Discovery of putative small non-coding RNAs from the obligate intracellular bacterium Wolbachia pipientis

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Woolfit, Megan ^a   Algama, Manjula ^a   Keith, Jonathan M ^a   McGraw, Elizabeth A ^a   Popovici, Jean ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; SMALL UNTRANSLATED RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BIOINFORMATICS; CISTRON; COMPARATIVE GENE MAPPING; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENDOSYMBIOSIS; FUNCTIONAL GENOMICS; GENE CONTROL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC CONSERVATION; GENETIC MODEL; INTRACELLULAR BACTERIUM; MATHEMATICAL MODEL; NONHUMAN; RNA ANALYSIS; RNA EXTRACTION; RNA GENE; RNA SEQUENCE; SEQUENCE HOMOLOGY; SEX DIFFERENCE; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION; WOLBACHIA PIPIENTIS; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGY; CONSERVED SEQUENCE; FEMALE; GENETIC TRANSCRIPTION; GENETICS; HOST RANGE; INTRACELLULAR SPACE; MALE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SEQUENCE ANALYSIS; WOLBACHIA;

BACTERIA (MICROORGANISMS); HEXAPODA; WOLBACHIA; WOLBACHIA PIPIENTIS;

ANIMALS; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; FEMALE; HOST SPECIFICITY; INTRACELLULAR SPACE; MALE; ORGAN SPECIFICITY; RNA, MESSENGER; RNA, SMALL UNTRANSLATED; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC; WOLBACHIA;

EID: 84928910962     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118595     Document Type: Article

References (62)

1. Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7:e38544. doi: 10.1371/journal.pone. 0038544 PMID: 22685581
2. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6:741-751. doi: 10.1038/nrmicro1969 PMID: 18794912
3. Hoffmann A, Turelli M (1997) Cytoplasmic incompatibility in insects. In: O'Neill SL, Hoffmann A, Werren JH, editors. Influential passengers Inherited microorganisms and arthropod reproduction. Oxford: Oxford University Press. pp. 42-80.
4. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN (2008) Wolbachia and Virus Protection in Insects. Science 322:702-702. doi: 10.1126/science.1162418 PMID: 18974344
5. Teixeira L, Ferreira A, Ashburner M (2008) The Bacterial Symbiont Wolbachia Induces Resistance to RNA Viral Infections in Drosophila melanogaster. Plos Biology 6:2753-2763.
6. Moreira LA, Iturbe-Ormaetxe I, Jeffery JAL, Lu G, Pyke AT, et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya and Plasmodium Cell 139:1268-1278. doi: 10.1016/j.cell.2009.11.042 PMID: 20064373
7. Hoffmann A, Montgomery B, Popovici J, Iturbe-Ormaetxe I, Johnson P, et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454-457. doi: 10.1038/nature10356 PMID: 21866160
8. Osei-Amo S, Hussain M, O'Neill SL, Asgari S (2012) Wolbachia-Induced aae-miR-12 miRNA Negatively Regulates the Expression of MCT1 and MCM6 Genes in Wolbachia-Infected Mosquito Cell Line. PLoS One 7:e50049. doi: 10.1371/journal.pone.0050049 PMID: 23166816
9. Hussain M, Frentiu FD, Moreira LA, O'Neill SL, Asgari S (2011) Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proceedings of the National Academy of Sciences 108:9250-9255. doi: 10.1073/pnas.1105469108 PMID: 21576469
10. Zhang G, Hussain M, O'Neill SL, Asgari S (2013) Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proceedings of the National Academy of Sciences 110:10276-10281. doi: 10.1073/pnas.1303603110 PMID: 23733960
11. Brennan LJ, Keddie BA, Braig HR, Harris HL (2008) The Endosymbiont Wolbachia pipientis Induces the Expression of Host Antioxidant Proteins in an Aedes albopictus Cell Line. PLoS ONE 3:e2083. doi: 10.1371/journal.pone.0002083 PMID: 18461124
12. Kremer N, Voronin D, Charif D, Mavingui P, Mollereau B, et al. (2009) Wolbachia Interferes with Ferritin Expression and Iron Metabolism in Insects. PLoS Pathog 5:e1000630. doi: 10.1371/journal.ppat. 1000630 PMID: 19851452
