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Comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility

BACKGROUND: The nematode Pristionchus pacificus has been established as a model for comparative studies using the well known Caenorhabditis elegans as a reference. Despite their relatedness, previous studies have revealed highly divergent development and a number of morphological differences includi...

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Autores principales: Lightfoot, James W., Chauhan, Veeren M., Aylott, Jonathan W., Rödelsperger, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4779222/
https://www.ncbi.nlm.nih.gov/pubmed/26944260
http://dx.doi.org/10.1186/s13104-016-1886-9
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author Lightfoot, James W.
Chauhan, Veeren M.
Aylott, Jonathan W.
Rödelsperger, Christian
author_facet Lightfoot, James W.
Chauhan, Veeren M.
Aylott, Jonathan W.
Rödelsperger, Christian
author_sort Lightfoot, James W.
collection PubMed
description BACKGROUND: The nematode Pristionchus pacificus has been established as a model for comparative studies using the well known Caenorhabditis elegans as a reference. Despite their relatedness, previous studies have revealed highly divergent development and a number of morphological differences including the lack of a pharyngal structure, the grinder, used to physically lyse the ingested bacteria in C. elegans. RESULTS: To complement current knowledge about developmental and ecological differences with a better understanding of their feeding modes, we have sequenced the intestinal transcriptomes of both nematodes. In total, we found 464 intestine-enriched genes in P. pacificus and 724 in C. elegans, of which the majority (66 %) has been identified by previous studies. Interestingly, only 15 genes could be identified with shared intestinal enrichment in both species, of which three genes are Hedgehog signaling molecules supporting a highly conserved role of this pathway for intestinal development across all metazoa. At the level of gene families, we find similar divergent trends with only five families displaying significant intestinal enrichment in both species. We compared our data with transcriptomic responses to various pathogens. Strikingly, C. elegans intestine-enriched genes showed highly significant overlaps with pathogen response genes whereas this was not the case for P. pacificus, indicating shifts in pathogen susceptibility that might be explained by altered feeding modes. CONCLUSIONS: Our study reveals first insights into the evolution of feeding systems and the associated changes in intestinal gene expression that might have facilitated nematodes of the P. pacificus lineage to colonize new environments. These findings deepen our understanding about how morphological and genomic diversity is created during the course of evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13104-016-1886-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-47792222016-03-06 Comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility Lightfoot, James W. Chauhan, Veeren M. Aylott, Jonathan W. Rödelsperger, Christian BMC Res Notes Research Article BACKGROUND: The nematode Pristionchus pacificus has been established as a model for comparative studies using the well known Caenorhabditis elegans as a reference. Despite their relatedness, previous studies have revealed highly divergent development and a number of morphological differences including the lack of a pharyngal structure, the grinder, used to physically lyse the ingested bacteria in C. elegans. RESULTS: To complement current knowledge about developmental and ecological differences with a better understanding of their feeding modes, we have sequenced the intestinal transcriptomes of both nematodes. In total, we found 464 intestine-enriched genes in P. pacificus and 724 in C. elegans, of which the majority (66 %) has been identified by previous studies. Interestingly, only 15 genes could be identified with shared intestinal enrichment in both species, of which three genes are Hedgehog signaling molecules supporting a highly conserved role of this pathway for intestinal development across all metazoa. At the level of gene families, we find similar divergent trends with only five families displaying significant intestinal enrichment in both species. We compared our data with transcriptomic responses to various pathogens. Strikingly, C. elegans intestine-enriched genes showed highly significant overlaps with pathogen response genes whereas this was not the case for P. pacificus, indicating shifts in pathogen susceptibility that might be explained by altered feeding modes. CONCLUSIONS: Our study reveals first insights into the evolution of feeding systems and the associated changes in intestinal gene expression that might have facilitated nematodes of the P. pacificus lineage to colonize new environments. These findings deepen our understanding about how morphological and genomic diversity is created during the course of evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13104-016-1886-9) contains supplementary material, which is available to authorized users. BioMed Central 2016-03-05 /pmc/articles/PMC4779222/ /pubmed/26944260 http://dx.doi.org/10.1186/s13104-016-1886-9 Text en © Lightfoot et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Lightfoot, James W.
Chauhan, Veeren M.
Aylott, Jonathan W.
Rödelsperger, Christian
Comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility
title Comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility
title_full Comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility
title_fullStr Comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility
title_full_unstemmed Comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility
title_short Comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility
title_sort comparative transcriptomics of the nematode gut identifies global shifts in feeding mode and pathogen susceptibility
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4779222/
https://www.ncbi.nlm.nih.gov/pubmed/26944260
http://dx.doi.org/10.1186/s13104-016-1886-9
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