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Understanding the Evolutionary Structural Variability Schwarz et al. BMC Evolutionary Biology 2014, 14:4 http://www.biomedcentral.com/1471-2148/14/4 RESEARCH ARTICLE Open Access Understanding the evolutionary structural variability and target specificity of tick salivary Kunitz peptides using next generation transcriptome data Alexandra Schwarz, Alejandro Cabezas-Cruz, Jan Kopecký and James J Valdés* Abstract 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. Keywords: Red Queen hypothesis, Tick saliva, Kunitz-domain proteins, Cysteine motif, Structural bioinformatics, Antigenicity, Protein disorder, Molecular clock, Evolution Background encephalitis, and, thus greatly impact human and animal Ticks have been successful as ectoparasites due to mor- health [2]. To combat host defense mechanisms, ticks phological and physiological adaptations [1]. As obligate possess powerful pharmacological proteins in their saliva hematophagous (blood-sucking) arthropods, ticks trans- that are injected into the vertebrate host during blood mit various bacterial and viral diseases, e.g., babesiosis, feeding [3,4]. Our current understanding of host-parasite theileriosis, anaplasmosis, Lyme disease and tick-borne interactions has been greatly impacted by the revolution in sequencing technologies that has provided a massive amount of data previously unimaginable [5]. Among the * Correspondence: [email protected] Institute of Parasitology, Biology Centre of the Academy of Sciences of the various transcriptome studies to date, transcriptome Czech Republic, 37005 České Budějovice, Czech Republic © 2014 Schwarz et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Schwarz et al. BMC Evolutionary Biology 2014, 14:4 Page 2 of 16 http://www.biomedcentral.com/1471-2148/14/4 projects from arthropod disease vectors are using Sanger possibly related to the tick’s necessity for prolonged feed- or next generation sequencing techniques. These include ing on the vertebrate host [23]. The authors are aware of several salivary gland (SG) transcriptome and proteome only one study that functionally and structurally character- projects (also known as sialomes) from hard tick [6-18] ized a tick Kunitz peptide as an ion channel effector, the and soft tick species [19-22]. Hundreds of novel SG maxiK channel modulator Ra-KLP from R. appendiculatus transcripts that putatively encode proteins were discov- [40]. This paucity must be remedied since Dai et al. [23] ered from these sialome projects, thus elucidating how putatively characterize the majority of I. scapularis Kunitz ticks may complete a blood meal while providing insight peptides as ion channel blockers/modulators. Further- towards their evolutionary expansion [23]. more, Fry et al. [41] have argued that hematophagous se- Available SG transcriptomes show that the most fre- creted proteins, such as of the Kunitz family, should be quently secreted tick salivary protein families are lipoca- classified as venomous. Most classified toxins are stabi- lins, enzymes, and protease inhibitors. Among protease lized by their disulfide bridges and once these toxins be- inhibitors, Kunitz-domain transcripts are one of the most come functionally essential as a venom, their adaptation is abundant protein families in tick SGs [9,18,19,21]. The oftenreinforcedbygeneduplication[41].Genesharing archetypal Kunitz fold is highly conserved, resembling the and gene duplication are the main mechanisms advocated first Kunitz-domain protein, the bovine pancreatic trypsin to explain the functional heterogeneity of tick salivary inhibitor (BPTI) that was functionally described in 1936 Kunitz family proteins [23,42]. by Moses Kunitz [24]. To date, about 15 single Kunitz- In our study, we used computational, structural bio- domain peptides from ticks have been functionally charac- informatics and phylogenetic methods to reevaluate tick terized. Classical serine protease inhibitors were analyzed salivary Kunitz peptides from a more in-depth structural from the hard ticks Rhipicephalus microplus (BMCL) [25], point of view by analyzing the functional, antigenic, and Rhipicephalus appendiculatus (TdPI) [26], Rhipicephalus evolutionary characteristics of Kunitz peptides from the haemaphysaloides (Rhipilin-1) [27],Haemaphysalislongicor- recently annotated Ixodes ricinus SG transcriptome [18]; nis (HlChl, HIMKI and Haemangin) [28-30], Amblyomma GenBank Bioproject PRJNA177622. Compared to clas- cajennense (Amblyomin-X) [31], and Ixodes scapularis sical biochemical analyses and classical Sanger sequen- (Tryptogalinin) [32]. Protease inhibitors were also character- cing techniques that revealed only a few thousands of ized from the soft ticks Ornithodoros moubata (TAP) [33] sequences from tick transcriptome studies presented and Ornithodoros savignyi (FXaI) that mainly function as until today (with the exception of the A. maculatum anti-clotting agents. Anti-platelet inhibitors were also identi- transcriptome), the large amount of available data of the fied as single Kunitz-domain inhibitors, such as the Mono- 454 pyrosequencing/Illumina I. ricinus SG transcriptome grins (1A and 1B) from Argas monolakensis [34], and, their makes it feasible to thoroughly analyze multigenic pro- orthologs Disagregin [35] and Savignygrin from Ornitho- tein families (i.e., the Kunitz-domain family). In the I. doros spp. [36]. Several tick salivary Kunitz-domain proteins ricinus transcriptome, 4% of all Illumina reads were that possess multiple domains (1–7 Kunitz-domains) were classified as transcripts encoding for Kunitz-domain pro- also characterized as serine protease inhibitors [37-39]. Of teins and of these, 1.4% accounted for single Kunitz- all the tick SGs Kunitz-domain proteins, however, single domain transcripts (that putatively encode archetypal Kunitz-domain peptides are highly represented (we will refer Kunitz peptides possessing more or less 6 Cys residues) to these single domains as Kunitz peptides, henceforth) [18]. Our approach demonstrates how to interpret next [9,12]. These Kunitz peptides vary in their cysteine (Cys) generation transcriptome data to expand our under- motifs (possessing more or less than 6 Cys residues) with standing of the molecular, structural and functional evo- some lacking the archetypal disulfide bonds causing a more lution of hematophagy in ticks. Our overall analysis flexible fold, therefore diversifying their inhibitory activity developed a novel concept that elucidates the divergence [26,32,40]. and adaptation of I. ricinus salivary Kunitz peptides that Kunitz SG peptides of I. scapularis were phylogenetically we call target-oriented evolution. analyzed to uncover their emergence in ticks and the expression trends of these Kunitz peptides were also sta- Results and discussion tistically analyzed [23]. These Kunitz peptides were cate- Organizing the different I. ricinus SG Kunitz peptides based gorized in three different groups (groups I, II and III) on their Cys motifs facilitates functional predictions based on their Cys motif. The I. scapularis Kunitz peptides From the 454/Illumina SG I. ricinus transcriptome [18], belonging to group I were suggested to represent the an- we found archetypal Kunitz peptides containing 6 Cys res-
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