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Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq

BACKGROUND: Drosophila melanogaster activates a variety of immune responses against microbial infections. However, information on the Drosophila immune response to entomopathogenic nematode infections is currently limited. The nematode Heterorhabditis bacteriophora is an insect parasite that forms a...

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Autores principales: Castillo, Julio C., Creasy, Todd, Kumari, Priti, Shetty, Amol, Shokal, Upasana, Tallon, Luke J., Eleftherianos, Ioannis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4499211/
https://www.ncbi.nlm.nih.gov/pubmed/26162375
http://dx.doi.org/10.1186/s12864-015-1690-2
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author Castillo, Julio C.
Creasy, Todd
Kumari, Priti
Shetty, Amol
Shokal, Upasana
Tallon, Luke J.
Eleftherianos, Ioannis
author_facet Castillo, Julio C.
Creasy, Todd
Kumari, Priti
Shetty, Amol
Shokal, Upasana
Tallon, Luke J.
Eleftherianos, Ioannis
author_sort Castillo, Julio C.
collection PubMed
description BACKGROUND: Drosophila melanogaster activates a variety of immune responses against microbial infections. However, information on the Drosophila immune response to entomopathogenic nematode infections is currently limited. The nematode Heterorhabditis bacteriophora is an insect parasite that forms a mutualistic relationship with the gram-negative bacteria Photorhabdus luminescens. Following infection, the nematodes release the bacteria that quickly multiply within the insect and produce several toxins that eventually kill the host. Although we currently know that the insect immune system interacts with Photorhabdus, information on interaction with the nematode vector is scarce. RESULTS: Here we have used next generation RNA-sequencing to analyze the transcriptional profile of wild-type adult flies infected by axenic Heterorhabditis nematodes (lacking Photorhabdus bacteria), symbiotic Heterorhabditis nematodes (carrying Photorhabdus bacteria), and Photorhabdus bacteria alone. We have obtained approximately 54 million reads from the different infection treatments. Bioinformatic analysis shows that infection with Photorhabdus alters the transcription of a large number of Drosophila genes involved in translational repression as well in response to stress. However, Heterorhabditis infection alters the transcription of several genes that participate in lipidhomeostasis and metabolism, stress responses, DNA/protein sythesis and neuronal functions. We have also identified genes in the fly with potential roles in nematode recognition, anti-nematode activity and nociception. CONCLUSIONS: These findings provide fundamental information on the molecular events that take place in Drosophila upon infection with the two pathogens, either separately or together. Such large-scale transcriptomic analyses set the stage for future functional studies aimed at identifying the exact role of key factors in the Drosophila immune response against nematode-bacteria complexes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1690-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-44992112015-07-12 Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq Castillo, Julio C. Creasy, Todd Kumari, Priti Shetty, Amol Shokal, Upasana Tallon, Luke J. Eleftherianos, Ioannis BMC Genomics Research Article BACKGROUND: Drosophila melanogaster activates a variety of immune responses against microbial infections. However, information on the Drosophila immune response to entomopathogenic nematode infections is currently limited. The nematode Heterorhabditis bacteriophora is an insect parasite that forms a mutualistic relationship with the gram-negative bacteria Photorhabdus luminescens. Following infection, the nematodes release the bacteria that quickly multiply within the insect and produce several toxins that eventually kill the host. Although we currently know that the insect immune system interacts with Photorhabdus, information on interaction with the nematode vector is scarce. RESULTS: Here we have used next generation RNA-sequencing to analyze the transcriptional profile of wild-type adult flies infected by axenic Heterorhabditis nematodes (lacking Photorhabdus bacteria), symbiotic Heterorhabditis nematodes (carrying Photorhabdus bacteria), and Photorhabdus bacteria alone. We have obtained approximately 54 million reads from the different infection treatments. Bioinformatic analysis shows that infection with Photorhabdus alters the transcription of a large number of Drosophila genes involved in translational repression as well in response to stress. However, Heterorhabditis infection alters the transcription of several genes that participate in lipidhomeostasis and metabolism, stress responses, DNA/protein sythesis and neuronal functions. We have also identified genes in the fly with potential roles in nematode recognition, anti-nematode activity and nociception. CONCLUSIONS: These findings provide fundamental information on the molecular events that take place in Drosophila upon infection with the two pathogens, either separately or together. Such large-scale transcriptomic analyses set the stage for future functional studies aimed at identifying the exact role of key factors in the Drosophila immune response against nematode-bacteria complexes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1690-2) contains supplementary material, which is available to authorized users. BioMed Central 2015-07-11 /pmc/articles/PMC4499211/ /pubmed/26162375 http://dx.doi.org/10.1186/s12864-015-1690-2 Text en © Castillo et al. 2015 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 work is properly credited. 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
Castillo, Julio C.
Creasy, Todd
Kumari, Priti
Shetty, Amol
Shokal, Upasana
Tallon, Luke J.
Eleftherianos, Ioannis
Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq
title Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq
title_full Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq
title_fullStr Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq
title_full_unstemmed Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq
title_short Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq
title_sort drosophila anti-nematode and antibacterial immune regulators revealed by rna-seq
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4499211/
https://www.ncbi.nlm.nih.gov/pubmed/26162375
http://dx.doi.org/10.1186/s12864-015-1690-2
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