BMC Genomics | |
Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis | |
Joachim Kurtz1  Erich Bornberg-Bauer1  Hinrich Schulenburg2  Philip Rosenstiel3  Daniela Esser3  Hendrik Eggert1  Barbara Milutinović1  Robert Peuß1  Sarah Behrens1  | |
[1] Institute for Evolution and Biodiversity, University of Münster, Hüfferstr. 1, 48149 Münster, Germany;Zoological Institute, Christian-Albrechts University Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany;Institute of Clinical Molecular Biology, Christian-Albrechts University Kiel, Schittenhelmstr. 12, 24105 Kiel, Germany | |
关键词: Transcriptome; RNA sequencing; Pricking infection; Oral infection; Host-parasite interactions; Bacillus thuringiensis; Tribolium castaneum; | |
Others : 1216646 DOI : 10.1186/1471-2164-15-445 |
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received in 2014-01-14, accepted in 2014-06-04, 发布年份 2014 | |
【 摘 要 】
Background
Pathogens can infect their hosts through different routes. For studying the consequences for host resistance, we here used the entomopathogen Bacillus thuringiensis and the red flour beetle Tribolium castaneum for oral and systemic (i. e. pricking the cuticle) experimental infection. In order to characterize the molecular mechanisms underpinning the two different infection routes, the transcriptomes of beetles of two different T. castaneum populations – one recently collected population (Cro1) and a commonly used laboratory strain (SB) – were analyzed using a next generation RNA sequencing approach.
Results
The genetically more diverse population Cro1 showed a significantly larger number of differentially expressed genes. While both populations exhibited similar reactions to pricking, their expression patterns in response to oral infection differed remarkably. In particular, the Cro1 population showed a strong response of cuticular proteins and developmental genes, which might indicate an adaptive developmental flexibility that was lost in the SB population presumably as a result of inbreeding. The immune response of SB was primarily based on antimicrobial peptides, while Cro1 relied on responses mediated by phenoloxidase and reactive oxygen species, which may explain the higher resistance of this strain against oral infection.
Conclusions
Our data demonstrate that immunological and physiological processes underpinning the two different routes of infection are clearly distinct, and that host populations particularly differ in responses to oral infection. Furthermore, gene expression upon pricking infection entailed a strong signal of wounding, highlighting the importance of pricking controls in future infection studies.
【 授权许可】
2014 Behrens et al.; licensee BioMed Central Ltd.
【 预 览 】
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20150413051405188.pdf | 484KB | download | |
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【 参考文献 】
- [1]Vizoso DB, Ebert D: Phenotypic plasticity of host-parasite interactions in response to the route of infection. J Evol Biol 2005, 18(4):911-921.
- [2]Leggett HC, Cornwallis CK, West SA: Mechanisms of pathogenesis, infective dose and virulence in human parasites. PLoS Pathog 2012, 8(2):1002512.
- [3]Martins NE, Faria VG, Teixeira L, Magalhaes S, Sucena E: Host adaptation is contingent upon the infection route taken by pathogens. PLoS Pathog 2013, 9(9):1003601.
- [4]Milutinović B, Stolpe C, Armitage SA, Kurtz J, Peuß R: The red flour beetle as a model for bacterial oral infections. PLoS ONE 2013, 8(5):64638.
- [5]Roth O, Sadd BM, Schmid-Hempel P, Kurtz J: Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc Biol Sci 1654, 276:145-151.
- [6]Wang Z, Gerstein M, Snyder M: RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009, 10(1):57-63.
- [7]Klingler M: Tribolium. Curr Biol 2004, 14(16):639-640.
- [8]Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Beeman RW, Brown SJ, Bucher G, Friedrich M, Grimmelikhuijzen CJ, Klingler M, Lorenzen M, Richards S, Roth S, Schröder R, Tautz D, Zdobnov EM, Muzny D, Gibbs RA, Weinstock GM, Attaway T, Bell S, Buhay CJ, Chandrabose MN, Chavez D, Clerk-Blankenburg KP, Cree A, Dao M, et al.: The genome of the model beetle and pest Tribolium castaneum. Nature 2008, 452(7190):949-955.
- [9]Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH: Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 1998, 62(3):775-806.
- [10]van Frankenhuyzen K: Insecticidal activity of Bacillus thuringiensis crystal proteins. J Invertebr Pathol 2009, 101(1):1-16.
- [11]Roth O, Joop G, Eggert H, Hilbert J, Daniel J, Schmid-Hempel P, Kurtz J: Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J Anim Ecol 2010, 79(2):403-413.
- [12]Moore AD, Bornberg-Bauer E: The dynamics and evolutionary potential of domain loss and emergence. Mol Biol Evol 2012, 29(2):787-796.
- [13]Johnston PR, Makarova O, Rolff J: Inducible defenses stay up late: temporal patterns of immune gene expression in Tenebrio molitor. G3 (Bethesda) 2013. doi:g3.113.008516
- [14]Zou Z, Evans JD, Lu Z, Zhao P, Williams M, Sumathipala N, Hetru C, Hultmark D, Jiang H: Comparative genomic analysis of the Tribolium immune system. Genome Biol 2007, 8(8):177.
