Reproductive Physiology of Glossina

Tobe, Stephen S.; Langley, P. A.

doi:10.1146/annurev.en.23.010178.001435

Cited by 113 publications

(89 citation statements)

References 55 publications

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“…In adenotrophic viviparity, the majority of larval development oc-curs in utero, where the mother provides nourishment, mostly in the form of amino acids and lipids (28), and vertically transmits the Wigglesworthia and Sodalis symbionts through highly specialized accessory organs, known as milk glands (29,30). Following the completion of intrauterine larval development, a late 3rd-instar larva is deposited and quickly enters into pupation.…”

mentioning

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

Snyder

Rio

2015

Appl Environ Microbiol

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“…), which are distributed throughout sub-Saharan Africa, are vectors of human and animal African trypanosomiasis. Several aspects of the tsetse's physiology are distinctive from those of other insects, including viviparous reproduction, exclusive reliance on proline as the major energy source, and dependence on obligate symbionts for fecundity (1)(2)(3)(4)(5). Due to their viviparous reproductive physiology, tsetse females are limited to a maximum of 8 to 12 progeny during their lifetime (1).…”

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“…Several aspects of the tsetse's physiology are distinctive from those of other insects, including viviparous reproduction, exclusive reliance on proline as the major energy source, and dependence on obligate symbionts for fecundity (1)(2)(3)(4)(5). Due to their viviparous reproductive physiology, tsetse females are limited to a maximum of 8 to 12 progeny during their lifetime (1). During each gonotrophic cycle, a single offspring undergoes embryonic and complete larval development within the female's uterus (expanded reproductive tract) (6).…”

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“…Immediately after birth, deposited larvae burrow into the ground, pupate, and remain dormant until eclosion (6). All nutrients required for larval and pupal development are provisioned through the female accessory gland (milk gland) in the form of intrauterine milk secretions (1,7,8). During each lactation cycle, the milk gland secretes up to 25 mg of milk that consists primarily of lipids and proteins (9).…”

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Vitamin B ₆ Generated by Obligate Symbionts Is Critical for Maintaining Proline Homeostasis and Fecundity in Tsetse Flies

Michalková

Benoit

Weiss

et al. 2014

Appl Environ Microbiol

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bThe 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 B 6 ) 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 B 6 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 B 6 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 B 6 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 B 6 production.

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“…This reproductive strategy involves high maternal investment and a low reproductive output of only 6 to 8 offspring in their 3-to-4-month life span (34). Unlike many higher Dipteran, female tsetse have highly modified reproductive tracts (39), enabling the deposition of a single fertilized egg into a muscular uterus, which is connected to highly specialized accessory glands, referred to as milk glands. Milk secretions provide nourishment and a route through which microbial symbionts (40,41) are transferred during intrauterine larval development.…”

Section: The Tsetse Flymentioning

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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Reproductive Physiology of Glossina

Cited by 113 publications

References 55 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

Vitamin B ₆ Generated by Obligate Symbionts Is Critical for Maintaining Proline Homeostasis and Fecundity in Tsetse Flies

Interwoven Biology of the Tsetse Holobiont

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Reproductive Physiology of Glossina

Cited by 113 publications

References 55 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

Vitamin B 6 Generated by Obligate Symbionts Is Critical for Maintaining Proline Homeostasis and Fecundity in Tsetse Flies

Interwoven Biology of the Tsetse Holobiont

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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

Vitamin B ₆ Generated by Obligate Symbionts Is Critical for Maintaining Proline Homeostasis and Fecundity in Tsetse Flies