Tripartite interactions between tsetse flies, Sodalis glossinidius and trypanosomes—An epidemiological approach in two historical human African trypanosomiasis foci in Cameroon

Farikou, Oumarou; Njiokou, Flobert; Mbida, Jean Arthur Mbida; Njitchouang, Guy R.; Djeunga, Hugues Nana; Asonganyi, Tazoacha; Simarro, Pere P.; Cuny, G; Geiger, Anne

doi:10.1016/j.meegid.2009.10.008

Cited by 115 publications

(126 citation statements)

References 28 publications

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“…The absence of W. morsitans through tsetse host generations (in which the host is capable of reproducing when maintained on yeast extract-supplemented blood meals) also resulted in the eventual loss of Sodalis (39), supporting a metabolic dependence of Sodalis on W. morsitans, which has previously been shown with thiamine (vitamin B 1 ) (5). Additionally, in the field, Sodalis is not present in all tsetse populations or individuals (23,74), indicating that this secondary symbiont has been established more recently and does not play a role as pivotal as that of W. morsitans in tsetse fitness. To ensure that this study solely examined the contributions of W. morsitans, folate production within the bacteriome organ, which is densely packed with W. morsitans cells, was measured, and the study also utilized primers that specifically amplify W. morsitans loci.…”

Section: Discussionmentioning

confidence: 99%

“Wigglesworthia morsitans” Folate (Vitamin B ₉ ) Biosynthesis Contributes to Tsetse Host Fitness

Snyder

Rio

2015

Appl Environ Microbiol

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Closely related ancient endosymbionts may retain minor genomic distinctions through evolutionary time, yet the biological relevance of these small pockets of unique loci remains unknown. The tsetse fly (Diptera: Glossinidae), the sole vector of lethal African trypanosomes (Trypanosoma spp.), maintains an ancient and obligate mutualism with species belonging to the gammaproteobacterium Wigglesworthia. Extensive concordant evolution with associated Wigglesworthia species has occurred through tsetse species radiation. Accordingly, the retention of unique symbiont loci between Wigglesworthia genomes may prove instrumental toward host species-specific biological traits. Genome distinctions between "Wigglesworthia morsitans" (harbored within Glossina morsitans bacteriomes) and the basal species Wigglesworthia glossinidia (harbored within Glossina brevipalpis bacteriomes) include the retention of chorismate and downstream folate (vitamin B 9 ) biosynthesis capabilities, contributing to distinct symbiont metabolomes. Here, we demonstrate that these W. morsitans pathways remain functionally intact, with folate likely being systemically disseminated through a synchronously expressed tsetse folate transporter within bacteriomes. The folate produced by W. morsitans is demonstrated to be pivotal for G. morsitans sexual maturation and reproduction. Modest differences between ancient symbiont genomes may still play key roles in the evolution of their host species, particularly if loci are involved in shaping host physiology and ecology. Enhanced knowledge of the Wigglesworthia-tsetse mutualism may also provide novel and specific avenues for vector control. Bacteria adapt to specific environments, including host-associated niches, through the retention, rearrangement, gain, or decay of functional capabilities. Research on ancient obligate host associations (i.e., in which bacteria display an extensive concordant evolution with their host) has demonstrated that microbial symbiont genome evolution can be influenced by microbial community dynamics (1-6), in addition to host physiology and ecology (7-9). One extreme case has been described within the mealybug, where dual symbiont species and the host have retained complementary loci that, only when integrated as a symbiotic system (i.e., a holobiont) and not as individual species, are capable of producing specific requisite nutrients (3, 9). Extensive gene purging is characteristic among ancient bacterial symbionts, as they challenge the lower limits of genome size (10, 11). These symbionts typically exhibit tremendous genomic stasis between strains and species, likely due to their environmental isolation, as their genomes encode only those capabilities necessary for the maintenance of the mutualism (reviewed in reference 10). In contrast, the genomes of free-living bacteria allow the bacteria to adapt to their surroundings by encoding a plethora of strain-specific loci, known as dispensable genes (12), contributing to increased habitat occupancy and their successful viability with...

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Section: Discussionmentioning

confidence: 99%

“Wigglesworthia morsitans” Folate (Vitamin B ₉ ) Biosynthesis Contributes to Tsetse Host Fitness

Snyder

Rio

2015

Appl Environ Microbiol

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“…Evidence lies in its ability to be cultured (64), providing a tremendous benefit for empirical analyses, wide tsetse tissue tropism with both intra-and extracellular localization (41,48), lack of coevolution with host species (10), and stochastic presence in the field (49,51,65). Similar to Wigglesworthia, Sodalis is vertically transmitted through the maternal milk glands (40,41).…”

Section: Tsetse Microbial Communitymentioning

confidence: 99%

“…In fact, a recent International Atomic Energy Agency (IAEA)-coordinated research project (CRP) aims to unravel the interactions between the tsetse host, Wigglesworthia, Sodalis, Wolbachia, and SGHV and the development of African trypanosomes to increase knowledge of ways to enhance refractoriness to trypanosome infection (116). Past studies have demonstrated a positive correlation between Sodalis presence and trypanosome infections in field flies (65,117). Sodalis is believed to contribute to the susceptibility of teneral flies (i.e., newly emerged unfed adults) through its endochitinase activity within the midgut which breaks down chitin (118), producing a byproduct of N-acetyl-D-glucosamine which inhibits the action of trypanocidal lectins (118,119).…”

