Obligate Symbionts Activate Immune System Development in the Tsetse Fly

Division of Epidemiology of Microbial Diseases, Department of Epidemiology and Public Health, Yale University School of Medicine, New Haven, CT 06520, USA.
The Journal of Immunology (Impact Factor: 4.92). 02/2012; 188(7):3395-403. DOI: 10.4049/jimmunol.1103691
Source: PubMed

ABSTRACT Many insects rely on the presence of symbiotic bacteria for proper immune system function. However, the molecular mechanisms that underlie this phenomenon are poorly understood. Adult tsetse flies (Glossina spp.) house three symbiotic bacteria that are vertically transmitted from mother to offspring during this insect's unique viviparous mode of reproduction. Larval tsetse that undergo intrauterine development in the absence of their obligate mutualist, Wigglesworthia, exhibit a compromised immune system during adulthood. In this study, we characterize the immune phenotype of tsetse that develop in the absence of all of their endogenous symbiotic microbes. Aposymbiotic tsetse (Glossina morsitans morsitans [Gmm(Apo)]) present a severely compromised immune system that is characterized by the absence of phagocytic hemocytes and atypical expression of immunity-related genes. Correspondingly, these flies quickly succumb to infection with normally nonpathogenic Escherichia coli. The susceptible phenotype exhibited by Gmm(Apo) adults can be reversed when they receive hemocytes transplanted from wild-type donor flies prior to infection. Furthermore, the process of immune system development can be restored in intrauterine Gmm(Apo) larvae when their mothers are fed a diet supplemented with Wigglesworthia cell extracts. Our finding that molecular components of Wigglesworthia exhibit immunostimulatory activity within tsetse is representative of a novel evolutionary adaptation that steadfastly links an obligate symbiont with its host.

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    • "In the absence of Wigglesworthia, vitamin supplementation of the blood meal can partially restore host fertility (Nogge, 1976, 1982). The presence of Wigglesworthia is necessary during the larval stages for proper immune development (Weiss et al., 2011, 2012). The presence of larval microbiota also contributes to the development of the adult peritrophic matrix (a structure that separates epithelial cells from the lumen content), which regulates immune induction following the trypanosome challenge to the fly (Weiss et al., 2013). "
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    ABSTRACT: Tsetse flies (Glossina sp.) that transmit trypanosomes causing human (and animal) African trypanosomiasis (HAT and AAT, respectively) harbor symbiotic microorganisms, including the obligate primary symbiont Wigglesworthia glossinidia. A relationship between Wigglesworthia and tsetse fly infection by trypanosomes has been suggested, as removal of the symbiont results in a higher susceptibility to midgut infection in adult flies. To investigate this relationship and to decipher the role of W. glossinidia in the fly's susceptibility to trypanosome infection, we challenged flies with trypanosomes and subsequently analyzed and compared the transcriptomes of W. glossinidia from susceptible and refractory tsetse flies at three time points (3, 10, and 20 days). More than 200 W. glossinidia genes were found to be differentially expressed between susceptible and refractory flies. The high specificity of these differentially expressed genes makes it possible to distinguish Wigglesworthia inhabiting these two distinct groups of flies. Furthermore, gene expression patterns were observed to evolve during the infection time course, such that very few differentially expressed genes were found in common in Wigglesworthia from the 3-, 10- and 20-day post-feeding fly samples. The overall results clearly demonstrate that the taking up of trypanosomes by flies, regardless of whether flies proceed with the developmental program of Trypanosoma brucei gambiense, strongly alters gene expression in Wigglesworthia. These results therefore provide a novel framework for studies that aim to decrease or even abolish tsetse fly vector competence.
    Frontiers in Microbiology 11/2014; DOI:10.3389/fmicb.2014.00620 · 3.99 Impact Factor
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    • "This 'two-way street' forms the basis of the observed mutualism which can play an important role in the host organism's environmental interactions. Invertebrate examples of this mutualism include cellulose and xylan digestive processes in wood-feeding termites (Warnecke et al., 2007), collagenolytic activity in Osedax boneworms (Goffredi et al., 2007), and immune system potentiation in Drosophila (Teixeira et al., 2008) and tsetse flies (Weiss et al., 2012). The location of such symbionts varies, including as organ-associated species [e.g. "
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    ABSTRACT: Earthworms are globally distributed and perform essential roles for soil health and microbial structure. We have investigated the effect of an anthropogenic contamination gradient on the bacterial community of the keystone ecological species Lumbricus rubellus through utilising 16S rRNA pyrosequencing for the first time to establish the microbiome of the host and surrounding soil.The earthworm-associated microbiome differs from the surrounding environment which appears to be a result of both filtering and stimulation likely linked to the altered environment associated with the gut micro-habitat (neutral pH, anoxia and increased carbon substrates). We identified a core earthworm community comprising Proteobacteria (∼50%) and Actinobacteria (∼30%), with lower abundances of Bacteroidetes (∼6%) and Acidobacteria (∼3%). In addition to the known earthworm symbiont (Verminephrobacter sp.) we identified a potential host-associated Gammaproteobacteria species (Serratia sp.) which was absent from soil yet observed in most earthworms.Although a distinct bacterial community defines these earthworms, clear family- and species-level modification were observed along an arsenic and iron contamination gradient. Several taxa observed in uncontaminated control microbiomes are suppressed by metal/metalloid field exposure, including eradication of the hereto ubiquitously associated Verminephrobacter symbiont, which raises implications to its functional role in the earthworm microbiome.
    Environmental Microbiology 11/2014; 17(6). DOI:10.1111/1462-2920.12712 · 6.20 Impact Factor
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    • "More specifically, when flies undergo intrauterine larval development in the absence of this bacterium they present a severely compromised immune system during adulthood. Under these conditions, Wigglesworthia-free tsetse are unusually susceptible to infection with normally non-pathogenic E. coli K12 and trypanosomes (Wang et al., 2009; Weiss et al., 2011, 2012, 2013). "
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    ABSTRACT: Tsetse flies are the primary vectors of African trypanosomes, which cause Human and Animal African trypanosomiasis in 36 countries in sub-Saharan Africa. These flies have also established symbiotic associations with bacterial and viral microorganisms. Laboratory-reared tsetse flies harbor up to four vertically transmitted organisms-obligate Wigglesworthia, commensal Sodalis, parasitic Wolbachia and Salivary Gland Hypertrophy Virus (SGHV). Field-captured tsetse can harbor these symbionts as well as environmentally acquired commensal bacteria. This microbial community influences several aspects of tsetse's physiology, including nutrition, fecundity and vector competence. This review provides a detailed description of tsetse's microbiome, and describes the physiology underlying host-microbe, and microbe-microbe, interactions that occur in this fly.
    Frontiers in Cellular and Infection Microbiology 10/2013; 3:69. DOI:10.3389/fcimb.2013.00069 · 3.72 Impact Factor
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