Trends in Symbiont-Induced Host Cellular Differentiation

Russell, Shelbi L.; Castillo, Jennie Ruelas

doi:10.1007/978-3-030-51849-3_5

Cited by 7 publications

(4 citation statements)

References 208 publications

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“…In the case of our lab generated mutant, it is possible that when bam is not fully functional that reproduction is more sensitive to manipulation by W. pipientis . W. pipientis have been documented to respond to changes in the host environment, as W. pipientis gene expression is affected by host age and sex, and as W. pipientis transmission requires functional oogenesis, it reasonable to hypothesize that W. pipientis is sensitive to changes in gametogenesis ( Rice et al 2017 ; Newton and Sheehan 2018 ; Russell et al 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Diverse wMel variants of Wolbachia pipientis differentially rescue fertility and cytological defects of the bag of marbles partial loss of function mutation in Drosophila melanogaster

Bubnell

Fernandez-Begne

Ulbing

et al. 2021

G3 Genes|Genomes|Genetics

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In Drosophila melanogaster, the maternally inherited endosymbiont Wolbachia pipientis interacts with germline stem cell genes during oogenesis. One such gene, bag of marbles (bam) is the key switch for differentiation and also shows signals of adaptive evolution for protein diversification. These observations have led us to hypothesize that W. pipientis could be driving the adaptive evolution of bam for control of oogenesis. To test this hypothesis, we must understand the specificity of the genetic interaction between bam and W. pipientis. Previously, we documented that the W. pipientis variant, wMel, rescued the fertility of the bamBW hypomorphic mutant as a transheterozygote over a bam null. However, bamBW was generated more than 20 years ago in an uncontrolled genetic background and maintained over a balancer chromosome. Consequently, the chromosome carrying bamBW accumulated mutations that have prevented controlled experiments to further assess the interaction. Here, we used CRISPR/Cas9 to engineer the same single amino acid bam hypomorphic mutation (bamL255F ) and a new bam null disruption mutation into the w1118 isogenic background. We assess the fertility of wildtype bam, bamL255F/bamnull hypomorphic, and bamL255F/bamL255F mutant females, each infected individually with ten W. pipientis wMel variants representing three phylogenetic clades. Overall, we find that all of the W. pipientis variants tested here rescue bam hypomorphic fertility defects with wMelCS-like variants exhibiting the strongest rescue effects. Additionally, these variants did not increase wildtype bam female fertility. Therefore, both bam and W. pipientis interact in genotype-specific ways to modulate female fertility, a critical fitness phenotype.

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Section: Discussionmentioning

confidence: 99%

Diverse wMel variants of Wolbachia pipientis differentially rescue fertility and cytological defects of the bag of marbles partial loss of function mutation in Drosophila melanogaster

Bubnell

Fernandez-Begne

Ulbing

et al. 2021

G3 Genes|Genomes|Genetics

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“…While some symbiotic microbes have adapted to the insect immune system in order to remain in symbiosis with their insect hosts (Russell and Castillo, 2020;Ganesan et al, 2022), many insects have resorted to confining their mutualists to specialized symbiotic organs (bacteriomes) or cells (bacteriocytes) for protection (Douglas, 2020). Conditions within these specialized organs are generally favorable for symbionts (Ferrarini et al, 2022), but hosts can still regulate the microbial populations within these tissues (Kim et al, 2013;Whittle et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Differential gene expression in the insect vector Anasa tristis in response to symbiont colonization but not infection with a vectored phytopathogen

Mendiola,

Chen,

Lukubye

et al. 2024

Front. Ecol. Evol.

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Many insects selectively associate with specific microbes in long-term, symbiotic relationships. Maintaining these associations can be vital for the insect hosts’ development, but insects must also contend with potential coinfections from other microbes in the environment. Fending off microbial threats while maintaining mutualistic microbes has resulted in many insects developing specialized symbiotic organs to house beneficial microbes. Though locally concentrated in these organs, symbiont establishment can have global consequences for the insect, including influence over the success of coinfecting microbes in colonizing the insect host. We use a transcriptomic approach to examine how the mutualistic symbiosis between the agricultural pest Anasa tristis and bacteria in the genus Caballeronia affects insect gene expression locally within the symbiotic organs and in the insect host at large. We simultaneously determine whether Caballeronia colonization impacts insect host responses to infection with the plant pathogen Serratia marcescens, which it vectors to plants. We found that no significant differential gene expression was elicited by infection with S. marcescens. This was a surprising finding given previous work indicating that symbiotic A. tristis clear S. marcescens infection rapidly compared to aposymbiotic individuals. Our results indicate that symbiotic and nonsymbiotic tissues in A. tristis differ greatly in their gene expression, particularly following successful symbiont colonization. We found evidence for local downregulation of host immunity and upregulation of cell communication within the symbiotic organs, functions which can facilitate the success of the A. tristis-Caballeronia symbiosis.

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“…Wolbachia strains have strong affinities for host germline tissues [ 26 , 27 ], positioning them at the right place to manipulate and enhance host fertility. In the strains that form obligate associations with Brugia filarial nematodes [ 28 ] and Asobara wasps [ 29 ], Wolbachia is required in the germline to prevent premature differentiation and achieve successful oogenesis (reviewed in [ 30 ]). In the facultative w Mel- D .…”

Section: Introductionmentioning

confidence: 99%

Wolbachia endosymbionts manipulate the self-renewal and differentiation of germline stem cells to reinforce fertility of their fruit fly host

Russell,

Castillo,

Sullivan

2023

PLoS Biol

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The alphaproteobacterium Wolbachia pipientis infects arthropod and nematode species worldwide, making it a key target for host biological control. Wolbachia-driven host reproductive manipulations, such as cytoplasmic incompatibility (CI), are credited for catapulting these intracellular bacteria to high frequencies in host populations. Positive, perhaps mutualistic, reproductive manipulations also increase infection frequencies, but are not well understood. Here, we identify molecular and cellular mechanisms by which Wolbachia influences the molecularly distinct processes of germline stem cell (GSC) self-renewal and differentiation. We demonstrate that wMel infection rescues the fertility of flies lacking the translational regulator mei-P26 and is sufficient to sustain infertile homozygous mei-P26-knockdown stocks indefinitely. Cytology revealed that wMel mitigates the impact of mei-P26 loss through restoring proper pMad, Bam, Sxl, and Orb expression. In Oregon R files with wild-type fertility, wMel infection elevates lifetime egg hatch rates. Exploring these phenotypes through dual-RNAseq quantification of eukaryotic and bacterial transcripts revealed that wMel infection rescues and offsets many gene expression changes induced by mei-P26 loss at the mRNA level. Overall, we show that wMel infection beneficially reinforces host fertility at mRNA, protein, and phenotypic levels, and these mechanisms may promote the emergence of mutualism and the breakdown of host reproductive manipulations.

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Trends in Symbiont-Induced Host Cellular Differentiation

Cited by 7 publications

References 208 publications

Diverse wMel variants of Wolbachia pipientis differentially rescue fertility and cytological defects of the bag of marbles partial loss of function mutation in Drosophila melanogaster

Diverse wMel variants of Wolbachia pipientis differentially rescue fertility and cytological defects of the bag of marbles partial loss of function mutation in Drosophila melanogaster

Differential gene expression in the insect vector Anasa tristis in response to symbiont colonization but not infection with a vectored phytopathogen

Wolbachia endosymbionts manipulate the self-renewal and differentiation of germline stem cells to reinforce fertility of their fruit fly host

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