Feminizing Wolbachia: a transcriptomics approach with insights on the immune response genes in Armadillidium vulgare

Chevalier, Frédéric D.; Herbinière-Gaboreau, Juline; Charif, Delphine; Mitta, Guillaume; Gavory, Frédérick; Wincker, Patrick; Grève, Pierre; Braquart‐Varnier, Christine; Bouchon, Didier

doi:10.1186/1471-2180-12-s1-s1

Cited by 49 publications

(47 citation statements)

References 84 publications

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“…In the isopod atg7 and atg12 were underexpressed in infected ovaries, and autophagy genes were down-regulated in the wasp association, suggesting widespread regulation of autophagy by Wolbachia is required for bacterial survival (25,26). Autophagy is not the only host-defense mechanism that can be activated by Wolbachia.…”

Section: Discussionmentioning

confidence: 99%

Autophagy regulates Wolbachia populations across diverse symbiotic associations

Voronin

Cook

Steven

et al. 2012

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

110

117

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Wolbachia are widespread and abundant intracellular symbionts of arthropods and filarial nematodes. Their symbiotic relationships encompass obligate mutualism, commensalism, parasitism, and pathogenicity. A consequence of these diverse associations is that Wolbachia encounter a wide range of host cells and intracellular immune defense mechanisms of invertebrates, which they must evade to maintain their populations and spread to new hosts. Here we show that autophagy, a conserved intracellular defense mechanism and regulator of cell homeostasis, is a major immune recognition and regulatory process that determines the size of Wolbachia populations. The regulation of Wolbachia populations by autophagy occurs across all distinct symbiotic relationships and can be manipulated either chemically or genetically to modulate the Wolbachia population load. The recognition and activation of host autophagy is particularly apparent in rapidly replicating strains of Wolbachia found in somatic tissues of Drosophila and filarial nematodes. In filarial nematodes, which host a mutualistic association with Wolbachia, the use of antibiotics such as doxycycline to eliminate Wolbachia has emerged as a promising approach to their treatment and control. Here we show that the activation of host nematode autophagy reduces bacterial loads to the same magnitude as antibiotic therapy; thus we identify a bactericidal mode of action targeting Wolbachia that can be exploited for the development of chemotherapeutic agents against onchocerciasis, lymphatic filariasis, and heartworm.Brugia malayi | innate immunity | chemotherapy | helminth | endosymbiont W olbachia is a widespread and abundant endosymbiotic bacterium of arthropods and filarial nematodes that resides in vacuoles of host germline and somatic cells. Wolbachia show a diverse variety of symbiotic associations with their host, ranging from obligate mutualism in filarial nematodes to commensal, parasitic, or pathogenic associations in insects and other arthropod hosts (1-5).In filarial nematodes Wolbachia is obligatory for normal larval growth and development, embryogenesis, and survival of adult worms (1). Although the molecular basis of this mutualistic relationship remains unknown, a comparison of host and bacterial genomes suggests that intact biosynthetic pathways for haem, nucleotides, riboflavin, and FAD may be among the contributions of the bacteria to the biology of the nematode host (6-8). The biological processes most sensitive to Wolbachia loss include larval growth and development and embryogenesis in adult females. These processes have a high metabolic demand because of the rapid growth, development, and organogenesis of the nematode and are associated with the rapid expansion of Wolbachia populations following larval infection of mammalian hosts and in reproductively active adult females (9). Loss of Wolbachia results in extensive apoptosis of germline and somatic cells of embryos, microfilariae, and fourth-stage (L4) larvae, presumably because of the lack of provision of ...

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Section: Discussionmentioning

confidence: 99%

Autophagy regulates Wolbachia populations across diverse symbiotic associations

Voronin

Cook

Steven

et al. 2012

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

110

117

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“…3; Table 3), suggesting a unique regulation of these defense-related genes in the context of host-symbiont interactions. It should be noted that, recently, a variety of correlations between lysozyme gene expression and symbiont infection have been reported in other symbiotic systems: expression of a c-type lysozyme gene is down-regulated in the ovary of Wolbachia -infected parasitic wasp Asobara tabida [16]; expression of an i-type lysozyme gene is down-regulated in Wolbachia -infected pill bug Armadillidium vulgare [15]; in the grain weevils Sitophilus zeamais and S. oryzae , expression of an i-type lysozyme gene is down-regulated in the bacteriocytes harboring Sodalis -allied symbiotic bacteria endocellularly [10], [11]; and in the pea aphid Acyrthosiphon pisum , strikingly, two i-type lysozyme genes are specifically expressed in the bacteriocytes harboring Buchnera , which represent the most abundant transcripts in the symbiotic cells [8]. Meanwhile, in the Sitophilus weevils, permanent infection of bacteriocytes with Sodalis- allied primary endosymbiont leads to up-regulation of an antimicrobial peptide, coleoptericin-A, whose function is to restrict the endosymbiont infection to the bacteriocytes [47].…”

