A detailed view of the intracellular transcriptome of Listeria monocytogenes in murine macrophages using RNA-seq

Frontiers in Microbiology

Volumn 6, Issue OCT, 2015, Pages

  Schultze, Tilman ^a   Hilker, Rolf ^a   Mannala, Gopala K ^a   Gentil, Katrin ^a   Weigel, Markus ^a   Farmani, Neda ^a   Windhorst, Anita C ^a   Goesmann, Alexander ^a   Chakraborty, Trinad ^a   Hain, Torsten ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Human pathogenic bacteria; Intracellular; Listeria monocytogenes; MRNA transcriptome analysis; RNA seq

Indexed keywords

ABC TRANSPORTER; BACTERIAL VECTOR; CAPSID PROTEIN; COMPLEMENTARY RNA; ION; MANNOSE; MESSENGER RNA; PHOSPHOLIPASE C; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DELETION MUTANT; ESCHERICHIA COLI; GENE EXPRESSION; LISTERIA MONOCYTOGENES; LISTERIOSIS; LMO1119 GENE; LMO2316 GENE; LYSOGENIZATION; MACROPHAGE; MICROARRAY ANALYSIS; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PLASMID; PROPHAGE; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSCRIPTION REGULATION; UPREGULATION;

EID: 84946848075     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01199     Document Type: Article

References (66)

