Universität zu Köln

Nakad, Rania, Snoek, L. Basten, Yang, Wentao, Ellendt, Sunna, Schneider, Franziska, Mohr, Timm G., Roesingh, Lone, Masche, Anna C., Rosenstiel, Philip C., Dierking, Katja ORCID: 0000-0002-5129-346X, Kammenga, Jan E. and Schulenburg, Hinrich (2016). Contrasting invertebrate immune defense behaviors caused by a single gene, the Caenorhabditis elegans neuropeptide receptor gene npr-1. BMC Genomics, 17. LONDON: BMC. ISSN 1471-2164

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Abstract

Background: The invertebrate immune system comprises physiological mechanisms, physical barriers and also behavioral responses. It is generally related to the vertebrate innate immune system and widely believed to provide nonspecific defense against pathogens, whereby the response to different pathogen types is usually mediated by distinct signalling cascades. Recent work suggests that invertebrate immune defense can be more specific at least at the phenotypic level. The underlying genetic mechanisms are as yet poorly understood. Results: We demonstrate in the model invertebrate Caenorhabditis elegans that a single gene, a homolog of the mammalian neuropeptide Y receptor gene, npr-1, mediates contrasting defense phenotypes towards two distinct pathogens, the Gram-positive Bacillus thuringiensis and the Gram-negative Pseudomonas aeruginosa. Our findings are based on combining quantitative trait loci (QTLs) analysis with functional genetic analysis and RNAseq-based transcriptomics. The QTL analysis focused on behavioral immune defense against B. thuringiensis, using recombinant inbred lines (RILs) and introgression lines (ILs). It revealed several defense QTLs, including one on chromosome X comprising the npr-1 gene. The wildtype N2 allele for the latter QTL was associated with reduced defense against B. thuringiensis and thus produced an opposite phenotype to that previously reported for the N2 npr-1 allele against P. aeruginosa. Analysis of npr-1 mutants confirmed these contrasting immune phenotypes for both avoidance behavior and nematode survival. Subsequent transcriptional profiling of C. elegans wildtype and npr-1 mutant suggested that npr-1 mediates defense against both pathogens through p38 MAPK signaling, insulin-like signaling, and C-type lectins. Importantly, increased defense towards P. aeruginosa seems to be additionally influenced through the induction of oxidative stress genes and activation of GATA transcription factors, while the repression of oxidative stress genes combined with activation of Ebox transcription factors appears to enhance susceptibility to B. thuringiensis. Conclusions: Our findings highlight the role of a single gene, npr-1, in fine-tuning nematode immune defense, showing the ability of the invertebrate immune system to produce highly specialized and potentially opposing immune responses via single regulatory genes.

Item Type:	Journal Article
Creators:	Creators Email ORCID ORCID Put Code Nakad, Rania UNSPECIFIED UNSPECIFIED UNSPECIFIED Snoek, L. Basten UNSPECIFIED UNSPECIFIED UNSPECIFIED Yang, Wentao UNSPECIFIED UNSPECIFIED UNSPECIFIED Ellendt, Sunna UNSPECIFIED UNSPECIFIED UNSPECIFIED Schneider, Franziska UNSPECIFIED UNSPECIFIED UNSPECIFIED Mohr, Timm G. UNSPECIFIED UNSPECIFIED UNSPECIFIED Roesingh, Lone UNSPECIFIED UNSPECIFIED UNSPECIFIED Masche, Anna C. UNSPECIFIED UNSPECIFIED UNSPECIFIED Rosenstiel, Philip C. UNSPECIFIED UNSPECIFIED UNSPECIFIED Dierking, Katja UNSPECIFIED orcid.org/0000-0002-5129-346X UNSPECIFIED Kammenga, Jan E. UNSPECIFIED UNSPECIFIED UNSPECIFIED Schulenburg, Hinrich UNSPECIFIED UNSPECIFIED UNSPECIFIED
URN:	urn:nbn:de:hbz:38-278752
DOI:	10.1186/s12864-016-2603-8
Journal or Publication Title:	BMC Genomics
Volume:	17
Date:	2016
Publisher:	BMC
Place of Publication:	LONDON
ISSN:	1471-2164
Language:	English
Faculty:	Unspecified
Divisions:	Unspecified
Subjects:	no entry
Uncontrolled Keywords:	Keywords Language PATHOGENIC BACILLUS-THURINGIENSIS; C. ELEGANS; NATURAL VARIATION; INNATE IMMUNITY; SERRATIA-MARCESCENS; EXPERIMENTAL COEVOLUTION; TRANSCRIPTION FACTOR; OXIDATIVE STRESS; LIFE-SPAN; EXPRESSION Multiple languages Biotechnology & Applied Microbiology; Genetics & Heredity Multiple languages
Refereed:	Yes
URI:	http://kups.ub.uni-koeln.de/id/eprint/27875