Secretory discharge and microflora of milk gland in tsetse flies

Ma, Wuqiang; Denlinger, David L.

doi:10.1038/247301a0

Cited by 77 publications

(52 citation statements)

References 5 publications

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“…After maturation and sequential molting, a third-instar larva is deposited and pupates shortly thereafter. Nutrients and tsetse symbionts are transmitted to the intrauterine progeny through the mother's milk-gland secretions 16,17 . It is not known, however, whether whole bacteriocytes or W. glossinidia cells are transferred from a mother to her larva.…”

Section: Lettermentioning

confidence: 99%

Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia

et al. 2002

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Many insects that rely on a single food source throughout their developmental cycle harbor beneficial microbes that provide nutrients absent from their restricted diet. Tsetse flies, the vectors of African trypanosomes, feed exclusively on blood and rely on one such intracellular microbe for nutritional provisioning and fecundity. As a result of co-evolution with hosts over millions of years, these mutualists have lost the ability to survive outside the sheltered environment of their host insect cells. We present the complete annotated genome of Wigglesworthia glossinidia brevipalpis, which is composed of one chromosome of 697,724 base pairs (bp) and one small plasmid, called pWig1, of 5,200 bp. Genes involved in the biosynthesis of vitamin metabolites, apparently essential for host nutrition and fecundity, have been retained. Unexpectedly, this obligate's genome bears hallmarks of both parasitic and free-living microbes, and the gene encoding the important regulatory protein DnaA is absent.Many arthropods with restricted diets, such as vertebrate blood, plant juice or wood, rely on symbiotic microorganisms to supply nutrients required for viability and fertility 1 . Among insects harboring such symbionts is the tsetse fly (Diptera: Glossinidae)-the vector of African trypanosomes, agents of deadly diseases in humans and animals in sub-Saharan Africa 2 . Tsetse flies harbor two symbiotic microorganisms in gut tissue: the obligate primary-symbiont Wigglesworthia glossinidia and the commensal secondarysymbiont Sodalis glossinidius. Whereas S. glossinidius may be found in various host tissue types, W. glossinidia is housed in differentiated host epithelial cells (bacteriocytes) that form the bacteriome organ 2 . The functional role of obligate symbionts in tsetses has been difficult to study, as their elimination results in retarded growth and a decrease in egg production and fecundity in the aposymbiotic host 3,4 . The ability to reproduce could be partially restored, however, when aposymbiotic flies received supplementation with B-complex vitamins, suggesting that the endosymbionts might have a metabolic role involving these compounds 5 .The phylogenetic characterization of W. glossinidia from distant tsetse species has shown that they form a distinct clade in the Enterobacteriaceae 6 and display concordant evolution with their host species 7 . This finding implies that a tsetse ancestor was infected with a bacterium some 50-100 million years ago, and extant species of tsetse and associated W. glossinidia strains radiated without horizontal transfer of genetic material between species.As a result of their intracellular lifestyle, the genomes of obligate symbionts have undergone massive reductions in comparison with their free-living relatives. The genome size of W. glossinidia has been estimated as 740-770 kilobases 8 (kb), and that of Buchnera sp., the obligate symbiont of the pea aphid (Homoptera:Aphidoidea), as 640,681 bp 9,10 . Both genomes approach the size of the smallest genome reported thus far, that of My...

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Section: Lettermentioning

confidence: 99%

Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia

et al. 2002

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“…1). An additional extracellular population is found in the female milk glands which is maternally transmitted to offspring (40,41). Described roles of this symbiont include both nutrient provisioning, where Wigglesworthia supplements B vitamins lacking in the tsetse blood diet (38,(53)(54)(55), and contributions to the maturation of host immunity (35,56,57).…”

Section: Tsetse Microbial Communitymentioning

confidence: 99%

“…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. This form of reproduction transmits the microbiota with high fidelity while preventing exposure to transient microbes during early tsetse development (35).…”

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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“…Females give birth to a single mature larva, which pupates and remains dormant until eclosion. All tsetse harbor the obligate mutualist Wigglesworthia glossinidia, which resides intracellularly in the midgut bacteriome organ and extracellularly in mother's milk (7,10). Wigglesworthia supplements tsetse's nutritionally restricted blood diet with vitamins (11), and without Wigglesworthia, females are reproductively sterile.…”

mentioning

confidence: 99%

PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring

Wang

Aksoy

2012

Proc. Natl. Acad. Sci. U.S.A.

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Beneficial microbe functions range from host dietary supplementation to development and maintenance of host immune system. In mammals, newborn progeny are quickly colonized with a symbiotic fauna that is provisioned in mother's milk and that closely resembles that of the parent. Tsetse fly (Diptera: Glossinidae) also depends on the obligate symbiont Wigglesworthia for nutritional supplementation, optimal fecundity, and immune system development. Tsetse progeny develop one at a time in an intrauterine environment and receive nourishment and symbionts in mother's milk. We show that the host Peptidoglycan Recognition Protein (PGRP-LB) is expressed only in adults and is a major component of the milk that nourishes the developing progeny. The amidase activity associated with PGRP-LB may scavenge the symbiotic peptidoglycan and prevent the induction of tsetse's Immune Deficiency pathway that otherwise can damage the symbionts. Reduction of PGRP-LB experimentally diminishes female fecundity and damages Wigglesworthia in the milk through induction of antimicrobial peptides, including Attacin. Larvae that receive less maternal PGRP-LB give rise to adults with fewer Wigglesworthia and hyperimmune responses. Such adults also suffer dysregulated immunity, as indicated by the presence of higher trypanosome densities in parasitized adults. We show that recPGRP-LB has antimicrobial and antitrypanosomal activities that may regulate symbiosis and impact immunity. Thus, PGRP-LB plays a pivotal role in tsetse's fitness by protecting symbiosis against host-inflicted damage during development and by controlling parasite infections in adults that can otherwise reduce host fecundity. maternal transfer | transgenerational immune effects | antimicrobial activity | antitrypanosomal activity

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Secretory discharge and microflora of milk gland in tsetse flies

Cited by 77 publications

References 5 publications

Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia

Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia

Interwoven Biology of the Tsetse Holobiont

PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring

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