Although pathogens are usually transmitted within the first 24-48 h of attachment of the castor bean tick Ixodes ricinus, little is known about the tick's biological responses at these earliest phases of attachment. Tick midgut and salivary glands are the main tissues involved in tick blood feeding and pathogen transmission but the limited genomic information for I. ricinus delays the application of high-throughput methods to study their physiology. We took advantage of the latest advances in the fields of Next Generation RNA-Sequencing and Label-free Quantitative Proteomics to deliver an unprecedented, quantitative description of the gene expression dynamics in the midgut and salivary glands of this disease vector upon attachment to the vertebrate host. A total of 373 of 1510 identified proteins had higher expression in the salivary glands, but only 110 had correspondingly high transcript levels in the same tissue. Furthermore, there was midgut-specific expression of 217 genes at both the transcriptome and proteome level. Tissue-dependent transcript, but not protein, accumulation was revealed for 552 of 885 genes. Moreover, we discovered the enrichment of tick salivary glands in proteins involved in gene transcription and translation, which agrees with the secretory role of this tissue; this finding also agrees with our finding of lower tick t-RNA representation in the salivary glands when compared with the midgut. The midgut, in turn, is enriched in metabolic components and proteins that support its mechanical integrity in order to accommodate and metabolize the ingested blood. Beyond understanding the physiological events that support hematophagy by arthropod ectoparasites, we discovered more than 1500 proteins located at the interface between ticks, the vertebrate host, and the tick-borne pathogens. Thus, our work significantly improves the knowledge of the genetics underlying the transmission lifecycle of this tick species, which is an essential step for developing alternative methods to better control tick-borne diseases.

‖Institute of Medical Biostatistics Epidemiology and Informatics University Medical Center of the Johannes Gutenberg Universität Mainz Mainz 55131 Germany;

§Institute for Immunology University Medical Center of the Johannes Gutenberg Universität Mainz Mainz 55131 Germany;

¶Computational Genomics and Bioinformatics Group Genetics Department University of Granada Granada 18071 Spain;

From the ‡Biology Center Academy of Sciences of Czech Republic Budweis 37005 Czech Republic;

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Schwarz A., von Reumont B. M., Erhart J., Chagas A. C., Ribeiro J. M., Kotsyfakis M. (2013) De novo Ixodes ricinus salivary gland transcriptome analysis using two next-generation sequencing methodologies. Faseb J 27, 4745–4756 PubMed PMC

Chmelar J., Calvo E., Pedra J. H., Francischetti I. M., Kotsyfakis M. (2012) Tick salivary secretion as a source of antihemostatics. J. Proteomics 75, 3842–3854 PubMed PMC

Kazimirova M., Stibraniova I. (2013) Tick salivary compounds: their role in modulation of host defences and pathogen transmission. Front. Cell. Infect. Microbiol. 3, 43. PubMed PMC

Toutoungi L. N., Gern L., Aeschlimann A. (1995) Biology of Ixodes (Pholeoixodes) hexagonus under laboratory conditions. Part II. Effect of mating on feeding and fecundity of females. Exp. Appl. Acarol. 19, 233–245 PubMed

Sojka D., Franta Z., Horn M., Caffrey C. R., Mares. M., Kopacek P. (2013) New insights into the machinery of blood digestion by ticks. Trends Parasitol 29, 276–285 PubMed

Hynote E. D., Mervine P. C., Stricker R. B. (2012) Clinical evidence for rapid transmission of Lyme disease following a tickbite. Diagn. Microbiol. Infect. Dis. 72, 188–192 PubMed

Narasimhan S., Deponte K., Marcantonio N., Liang X., Royce T. E., Nelson K. F., Booth C. J., Koski B., Anderson J. F., Kantor F., Fikrig E. (2007) Immunity against Ixodes scapularis salivary proteins expressed within 24 hours of attachment thwarts tick feeding and impairs Borrelia transmission. PloS One 2, e451. PubMed PMC

McNally K. L., Mitzel D. N., Anderson J. M., Ribeiro J. M., Valenzuela J. G., Myers T. G., Godinez A., Wolfinbarger J. B., Best S. M., Bloom M. E. (2012) Differential salivary gland transcript expression profile in Ixodes scapularis nymphs upon feeding or flavivirus infection. Ticks Tick Borne Dis. 3, 18–26 PubMed PMC

Stutzer C., van Zyl W. A., Olivier N. A., Richards S., Maritz-Olivier C. (2013) Gene expression profiling of adult female tissues in feeding Rhipicephalus microplus cattle ticks. Int. J. Parasitol. 43, 541–554 PubMed

Distler U., Kuharev J., Navarro P., Levin Y., Schild H., Tenzer S. (2014) Drift-time specific collision energies enable deep coverage data-independent acquisition proteomics. Nat. Methods 11, 167–170 PubMed

Green M. R., Sambrook J., MacCalum P. (2012) Molecular Cloning: A Laboratory Manual, 4 Ed., Cold Spring Harbor Laboratory Press