13. Kremer N, Charif D, Henri H, Gavory F, Wincker P, et al. (2012) Influence of Wolbachia on host gene expression in an obligatory symbiosis. BMC Microbiology 12:S7. doi: 10.1186/1471-2180-12-S1-S7 PMID: 22376153
14. Rances E, Voronin D, Tran-Van V, Mavingui P (2008) Genetic and functional characterization of the type IV secretion system in Wolbachia. Journal of Bacteriology 190:5020-5030. doi: 10.1128/JB. 00377-08 PMID: 18502862
15. Voth DE, Broederdorf LJ, Graham JG (2012) Bacterial Type IV secretion systems: versatile virulence machines. Future microbiology 7:241-257. doi: 10.2217/fmb.11.150 PMID: 22324993
16. Siozios S, Ioannidis P, Klasson L, Andersson SG, Braig HR, et al. (2013) The Diversity and Evolution of Wolbachia Ankyrin Repeat Domain Genes. PLoS One 8:e55390. doi: 10.1371/journal.pone.0055390 PMID: 23390535
17. Walker T, Klasson L, Sebaihia M, Sanders MJ, Thomson NR, et al. (2007) Ankyrin repeat domain-encoding genes in the wPip strain of Wolbachia from the Culex pipiens group. Bmc Biology 5.
18. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements. Plos Biology 2:327-341.
19. Iturbe-Ormaetxe I, Burke GR, Riegler M, O'Neill SL (2005) Distribution, expression, and motif variability of ankyrin domain genes in Wolbachia pipientis. Journal of Bacteriology 187:5136-5145. PMID: 16030207
20. Rikihisa Y, Lin M, Niu H (2010) Microreview: Type IV secretion in the obligatory intracellular bacterium Anaplasma phagocytophilum. Cellular Microbiology 12:1213-1221. doi: 10.1111/j.1462-5822.2010. 01500.x PMID: 20670295
21. Darby AC, Armstrong SD, Bah GS, Kaur G, Hughes MA, et al. (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Research 22:2467-2477. doi: 10.1101/gr.138420.112 PMID: 22919073
22. Papafotiou G, Oehler S, Savakis C, Bourtzis K (2011) Regulation of Wolbachia ankyrin domain encoding genes in Drosophila gonads. Research in Microbiology 162:764-772. doi: 10.1016/j.resmic.2011. 06.012 PMID: 21726632
23. Li Z, Carlow CKS (2012) Characterization of Transcription Factors That Regulate the Type IV Secretion System and Riboflavin Biosynthesis in Wolbachia of Brugia malayi. PLoS ONE 7:e51597. doi: 10.1371/journal.pone.0051597 PMID: 23251587
24. Boughammoura A, Matzanke BF, Böttger L, Reverchon S, Lesuisse E, et al. (2008) Differential role of ferritins in iron metabolism and virulence of the plant-pathogenic bacterium Erwinia chrysanthemi 3937. Journal of Bacteriology 190:1518-1530. doi: 10.1128/JB.01640-07 PMID: 18165304
25. Grieshaber NA, Grieshaber SS, Fischer ER, Hackstadt T (2006) A small RNA inhibits translation of the histone-like protein Hc1 in Chlamydia trachomatis. Molecular Microbiology 59:541-550. PMID: 16390448
26. Bejerano-Sagie M, Xavier KB (2007) The role of small RNAs in quorum sensing. Current Opinion in Microbiology 10:189-198. PMID: 17387037
27. Murphy ER, Payne SM (2007) RyhB, an Iron-Responsive Small RNA Molecule, Regulates Shigella dysenteriae Virulence. Infection and Immunity 75:3470-3477. PMID: 17438026
28. Podkaminski D, Vogel J (2010) Small RNAs promote mRNA stability to activate the synthesis of virulence factors. Molecular Microbiology 78:1327-1331. doi: 10.1111/j.1365-2958.2010.07428.x PMID: 21143308
29. Bradley ES, Bodi K, Ismail AM, Camilli A (2011) A genome-wide approach to discovery of small RNAs involved in regulation of virulence in Vibrio cholerae. Plos Pathogens 7:e1002126. doi: 10.1371/journal.ppat.1002126 PMID: 21779167
30. Koo JT, Alleyne TM, Schiano CA, Jafari N, Lathem WW (2011) Global discovery of small RNAs in Yersinia pseudotuberculosis identifies Yersinia-specific small, noncoding RNAs required for virulence. Proceedings of the National Academy of Sciences 108:E709-E717. doi: 10.1073/pnas.1101655108 PMID: 21876162
31. Gottesman S, Storz G (2011) Bacterial Small RNA Regulators: Versatile Roles and Rapidly Evolving Variations. Cold Spring Harbor Perspectives in Biology 3.