Section: Understanding the Tsetse Holobiont For Enhanced Vector Controlmentioning

confidence: 99%

Interwoven Biology of the Tsetse Holobiont

Snyder

Rio

2013

J Bacteriol

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Microbial symbionts can be instrumental to the evolutionary success of their hosts. Here, we discuss medically significant tsetse flies (Diptera: Glossinidae), a group comprised of over 30 species, and their use as a valuable model system to study the evolution of the holobiont (i.e., the host and associated microbes). We first describe the tsetse microbiota, which, despite its simplicity, harbors a diverse range of associations. The maternally transmitted microbes consistently include two Gammaproteobacteria, the obligate mutualists Wigglesworthia spp. and the commensal Sodalis glossinidius, along with the parasitic Alphaproteobacteria Wolbachia. These associations differ in their establishment times, making them unique and distinct from previously characterized symbioses, where multiple microbial partners have associated with their host for a significant portion of its evolution. We then expand into discussing the functional roles and intracommunity dynamics within this holobiont, which enhances our understanding of tsetse biology to encompass the vital functions and interactions of the microbial community. Potential disturbances influencing the tsetse microbiome, including salivary gland hypertrophy virus and trypanosome infections, are highlighted. While previous studies have described evolutionary consequences of host association for symbionts, the initial steps facilitating their incorporation into a holobiont and integration of partner biology have only begun to be explored. Research on the tsetse holobiont will contribute to the understanding of how microbial metabolic integration and interdependency initially may develop within hosts, elucidating mechanisms driving adaptations leading to cooperation and coresidence within the microbial community. Lastly, increased knowledge of the tsetse holobiont may also contribute to generating novel African trypanosomiasis disease control strategies.

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“…Both endosymbionts are also found extracellularly in the lumen of female milk glands and are vertically transmitted to intrauterine larvae in milk secretions during larval nourishment (23). While all individuals in different tsetse species carry Wigglesworthia, the prevalence of Sodalis in natural populations varies (24,25). Previous studies have found a positive correlation between the presence of Sodalis and trypanosome infections in natural tsetse populations (reviewed in reference 26), and various Sodalis genotypes have been found in different tsetse species (27,28).…”

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confidence: 99%

Analysis of Multiple Tsetse Fly Populations in Uganda Reveals Limited Diversity and Species-Specific Gut Microbiota

Aksoy

Telleria

Echodu

et al. 2014

Appl Environ Microbiol

110

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The invertebrate microbiome contributes to multiple aspects of host physiology, including nutrient supplementation and immune maturation processes. We identified and compared gut microbial abundance and diversity in natural tsetse flies from Uganda using five genetically distinct populations of Glossina fuscipes fuscipes and multiple tsetse species (Glossina morsitans morsitans, G. f. fuscipes, and Glossina pallidipes) that occur in sympatry in one location. We used multiple approaches, including deep sequencing of the V4 hypervariable region of the 16S rRNA gene, 16S rRNA gene clone libraries, and bacterium-specific quantitative PCR (qPCR), to investigate the levels and patterns of gut microbial diversity from a total of 151 individuals. Our results show extremely limited diversity in field flies of different tsetse species. The obligate endosymbiont Wigglesworthia dominated all samples (>99%), but we also observed wide prevalence of low-density Sodalis (tsetse's commensal endosymbiont) infections (<0.05%). There were also several individuals (22%) with high Sodalis density, which also carried coinfections with Serratia. Albeit in low density, we noted differences in microbiota composition among the genetically distinct G. f. fuscipes flies and between different sympatric species. Interestingly, Wigglesworthia density varied in different species (10 4 to 10 6 normalized genomes), with G. f. fuscipes having the highest levels. We describe the factors that may be responsible for the reduced diversity of tsetse's gut microbiota compared to those of other insects. Additionally, we discuss the implications of Wigglesworthia and Sodalis density variations as they relate to trypanosome transmission dynamics and vector competence variations associated with different tsetse species.

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Tripartite interactions between tsetse flies, Sodalis glossinidius and trypanosomes—An epidemiological approach in two historical human African trypanosomiasis foci in Cameroon

Cited by 115 publications

References 28 publications

“Wigglesworthia morsitans” Folate (Vitamin B ₉ ) Biosynthesis Contributes to Tsetse Host Fitness

“Wigglesworthia morsitans” Folate (Vitamin B ₉ ) Biosynthesis Contributes to Tsetse Host Fitness

Interwoven Biology of the Tsetse Holobiont

Analysis of Multiple Tsetse Fly Populations in Uganda Reveals Limited Diversity and Species-Specific Gut Microbiota

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Tripartite interactions between tsetse flies, Sodalis glossinidius and trypanosomes—An epidemiological approach in two historical human African trypanosomiasis foci in Cameroon

Cited by 115 publications

References 28 publications

“Wigglesworthia morsitans” Folate (Vitamin B 9 ) Biosynthesis Contributes to Tsetse Host Fitness

“Wigglesworthia morsitans” Folate (Vitamin B 9 ) Biosynthesis Contributes to Tsetse Host Fitness

Interwoven Biology of the Tsetse Holobiont

Analysis of Multiple Tsetse Fly Populations in Uganda Reveals Limited Diversity and Species-Specific Gut Microbiota

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Product

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“Wigglesworthia morsitans” Folate (Vitamin B ₉ ) Biosynthesis Contributes to Tsetse Host Fitness

“Wigglesworthia morsitans” Folate (Vitamin B ₉ ) Biosynthesis Contributes to Tsetse Host Fitness