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Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing

BACKGROUND: Defence mechanisms of organisms are shaped by their lifestyle, environment and pathogen pressure. Carpenter ants are social insects which live in huge colonies comprising genetically closely related individuals in high densities within nests. This lifestyle potentially facilitates the ra...

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Autores principales: Gupta, Shishir K., Kupper, Maria, Ratzka, Carolin, Feldhaar, Heike, Vilcinskas, Andreas, Gross, Roy, Dandekar, Thomas, Förster, Frank
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4508827/
https://www.ncbi.nlm.nih.gov/pubmed/26198742
http://dx.doi.org/10.1186/s12864-015-1748-1
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author Gupta, Shishir K.
Kupper, Maria
Ratzka, Carolin
Feldhaar, Heike
Vilcinskas, Andreas
Gross, Roy
Dandekar, Thomas
Förster, Frank
author_facet Gupta, Shishir K.
Kupper, Maria
Ratzka, Carolin
Feldhaar, Heike
Vilcinskas, Andreas
Gross, Roy
Dandekar, Thomas
Förster, Frank
author_sort Gupta, Shishir K.
collection PubMed
description BACKGROUND: Defence mechanisms of organisms are shaped by their lifestyle, environment and pathogen pressure. Carpenter ants are social insects which live in huge colonies comprising genetically closely related individuals in high densities within nests. This lifestyle potentially facilitates the rapid spread of pathogens between individuals. In concert with their innate immune system, social insects may apply external immune defences to manipulate the microbial community among individuals and within nests. Additionally, carpenter ants carry a mutualistic intracellular and obligate endosymbiotic bacterium, possibly maintained and regulated by the innate immune system. Thus, different selective forces could shape internal immune defences of Camponotus floridanus. RESULTS: The immune gene repertoire of C. floridanus was investigated by re-evaluating its genome sequence combined with a full transcriptome analysis of immune challenged and control animals using Illumina sequencing. The genome was re-annotated by mapping transcriptome reads and masking repeats. A total of 978 protein sequences were characterised further by annotating functional domains, leading to a change in their original annotation regarding function and domain composition in about 8 % of all proteins. Based on homology analysis with key components of major immune pathways of insects, the C. floridanus immune-related genes were compared to those of Drosophila melanogaster, Apis mellifera, and other hymenoptera. This analysis revealed that overall the immune system of carpenter ants comprises many components found in these insects. In addition, several C. floridanus specific genes of yet unknown functions but which are strongly induced after immune challenge were discovered. In contrast to solitary insects like Drosophila or the hymenopteran Nasonia vitripennis, the number of genes encoding pattern recognition receptors specific for bacterial peptidoglycan (PGN) and a variety of known antimicrobial peptide (AMP) genes is lower in C. floridanus. The comparative analysis of gene expression post immune-challenge in different developmental stages of C. floridanus suggests a stronger induction of immune gene expression in larvae in comparison to adults. CONCLUSIONS: The comparison of the immune system of C. floridanus with that of other insects revealed the presence of a broad immune repertoire. However, the relatively low number of PGN recognition proteins and AMPs, the identification of Camponotus specific putative immune genes, and stage specific differences in immune gene regulation reflects Camponotus specific evolution including adaptations to its lifestyle. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1748-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-45088272015-07-22 Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing Gupta, Shishir K. Kupper, Maria Ratzka, Carolin Feldhaar, Heike Vilcinskas, Andreas Gross, Roy Dandekar, Thomas Förster, Frank BMC Genomics Research Article BACKGROUND: Defence mechanisms of organisms are shaped by their lifestyle, environment and pathogen pressure. Carpenter ants are social insects which live in huge colonies comprising genetically closely related individuals in high densities within nests. This lifestyle potentially facilitates the rapid spread of pathogens between individuals. In concert with their innate immune system, social insects may apply external immune defences to manipulate the microbial community among individuals and within nests. Additionally, carpenter ants carry a mutualistic intracellular and obligate endosymbiotic bacterium, possibly maintained and regulated by the innate immune system. Thus, different selective forces could shape internal immune defences of Camponotus floridanus. RESULTS: The immune gene repertoire of C. floridanus was investigated by re-evaluating its genome sequence combined with a full transcriptome analysis of immune challenged and control animals using Illumina sequencing. The genome was re-annotated by mapping transcriptome reads and masking repeats. A total of 978 protein sequences were characterised further by annotating functional domains, leading to a change in their original annotation regarding function and domain composition in about 8 % of all proteins. Based on homology analysis with key components of major immune pathways of insects, the C. floridanus immune-related genes were compared to those of Drosophila melanogaster, Apis mellifera, and other hymenoptera. This analysis revealed that overall the immune system of carpenter ants comprises many components found in these insects. In addition, several C. floridanus specific genes of yet unknown functions but which are strongly induced after immune challenge were discovered. In contrast to solitary insects like Drosophila or the hymenopteran Nasonia vitripennis, the number of genes encoding pattern recognition receptors specific for bacterial peptidoglycan (PGN) and a variety of known antimicrobial peptide (AMP) genes is lower in C. floridanus. The comparative analysis of gene expression post immune-challenge in different developmental stages of C. floridanus suggests a stronger induction of immune gene expression in larvae in comparison to adults. CONCLUSIONS: The comparison of the immune system of C. floridanus with that of other insects revealed the presence of a broad immune repertoire. However, the relatively low number of PGN recognition proteins and AMPs, the identification of Camponotus specific putative immune genes, and stage specific differences in immune gene regulation reflects Camponotus specific evolution including adaptations to its lifestyle. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1748-1) contains supplementary material, which is available to authorized users. BioMed Central 2015-07-22 /pmc/articles/PMC4508827/ /pubmed/26198742 http://dx.doi.org/10.1186/s12864-015-1748-1 Text en © Gupta 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
Gupta, Shishir K.
Kupper, Maria
Ratzka, Carolin
Feldhaar, Heike
Vilcinskas, Andreas
Gross, Roy
Dandekar, Thomas
Förster, Frank
Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing
title Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing
title_full Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing
title_fullStr Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing
title_full_unstemmed Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing
title_short Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing
title_sort scrutinizing the immune defence inventory of camponotus floridanus applying total transcriptome sequencing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4508827/
https://www.ncbi.nlm.nih.gov/pubmed/26198742
http://dx.doi.org/10.1186/s12864-015-1748-1
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