Wbm0076, a candidate effector protein of the Wolbachia endosymbiont of Brugia malayi, disrupts eukaryotic actin dynamics

Mills, Michael K.; McCabe, Lindsey G; Rodrigue, Eugenie M; Lechtreck, Karl‐Ferdinand; Starai, Vincent J.

doi:10.1371/journal.ppat.1010777

Cited by 9 publications

(4 citation statements)

References 89 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In silkworm cell cultures, Wolbachia infection did not alter gene expression or induce or suppress immune responses, while Cardinium infection induced immune-related genes, including antimicrobial peptides, pattern recognition receptors, and a serine protease [104]. Additionally, the outer membrane protein of Wolbachia interacts with host actin and tubulin to disrupt endosomal tra cking [101,105].…”

Section: Discussionmentioning

confidence: 97%

The Cardinium wins on Wolbachia in double-infected mite cultures

Tresnakova,

Glowska,

Hubert

2024

Preprint

View full text Add to dashboard Cite

The different cultures of stored product mite Tyrophagus putrescentiae are single-infected by intracellular bacteria Cardinium or Wolbachia. No natural double-infected Cardinium/Wolbachia-infected mites are known. Under the experiment, single-infected mite (Wolbachia 5N, 5P and Cardinium 5L, 5S) cultures were mixed to double-infected cultures (5LP, 5LN, 5SP, 5SN). The mite fitness and symbionts' presence were analyzed during 5-month-long experiment. Cardinium, Wolbachia and mite genomes were assembled and gene expression in single and double-infected cultures was analyzed. In double-infected cultures, Cardinium infection increased with the time of the experiment from 50 to 95% of infected mites. Cardinium + Wolbachia-infected mite individuals proportion ranged from 0 to 20% of mites in double-infected cultures. Wolbachia infection disappeared in all double-infected cultures up to 5 months of the experiment duration. The double-infected cultures had lower fitness than single-infected cultures. After a month of experiment, the fitness of originally double-infected cultures increased to the level of parental cultures. The correlation analyses of gene expression showed that Wolbachia had well-established interactions with mite predicted KEGG gene expression in a single-infected population. The expression of mite protein was strongly influenced by the presence of Wolbachia, but not by Cardinium. The total numbers of Cardinium-expressed genes did not change, while there was a ten-fold decrease in Wolbachia in double-infected cultures. Cardinium and Wolbachia gene expression showed 30% negative and 70% positive (N = 3793) correlations. The number of correlations between Wolbachia and mite gene expression 5 times decreased in double-infected cultures. The Cardinium had a 6-fold higher number of genes than Wolbachia with significantly higher expression in the multiple infected samples. The gene expression analysis provides a suggestion that the presence of Cardinium inhibits the growth of Wolbachia by the disruption of the Wolbachia interaction with mite host. However, we cannot eliminate stochastic processes resulting in the increase of Wolbachia abundance and symbiont change. Importance We sought insight into the intracellular symbionts’ competition in the novel mite host model. The manipulative experiments established double-infected Wolbachia Cardinium cultures, which were unstable due to their low fitness. Cardinium prevailed during five months in all 4 double-infected cultures. The competition disrupted Wolbachia's interaction with its host on the level of gene expression. The genome expression is highly correlated between Wolbachia and mite hosts in single Wolbachia-infected cultures. These correlations disappeared in multi-infected cultures. Differently, the interaction among host and Cardinium genes showed low differences in the gene expression level. Although Cardinium/Wolbachia-infested individuals are rare, the gene expression of Cardinium and Wolbachia had a high number of positive correlations. It indicates that the symbionts reacted to each other. The data indicates that we have established a new model to study Wolbachia and Cardinium interactions.

show abstract

Section: Discussionmentioning

confidence: 97%

The Cardinium wins on Wolbachia in double-infected mite cultures

Tresnakova,

Glowska,

Hubert

2024

Preprint

View full text Add to dashboard Cite

show abstract

“…Many bacterial pathogens deploy effectors that alter host endocytosis and vesicle trafficking, as these cellular processes are important for signaling, interactions with the extracellular environment, and metabolism. Indeed, the Wolbachia strain that colonizes filarial nematodes ( w Bm) encodes a protein that when overexpressed in yeast, decouples actin patches from sites of endocytosis (wBm0076, [ 36 ]), and it is likely that multiple Wolbachia strains use similar strategies for host interaction. By altering host endocytosis and vesicle trafficking, pathogens can avoid phago-lysozome fusion, as Mycobacterium tuberculosis does using EsxH [ 37 ], or even induce uptake of the microbe, as is the case for Helicobacter pylori’s CagA [ 38 ].…”

