterns. It is imperative to note that these novel findings would have been missed if we had employed the standard univariate analysis used in previous studies. Our results are discussed in the context of disease epidemiology and vector control.
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Tsetse immune system maturation requires the presence of obligate symbionts in larvae.
PLoS biology, 2011Co-Authors: Brian L Weiss, Jingwen Wang, Serap AksoyAbstract:Beneficial microbial symbionts serve important functions within their hosts, including dietary supplementation and maintenance of immune system homeostasis. Little is known about the mechanisms that enable these bacteria to induce specific host phenotypes during development and into adulthood. Here we used the tsetse fly, Glossina morsitans, and its obligate mutualist, Wigglesworthia glossinidia, to investigate the co-evolutionary adaptations that influence the development of host physiological processes. Wigglesworthia is maternally transmitted to tsetse's intrauterine larvae through milk gland secretions. We can produce flies that lack Wigglesworthia (Gmm(Wgm-) yet retain their other symbiotic microbes. Such offspring give rise to adults that exhibit a largely normal phenotype, with the exception being that they are reproductively sterile. Our results indicate that when reared under normal environmental conditions Gmm(Wgm-) adults are also immuno-compromised and highly susceptible to hemocoelic E. coli infections while age-matched wild-type individuals are refractory. Adults that lack Wigglesworthia during larval development exhibit exceptionally compromised cellular and humoral immune responses following microbial challenge, including reduced expression of genes that encode antimicrobial peptides (cecropin and attacin), hemocyte-mediated processes (thioester-containing proteins 2 and 4 and prophenoloxidase), and signal-mediating molecules (inducible nitric oxide synthase). Furthermore, Gmm(Wgm-) adults harbor a reduced population of sessile and circulating hemocytes, a phenomenon that likely results from a significant decrease in larval expression of serpent and lozenge, both of which are associated with the process of early hemocyte differentiation. Our results demonstrate that Wigglesworthia must be present during the development of immature progeny in order for the immune system to function properly in adult tsetse. This phenomenon provides evidence of yet another important physiological adaptation that further anchors the obligate symbiosis between tsetse and Wigglesworthia.
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the obligate mutualist Wigglesworthia glossinidia influences reproduction digestion and immunity processes of its host the tsetse fly
Applied and Environmental Microbiology, 2008Co-Authors: Roshan Pais, Claudia Lohs, Jingwen Wang, Serap AksoyAbstract:Tsetse flies (Diptera: Glossinidae) are vectors for trypanosome parasites, the agents of the deadly sleeping sickness disease in Africa. Tsetse also harbor two maternally transmitted enteric mutualist endosymbionts: the primary intracellular obligate Wigglesworthia glossinidia and the secondary commensal Sodalis glossinidius. Both endosymbionts are transmitted to the intrauterine progeny through the milk gland secretions of the viviparous female. We administered various antibiotics either continuously by per os supplementation of the host blood meal diet or discretely by hemocoelic injections into fertile females in an effort to selectively eliminate the symbionts to study their individual functions. A symbiont-specific PCR amplification assay and fluorescence in situ hybridization analysis were used to evaluate symbiont infection outcomes. Tetracycline and rifampin treatments eliminated all tsetse symbionts but reduced the fecundity of the treated females. Ampicillin treatments did not affect the intracellular Wigglesworthia localized in the bacteriome organ and retained female fecundity. The resulting progeny of ampicillin-treated females, however, lacked Wigglesworthia but still harbored the commensal Sodalis. Our results confirm the presence of two physiologically distinct Wigglesworthia populations: the bacteriome-localized Wigglesworthia involved with nutritional symbiosis and free-living Wigglesworthia in the milk gland organ responsible for maternal transmission to the progeny. We evaluated the reproductive fitness, longevity, digestion, and vectorial competence of flies that were devoid of Wigglesworthia. The absence of Wigglesworthia completely abolished the fertility of females but not that of males. Both the male and female Wigglesworthia-free adult progeny displayed longevity costs and were significantly compromised in their blood meal digestion ability. Finally, while the vectorial competence of the young newly hatched adults without Wigglesworthia was comparable to that of their wild-type counterparts, older flies displayed higher susceptibility to trypanosome infections, indicating a role for the mutualistic symbiosis in host immunobiology. The ability to rear adult tsetse that lack the obligate Wigglesworthia endosymbionts will now enable functional investigations into this ancient symbiosis.
