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

Gupta SK, Kupper M, Ratzka C, Feldhaar H, Vilcinskas A, Gross R, Dandekar T, Förster F - BMC Genomics (2015)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioinformatics, Biocentre, University of Würzburg, Am Hubland, D-97074, Würzburg, Germany. shishir.bioinfo@gmail.com.

ABSTRACT

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.

No MeSH data available.


Related in: MedlinePlus

Comparison of insect proteomes. Specific numbers of shared orthologous clusters are indicated (black numbers) comparing the proteomes of 11 insect species (eight ant species (blue) as well as A. mellifera, N. vitripennis (green) and D. melanogaster (red)
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Fig10: Comparison of insect proteomes. Specific numbers of shared orthologous clusters are indicated (black numbers) comparing the proteomes of 11 insect species (eight ant species (blue) as well as A. mellifera, N. vitripennis (green) and D. melanogaster (red)

Mentions: Orthologous clusters were identified using OrthoMCL analysis on the proteomes of 11 insect species (Additional file 14: Table S11). OrthoMCL clustering included the eight ant species as well as A. mellifera, N. vitripennis and D. melanogaster. These proteomes clustered into 18,763 groups from 188,092 protein sequences. All eight ant species cluster into 6620 ortholog groups (Fig. 10; details in Additional file 15: Table S12). Looking at the species distribution we found that 4818 groups were shared by all the species analysed, while 5797 groups were shared by all hymenopterans. 79 groups represent genes that are conserved exclusively among the eight ant species (Additional file 16: Table S13). We further parsed the 18,763 groups with perl scripts to reveal the presence of orthologs of C. floridanus immune proteins in selected species. Table S14 (Additional file 17) lists the identified immune proteins of C. floridanus and their orthologs, if present in the other sequenced ants, A. mellifera and N. vitripennis. Nine differentially regulated genes encoding putative immune-related proteins of C. floridanus do not have any homologs in other insects. KOG annotations of these proteins, listed in Table S15 (Additional file 18), reveal features of some of these proteins including the presence of signal peptides, a chemosensory domain and a DNA-binding domain. Additionally, in a recent study Hamilton and co-workers reported Cathepsin D as a protein that contributes to social immunity in Camponotus pennsylvanicus [12]. C. floridanus also encodes an ortholog of Cathepsin D (Cflo_N_g9172t1) and it will be interesting to investigate a general role of this protein in social immunity in the future.Fig. 10


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

Gupta SK, Kupper M, Ratzka C, Feldhaar H, Vilcinskas A, Gross R, Dandekar T, Förster F - BMC Genomics (2015)

Comparison of insect proteomes. Specific numbers of shared orthologous clusters are indicated (black numbers) comparing the proteomes of 11 insect species (eight ant species (blue) as well as A. mellifera, N. vitripennis (green) and D. melanogaster (red)
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4508827&req=5

Fig10: Comparison of insect proteomes. Specific numbers of shared orthologous clusters are indicated (black numbers) comparing the proteomes of 11 insect species (eight ant species (blue) as well as A. mellifera, N. vitripennis (green) and D. melanogaster (red)
Mentions: Orthologous clusters were identified using OrthoMCL analysis on the proteomes of 11 insect species (Additional file 14: Table S11). OrthoMCL clustering included the eight ant species as well as A. mellifera, N. vitripennis and D. melanogaster. These proteomes clustered into 18,763 groups from 188,092 protein sequences. All eight ant species cluster into 6620 ortholog groups (Fig. 10; details in Additional file 15: Table S12). Looking at the species distribution we found that 4818 groups were shared by all the species analysed, while 5797 groups were shared by all hymenopterans. 79 groups represent genes that are conserved exclusively among the eight ant species (Additional file 16: Table S13). We further parsed the 18,763 groups with perl scripts to reveal the presence of orthologs of C. floridanus immune proteins in selected species. Table S14 (Additional file 17) lists the identified immune proteins of C. floridanus and their orthologs, if present in the other sequenced ants, A. mellifera and N. vitripennis. Nine differentially regulated genes encoding putative immune-related proteins of C. floridanus do not have any homologs in other insects. KOG annotations of these proteins, listed in Table S15 (Additional file 18), reveal features of some of these proteins including the presence of signal peptides, a chemosensory domain and a DNA-binding domain. Additionally, in a recent study Hamilton and co-workers reported Cathepsin D as a protein that contributes to social immunity in Camponotus pennsylvanicus [12]. C. floridanus also encodes an ortholog of Cathepsin D (Cflo_N_g9172t1) and it will be interesting to investigate a general role of this protein in social immunity in the future.Fig. 10

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioinformatics, Biocentre, University of Würzburg, Am Hubland, D-97074, Würzburg, Germany. shishir.bioinfo@gmail.com.

ABSTRACT

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.

No MeSH data available.


Related in: MedlinePlus