1. Allerberger, F., and Wagner, M. (2010). Listeriosis: a resurgent foodborne infection. Clin. Microbiol. Infect. 16, 16-23. doi: 10.1111/j.1469-0691.2009.03109.x
2. Alonzo, F., Port, G. C., Cao, M., and Freitag, N. E. (2009). The posttranslocation chaperone PrsA2 contributes to multiple facets of Listeria monocytogenes pathogenesis. Infect. Immun. 77, 2612-2623. doi: 10.1128/IAI.00280-09
3. Anders, S., Pyl, P. T., and Huber, W. (2014). HTSeq A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169. doi: 10.1101/002824
4. Behrens, S., Widder, S., Mannala, G. K., Qing, X., Madhugiri, R., Kefer, N., et al. (2014). Ultra deep sequencing of Listeria monocytogenes sRNA transcriptome revealed new antisense RNAs. PLoS ONE 9:e83979. doi: 10.1371/journal.pone.0083979
5. Cahoon, L. A., and Freitag, N. E. (2015). Identification of conserved and species-specific functions of the Listeria monocytogenes PrsA2 secretion chaperone. Infect. Immun. 83, 4028-4041. doi: 10.1128/IAI.00504-15
6. Camejo, A., Buchrieser, C., Couvé, E., Carvalho, F., Reis, O., Ferreira, P., et al. (2009). In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog. 5:449. doi: 10.1371/journal.ppat.1000449
7. Chambers, J. M., and Hastie, T. J. (1992). "Linear models". in Statistical Models, Chap. 4, eds J. M. Chambers and T. J. Hast (Pacific Grove, CA: Wadsworth Brooks Chambers JM).
8. Chastanet, A., Derre, I., Nair, S., and Msadek, T. (2004). ClpB, a Novel Member of the Listeria monocytogenes CtsR Regulon. Is involved in virulence but not in general stress tolerance. J. Bacteriol. 186, 1165-1174. doi: 10.1128/JB.186.4.1165
9. Chatterjee, S. S., Hossain, H., Otten, S., Kuenne, C., Kuchmina, K., Machata, S., et al. (2006). Intracellular gene expression profile of Listeria monocytogenes. Infect. Immun. 74, 1323-1338. doi: 10.1128/IAI.74.2.1323
10. Chico-Calero, I., Suárez, M., González-Zorn, B., Scortti, M., Slaghuis, J., Goebel, W., et al. (2002). Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc. Natl. Acad. Sci. U.S.A. 99, 431-436. doi: 10.1073/pnas.012363899
11. Christiansen, J. K., Nielsen, J. S., Ebersbach, T., Valentin-Hansen, P., Søgaard-Andersen, L., and Kallipolitis, B. H. (2006). Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA 12, 1383-1396. doi: 10.1261/rna.49706
12. Cossart, P. (2011). Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc. Natl. Acad. Sci. U.S.A. 108, 19484-19491. doi: 10.1073/pnas.1112371108
13. Cossart, P., and Lebreton, A. (2014). A trip in the "new microbiology" with the bacterial pathogen Listeria monocytogenes. FEBS Lett. 588, 2437-2445. doi: 10.1016/j.febslet.2014.05.051
14. Cossart, P., and Toledo-Arana, A. (2008). Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect. 10, 1041-1050. doi: 10.1016/j.micinf.2008.07.043
15. Cotter, P. D., Draper, L. A., Lawton, E. M., Daly, K. M., Groeger, D. S., Casey, P. G., et al. (2008). Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog. 4:e1000144. doi: 10.1371/journal.ppat.1000144
16. Denes, T., and Wiedmann, M. (2014). Environmental responses and phage susceptibility in foodborne pathogens: implications for improving applications in food safety. Curr. Opin. Biotechnol. 26, 45-49. doi: 10.1016/j.copbio.2013.09.001
17. Dodd, I. B., Shearwin, K. E., and Egan, J. B. (2005). Revisited gene regulation in bacteriophage aaa. Curr. Opin. Genet. Dev. 15, 145-152. doi: 10.1016/j.gde.2005.02.001
18. Elinav, H., Hershko-Klement, A., Valinsky, L., Jaffe, J., Wiseman, A., Shimon, H., et al. (2014). Pregnancy-associated listeriosis: clinical characteristics and geospatial analysis of a 10-year period in israel. Clin. Infect. Dis. 59, 953-961. doi: 10.1093/cid/ciu504
19. Engelbrecht, F., Chun, S. K., Ochs, C., Hess, J., Lottspeich, F., Goebel, W., et al. (1996). A new PrfA-regulated gene of Listeria monocytogenes encoding a small, secreted protein which belongs to the family of internalins. Mol. Microbiol. 21, 823-837.
20. Gaillard, J. L., Berche, P., Frehel, C., Gouin, E., and Cossart, P. (1991). Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 65, 1127-1141. doi: 10.1016/0092-8674(91)90009-N
21. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., et al. (2001). Comparative genomics of listeria species. Science 294, 849-852. doi: 10.1126/science.1063447
22. Goldfarb, T., Sberro, H., Weinstock, E., Cohen, O., Doron, S., Charpak-amikam, Y., et al. (2015). BREX is a novel phage resistance system widespread in microbial genomes. EMBO J. 34, 169-184.
23. Gouin, E., Adib-Conquy, M., Balestrino, D., Nahori, M.-A., Villiers, V., Colland, F., et al. (2010). The Listeria monocytogenes InlC protein interferes with innate immune responses by targeting the IκB kinase subunit IKKα. Proc. Natl. Acad. Sci. U.S.A. 107, 17333-17338. doi: 10.1073/pnas.1007765107