Uzma Alam - One of the best experts on this subject based on the ideXlab platform.
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Presence of Extensive Wolbachia Symbiont Insertions Discovered in the Genome of Its Host Glossina morsitans morsitans
2016Co-Authors: Corey Brelsfoard, Vangelis Doudoumis, George Tsiamis, Uzma Alam, Francesca Scolari, Joshua B Benoit, Marco Falchetto, Ludvik M. Gomulski, Erich Telleria, Martin SwainAbstract:Tsetse flies (Glossina spp.) are the cyclical vectors of Trypanosoma spp., which are unicellular parasites responsible for multiple diseases, including nagana in livestock and sleeping sickness in humans in Africa. Glossina species, including Glossina morsitans morsitans (Gmm), for which the Whole Genome Sequence (WGS) is now available, have established symbiotic associations with three endosymbionts: Wigglesworthia glossinidia, Sodalis glossinidius and Wolbachia pipientis (Wolbachia). The presence of Wolbachia in both natural and laboratory populations of Glossina species, including the presence of horizontal gene transfer (HGT) events in a laboratory colony of Gmm, has already been shown. We herein report on the draft genome sequence of the cytoplasmic Wolbachia endosymbiont (cytWol) associated with Gmm. By in silico and molecular and cytogenetic analysis, we discovered and validated the presence of multiple insertions of Wolbachia (chrWol) in the host Gmm genome. We identified at least two large insertions of chrWol, 527,507 and 484,123 bp in size, from Gm
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Presence of Extensive Wolbachia Symbiont Insertions Discovered in the Genome of Its Host Glossina morsitans morsitans
PLoS neglected tropical diseases, 2014Co-Authors: Corey Brelsfoard, Vangelis Doudoumis, George Tsiamis, Uzma Alam, Marco Falchetto, Ludvik M. Gomulski, Erich Telleria, Martin T. SwainAbstract:Tsetse flies (Glossina spp.) are the cyclical vectors of Trypanosoma spp., which are unicellular parasites responsible for multiple diseases, including nagana in livestock and sleeping sickness in humans in Africa. Glossina species, including Glossina morsitans morsitans (Gmm), for which the Whole Genome Sequence (WGS) is now available, have established symbiotic associations with three endosymbionts: Wigglesworthia glossinidia, Sodalis glossinidius and Wolbachia pipientis (Wolbachia). The presence of Wolbachia in both natural and laboratory populations of Glossina species, including the presence of horizontal gene transfer (HGT) events in a laboratory colony of Gmm, has already been shown. We herein report on the draft genome sequence of the cytoplasmic Wolbachia endosymbiont (cytWol) associated with Gmm. By in silico and molecular and cytogenetic analysis, we discovered and validated the presence of multiple insertions of Wolbachia (chrWol) in the host Gmm genome. We identified at least two large insertions of chrWol, 527,507 and 484,123 bp in size, from Gmm WGS data. Southern hybridizations confirmed the presence of Wolbachia insertions in Gmm genome, and FISH revealed multiple insertions located on the two sex chromosomes (X and Y), as well as on the supernumerary B-chromosomes. We compare the chrWol insertions to the cytWol draft genome in an attempt to clarify the evolutionary history of the HGT events. We discuss our findings in light of the evolution of Wolbachia infections in the tsetse fly and their potential impacts on the control of tsetse populations and trypanosomiasis.