- [15]Altincicek B, Elashry A, Guz N, Grundler FM, Vilcinskas A, Dehne HW: Next generation sequencing based transcriptome analysis of septic-injury responsive genes in the beetle Tribolium castaneum. PLoS ONE 2013, 8(1):52004.
- [16]Contreras E, Rausell C, Real MD: Proteome response of Tribolium castaneum larvae to Bacillus thuringiensis toxin producing strains. PLoS ONE 2013, 8(1):55330.
- [17]Roth O, Kurtz J: The stimulation of immune defence accelerates development in the red flour beetle (Tribolium castaneum). J Evol Biol 2008, 21(6):1703-1710.
- [18]Boman HG, Nilsson I, Rasmuson B: Inducible antibacterial defence system in Drosophila. Nature 1972, 237(5352):232-235.
- [19]Hoffmann JA, Reichhart JM: Drosophila innate immunity: an evolutionary perspective. Nat Immunol 2002, 3(2):121-126.
- [20]Rolff J, Siva-Jothy MT: Invertebrate ecological immunology. Science 472., 301(5632)
- [21]Lemaitre B, Hoffmann J: The host defense of Drosophila melanogaster. Annu Rev Immunol 2007, 25:697-743.
- [22]Chambers MC, Schneider DS: Pioneering immunology: insect style. Curr Opin Immunol 2012, 24(1):10-14.
- [23]Nehme NT, Liegeois S, Kele B, Giammarinaro P, Pradel E, Hoffmann JA, Ewbank JJ, Ferrandon D: A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog 2007, 3(11):173.
- [24]Vlisidou I, Dowling AJ, Evans IR, Waterfield N, ffrench-Constant RH, Wood W: Drosophila embryos as model systems for monitoring bacterial infection in real time. PLoS Pathog 2009, 5(7):1000518.
- [25]Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B: Drosophila intestinal response to bacterial infection activation of host defense and stem cell proliferation. Cell Host Microbe 2009, 5(2):200-211.
- [26]Chakrabarti S, Liehl P, Buchon N, Lemaitre B: Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe 2012, 12(1):60-70.
- [27]Cornman RS, Lopez D, Evans JD: Transcriptional response of honey bee larvae infected with the bacterial pathogen Paenibacillus larvae. PLoS ONE 2013, 8(6):65424.
- [28]Fritzlar S, Kurtz J, Milutinović B: Increased survival in the red flour beetle after oral priming with bacteria-conditioned media. J Innate Immun 2014, 6(3):306-314.
- [29]Mukherjee K, Fischer R, Vilcinskas A: Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. Front Zool 2012, 9(1):25.
- [30]Lehane MJ: Peritrophic matrix structure and function. Annu Rev Entomol 1997, 42:525-550.
- [31]Arakane Y, Dixit R, Begum K, Park Y, Specht CA, Merzendorfer H, Kramer KJ, Muthukrishnan S, Beeman RW: Analysis of functions of the chitin deacetylase gene family in Tribolium castaneum. Insect Biochem Mol Biol 2009, 39(5–6):355-365.
- [32]Li B, Su T, Chen X, Liu B, Zhu B, Fang Y, Qiu W, Xie G: Effect of chitosan solution on the bacterial septicemia disease of Bombyx mori (Lepidoptera: Bombycidae) caused by Serratia marcescens. Appl Entomol Zool 2010, 45(1):145-152.
- [33]Kong M, Chen XG, Xing K, Park HJ: Antimicrobial properties of chitosan and mode of action: a state of the art review. Int J Food Microbiol 2010, 144(1):51-63.
- [34]Cerenius L, Soderhall K: The prophenoloxidase-activating system in invertebrates. Immunol Rev 2004, 198:116-126.
- [35]Feyereisen R: Insect P450 enzymes. Annu Rev Entomol 1999, 44:507-533.
- [36]Scott JG, Wen Z: Cytochromes P450 of insects: the tip of the iceberg. Pest Manag Sci 2001, 57(10):958-967.
- [37]Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C: Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010, 329(5997):1353-1355.
- [38]Broderick NA, Raffa KF, Handelsman J: Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc Natl Acad Sci U S A 2006, 103(41):15196-15199.
- [39]Broderick NA, Robinson CJ, McMahon MD, Holt J, Handelsman J, Raffa KF: Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biol 2009, 7:11.
- [40]Johnston PR, Crickmore N: Gut bacteria are not required for the insecticidal activity of Bacillus thuringiensis toward the tobacco hornworm, Manduca sexta. Appl Environ Microbiol 2009, 75(15):5094-5099.
- [41]Pigott CR, Ellar DJ: Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 2007, 71(2):255-281.
- [42]Contreras E, Rausell C, Real MD: Tribolium castaneum Apolipophorin-III acts as an immune response protein against Bacillus thuringiensis Cry3Ba toxic activity. J Invertebr Pathol 2013, 113(3):209-213.