Section: Discussionmentioning

confidence: 99%

Gene Expression in Gut Symbiotic Organ of Stinkbug Affected by Extracellular Bacterial Symbiont

et al. 2013

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The bean bug Riptortus pedestris possesses a specialized symbiotic organ in a posterior region of the midgut, where numerous crypts harbor extracellular betaproteobacterial symbionts of the genus Burkholderia. Second instar nymphs orally acquire the symbiont from the environment, and the symbiont infection benefits the host by facilitating growth and by occasionally conferring insecticide resistance. Here we performed comparative transcriptomic analyses of insect genes expressed in symbiotic and non-symbiotic regions of the midgut dissected from Burkholderia-infected and uninfected R. pedestris. Expression sequence tag analysis of cDNA libraries and quantitative reverse transcription PCR identified a number of insect genes expressed in symbiosis- or aposymbiosis-associated patterns. For example, genes up-regulated in symbiotic relative to aposymbiotic individuals, including many cysteine-rich secreted protein genes and many cathepsin protease genes, are likely to play a role in regulating the symbiosis. Conversely, genes up-regulated in aposymbiotic relative to symbiotic individuals, including a chicken-type lysozyme gene and a defensin-like protein gene, are possibly involved in regulation of non-symbiotic bacterial infections. Our study presents the first transcriptomic data on gut symbiotic organ of a stinkbug, which provides initial clues to understanding of molecular mechanisms underlying the insect-bacterium gut symbiosis and sheds light on several intriguing commonalities between endocellular and extracellular symbiotic associations.

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“…Armadillidium vulgare/Wolbachia and Sitophilus orizae/SOPE ) [66,67]. Functions such as oxidative stress regulation [8,14] and classical immune pathways [62] have already been highlighted, and appear again as being shared between symbiotic associations.…”

Section: Discussionmentioning

confidence: 99%

Influence of Wolbachia on host gene expression in an obligatory symbiosis

et al. 2012

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BackgroundWolbachia are intracellular bacteria known to be facultative reproductive parasites of numerous arthropod hosts. Apart from these reproductive manipulations, recent findings indicate that Wolbachia may also modify the host’s physiology, notably its immune function. In the parasitoid wasp, Asobara tabida, Wolbachia is necessary for oogenesis completion, and aposymbiotic females are unable to produce viable offspring. The absence of egg production is also associated with an increase in programmed cell death in the ovaries of aposymbiotic females, suggesting that a mechanism that ensures the maintenance of Wolbachia in the wasp could also be responsible for this dependence. In order to decipher the general mechanisms underlying host-Wolbachia interactions and the origin of the dependence, we developed transcriptomic approaches to compare gene expression in symbiotic and aposymbiotic individuals.ResultsAs no genetic data were available on A. tabida, we constructed several Expressed Sequence Tags (EST) libraries, and obtained 12,551 unigenes from this species. Gene expression was compared between symbiotic and aposymbiotic ovaries through in silico analysis and in vitro subtraction (SSH). As pleiotropic functions involved in immunity and development could play a major role in the establishment of dependence, the expression of genes involved in oogenesis, programmed cell death (PCD) and immunity (broad sense) was analyzed by quantitative RT-PCR. We showed that Wolbachia might interfere with these numerous biological processes, in particular some related to oxidative stress regulation. We also showed that Wolbachia may interact with immune gene expression to ensure its persistence within the host.ConclusionsThis study allowed us to constitute the first major dataset of the transcriptome of A. tabida, a species that is a model system for both host/Wolbachia and host/parasitoid interactions. More specifically, our results highlighted that symbiont infection may interfere with numerous pivotal processes at the individual level, suggesting that the impact of Wolbachia should also be investigated beyond reproductive manipulations.

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Feminizing Wolbachia: a transcriptomics approach with insights on the immune response genes in Armadillidium vulgare

Cited by 49 publications

References 84 publications

Autophagy regulates Wolbachia populations across diverse symbiotic associations

Autophagy regulates Wolbachia populations across diverse symbiotic associations

Gene Expression in Gut Symbiotic Organ of Stinkbug Affected by Extracellular Bacterial Symbiont

Influence of Wolbachia on host gene expression in an obligatory symbiosis

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