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Wolbachia, Sodalis and trypanosome co-infections in natural populations of Glossina austeni and Glossina pallidipes
Parasites & vectors, 2013Co-Authors: Florence N. Wamwiri, Uzma Alam, Emre Aksoy, Serap Aksoy, Paul C. Thande, R. M. Ngure, Johnson O. Ouma, Grace MurillaAbstract:Background: Tsetse flies harbor at least three bacterial symbionts: Wigglesworthia glossinidia, Wolbachia pipientis and Sodalis glossinidius. Wigglesworthia and Sodalis reside in the gut in close association with trypanosomes and may influence establishment and development of midgut parasite infections. Wolbachia has been shown to induce reproductive effects in infected tsetse. This study was conducted to determine the prevalence of these endosymbionts in natural populations of G. austeni and G. pallidipes and to assess the degree of concurrent infections with trypanosomes. Methods: Fly samples analyzed originated from Kenyan coastal forests (trapped in 2009–2011) and South African G. austeni collected in 2008. The age structure was estimated by standard methods. G. austeni (n=298) and G. pallidipes (n= 302) were analyzed for infection with Wolbachia and Sodalis using PCR. Trypanosome infection was determined either by microscopic examination of dissected organs or by PCR amplification. Results: Overall we observed that G. pallidipes females had a longer lifespan (70 d) than G. austeni (54 d) in natural populations. Wolbachia infections were present in all G. austeni flies analysed, while in contrast, this symbiont was absent from G. pallidipes. The density of Wolbachia infections in the Kenyan G. austeni population was higher than that observed in South African flies. The infection prevalence of Sodalis ranged from 3.7% in G. austeni to about 16% in G. pallidipes. Microscopic examination of midguts revealed an overall trypanosome infection prevalence of 6% (n = 235) and 5% (n = 552), while evaluation with ITS1 primers indicated a prevalence of about 13% (n = 296) and 10% (n = 302) in G. austeni and G. pallidipes, respectively. The majority of infections (46%) were with T. congolense. Co-infection with all three organisms was observed at 1% and 3.3% in G. austeni and G. pallidipes, respectively. Eleven out of the thirteen (85%) co-infected flies harboured T. congolense and T. simiae parasites. While the association between trypanosomes and Sodalis infection was statistically significant in G. pallidipes (P = 0.0127), the number of co-infected flies was too few for a definite conclusion. Conclusions: The tsetse populations analyzed differed in the prevalence of symbionts, despite being sympatric and therefore exposed to identical environmental factors. The density of infections with Wolbachia also differed between G. austeni populations. There were too few natural co-infections detected with the Sodalis and trypanosomes to suggest extensive inter-relations between these infections in natural populations. We discuss these findings in the context of potential symbiont-mediated control interventions to reduce parasite infections and/or fly populations.
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Implications of microfauna-host interactions for trypanosome transmission dynamics in Glossina fuscipes fuscipes in Uganda.
Applied and environmental microbiology, 2012Co-Authors: Uzma Alam, Jingwen Wang, Rebecca E. Symula, Chaz Hyseni, Oleg Kruglov, Richard Echodu, Victor Alioni, Loyce M. OkediAbstract:Tsetse flies (Diptera: Glossinidae) are vectors for African trypanosomes (Euglenozoa: kinetoplastida), protozoan parasites that cause African trypanosomiasis in humans (HAT) and nagana in livestock. In addition to trypanosomes, two symbiotic bacteria (Wigglesworthia glossinidia and Sodalis glossinidius) and two parasitic microbes, Wolbachia and a salivary gland hypertrophy virus (SGHV), have been described in tsetse. Here we determined the prevalence of and coinfection dynamics between Wolbachia, trypanosomes, and SGHV in Glossina fuscipes fuscipes in Uganda over a large geographical scale spanning the range of host genetic and spatial diversity. Using a multivariate analysis approach, we uncovered complex coinfection dynamics between the pathogens and statistically significant associations between host genetic groups and pathogen prevalence. It is important to note that these coinfection dynamics and associations with the host were not apparent by univariate analysis. These associations between host genotype and pathogen are particularly evident for Wolbachia and SGHV where host groups are inversely correlated for Wolbachia and SGHV prevalence. On the other hand, trypanosome infection prevalence is more complex and covaries with the presence of the other two pathogens, highlighting the importance of examining multiple pathogens simultaneously before making generalizations about infection and spatial patterns. It is imperative to note that these novel findings would have been missed if we had employed the standard univariate analysis used in previous studies. Our results are discussed in the context of disease epidemiology and vector control.
