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.

scholarly journals Characterization of the Achromobactin Iron Acquisition Operon in Sodalis glossinidius

2013 ◽  
Vol 79 (9) ◽  
pp. 2872-2881 ◽  
Author(s):  
Caitlin L. Smith ◽  
Brian L. Weiss ◽  
Serap Aksoy ◽  
Laura J. Runyen-Janecky
Keyword(s):  
Iron Acquisition ◽  
Tsetse Fly ◽  
Pcr Analysis ◽  
Outer Membrane Receptor ◽  
Content Type ◽  
Sodalis Glossinidius ◽  
Intracellular Symbiont ◽  
Insect Symbionts ◽  
Siderophore Synthesis

ABSTRACTSodalis glossinidiusis a facultative, extra- and intracellular symbiont found in most tissues of the tsetse fly (Glossiniasp.).Sodalishas 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 whenSodalisis 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 theSodalisachromobactin promoter bound Fur inEscherichia coliFur titration assays. Wild-typeSodalisproduced detectable siderophorein vitro, but a mutation in the putative achromobactin biosynthesis geneacsDeliminated detectable siderophore production inSodalis. 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 aSodalisferric-siderophore outer membrane receptor mutant with a mutation inacrwas not reconstituted by exogenous siderophore due to its defective transporter. TheSodalissiderophore synthesis mutant showed reduced growth in tsetse that lacked endogenous symbionts (aposymbiotic) when the flies were inoculated withSodalisintrathoracically, but not when inoculatedper os. Our findings suggest thatSodalissiderophores play a role in iron acquisition in certain tsetse fly tissues and provide evidence for the regulation of iron acquisition mechanisms in insect symbionts.

scholarly journals Conjugal DNA Transfer in Sodalis glossinidius, a Maternally Inherited Symbiont of Tsetse Flies

mSphere ◽  
2020 ◽  
Vol 5 (6) ◽  
Author(s):  
Christopher G. Kendra ◽  
Chelsea M. Keller ◽  
Roberto E. Bruna ◽  
Mauricio H. Pontes
Keyword(s):  
Genetic Manipulation ◽  
Bacterial Species ◽  
Zoonotic Disease ◽  
Tsetse Fly ◽  
Dna Transfer ◽  
Sub Saharan Africa ◽  
Tsetse Flies ◽  
Dna Uptake ◽  
Content Type ◽  
Sodalis Glossinidius

ABSTRACT Stable associations between insects and bacterial species are widespread in nature. This is the case for many economically important insects, such as tsetse flies. Tsetse flies are the vectors of Trypanosoma brucei, the etiological agent of African trypanosomiasis—a zoonotic disease that incurs a high socioeconomic cost in regions of endemicity. Populations of tsetse flies are often infected with the bacterium Sodalis glossinidius. Following infection, S. glossinidius establishes a chronic, stable association characterized by vertical (maternal) and horizontal (paternal) modes of transmission. Due to the stable nature of this association, S. glossinidius has been long sought as a means for the implementation of anti-Trypanosoma paratransgenesis in tsetse flies. However, the lack of tools for the genetic modification of S. glossinidius has hindered progress in this area. Here, we establish that S. glossinidius is amenable to DNA uptake by conjugation. We show that conjugation can be used as a DNA delivery method to conduct forward and reverse genetic experiments in this bacterium. This study serves as an important step in the development of genetic tools for S. glossinidius. The methods highlighted here should guide the implementation of genetics for the study of the tsetse-Sodalis association and the evaluation of S. glossinidius-based tsetse fly paratransgenesis strategies. IMPORTANCE Tsetse flies are the insect vectors of T. brucei, the causative agent of African sleeping sickness—a zoonotic disease that inflicts a substantial economic cost on a broad region of sub-Saharan Africa. Notably, tsetse flies can be infected with the bacterium S. glossinidius to establish an asymptomatic chronic infection. This infection can be inherited by future generations of tsetse flies, allowing S. glossinidius to spread and persist within populations. To this effect, S. glossinidius has been considered a potential expression platform to create flies which reduce T. brucei stasis and lower overall parasite transmission to humans and animals. However, the efficient genetic manipulation of S. glossinidius has remained a technical challenge due to its complex growth requirements and uncharacterized physiology. Here, we exploit a natural mechanism of DNA transfer among bacteria and develop an efficient technique to genetically manipulate S. glossinidius for future studies in reducing trypanosome transmission.

scholarly journals Human Serum Albumin Facilitates Heme-Iron Utilization by Fungi

mBio ◽  
2020 ◽  
Vol 11 (2) ◽  
Author(s):  
Mariel Pinsky ◽  
Udita Roy ◽  
Shilat Moshe ◽  
Ziva Weissman ◽  
Daniel Kornitzer
Keyword(s):  
Human Serum Albumin ◽  
Serum Albumin ◽  
Human Serum ◽  
Heme Iron ◽  
Content Type ◽  
Animal Host ◽  
Iron Source ◽  
Free Heme ◽  
Pathogenic Microbes ◽  
Iron Utilization

