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

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 mo...

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Autores principales: Grover, Manish, Fasseas, Michael K., Essmann, Clara, Liu, Kenneth, Braendle, Christian, Félix, Marie-Anne, Glockling, Sally L., Barkoulas, Michalis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8552708/
https://www.ncbi.nlm.nih.gov/pubmed/34722333
http://dx.doi.org/10.3389/fcimb.2021.733094
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author Grover, Manish
Fasseas, Michael K.
Essmann, Clara
Liu, Kenneth
Braendle, Christian
Félix, Marie-Anne
Glockling, Sally L.
Barkoulas, Michalis
author_facet Grover, Manish
Fasseas, Michael K.
Essmann, Clara
Liu, Kenneth
Braendle, Christian
Félix, Marie-Anne
Glockling, Sally L.
Barkoulas, Michalis
author_sort Grover, Manish
collection PubMed
description 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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spelling pubmed-85527082021-10-29 Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection Grover, Manish Fasseas, Michael K. Essmann, Clara Liu, Kenneth Braendle, Christian Félix, Marie-Anne Glockling, Sally L. Barkoulas, Michalis Front Cell Infect Microbiol Cellular and Infection Microbiology 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. Frontiers Media S.A. 2021-10-14 /pmc/articles/PMC8552708/ /pubmed/34722333 http://dx.doi.org/10.3389/fcimb.2021.733094 Text en Copyright © 2021 Grover, Fasseas, Essmann, Liu, Braendle, Félix, Glockling and Barkoulas https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Grover, Manish
Fasseas, Michael K.
Essmann, Clara
Liu, Kenneth
Braendle, Christian
Félix, Marie-Anne
Glockling, Sally L.
Barkoulas, Michalis
Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection
title Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection
title_full Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection
title_fullStr Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection
title_full_unstemmed Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection
title_short Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection
title_sort infection of c. elegans by haptoglossa species reveals shared features in the host response to oomycete detection
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8552708/
https://www.ncbi.nlm.nih.gov/pubmed/34722333
http://dx.doi.org/10.3389/fcimb.2021.733094
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