24. Grubmüller, S., Schauer, K., Goebel, W., Fuchs, T. M., and Eisenreich, W. (2014). Analysis of carbon substrates used by Listeria monocytogenes during growth in J774A.1 macrophages suggests a bipartite intracellular metabolism. Front. Cell. Infect. Microbiol. 4:156. doi: 10.3389/fcimb.2014.00156
25. Hamon, M., Bierne, H., and Cossart, P. (2006). Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4, 423-434. doi: 10.1038/nrmicro1413
26. Heusipp, G., Fälker, S., and Alexander Schmidt, M. (2007). DNA adenine methylation and bacterial pathogenesis. Int. J. Med. Microbiol. 297, 1-7. doi: 10.1016/j.ijmm.2006.10.002
27. Hilker, R., Stadermann, K. B., Doppmeier, D., Kalinowski, J., Stoye, J., Straube, J., et al. (2014). ReadXplorer-visualization and analysis of mapped sequences. Bioinformatics 30, 2247-2254. doi: 10.1093/bioinformatics/btu205
28. Hothorn, T., Bretz, F., and Westfall, P. (2008). Simultaneous inference in general parametric models. Biom. J. 50, 346-363. doi: 10.1002/bimj.200810425
29. Johansson, J., Mandin, P., Renzoni, A., Chiaruttini, C., Springer, M., and Cossart, P. (2002). An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110, 551-561. doi: 10.1016/S0092-8674(02)00905-4
30. Joseph, B., Joseph, B., Schauer, K., Schauer, K., Fuchs, T. M., Fuchs, T. M., et al. (2006). Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. Society 188, 556-568. doi: 10.1128/JB.188.2.556
31. Joseph, B., Mertins, S., Stoll, R., Schar, J., Umesha, K. R., Luo, Q., et al. (2008). Glycerol metabolism and PrfA activity in Listeria monocytogenes. J. Bacteriol. 190, 5412-5430. doi: 10.1128/JB.00259-08
32. Kim, J. W., Dutta, V., Elhanafi, D., Lee, S., Osborne, J. A., and Kathariou, S. (2012). A novel restriction-modification system is responsible for temperature-dependent phage resistance in Listeria monocytogenes ECII. Appl. Environ. Microbiol. 78, 1995-2004. doi: 10.1128/AEM.07086-11
33. Kodaira, K., Oki, M., Kakikawa, M., Watanabe, N., Hirakawa, M., Yamada, K., et al. (1997). Genome structure of the Lactobacillus temperate phage fg1e: the whole genome sequence and the putative promoter/repressor system. Gene 187, 45-53. doi: 10.1016/S0378-1119(96)00687-7
34. Kuenne, C., Billion, A., Mraheil, M. A., Strittmatter, A., Daniel, R., Goesmann, A., et al. (2013). Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics 14:47. doi: 10.1186/1471-2164-14-47
35. Kuenne, C. T., Ghai, R., Chakraborty, T., and Hain, T. (2007). GECO-Linear visualization for comparative genomics. Bioinformatics 23, 125-126. doi: 10.1093/bioinformatics/btl556
36. Labrie, S. J., Samson, J. E., and Moineau, S. (2010). Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317-327. doi: 10.1038/nrmicro2315
37. Langmead, B., and Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359. doi: 10.1038/nmeth.1923
38. Lecuit, M. (2007). Human listeriosis and animal models. Microbes Infect. 9, 1216-1225. doi: 10.1016/j.micinf.2007.05.009
39. Lee, S., Ward, T. J., Siletzky, R. M., and Kathariou, S. (2012). Two novel type II restriction-modification systems occupying genomically equivalent locations on the chromosomes of Listeria monocytogenes strains. Appl. Environ. Microbiol. 78, 2623-2630. doi: 10.1128/AEM.07203-11
40. Loessner, M. J., Inman, R. B., and Lauer, P. (2000). Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Mol. Microbiol. 35, 324-340. doi: 10.1046/j.1365-2958.2000.01720.x
41. Love, M. I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 1-21. doi: 10.1186/s13059-014-0550-8
42. Mandin, P., Geissmann, T., Cossart, P., Repoila, F., and Vergassola, M. (2007). Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res. 35, 962-974. doi: 10.1093/nar/gkl1096
43. Mansjö, M., and Johansson, J. (2011). The riboflavin analog roseoflavin targets an FMN-riboswitch and blocks Listeria monocytogenes growth, but also stimulates virulence gene-expression and infection. RNA Biol. 8, 674-680. doi: 10.4161/rna.8.4.15586
44. Mellin, J. R., and Cossart, P. (2012). The non-coding RNA world of the bacterial pathogen Listeria monocytogenes. RNA Biol. 9, 372-378. doi: 10.4161/rna.19235
45. Mraheil, M. A., Billion, A., Mohamed, W., Mukherjee, K., Kuenne, C., Pischimarov, J., et al. (2011). The intracellular sRNA transcriptome of Listeria monocytogenes during growth in macrophages. Nucleic Acids Res. 39, 4235-4248. doi: 10.1093/nar/gkr033
46. Nair, S., Frehel, C., Nguyen, L., Escuyer, V., and Berche, P. (1999). ClpE, a novel member of the HSP100 family, is involved in cell division and virulence of Listeria monocytogenes. Mol. Microbiol. 31, 185-196. doi: 10.1046/j.1365-2958.1999.01159.x