ABSTRACT A large portion of biological iron is found in the form of an iron-protoporphyrin IX complex, or heme. In the human host environment, which is exceptionally poor in free iron, heme iron, particularly from hemoglobin, constitutes a major source of iron for invading microbial pathogens. Several fungi were shown to utilize free heme, and Candida albicans, a major opportunistic pathogen, is able both to capture free heme and to extract heme from hemoglobin using a network of extracellular hemophores. Human serum albumin (HSA) is the most abundant host heme-scavenging protein. Tight binding of heme by HSA restricts its toxic chemical reactivity and could diminish its availability as an iron source for pathogenic microbes. We found, however, that rather than inhibiting heme utilization, HSA greatly increases availability of heme as an iron source for C. albicans and other fungi. In contrast, hemopexin, a low-abundance but high-affinity heme-scavenging serum protein, does inhibit heme utilization by C. albicans. However, inhibition by hemopexin is mitigated in the presence of HSA. Utilization of albumin-bound heme requires the same hemophore cascade as that which mediates hemoglobin-iron utilization. Accordingly, we found that the C. albicans hemophores are able to extract heme bound to HSA in vitro. Since many common drugs are known to bind to HSA, we tested whether they could interfere with heme-iron utilization. We show that utilization of albumin-bound heme by C. albicans can be inhibited by the anti-inflammatory drugs naproxen and salicylic acid. IMPORTANCE Heme constitutes a major iron source for microorganisms and particularly for pathogenic microbes; to overcome the iron scarcity in the animal host, many pathogenic bacteria and fungi have developed systems to extract and take up heme from host proteins such as hemoglobin. Microbial heme uptake mechanisms are usually studied using growth media containing free heme or hemoglobin as a sole iron source. However, the animal host contains heme-scavenging proteins that could prevent this uptake. In the human host in particular, the most abundant serum heme-binding protein is albumin. Surprisingly, however, we found that in the case of fungi of the Candida species family, albumin promoted rather than prevented heme utilization. Albumin thus constitutes a human-specific factor that can affect heme-iron utilization and could serve as target for preventing heme-iron utilization by fungal pathogens. As a proof of principle, we identify two drugs that can inhibit albumin-stimulated heme utilization.

scholarly journals A Tale of Three Species: Adaptation ofSodalis glossinidiusto Tsetse Biology,WigglesworthiaMetabolism, and Host Diet

mBio ◽  
2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Rebecca J. Hall ◽  
Lindsey A. Flanagan ◽  
Michael J. Bottery ◽  
Vicki Springthorpe ◽  
Stephen Thorpe ◽  
...  
Keyword(s):  
Trypanosoma Brucei ◽  
Human African Trypanosomiasis ◽  
Strong Dependence ◽  
Tsetse Fly ◽  
Disease Spread ◽  
Growth Media ◽  
Insect Vector ◽  
African Trypanosomiasis ◽  
Content Type ◽  
Sodalis Glossinidius

ABSTRACTThe tsetse fly is the insect vector for theTrypanosoma bruceiparasite, the causative agent of human African trypanosomiasis. The colonization and spread of the trypanosome correlate positively with the presence of a secondary symbiotic bacterium,Sodalis glossinidius. The metabolic requirements and interactions of the bacterium with its host are poorly understood, and herein we describe a metabolic model ofS. glossinidiusmetabolism. The model enabled the design and experimental verification of a defined medium that supportsS. glossinidiusgrowthex vivo. This has been used subsequently to analyzein vitroaspects ofS. glossinidiusmetabolism, revealing multiple unique adaptations of the symbiont to its environment. Continued dependence on a sugar, and the importance of the chitin monomerN-acetyl-d-glucosamine as a carbon and energy source, suggests adaptation to host-derived molecules. Adaptation to the amino acid-rich blood diet is revealed by a strong dependence onl-glutamate as a source of carbon and nitrogen and by the ability to rescue a predictedl-arginine auxotrophy. Finally, the selective loss of thiamine biosynthesis, a vitamin provided to the host by the primary symbiontWigglesworthia glossinidia, reveals an intersymbiont dependence. The reductive evolution ofS. glossinidiusto exploit environmentally derived metabolites has resulted in multiple weaknesses in the metabolic network. These weaknesses may become targets for reagents that inhibitS. glossinidiusgrowth and aid the reduction of trypanosomal transmission.IMPORTANCEHuman African trypanosomiasis is caused by theTrypanosoma bruceiparasite. The tsetse fly vector is of interest for its potential to prevent disease spread, as it is essential forT. bruceilife cycle progression and transmission. The tsetse’s mutualistic endosymbiontSodalis glossinidiushas a link to trypanosome establishment, providing a disease control target. Here, we describe a new, experimentally verified model ofS. glossinidiusmetabolism. This model has enabled the development of a defined growth medium that was used successfully to test aspects ofS. glossinidiusmetabolism. We presentS. glossinidiusas uniquely adapted to life in the tsetse, through its reliance on the blood diet and host-derived sugars. Additionally,S. glossinidiushas adapted to the tsetse’s obligate symbiontWigglesworthia glossinidiaby scavenging a vitamin it produces for the insect. This work highlights the use of metabolic modeling to design defined growth media for symbiotic bacteria and may provide novel inhibitory targets to block trypanosome transmission.

