scholarly journals The Obligate Mutualist Wigglesworthia glossinidia Influences Reproduction, Digestion, and Immunity Processes of Its Host, the Tsetse Fly

2008 ◽  
Vol 74 (19) ◽  
pp. 5965-5974 ◽  
Author(s):  
Roshan Pais ◽  
Claudia Lohs ◽  
Yineng Wu ◽  
Jingwen Wang ◽  
Serap Aksoy
Keyword(s):  
Blood Meal ◽  
Pcr Amplification ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
Mutualistic Symbiosis ◽  
Sodalis Glossinidius ◽  
Specific Pcr ◽  
Amplification Assay ◽  
Blood Meal Digestion ◽  
Vectorial Competence

ABSTRACT 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.

scholarly journals Tsetse blood-meal sources, endosymbionts and trypanosome-associations in the Maasai Mara National Reserve, a wildlife-human-livestock interface

2021 ◽  
Vol 15 (1) ◽  
pp. e0008267
Author(s):  
Edward Edmond Makhulu ◽  
Jandouwe Villinger ◽  
Vincent Owino Adunga ◽  
Maamun M. Jeneby ◽  
Edwin Murungi Kimathi ◽  
...  
Keyword(s):  
Blood Meal ◽  
Glossina Pallidipes ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
African Buffalo ◽  
African Trypanosomiasis ◽  
African Trypanosomes ◽  
Sodalis Glossinidius ◽  
Vertebrate Hosts ◽  
Blood Meals

African trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Knowledge on tsetse fly vertebrate hosts and the influence of tsetse endosymbionts on trypanosome presence, especially in wildlife-human-livestock interfaces, is limited. We identified tsetse species, their blood-meal sources, and correlations between endosymbionts and trypanosome presence in tsetse flies from the trypanosome-endemic Maasai Mara National Reserve (MMNR) in Kenya. Among 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosome DNA, most (17/28) being of Trypanosoma vivax species. Blood-meal analyses based on high-resolution melting analysis of vertebrate cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 354) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Flies positive for trypanosome DNA had fed on hippopotamus and buffalo. Tsetse flies were more likely to be positive for trypanosomes if they had the Sodalis glossinidius endosymbiont (P = 0.0002). These findings point to complex interactions of tsetse flies with trypanosomes, endosymbionts, and diverse vertebrate hosts in wildlife ecosystems such as in the MMNR, which should be considered in control programs. These interactions may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes. Although the African buffalo is a key reservoir of AT, the higher proportion of hippopotamus blood-meals in flies with trypanosome DNA indicates that other wildlife species may be important in AT transmission. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis risk. Our results add to existing data suggesting that Sodalis endosymbionts are associated with increased trypanosome presence in tsetse flies.

A model for blood meal digestion and fat metabolism in male tsetse flies (Glossinidae)

1998 ◽  
Vol 23 (1) ◽  
pp. 43-52 ◽  
Author(s):  
PHILIP M. J. LODER ◽  
JOHN W. HARGROVE ◽  
SARAH E. RANDOLPH
Keyword(s):  
Blood Meal ◽  
Fat Metabolism ◽  
Tsetse Flies ◽  
Blood Meal Digestion

scholarly journals Apparent density, trypanosome infection rates and host preference of tsetse flies in the sleeping sickness endemic focus of   Northwestern Uganda

2020 ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  
Keyword(s):  
Infection Rate ◽  
Apparent Density ◽  
Blood Meal ◽  
Nested Pcr ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
Trypanosome Species ◽  
Trypanosome Infection ◽  
Infection Rates ◽  
Monitor Lizard

Abstract Background: African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies.Methodology: We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, trypanosome infection rates and blood meal sources of tsetse flies. A subset (272) of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results: Out of the 109 traps deployed, we captured 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females). Apparent density (AD) ranged from 0.6 to 3.7 flies/trap/day in the two districts. 29 (10.7%) of the flies were infected with one or more trypanosome species. Infection rate was not significantly associated with neither age group (χ2 = 5.001, df=2, 0.082), sex of the fly (χ2 = 0.099, df = 1, p = 0.753), district of origin (χ2= 0.629, df = 1, p = 0.428) nor village (χ2= 9.252, df = 9, p = 0.414). Nested PCR revealed several species of trypanosomes: T. vivax (6.62%), T. congolense (2.57%), T. brucei and T. simiae each at 0.73%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusio schapini) and the African Savanna elephant (Loxodonta africana).Conclusion: We found an infection rate of 10.78 %, with all infections attributed to trypanosome species that are causative agents for the animal disease only. However, more verification of this finding using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of interventions.

scholarly journals Apparent density, trypanosome infection rates and host preference of tsetse flies in the sleeping sickness endemic focus of Northwestern Uganda

2020 ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  
Keyword(s):  
Infection Rate ◽  
Apparent Density ◽  
Blood Meal ◽  
Nested Pcr ◽  
Large Scale ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
Trypanosome Species ◽  
Infection Rates ◽  
Monitor Lizard