Section: Discussionmentioning

confidence: 99%

The Wolbachia WalE1 effector alters Drosophila endocytosis

Martin,

López-Madrigal,

Newton

2024

PLoS Pathog

View full text Add to dashboard Cite

The most common intracellular bacterial infection is Wolbachia pipientis, a microbe that manipulates host reproduction and is used in control of insect vectors. Phenotypes induced by Wolbachia have been studied for decades and range from sperm-egg incompatibility to male killing. How Wolbachia alters host biology is less well understood. Previously, we characterized the first Wolbachia effector–WalE1, which encodes an alpha-synuclein domain at the N terminus. Purified WalE1 sediments with and bundles actin and when heterologously expressed in flies, increases Wolbachia titer in the developing oocyte. In this work, we first identify the native expression of WalE1 by Wolbachia infecting both fly cells and whole animals. WalE1 appears as aggregates in the host cell cytosol. We next show that WalE1 co-immunoprecipitates with the host protein Past1, although might not directly interact with it, and that WalE1 manipulates host endocytosis. Yeast expressing WalE1 show deficiency in uptake of FM4-64 dye, and flies harboring mutations in Past1 or overexpressing WalE1 are sensitive to AgNO3, a hallmark of endocytosis defects. We also show that flies expressing WalE1 suffer from endocytosis defects in larval nephrocytes. Finally, we also show that Past1 null flies harbor more Wolbachia overall and in late egg chambers. Our results identify interactions between Wolbachia and a host protein involved in endocytosis and point to yet another important host cell process impinged upon by Wolbachia’s WalE1 effector.

show abstract

“…The deoxyribonucleic acid (DNA) sequencing data revealed that W. bancrofti and B. malayi , which are the primary species for lymphatic filariasis, were found to include an internal bacterium that resembled Wolbachia [ 24 ]. Furthermore, these lymphatic filarial nematodes were found to be infected with Wolbachia [ 25 ]. All stages of the life cycle of filarial worms are infected with this bacteria, but the severity of infections differs between different stages of the nematodes [ 26 , 27 ].…”

Section: Mutualistic Association Between Wolbachia ...mentioning

confidence: 99%

Wolbachia and Lymphatic Filarial Nematodes and Their Implications in the Pathogenesis of the Disease

Setegn,

Amare,

Mihret

2024

Journal of Parasitology Research

View full text Add to dashboard Cite

Lymphatic filariasis (LF) is an infection of three closely related filarial worms such as Wuchereria bancrofti, Brugia malayi, and Brugia timori. These worms can cause a devastating disease that involves acute and chronic lymphoedema of the extremities, which can cause elephantiasis in both sexes and hydroceles in males. These important public health nematodes were found to have a mutualistic relationship with intracellular bacteria of the genus Wolbachia, which is essential for the development and survival of the nematode. The host’s inflammatory response to parasites and possibly also to the Wolbachia endosymbiont is the cause of lymphatic damage and disease pathogenesis. This review tried to describe and highlight the mutualistic associations between Wolbachia and lymphatic filarial nematodes and the role of bacteria in the pathogenesis of lymphatic filariasis. Articles for this review were searched from PubMed, Google Scholar, and other databases. Article searching was not restricted by publication year; however, only English version full-text articles were included.

show abstract

Wbm0076, a candidate effector protein of the Wolbachia endosymbiont of Brugia malayi, disrupts eukaryotic actin dynamics

Cited by 9 publications

References 89 publications

The Cardinium wins on Wolbachia in double-infected mite cultures

The Cardinium wins on Wolbachia in double-infected mite cultures

The Wolbachia WalE1 effector alters Drosophila endocytosis

Wolbachia and Lymphatic Filarial Nematodes and Their Implications in the Pathogenesis of the Disease

Contact Info

Product

Resources

About