Schwarz A., von Reumont B. M., Erhart J., Chagas A. C., Ribeiro J. M., Kotsyfakis M. (2013) De novo Ixodes ricinus salivary gland transcriptome analysis using two next-generation sequencing methodologies. Faseb J. 27, 4745–4756 PubMed PMC

Birol I., Jackman S. D., Nielsen C. B., Qian J. Q., Varhol R., Stazyk G., Morin R. D., Zhao Y., Hirst M., Schein J. E., Horsman D. E., Connors J. M., Gascoyne R. D., Marra M. A., Jones S. J. (2009) De novo transcriptome assembly with ABySS. Bioinformatics 25, 2872–2877 PubMed

Simpson J. T., Wong K., Jackman S. D., Schein J. E., Jones S. J., Birol I. (2009) ABySS: a parallel assembler for short read sequence data. Genome Res. 19, 1117–1123 PubMed PMC

Yang Y., Smith S. A. (2013) Optimizing de novo assembly of short-read RNA-seq data for phylogenomics. BMC Genomics 14, 328. PubMed PMC

Karim S., Singh P., Ribeiro J. M. (2011) A deep insight into the sialotranscriptome of the Gulf Coast tick, Amblyomma maculatum. PLoS One 6, e28525. PubMed PMC

Chagas A. C., Calvo E., Rios-Velasquez C. M., Pessoa F. A., Medeiros J. F., Ribeiro J. M. (2013) A deep insight into the sialotranscriptome of the mosquito, Psorophora albipes. BMC Genomics 14, 875. PubMed PMC

Wisniewski J. R., Zougman A., Nagaraj N., Mann M. (2009) Universal sample preparation method for proteome analysis. Nat. Methods 6, 359–362 PubMed

Tenzer S., Docter D., Rosfa S., Wlodarski A., Kuharev J., Rekik A., Knauer S. K., Bantz C., Nawroth T., Bier C., Sirirattanapan J., Mann W., Treuel L., Zellner R., Maskos M., Schild H., Stauber R. H. (2011) Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis. ACS Nano 5, 7155–7167 PubMed

Geromanos S. J., Vissers J. P., Silva J. C., Dorschel C. A., Li G. Z., Gorenstein M. V., Bateman R. H., Langridge J. I. (2009) The detection, correlation, and comparison of peptide precursor and product ions from data independent LC-MS with data dependant LC-MS/MS. Proteomics 9, 1683–1695 PubMed

Silva J. C., Denny R., Dorschel C. A., Gorenstein M., Kass I. J., Li G. Z., McKenna T., Nold M. J., Richardson K., Young P., Geromanos S. (2005) Quantitative proteomic analysis by accurate mass retention time pairs. Anal. Chem. 77, 2187–2200 PubMed

Giles K., Pringle S. D., Worthington K. R., Little D., Wildgoose J. L., Bateman R. H. (2004) Applications of a travelling wave-based radio-frequency-only stacked ring ion guide. Rapid Commun. Mass Spectrom. 18, 2401–2414 PubMed

Patzig J., Jahn O., Tenzer S., Wichert S. P., de Monasterio-Schrader P., Rosfa S., Kuharev J., Yan K., Bormuth I., Bremer J., Aguzzi A., Orfaniotou F., Hesse D., Schwab M. H., Mobius W., Nave K. A., Werner H. B. (2011) Quantitative and integrative proteome analysis of peripheral nerve myelin identifies novel myelin proteins and candidate neuropathy loci. J. Neurosci. 31, 16369–16386 PubMed PMC

Bradshaw R. A., Burlingame A. L., Carr S., Aebersold R. (2006) Reporting protein identification data: the next generation of guidelines. Mol. Cell. Proteomics 5, 787–788 PubMed

Hochberg Y., Benjamini Y. (1990) More powerful procedures for multiple significance testing. Stat. Med. 9, 811–818 PubMed

Burkhart J. M., Vaudel M., Gambaryan S., Radau S., Walter U., Martens L., Geiger J., Sickmann A., Zahedi R. P. (2012) The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood 120, e73–e82 PubMed

Florin-Christensen M., Schnittger L. (2009) Piroplasmids and ticks: a long-lasting intimate relationship. Front. Biosci. 14, 3064–3073 PubMed

Stanek G. (2009) [Pandora's Box: pathogens in Ixodes ricinus ticks in Central Europe]. Wien Klin. Wochenschri. 121, 673–683 PubMed

Mansfield K. L., Johnson N., Phipps L. P., Stephenson J. R., Fooks A. R., Solomon T. (2009) Tick-borne encephalitis virus - a review of an emerging zoonosis. J. Gen. Virol. 90, 1781–1794 PubMed

Medlock J. M., Hansford K. M., Bormane A., Derdakova M., Estrada-Pena A., George J. C., Golovljova I., Jaenson T. G., Jensen J. K., Jensen P. M., Kazimirova M., Oteo J. A., Papa A., Pfister K., Plantard O., Randolph S. E., Rizzoli A., Santos-Silva M. M., Sprong H., Vial L., Hendrickx G., Zeller H., Van Bortel W. (2013) Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit. Vectors 6, 1. PubMed PMC

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