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Influence of Host Phylogeographic Patterns and Incomplete Lineage Sorting on Within-Species Genetic Variability in Wigglesworthia Species, Obligate Symbionts of Tsetse Flies
Applied and environmental microbiology, 2011Co-Authors: Rebecca E. Symula, Uzma Alam, Serap Aksoy, Ian Marpuri, Robert D. Bjornson, Loyce M. Okedi, Jon S. Beadell, Adalgisa CacconeAbstract:Vertical transmission of obligate symbionts generates a predictable evolutionary history of symbionts that reflects that of their hosts. In insects, evolutionary associations between symbionts and their hosts have been investigated primarily among species, leaving population-level processes largely unknown. In this study, we investigated the tsetse (Diptera: Glossinidae) bacterial symbiont, Wigglesworthia glossinidia, to determine whether observed codiversification of symbiont and tsetse host species extends to a single host species (Glossina fuscipes fuscipes) in Uganda. To explore symbiont genetic variation in G. f. fuscipes populations, we screened two variable loci (lon and lepA) from the Wigglesworthia glossinidia bacterium in the host species Glossina fuscipes fuscipes (W. g. fuscipes) and examined phylogeographic and demographic characteristics in multiple host populations. Symbiont genetic variation was apparent within and among populations. We identified two distinct symbiont lineages, in northern and southern Uganda. Incongruence length difference (ILD) tests indicated that the two lineages corresponded exactly to northern and southern G. f. fuscipes mitochondrial DNA (mtDNA) haplogroups (P = 1.0). Analysis of molecular variance (AMOVA) confirmed that most variation was partitioned between the northern and southern lineages defined by host mtDNA (85.44%). However, ILD tests rejected finer-scale congruence within the northern and southern populations (P = 0.009). This incongruence was potentially due to incomplete lineage sorting that resulted in novel combinations of symbiont genetic variants and host background. Identifying these novel combinations may have public health significance, since tsetse is the sole vector of sleeping sickness and Wigglesworthia is known to influence host vector competence. Thus, understanding the adaptive value of these host-symbiont combinations may afford opportunities to develop vector control methods.
Abdelaziz Heddi - One of the best experts on this subject based on the ideXlab platform.
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What can a weevil teach a fly, and reciprocally? Interaction of host immune systems with endosymbionts in Glossina and Sitophilus
BMC Microbiology, 2018Co-Authors: Anna Zaidman-rémy, Brian Weiss, Abdelaziz HeddiAbstract:The tsetse fly (Glossina genus) is the main vector of African trypanosomes, which are protozoan parasites that cause human and animal African trypanosomiases in Sub-Saharan Africa. In the frame of the IAEA/FAO program 'Enhancing Vector Refractoriness to Trypanosome Infection', in addition to the tsetse, the cereal weevil Sitophilus has been introduced as a comparative system with regards to immune interactions with endosymbionts. The cereal weevil is an agricultural pest that destroys a significant proportion of cereal stocks worldwide. Tsetse flies are associated with three symbiotic bacteria, the multifunctional obligate Wigglesworthia glossinidia, the facultative commensal Sodalis glossinidius and the parasitic Wolbachia. Cereal weevils house an obligatory nutritional symbiosis with the bacterium Sodalis pierantonius, and occasionally Wolbachia. Studying insect host-symbiont interactions is highly relevant both for understanding the evolution of symbiosis and for envisioning novel pest control strategies. In both insects, the long co-evolution between host and endosymbiont has led to a stringent integration of the host-bacteria partnership. These associations were facilitated by the development of specialized host traits, including symbiont-housing cells called bacteriocytes and specific immune features that enable both tolerance and control of the bacteria. In this review, we compare the tsetse and weevil model systems and compile the latest research findings regarding their biological and ecological similarities, how the immune system controls endosymbiont load and location, and how host-symbiont interactions impact developmental features including cuticle synthesis and immune system maturation. We focus mainly on the interactions between the obligate symbionts and their host's immune systems, a central theme in both model systems. Finally, we highlight how parallel studies on cereal weevils and tsetse flies led to mutual discoveries and stimulated research on each model, creating a pivotal example of scientific improvement through comparison between relatively distant models.
