Abstract
BackgroundDefence 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.ResultsThe 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.ConclusionsThe 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 materialThe online version of this article (doi:10.1186/s12864-015-1748-1) contains supplementary material, which is available to authorized users.
Highlights
Defence mechanisms of organisms are shaped by their lifestyle, environment and pathogen pressure
The optimised parameters with 80.8 % exon level accuracy allowed the improvement of annotation of the C. floridanus genome
Additional receptor proteins and Jak-Stat signalling pathway Besides the above mentioned pattern recognition receptors (PRRs), we identified proteins known to be involved in pathogen recognition and/or promotion of phagocytosis including scavenger receptors, croquemort family members, nimrod and draper orthologs, vitellogenin, galectins, c-type lectins, brain angiogenesis inhibitor 1 (BAI1), fibrinogen-related protein, down syndrome cell adhesion molecular (Dscam) and thioester containing proteins (TEPs)
Summary
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. As a second line of defence a powerful antimicrobial immune response is mounted, mainly based on AMPs and including serine proteases, stress factors and factors involved in opsonisation and clotting [3, 4]. Based on several structural features, the AMPs can be classified into several groups such as α-helical peptides, glycine-rich peptides, cysteine-rich peptides or prolinerich peptides [5]
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