Asymmetric Wolbachia Segregation during Early Brugia malayi Embryogenesis Determines Its Distribution in Adult Host Tissues

Landmann, Frédéric; Foster, Jeremy M.; Slatko, Barton E.; Sullivan, William

doi:10.1371/journal.pntd.0000758

Cited by 88 publications

(127 citation statements)

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“…Since Nuc has a signal peptide, it could be involved in the recycling of nucleotides in the host germline to facilitate symbiont cell division. Taken together, the repertoire of genes displaying elevated expression in the gonad is fully consistent with the current understanding of Wolbachia biology in filarial nematodes, as wBm divides rapidly during the mitotic proliferation of host oogoniae, and this precedes fertilization of the mature oocytes (Landmann et al 2010).…”

Section: Differential Expression Analysis Supports Limited Regulationsupporting

confidence: 76%

“…In adults of B. malayi, O. volvulus, and Onchocerca ochengi (a parasite of cattle representing the closest relative of O. volvulus) (Trees 1992;Morales-Hojas et al 2006), Wolbachia are found both in the somatic hypodermal cords that run along the length of the worms and in the germinal zones of the female gonad, where they are transmitted into the oocytes and maintained throughout larval development. However, they are completely absent from the reproductive system of adult males (Landmann et al 2010).…”

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confidence: 99%

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Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

et al. 2012

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The a-proteobacterium Wolbachia is probably the most prevalent, vertically transmitted symbiont on Earth. In contrast with its wide distribution in arthropods, Wolbachia is restricted to one family of animal-parasitic nematodes, the Onchocercidae. This includes filarial pathogens such as Onchocerca volvulus, the cause of human onchocerciasis, or river blindness. The symbiosis between filariae and Wolbachia is obligate, although the basis of this dependency is not fully understood. Previous studies suggested that Wolbachia may provision metabolites (e.g., haem, riboflavin, and nucleotides) and/or contribute to immune defense. Importantly, Wolbachia is restricted to somatic tissues in adult male worms, whereas females also harbor bacteria in the germline. We sought to characterize the nature of the symbiosis between Wolbachia and O. ochengi, a bovine parasite representing the closest relative of O. volvulus. First, we sequenced the complete genome of Wolbachia strain wOo, which revealed an inability to synthesize riboflavin de novo. Using RNA-seq, we also generated endobacterial transcriptomes from male soma and female germline. In the soma, transcripts for membrane transport and respiration were up-regulated, while the gonad exhibited enrichment for DNA replication and translation. The most abundant Wolbachia proteins, as determined by geLC-MS, included ligands for mammalian Toll-like receptors. Enzymes involved in nucleotide synthesis were dominant among metabolism-related proteins, whereas the haem biosynthetic pathway was poorly represented. We conclude that Wolbachia may have a mitochondrion-like function in the soma, generating ATP for its host. Moreover, the abundance of immunogenic proteins in wOo suggests a role in diverting the immune system toward an ineffective antibacterial response.

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Section: Differential Expression Analysis Supports Limited Regulationsupporting

confidence: 76%

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confidence: 99%

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

et al. 2012

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“…2C), and for Wolbachia-infected nematodes (15). Wolbachia imaging in other insect tissues by Syto-11 is also possible, such as Drosophila brain (1) (Fig.…”

Section: Resultsmentioning

confidence: 99%

Rapid Fluorescence-Based Screening for Wolbachia Endosymbionts in Drosophila Germ Line and Somatic Tissues