Abstract Background: African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies.Methodology: We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, infection rates and blood meal sources of tsetse flies. A subset (272) of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results: Out of the 109 traps deployed, we captured 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females). Apparent density (AD) ranged from 0.6 to 3.7 flies/trap/day in the two districts. 29 (10.7%) of the flies were infected with one or more trypanosome species. Infection rate was not significantly associated with neither age group (χ2 = 5.001, df=2, 0.082), sex of the fly (χ2 = 0.099, df = 1, p = 0.753), district of origin (χ2= 0.629, df = 1, p = 0.428) nor village (χ2= 9.252, df = 9, p = 0.414). Nested PCR revealed several species of trypanosomes: T. vivax (6.62%), T. congolense (2.57%), and T. brucei and T. simiae each at 0.73%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusio schapini) and the African Savanna elephant (Loxodonta africana).Conclusion: We found a moderately high infection rate of 10.78%, with all infections attributed to trypanosome species that are causative agents for the animal disease only. However, more validation using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of interventions.

scholarly journals Apparent density, trypanosome infection rates and host preference of tsetse flies in the sleeping sickness endemic focus of northwestern Uganda

2021 ◽  
Vol 17 (1) ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  
Keyword(s):  
Infection Rate ◽  
Apparent Density ◽  
Blood Meal ◽  
Nested Pcr ◽  
Large Scale ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
Trypanosome Species ◽  
Trypanosome Infection ◽  
Monitor Lizard

Abstract Background African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies. Methodology We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, trypanosome infection status and blood meal sources of tsetse flies. A subset (272) of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results We captured a total of 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females) in the two districts with apparent density (AD) ranging from 0.6 to 3.7 flies/trap/day (FTD). 10.7% (29/272) of the flies were infected with one or more trypanosome species. Infection rate was not significantly associated with district of origin (Generalized linear model (GLM), χ2 = 0.018, P = 0.895, df = 1, n = 272) and sex of the fly (χ2 = 1.723, P = 0.189, df = 1, n = 272). However, trypanosome infection was highly significantly associated with the fly’s age based on wing fray category (χ2 = 22.374, P < 0.001, df = 1, n = 272), being higher among the very old than the young tsetse. Nested PCR revealed several species of trypanosomes: T. vivax (6.62%), T. congolense (2.57%), T. brucei and T. simiae each at 0.73%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusios chapini) and the African Savanna elephant (Loxodonta africana). Conclusion We found an infection rate of 10.8% in the tsetse sampled, with all infections attributed to trypanosome species that are causative agents for AAT. However, more verification of this finding using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of control interventions.

scholarly journals Apparent Density, Trypanosome Infection Rates and Host Preference of Tsetse Flies in the Sleeping Sickness Endemic Focus of North-Western Uganda

2020 ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  
Keyword(s):  
Infection Rate ◽  
Apparent Density ◽  
Blood Meal ◽  
Nested Pcr ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
Trypanosome Species ◽  
Trypanosome Infection ◽  
Infection Rates ◽  
Monitor Lizard

Abstract Background: African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies.Methodology: We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, trypanosome infection rates and blood meal sources of tsetse flies. A subset of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results: Out of the 109 traps deployed, we captured 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females). Apparent density (AD) ranged from 0.6 to 3.7 flies/trap/day in the two districts. 29 (10.7%) of the flies were infected with one or more trypanosome species, with infection rate significantly associated with age group (χ2 = 29.733, df = 2, p < 0.05) but not with sex (χ2 = 0.43, df = 1, p = 0.835) and district of origin (χ2 = 1.374, df = 1, p = 0.241). Nested PCR revealed several species of trypanosomes: T. vivax (62.1%), T. congolense (24.14 %), and T. brucei and T. simiae each at 6.89%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusio schapini) and the African Savanna elephant (Loxodonta africana).Conclusion: We found a moderately high infection rate at 10.78%, with all infections attributed to trypanosome species that are causative agents for the animal disease only. However, more validation using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of interventions.

scholarly journals Apparent density, trypanosome infection rates and host preference of tsetse flies in the sleeping sickness endemic focus of Northwestern Uganda

2020 ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  
Keyword(s):  
Infection Rate ◽  
Apparent Density ◽  
Blood Meal ◽  
Nested Pcr ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
Trypanosome Species ◽  
Trypanosome Infection ◽  
Infection Rates ◽  
Monitor Lizard

Abstract Background: African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies.Methodology: We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, trypanosome infection rates and blood meal sources of tsetse flies. A subset (272) of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results: Out of the 109 traps deployed, we captured 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females). Apparent density (AD) ranged from 0.6 to 3.7 flies/trap/day in the two districts. 29 (10.7%) of the flies were infected with one or more trypanosome species. Infection rate was not significantly associated with age group (χ2 = 5.001, df=2, p = 0.082), sex of the fly (χ2 = 0.099, df = 1, p = 0.753), district of origin (χ2= 0.629, df = 1, p = 0.428) and village of origin (χ2= 9.252, df = 9, p = 0.414). Nested PCR revealed several species of trypanosomes: T. vivax (6.62%), T. congolense (2.57%), T. brucei and T. simiae each at 0.73%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusio schapini) and the African Savanna elephant (Loxodonta africana).Conclusion: We found an infection rate of 10.78 %, with all infections attributed to trypanosome species that are causative agents for the animal disease only. However, more verification of this finding using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of interventions.