47. Nielsen, J. S., Larsen, M. H., Lillebaek, E. M. S., Bergholz, T. M., Christiansen, M. H. G., Boor, K. J., et al. (2011). A small RNA controls expression of the chitinase ChiA in Listeria monocytogenes. PLoS ONE 6:e19019. doi: 10.1371/journal.pone.0019019
48. Nielsen, J. S., Olsen, A. S., Bonde, M., Valentin-Hansen, P., and Kallipolitis, B. H. (2008). Identification of a sigma B-dependent small noncoding RNA in Listeria monocytogenes. J. Bacteriol. 190, 6264-6270. doi: 10.1128/JB.00740-08
49. Oliver, H. F., Orsi, R. H., Ponnala, L., Keich, U., Wang, W., Sun, Q., et al. (2009). Deep RNA sequencing of L. monocytogenes reveals overlapping and extensive stationary phase and sigma B-dependent transcriptomes, including multiple highly transcribed noncoding RNAs. BMC Genomics 10:641. doi: 10.1186/1471-2164-10-641
50. Oppenheim, A. B., Kobiler, O., Stavans, J., Court, D. L., and Adhya, S. (2005). Switches in bacteriophage lambda development. Annu. Rev. Genet. 39, 409-429. doi: 10.1146/annurev.genet.39.073003.113656
51. Pfaffl, M. W., and Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. doi: 10.1093/nar/29.9.e45
52. Rabinovich, L., Sigal, N., Borovok, I., Nir-Paz, R., and Herskovits, A. A. (2012). Prophage excision activates listeria competence genes that promote phagosomal escape and virulence. Cell 150, 792-802. doi: 10.1016/j.cell.2012.06.036
53. Rajabian, T., Gavicherla, B., Heisig, M., Muller-Altrock, S., Goebel, W., Gray-Owen, S. D., et al. (2009). The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of Listeria. Nat. Cell Biol. 11, 1212-1218. doi: 10.1038/ncb1964
54. R Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available at: http://www.R-project.org/
55. Rouquette, C., Ripio, M. T., Pellegrini, E., Bolla, J. M., Tascon, R. I., Vázquez-Boland, J. A., et al. (1996). Identification of a ClpC ATPase required for stress tolerance and in vivo survival of Listeria monocytogenes. Mol. Microbiol. 21, 977-987. doi: 10.1046/j.1365-2958.1996.641432.x
56. Sánchez-Romero, M. A., Cota, I., and Casadesús, J. (2015). DNA methylation in bacteria: from the methyl group to the methylome. Curr. Opin. Microbiol. 25, 9-16. doi: 10.1016/j.mib.2015.03.004
57. Schäferkordt, S., and Chakraborty, T. (1995). Vector plasmid for insertional mutagenesis and directional cloning in Listeria spp. Biotechniques 19, 720-722, 724-725.
58. Schultze, T., Izar, B., Qing, X., Mannala, G. K., and Hain, T. (2014). Current status of antisense RNA-mediated gene regulation in Listeria monocytogenes. Front. Cell. Infect. Microbiol. 4:135. doi: 10.3389/fcimb.2014.00135
59. Seifart Gomes, C., Izar, B., Pazan, F., Mohamed, W., Mraheil, M. A., Mukherjee, K., et al. (2011). Universal stress proteins are important for oxidative and acid stress resistance and growth of Listeria monocytogenes EGD-e in vitro and in vivo. PLoS ONE 6:e24965. doi: 10.1371/journal.pone.0024965
60. Sievers, S., Lund, A., Menendez-Gil, P., Nielsen, A., Storm Mollerup, M., Lambert Nielsen, S., et al. (2015). The multicopy sRNA LhrC controls expression of the oligopeptide-binding protein OppA in Listeria monocytogenes. RNA Biol. 12, 985-997. doi: 10.1080/15476286.2015.1071011
61. Sievers, S., Sternkopf Lillebaek, E. M., Jacobsen, K., Lund, A., Mollerup, M. S., Nielsen, P. K., et al. (2014). A multicopy sRNA of Listeria monocytogenes regulates expression of the virulence adhesin LapB. Nucleic Acids Res. 42, 9383-9398. doi: 10.1093/nar/gku630
62. Toledo-Arana, A., Dussurget, O., Nikitas, G., Sesto, N., Guet-Revillet, H., Balestrino, D., et al. (2009). The Listeria transcriptional landscape from saprophytism to virulence. Nature 459, 950-956. doi: 10.1038/nature08080
63. Wehner, S., Mannala, G. K., Qing, X., Madhugiri, R., Chakraborty, T., Mraheil, M. A., et al. (2014). Detection of very long antisense transcripts by whole transcriptome RNA-seq analysis of Listeria monocytogenes by semiconductor sequencing technology. PLoS ONE 9:e108639. doi: 10.1371/journal.pone.0108639
64. Wurtzel, O., Sesto, N., Mellin, J. R., Karunker, I., Edelheit, S., Bécavin, C., et al. (2012). Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol. Syst. Biol. 8, 1-14. doi: 10.1038/msb.2012.11
65. Yildirim, S., Elhanafi, D., Lin, W., Hitchins, A. D., Siletzky, R. M., and Kathariou, S. (2010). Conservation of genomic localization and sequence content of Sau3AI-like restriction-modification gene cassettes among Listeria monocytogenes epidemic clone I and selected strains of serotype 1/2a. Appl. Environ. Microbiol. 76, 5577-5584. doi: 10.1128/AEM.00648-10
66. Mpo exert antagonistic effects on the transcriptional activator ManR of Listeria monocytogenes. J. Bacteriol. 197, 1559-1572. doi: 10.1128/JB.02522-14