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.

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 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 Vitamin B6Generated by Obligate Symbionts Is Critical for Maintaining Proline Homeostasis and Fecundity in Tsetse Flies

2014 ◽  
Vol 80 (18) ◽  
pp. 5844-5853 ◽  
Author(s):  
Veronika Michalkova ◽  
Joshua B. Benoit ◽  
Brian L. Weiss ◽  
Geoffrey M. Attardo ◽  
Serap Aksoy
Keyword(s):  
Pyridoxal Phosphate ◽  
Tsetse Fly ◽  
Tsetse Flies ◽  
Vitamin B ◽  
Lactation Period ◽  
Content Type ◽  
African Trypanosomes ◽  
Microbial Extracts ◽  
Lactating Females ◽  
Interfering Rna

ABSTRACTThe 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 ofWigglesworthia-produced vitamin B6for maintenance of proline homeostasis, specifically during the energetically expensive lactation period of the tsetse's reproductive cycle. We found that expression ofagat, as well as genes involved in vitamin B6metabolism 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 B6in lactating females, and decreased fecundity. Proline homeostasis and fecundity recovered partially when aposymbiotic tsetse were fed a diet supplemented with either yeast orWigglesworthiaextracts. RNA interference-mediated knockdown ofagatin wild-type flies reduced hemolymph proline levels to that of aposymbiotic females. Aposymbiotic flies treated withagatshort 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 ofWigglesworthiain tsetse is critical for the maintenance of proline homeostasis through vitamin B6production.

scholarly journals Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont Wigglesworthia

mBio ◽  
2012 ◽  
Vol 3 (1) ◽  
Author(s):  
Rita V. M. Rio ◽  
Rebecca E. Symula ◽  
Jingwen Wang ◽  
Claudia Lohs ◽  
Yi-neng Wu ◽  
...  
Keyword(s):  
Transcriptional Regulation ◽  
Host Species ◽  
Tsetse Fly ◽  
Sister Species ◽  
Tsetse Flies ◽  
Specific Gene ◽  
Glossina Morsitans ◽  
Content Type ◽  
African Trypanosomes ◽  
Species Specific

ABSTRACT Ancient endosymbionts have been associated with extreme genome structural stability with little differentiation in gene inventory between sister species. Tsetse flies (Diptera: Glossinidae) harbor an obligate endosymbiont, Wigglesworthia, which has coevolved with the Glossina radiation. We report on the ~720-kb Wigglesworthia genome and its associated plasmid from Glossina morsitans morsitans and compare them to those of the symbiont from Glossina brevipalpis. While there was overall high synteny between the two genomes, a large inversion was noted. Furthermore, symbiont transcriptional analyses demonstrated host tissue and development-specific gene expression supporting robust transcriptional regulation in Wigglesworthia, an unprecedented observation in other obligate mutualist endosymbionts. Expression and immunohistochemistry confirmed the role of flagella during the vertical transmission process from mother to intrauterine progeny. The expression of nutrient provisioning genes (thiC and hemH) suggests that Wigglesworthia may function in dietary supplementation tailored toward host development. Furthermore, despite extensive conservation, unique genes were identified within both symbiont genomes that may result in distinct metabolomes impacting host physiology. One of these differences involves the chorismate, phenylalanine, and folate biosynthetic pathways, which are uniquely present in Wigglesworthia morsitans. Interestingly, African trypanosomes are auxotrophs for phenylalanine and folate and salvage both exogenously. It is possible that W. morsitans contributes to the higher parasite susceptibility of its host species. IMPORTANCE Genomic stasis has historically been associated with obligate endosymbionts and their sister species. Here we characterize the Wigglesworthia genome of the tsetse fly species Glossina morsitans and compare it to its sister genome within G. brevipalpis. The similarity and variation between the genomes enabled specific hypotheses regarding functional biology. Expression analyses indicate significant levels of transcriptional regulation and support development- and tissue-specific functional roles for the symbiosis previously not observed in obligate mutualist symbionts. Retention of the genetically expensive flagella within these small genomes was demonstrated to be significant in symbiont transmission and tailored to the unique tsetse fly reproductive biology. Distinctions in metabolomes were also observed. We speculate an additional role for Wigglesworthia symbiosis where infections with pathogenic trypanosomes may depend upon symbiont species-specific metabolic products and thus influence the vector competence traits of different tsetse fly host species.

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