Understanding the evolutionary structural variability and target specificity of tick salivary Kunitz peptides using next generation transcriptome data

BMC Evolutionary Biology

James J Valdés¹  Jan Kopecký¹  Alejandro Cabezas-Cruz¹  Alexandra Schwarz¹ 

[1] Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, 37005 České Budějovice Czech Republic

关键词: Evolution;    Molecular clock;    Protein disorder;    Antigenicity;    Structural bioinformatics;    Cysteine motif;    Kunitz-domain proteins;    Tick saliva;    Red Queen hypothesis;   

Others  :  858137
DOI  :  10.1186/1471-2148-14-4

 received in 2013-06-17, accepted in 2013-12-13,  发布年份 2014

【 摘 要 】

Background

Ticks are blood-sucking arthropods and a primary function of tick salivary proteins is to counteract the host’s immune response. Tick salivary Kunitz-domain proteins perform multiple functions within the feeding lesion and have been classified as venoms; thereby, constituting them as one of the important elements in the arms race with the host. The two main mechanisms advocated to explain the functional heterogeneity of tick salivary Kunitz-domain proteins are gene sharing and gene duplication. Both do not, however, elucidate the evolution of the Kunitz family in ticks from a structural dynamic point of view. The Red Queen hypothesis offers a fruitful theoretical framework to give a dynamic explanation for host-parasite interactions. Using the recent salivary gland Ixodes ricinus transcriptome we analyze, for the first time, single Kunitz-domain encoding transcripts by means of computational, structural bioinformatics and phylogenetic approaches to improve our understanding of the structural evolution of this important multigenic protein family.

Results

Organizing the I. ricinus single Kunitz-domain peptides based on their cysteine motif allowed us to specify a putative target and to relate this target specificity to Illumina transcript reads during tick feeding. We observe that several of these Kunitz peptide groups vary in their translated amino acid sequence, secondary structure, antigenicity, and intrinsic disorder, and that the majority of these groups are subject to a purifying (negative) selection. We finalize by describing the evolution and emergence of these Kunitz peptides. The overall interpretation of our analyses discloses a rapidly emerging Kunitz group with a distinct disulfide bond pattern from the I. ricinus salivary gland transcriptome.

Conclusions

We propose a model to explain the structural and functional evolution of tick salivary Kunitz peptides that we call target-oriented evolution. Our study reveals that combining analytical approaches (transcriptomes, computational, bioinformatics and phylogenetics) improves our understanding of the biological functions of important salivary gland mediators during tick feeding.

【 授权许可】

   
2014 Schwarz et al.; licensee BioMed Central Ltd.

【 图 表 】

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