32. Storz G, Vogel J, Wassarman Karen M Regulation by Small RNAs in Bacteria: Expanding Frontiers. Molecular Cell 43:880-891. doi: 10.1016/j.molcel.2011.08.022 PMID: 21925377
33. Yamada R, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL (2011) Functional test of the influence of Wolbachia genes on cytoplasmic incompatibility expression in Drosophila melanogaster. Insect Molecular Biology 20:75-85. doi: 10.1111/j.1365-2583.2010.01042.x PMID: 20854481
34. Min KT, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proceedings of the National Academy of Sciences of the United States of America 94:10792-10796. PMID: 9380712
35. Frentiu FD, Robinson J, Young PR, McGraw EA, O'Neill SL (2010) Wolbachia-Mediated Resistance to Dengue Virus Infection and Death at the Cellular Level. PLoS One 5:e13398. doi: 10.1371/journal. pone.0013398 PMID: 20976219
36. Iturbe-Ormaetxe I, Woolfit M, Rances E, Duplouy A, O'Neill SL (2011) A simple protocol to obtain highly pure Wolbachia endosymbiont DNA for genome sequencing. J Microbiol Methods 84:134-136. doi: 10.1016/j.mimet.2010.10.019 PMID: 21047535
37. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Research 40:W622-W627. doi: 10.1093/nar/gks540 PMID: 22684630
38. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. doi: 10.1093/bioinformatics/btp324 PMID: 19451168
39. Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA (2012) Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 28:464-469. doi: 10.1093/bioinformatics/btr703 PMID: 22199388
40. Shelby KS, Popham HJR (2007) Increased plasma selenium levels correlate with elevated resistance of Heliothis virescens larvae against baculovirus infection. Journal of Invertebrate Pathology 95:77-83. PMID: 17316679
41. Woolfit M, Iturbe-Ormaetxe I, McGraw EA, O'Neill SL (2009) An Ancient Horizontal Gene Transfer between Mosquito and the Endosymbiotic Bacterium Wolbachia pipientis. Molecular Biology and Evolution 26:367-374. doi: 10.1093/molbev/msn253 PMID: 18988686
42. Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements. Genome Research 14:1394-1403. PMID: 15231754
43. Oldmeadow C, Keith JM (2011) Model selection in Bayesian segmentation of multiple DNA alignments. Bioinformatics 27:604-610. doi: 10.1093/bioinformatics/btq716 PMID: 21208984
44. Keith J (2008) Sequence Segmentation. In: Keith J, editor. Bioinformatics: Humana Press. pp. 207-229.
45. Algama M, Keith JM (2014) Investigating genomic structure using changept: A Bayesian segmentation model. Computational and Structural Biotechnology Journal 10:107-115. doi: 10.1016/j.csbj.2014.08. 003 PMID: 25349679
46. Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences 85:8998-9002. PMID: 2461560
47. Gerhart E, Wagner H, Vogel J (2008) Approaches to Identify Novel Non-messenger RNAs in Bacteria and to Investigate their Biological Functions: Functional Analysis of Identified Non-mRNAs. Handbook of RNA biochemistry: 614-642.
