Chemosensory Neurons Modulate the Response to Oomycete Recognition in Caenorhabditis elegans

Fasseas, Michael K.; Grover, Manish; Drury, Florence; Essmann, Clara L.; Kaulich, Eva; Schafer, William R.; Barkoulas, Michalis

doi:10.1016/j.celrep.2020.108604

Cited by 20 publications

(60 citation statements)

References 62 publications

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“…The gun cells show remarkable diversity in their shape and size and arise from flagellated motile zoospores or nonmotile aplanospores depending on the species (Glockling and Beakes, 2000a;Hakariya et al, 2007). We investigate the host response to Haptoglossa infection and report similarities with what has previously been discovered for M. humicola recognition (Fasseas et al, 2021). We finally reveal that distinct Haptoglossa strains from different geographical locations are all capable of triggering chil-27 gene induction, which highlights a common response associated with oomycete recognition in C. elegans.…”

Section: Introductionmentioning

confidence: 83%

“…CHIL proteins are thought to be catalytically inactive chitinases and may act by modifying the cuticle properties, thereby antagonising infection by limiting pathogen attachment to the host ( Osman et al., 2018 ). Interestingly, chil gene induction is part of a broader oomycete recognition response (ORR) programme, which is likely to be triggered upon neuronal detection of a pathogen-associated molecular pattern that remains currently unknown ( Fasseas et al., 2021 ).…”

Section: Introductionmentioning

confidence: 99%

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Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection

Grover

Fasseas

Essmann

et al. 2021

Front. Cell. Infect. Microbiol.

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Oomycetes are a group of eukaryotic organisms that includes many important pathogens of animals and plants. Within this group, the Haptoglossa genus is characterised by the presence of specialised gun cells carrying a harpoon-like infection apparatus. While several Haptoglossa pathogens have been morphologically described, there are currently no host systems developed to study the infection process or host responses in the lab. In this study, we report that Haptoglossa species are potent natural pathogens of Caenorhabditis nematodes. Using electron microscopy, we characterise the infection process in C. elegans and demonstrate that the oomycete causes excessive tissue degradation upon entry in the body cavity, whilst leaving the host cuticle intact. We also report that the host transcriptional response to Haptoglossa infection shares similarities with the response against the oomycete Myzocytiopsis humicola, a key example of which is the induction of chitinase-like (chil) genes in the hypodermis. We demonstrate that this shared feature of the host response can be mounted by pathogen detection without any infection, as previously shown for M. humicola. These results highlight similarities in the nematode immune response to natural infection by phylogenetically distinct oomycetes.

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Section: Introductionmentioning

confidence: 83%

Section: Introductionmentioning

confidence: 99%

Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection

Grover

Fasseas

Essmann

et al. 2021

Front. Cell. Infect. Microbiol.

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“…S6B, Table S3). Previous studies have shown connections between the IPR and genes induced either by M. humicola infection, or by extract from M. humicola as part of the oomycete recognition response in the epidermis (13, 20, 21).…”

Section: Resultsmentioning

confidence: 99%

“…An R studio package GeneOverlap was used for RNA-seq datasets comparative analyses. Differentially expressed genes from RNA-seq analyses from this study were compared with relevant previously published datasets (11, 13, 15, 24, 25, 34, 70–72). Statistical similarity between datasets was determined using Fisher’s exact test.…”

Section: Methodsmentioning

confidence: 99%

The predicted bZIP transcription factor ZIP-1 promotes resistance to intracellular infection in Caenorhabditis elegans

Lazetic

et al. 2021

Preprint

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Defense against intracellular infection has been extensively studied in vertebrate hosts, but less is known about invertebrate hosts. For example, almost nothing is known about the transcription factors that induce defense against intracellular infection in the model nematode Caenorhabditis elegans. Two types of intracellular pathogens that naturally infect C. elegans are the Orsay virus, which is a positive-sense RNA virus, and microsporidia, which are fungal pathogens. Surprisingly, these molecularly distinct pathogens induce a common host transcriptional response called the Intracellular Pathogen Response (IPR). Here we describe zip-1 as an IPR regulator that functions downstream of all known IPR activating and regulatory pathways. zip-1 encodes a putative bZIP transcription factor of previously unknown function, and we show how zip-1 controls induction of a subset of genes upon IPR activation. ZIP-1 protein is expressed in the nuclei of intestinal cells, and is required in the intestine to upregulate IPR gene expression. Importantly, zip-1 promotes resistance to infection by the Orsay virus and by microsporidia in intestinal cells. Altogether, our results indicate that zip-1 represents a central hub for all triggers of the IPR, and that this transcription factor plays a protective role against intracellular pathogen infection in C. elegans.

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“…Interestingly, the induction of CLPs was observed even upon exposure to an innocuous extract prepared from infected animals with M. humicola [36], so it is more likely to constitute a response to pathogen sensing rather than a response to pathogen-induced host perturbation. In addition, the C. elegans response to M. humicola was found to be modulated by chemosensory neurons, which through currently unknown mechanisms, trigger the induction of CLPs in the epidermis [36]. Pathogen recognition in C. elegans does not use classical innate immune receptors such as Toll-like receptors (TLRs), and the underlying mechanisms remain elusive.…”

Section: Chitinase-like Proteins As Part Of the Host Immune Responsementioning

confidence: 99%

C. elegans as a new tractable host to study infections by animal pathogenic oomycetes

Grover

Barkoulas

2021

PLoS Pathog

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Chemosensory Neurons Modulate the Response to Oomycete Recognition in Caenorhabditis elegans

Cited by 20 publications

References 62 publications

Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection

Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection

The predicted bZIP transcription factor ZIP-1 promotes resistance to intracellular infection in Caenorhabditis elegans

C. elegans as a new tractable host to study infections by animal pathogenic oomycetes

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