Casper-Lindley

Kimura

Saxton

et al. 2011

Appl Environ Microbiol

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Wolbachia is a globally distributed bacterial endosymbiont present in arthropods and nematodes. The advent of sensitive PCR-based approaches has greatly facilitated the identification of Wolbachia-infected individuals and analysis of population infection levels. Here, a complementary visual fluorescence-based Wolbachia screening approach is described. Through the use of the fluorescent dye Syto-11, Wolbachia can be efficiently detected in various Drosophila tissues, including ovaries. Syto-11 also stains Wolbachia in other insects. Because Wolbachia is inherited through the maternal germ line, bacteria reside in the ovaries of flies in infected populations. An advantage of this staining approach is that it informs about Wolbachia titer as well as its tissue and cellular distribution. Using this method, the infection status of insect populations in two central California locations was determined, and variants with unusually low or high Wolbachia titers were isolated. In addition, a variant with ovarioles containing both infected and uninfected egg chambers was identified. Syto-11 staining of Cardinium-and Spiroplasma-infected insects was also analyzed.Wolbachia species are obligate intracellular, bacterial endosymbionts present in over 60% of all insect species (10). Manipulation of host reproduction and efficient maternal transmission have facilitated the global spread of Wolbachia in arthropods. Under optimal laboratory conditions, Wolbachia transmission in Drosophila melanogaster (11) and Drosophila simulans (10a) is 100%, but infection rates in the field can be highly variable with location, season, and host species (10a, 11). In addition, different Wolbachia strains that have various effects on host reproduction and fecundity seem to exist in single collection sites (24). Determining the Wolbachia status quickly and reliably is important for ecological work, as well as for biochemical and genetics studies of host-pathogen interaction. It has been estimated that 30% of the strains in the Bloomington Stock Center are Wolbachia infected (4). Because Wolbachia is present in a number of somatic tissues (6), including the adult brain (1, 17), an infection may influence fly behavior and metabolism (12,14,18), thus having implications for the larger Drosophila research community.The infection status of fly stocks is commonly determined by PCR (2, 11a, 18), which involves a 3-step process to first prepare the DNA, followed by the actual PCR step and gel electrophoreses (19,25). The PCR method is efficient, especially when many samples are analyzed. However, the infection status of some species has been underestimated with conventional PCR and was revealed only after "long PCR" involving 2 polymerase enzymes (13). On the other hand, too-sensitive PCR conditions may produce false positives. Standard PCR methods do not reveal the degree of Wolbachia infection, tissue of origin, and variations in Wolbachia localization or titers in the host. To complement the PCR detection, a quick method to visualize Wolbachia in live i...

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“…However, Wolbachia are often found in several somatic tissues as well, and this distribution varies among different Wolbachia-host associations (7)(8)(9)(10)(11). The role of these bacteria in somatic cells is not clear.…”

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confidence: 99%

Evolutionarily conserved Wolbachia -encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection

Toomey

Panaram²,

Fast³

et al. 2013

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

110

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Wolbachia are intracellular bacteria that infect invertebrates at pandemic levels, including insect vectors of devastating infectious diseases. Although Wolbachia are providing novel strategies for the control of several human pathogens, the processes underlying Wolbachia's successful propagation within and across species remain elusive. Wolbachia are mainly vertically transmitted; however, there is also evidence of extensive horizontal transmission. Here, we provide several lines of evidence supporting Wolbachia's targeting of ovarian stem cell niches-referred to as "niche tropism"-as a previously overlooked strategy for Wolbachia thriving in nature. Niche tropism is pervasive in Wolbachia infecting the Drosophila genus, and different patterns of niche tropism are evolutionarily conserved. Phylogenetic analysis, confirmed by hybrid introgression and transinfection experiments, demonstrates that bacterial factors are the major determinants of differential patterns of niche tropism. Furthermore, bacterial load is increased in germ-line cells passing through infected niches, supporting previous suggestions of a contribution of Wolbachia from stem-cell niches toward vertical transmission. These results support the role of stem-cell niches as a key component for the spreading of Wolbachia in the Drosophila genus and provide mechanistic insights into this unique tissue tropism.endosymbiont | maternal transmission | microbial tissue tropism | germline stem cell niche | somatic stem cell niche

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Asymmetric Wolbachia Segregation during Early Brugia malayi Embryogenesis Determines Its Distribution in Adult Host Tissues

Cited by 88 publications

References 58 publications

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

Rapid Fluorescence-Based Screening for Wolbachia Endosymbionts in Drosophila Germ Line and Somatic Tissues

Evolutionarily conserved Wolbachia -encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection

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