48. Walker T, Klasson L, Sebaihia M, Sanders MJ, Thomson NR, et al. (2007) Ankyrin repeat domain-encoding genes in the wPip strain of Wolbachia from the Culex pipiens group. BMC Biol 5:39. PMID: 17883830
49. Darby AC, Christina Gill A, Armstrong SD, Hartley CS, Xia D, et al. (2014) Integrated transcriptomic and proteomic analysis of the global response of Wolbachia to doxycycline-induced stress. ISME J 8:925-937. doi: 10.1038/ismej.2013.192 PMID: 24152719
50. Kumar N, Creasy T, Sun Y, Flowers M, Tallon LJ, et al. (2012) Efficient subtraction of insect rRNA prior to transcriptome analysis of Wolbachia-Drosophila lateral gene transfer. BMC research notes 5:230. doi: 10.1186/1756-0500-5-230 PMID: 22583543
51. Albrecht M, Sharma CM, Dittrich MT, Muller T, Reinhardt R, et al. (2011) The transcriptional landscape of Chlamydia pneumoniae. Genome Biol 12:R98. doi: 10.1186/gb-2011-12-10-r98 PMID: 21989159
52. Skippington E, Ragan MA (2012) Evolutionary Dynamics of Small RNAs in 27 Escherichia coli and Shigella Genomes. Genome Biology and Evolution 4:330-345. doi: 10.1093/gbe/evs001 PMID: 22223756
53. Klasson L, Walker T, Sebaihia M, Sanders MJ, Quail MA, et al. (2008) Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Molecular Biology and Evolution 25:1877-1887. doi: 10. 1093/molbev/msn133 PMID: 18550617
54. Keith J, Kroese D, Bryant D (2004) A Generalized Markov Sampler. Methodology And Computing In Applied Probability 6:29-53.
55. Keith JM, Adams P, Stephen S, Mattick JS (2008) Delineating slowly and rapidly evolving fractions of the Drosophila genome. Journal of Computational Biology 15:407-430. doi: 10.1089/cmb.2007.0173 PMID: 18435570
56. Keith JM (2006) Segmenting eukaryotic genomes with the generalized Gibbs sampler. Journal of Computational Biology 13:1369-1383. PMID: 17037964
57. Degnan PH, Ochman H, Moran NA (2011) Sequence conservation and functional constraint on intergenic spacers in reduced genomes of the obligate symbiont Buchnera. PLoS genetics 7:e1002252. doi: 10.1371/journal.pgen. 1002252 PMID: 21912528
58. Woolfit M, Iturbe-Ormaetxe I, Brownlie JC, Walker T, Riegler M, et al. (2013) Genomic evolution of the pathogenic Wolbachia strain, wMelPop. Genome Biol Evol 5:2189-2204. doi: 10.1093/gbe/evt169 PMID: 24190075
59. Paraskevopoulos C, Bordenstein SR, Wernegreen JJ, Werren JH, Bourtzis K (2006) Toward a Wolbachia multilocus sequence typing system: Discrimination of Wolbachia strains present in Drosophila species. Current Microbiology 53:388-395. PMID: 17036209
60. Storz G, Vogel J, Wassarman KM (2011) Regulation by small RNAs in bacteria: expanding frontiers. Molecular Cell 43:880-891. doi: 10.1016/j.molcel.2011.08.022 PMID: 21925377
61. Smith NA, Eamens AL, Wang M-B (2011) Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS pathogens 7:e1002022. doi: 10.1371/journal.ppat.1002022 PMID: 21573142
62. Sutton E, Harris S, Parkhill J, Sinkins S (2014) Comparative genome analysis of Wolbachia strain wAu. BMC Genomics 15:928. doi: 10.1186/1471-2164-15-928 PMID: 25341639