scholarly journals Extrachromosomal DNA of the Symbiont Sodalis glossinidius

2005 ◽  
Vol 187 (14) ◽  
pp. 5003-5007 ◽  
Author(s):  
A. C. Darby ◽  
J. Lagnel ◽  
C. Z. Matthew ◽  
K. Bourtzis ◽  
I. Maudlin ◽  
...  
Keyword(s):  
Tsetse Fly ◽  
Tsetse Flies ◽  
Extrachromosomal Dna ◽  
Sodalis Glossinidius

ABSTRACT The extrachromosomal DNA of Sodalis glossinidius from two tsetse fly species was sequenced and contained four circular elements: three plasmids, pSG1 (82 kb), pSG2 (27 kb), and pSG4 (11 kb), and a bacteriophage-like pSG3 (19 kb) element. The information suggests S. glossinidius is evolving towards an obligate association with tsetse flies.

scholarly journals TonB-Dependent Heme Iron Acquisition in the Tsetse Fly Symbiont Sodalis glossinidius

2015 ◽  
Vol 81 (8) ◽  
pp. 2900-2909 ◽  
Author(s):  
Gili Hrusa ◽  
William Farmer ◽  
Brian L. Weiss ◽  
Taylor Applebaum ◽  
Jose Santinni Roma ◽  
...  
Keyword(s):  
Iron Acquisition ◽  
Physiological Role ◽  
Enteric Bacteria ◽  
Heme Iron ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
Content Type ◽  
Iron Source ◽  
Sodalis Glossinidius ◽  
Acquisition Processes

ABSTRACTSodalis glossinidiusis an intra- and extracellular symbiont of the tsetse fly (Glossinasp.), which feeds exclusively on vertebrate blood.S. glossinidiusresides in a wide variety of tsetse tissues and may encounter environments that differ dramatically in iron content. TheSodalischromosome encodes a putative TonB-dependent outer membrane heme transporter (HemR) and a putative periplasmic/inner membrane ABC heme permease system (HemTUV). Because these gene products mediate iron acquisition processes by other enteric bacteria, we characterized their regulation and physiological role in theSodalis/tsetse system. Our results show that thehemRandtonBgenes are expressed byS. glossinidiusin the tsetse fly. Furthermore, transcription ofhemRinSodalisis repressed in a high-iron environment by the iron-responsive transcriptional regulator Fur. Expression of theS. glossinidiushemRandhemTUVgenes in anEscherichia colistrain unable to use heme as an iron source stimulated growth in the presence of heme or hemoglobin as the sole iron source. This stimulation was dependent on the presence of either theE. coliorSodalistonBgene.SodalistonBandhemRmutant strains were defective in their ability to colonize the gut of tsetse flies that lacked endogenous symbionts, while wild-typeS. glossinidiusproliferated in this same environment. Finally, we show that theSodalisHemR protein is localized to the bacterial membrane and appears to bind hemin. Collectively, this study provides strong evidence that TonB-dependent, HemR-mediated iron acquisition is important for the maintenance of symbiont homeostasis in the tsetse fly, and it provides evidence for the expression of bacterial high-affinity iron acquisition genes in insect symbionts.

scholarly journals OmpA-Mediated Biofilm Formation Is Essential for the Commensal Bacterium Sodalis glossinidius To Colonize the Tsetse Fly Gut

2012 ◽  
Vol 78 (21) ◽  
pp. 7760-7768 ◽  
Author(s):  
Michele A. Maltz ◽  
Brian L. Weiss ◽  
Michelle O'Neill ◽  
Yineng Wu ◽  
Serap Aksoy
Keyword(s):  
Immune System ◽  
Pathogenic Bacteria ◽  
Tsetse Fly ◽  
Symbiotic Bacteria ◽  
Tsetse Flies ◽  
Host Immune System ◽  
Content Type ◽  
African Trypanosomes ◽  
Sodalis Glossinidius

ABSTRACTMany 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 (Glossinaspp.) house 3 maternally transmitted symbionts, one of which is a commensal (Sodalis glossinidius) found in several host tissues, including the gut. We determined thatSodalisforms biofilms in the tsetse gut and that this process is influenced by theSodalisouter membrane protein A (OmpA). MutantSodalisstrains that do not produce OmpA (SodalisΔOmpA mutants) fail to form biofilmsin vitroand are unable to colonize the tsetse gut unless endogenous symbiotic bacteria are present. Our data indicate that in the absence of biofilms,SodalisΔOmpA mutant cells are exposed to and eliminated by tsetse's innate immune system, suggesting that biofilms helpSodalisevade 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 promoteSodaliscolonization of the tsetse gut may enhance the development of novel disease control strategies.

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