- [43]Whitten MM, Tew IF, Lee BL, Ratcliffe NA: A novel role for an insect apolipoprotein (apolipophorin III) in beta-1,3-glucan pattern recognition and cellular encapsulation reactions. J Immunol 2004, 172(4):2177-2185.
- [44]Gupta L, Noh JY, Jo YH, Oh SH, Kumar S, Noh MY, Lee YS, Cha SJ, Seo SJ, Kim I, Han YS, Barillas-Mury C: Apolipophorin-III mediates antiplasmodial epithelial responses in Anopheles gambiae (G3) mosquitoes. PLoS ONE 2010, 5(11):15410.
- [45]Pelosi P, Calvello M, Ban L: Diversity of odorant-binding proteins and chemosensory proteins in insects. Chem Senses 2005, 30 Suppl 1:291-292.
- [46]Oppert B, Dowd SE, Bouffard P, Li L, Conesa A, Lorenzen MD, Toutges M, Marshall J, Huestis DL, Fabrick J, Oppert C, Jurat-Fuentes JL: Transcriptome profiling of the intoxication response of Tenebrio molitor larvae to Bacillus thuringiensis Cry3Aa protoxin. PLoS ONE 2012, 7(4):34624.
- [47]Shah N, Dorer DR, Moriyama EN, Christensen AC: Evolution of a large, conserved, and syntenic gene family in insects. G3 (Bethesda) 2012, 2(2):313-319.
- [48]Yokoi K, Koyama H, Ito W, Minakuchi C, Tanaka T, Miura K: Involvement of NF-κB transcription factors in antimicrobial peptide gene induction in the red flour beetle, Tribolium castaneum. Dev Comp Immunol 2012, 38(2):342-351.
- [49]Obbard DJ, Welch JJ, Kim KW, Jiggins FM: Quantifying adaptive evolution in the Drosophila immune system. PLoS Genet 2009, 5(10):1000698.
- [50]St. John J: SeqPrep. [https://github.com/jstjohn/SeqPrep webcite]
- [51]Hansen KD, Brenner SE, Dudoit S: Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res 2010, 38(12):131.
- [52]Hannon laboratory: Fastx Toolkit. [http://hannonlab.cshl.edu/fastx_toolkit/ webcite]
- [53]Kim HS, Murphy T, Xia J, Caragea D, Park Y, Beeman RW, Lorenzen MD, Butcher S, Manak JR, Brown SJ: BeetleBase in 2010: revisions to provide comprehensive genomic information for Tribolium castaneum. Nucleic Acids Res 2010, 38(Database issue):437-442.
- [54]Wang L, Wang S, Li Y, Paradesi MS, Brown SJ: BeetleBase: the model organism database for Tribolium castaneum. Nucleic Acids Res 2007, 35(Database issue):476-479.
- [55]K-State Bioinformatics Center: BeetleBase Website. [http://www.Beetlebase.org webcite]
- [56]Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25(9):1105-1111.
- [57]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):25.
- [58]iBeetle consortium: iBeetle Website. [http://bioinf.uni-greifswald.de/tcas/index.html webcite]
- [59]Stanke M, Diekhans M, Baertsch R, Haussler D: Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 2008, 24(5):637-644.
- [60]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28(5):511-515.
- [61]Bullard JH, Purdom E, Hansen KD, Dudoit S: Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 2010, 11:94.
- [62]Goff L, Trapnell C, Kelley D: cummeRbund: analysis, exploration, manipulation, and visualization of Cufflinks high-throughput sequencing data. R package version 2.0.0. [http://compbio.mit.edu/cummeRbund/ webcite]
- [63]Roberts DW: labdsv: Ordination and Multivariate Analysis for Ecology. R package version 1.6-1. [http://CRAN.R-project.org/package=labdsv webcite]
- [64]Gaudet P, Chisholm R, Berardini T, Dimmer E, Engel SR, Fey P, Hill DP, Howe D, Hu JC, Huntley R, Khodiyar VK, Kishore R, Li D, Lovering RC, McCarthy F, Ni L, Petri V, Siegele DA, Tweedie S, Van Auken K, Wood V, Basu S, Carbon S, Dolan M, Mungall CJ, Dolinski K, Thomas P, Ashburner M, Blake JA, Cherry JM, et al.: The Gene Ontology’s Reference Genome Project: a unified framework for functional annotation across species. PLoS Comput Biol 2009, 5(7):1000431.
- [65]Kinsella RJ, Kahari A, Haider S, Zamora J, Proctor G, Spudich G, Almeida-King J, Staines D, Derwent P, Kerhornou A, Kersey P, Flicek P: Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database (Oxford) 2011, 2011:030.
- [66]Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676.
- [67]Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R: InterProScan: protein domains identifier. Nucleic Acids Res 2005, 33(Web Server issue):116-120.
- [68]Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Venables B, Schwartz M: gplots: Various R Programming Tools for Plotting Data. R Package Version 2.11.0. [http://CRAN.R-project.org/package=gplots webcite]