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Activated entomopathogenic nematode infective juveniles release lethal venom proteins

Entomopathogenic nematodes (EPNs) are unique parasites due to their symbiosis with entomopathogenic bacteria and their ability to kill insect hosts quickly after infection. It is widely believed that EPNs rely on their bacterial partners for killing hosts. Here we disproved this theory by demonstrat...

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Autores principales: Lu, Dihong, Macchietto, Marissa, Chang, Dennis, Barros, Mirayana M., Baldwin, James, Mortazavi, Ali, Dillman, Adler R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5398726/
https://www.ncbi.nlm.nih.gov/pubmed/28426766
http://dx.doi.org/10.1371/journal.ppat.1006302
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author Lu, Dihong
Macchietto, Marissa
Chang, Dennis
Barros, Mirayana M.
Baldwin, James
Mortazavi, Ali
Dillman, Adler R.
author_facet Lu, Dihong
Macchietto, Marissa
Chang, Dennis
Barros, Mirayana M.
Baldwin, James
Mortazavi, Ali
Dillman, Adler R.
author_sort Lu, Dihong
collection PubMed
description Entomopathogenic nematodes (EPNs) are unique parasites due to their symbiosis with entomopathogenic bacteria and their ability to kill insect hosts quickly after infection. It is widely believed that EPNs rely on their bacterial partners for killing hosts. Here we disproved this theory by demonstrating that the in vitro activated infective juveniles (IJs) of Steinernema carpocapsae (a well-studied EPN species) release venom proteins that are lethal to several insects including Drosophila melanogaster. We confirmed that the in vitro activation is a good approximation of the in vivo process by comparing the transcriptomes of individual in vitro and in vivo activated IJs. We further analyzed the transcriptomes of non-activated and activated IJs and revealed a dramatic shift in gene expression during IJ activation. We also analyzed the venom proteome using mass spectrometry. Among the 472 venom proteins, proteases and protease inhibitors are especially abundant, and toxin-related proteins such as Shk domain-containing proteins and fatty acid- and retinol-binding proteins are also detected, which are potential candidates for suppressing the host immune system. Many of the venom proteins have conserved orthologs in vertebrate-parasitic nematodes and are differentially expressed during IJ activation, suggesting conserved functions in nematode parasitism. In summary, our findings strongly support a new model that S. carpocapsae and likely other Steinernema EPNs have a more active role in contributing to the pathogenicity of the nematode-bacterium complex than simply relying on their symbiotic bacteria. Furthermore, we propose that EPNs are a good model system for investigating vertebrate- and human-parasitic nematodes, especially regarding the function of excretory/secretory products.
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spelling pubmed-53987262017-05-04 Activated entomopathogenic nematode infective juveniles release lethal venom proteins Lu, Dihong Macchietto, Marissa Chang, Dennis Barros, Mirayana M. Baldwin, James Mortazavi, Ali Dillman, Adler R. PLoS Pathog Research Article Entomopathogenic nematodes (EPNs) are unique parasites due to their symbiosis with entomopathogenic bacteria and their ability to kill insect hosts quickly after infection. It is widely believed that EPNs rely on their bacterial partners for killing hosts. Here we disproved this theory by demonstrating that the in vitro activated infective juveniles (IJs) of Steinernema carpocapsae (a well-studied EPN species) release venom proteins that are lethal to several insects including Drosophila melanogaster. We confirmed that the in vitro activation is a good approximation of the in vivo process by comparing the transcriptomes of individual in vitro and in vivo activated IJs. We further analyzed the transcriptomes of non-activated and activated IJs and revealed a dramatic shift in gene expression during IJ activation. We also analyzed the venom proteome using mass spectrometry. Among the 472 venom proteins, proteases and protease inhibitors are especially abundant, and toxin-related proteins such as Shk domain-containing proteins and fatty acid- and retinol-binding proteins are also detected, which are potential candidates for suppressing the host immune system. Many of the venom proteins have conserved orthologs in vertebrate-parasitic nematodes and are differentially expressed during IJ activation, suggesting conserved functions in nematode parasitism. In summary, our findings strongly support a new model that S. carpocapsae and likely other Steinernema EPNs have a more active role in contributing to the pathogenicity of the nematode-bacterium complex than simply relying on their symbiotic bacteria. Furthermore, we propose that EPNs are a good model system for investigating vertebrate- and human-parasitic nematodes, especially regarding the function of excretory/secretory products. Public Library of Science 2017-04-20 /pmc/articles/PMC5398726/ /pubmed/28426766 http://dx.doi.org/10.1371/journal.ppat.1006302 Text en © 2017 Lu et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Lu, Dihong
Macchietto, Marissa
Chang, Dennis
Barros, Mirayana M.
Baldwin, James
Mortazavi, Ali
Dillman, Adler R.
Activated entomopathogenic nematode infective juveniles release lethal venom proteins
title Activated entomopathogenic nematode infective juveniles release lethal venom proteins
title_full Activated entomopathogenic nematode infective juveniles release lethal venom proteins
title_fullStr Activated entomopathogenic nematode infective juveniles release lethal venom proteins
title_full_unstemmed Activated entomopathogenic nematode infective juveniles release lethal venom proteins
title_short Activated entomopathogenic nematode infective juveniles release lethal venom proteins
title_sort activated entomopathogenic nematode infective juveniles release lethal venom proteins
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5398726/
https://www.ncbi.nlm.nih.gov/pubmed/28426766
http://dx.doi.org/10.1371/journal.ppat.1006302
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