Parallel evolution of genome structure and transcriptional landscape in the Epsilonproteobacteria

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Porcelli, Ida ^a   Reuter, Mark ^a   Pearson, Bruce M ^a   Wilhelm, Thomas ^a   van Vliet, Arnoud H M ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSCRIPTOME; UNTRANSLATED RNA;

AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL GENOME; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; EPSILONPROTEOBACTERIA; GENE FUNCTION; GENE STRUCTURE; GENETIC ORGANIZATION; HELICOBACTER PYLORI; MOLECULAR EVOLUTION; NONHUMAN; OPERON; RNA SEQUENCE; SPECIES COMPARISON; TRANSCRIPTION INITIATION SITE; TRANSCRIPTOMICS;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; EPSILONPROTEOBACTERIA; HELICOBACTER PYLORI;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; CAMPYLOBACTER JEJUNI; COMPARATIVE GENOMIC HYBRIDIZATION; CONSERVED SEQUENCE; EPSILONPROTEOBACTERIA; EVOLUTION, MOLECULAR; GENE LIBRARY; GENE ORDER; GENOME, BACTERIAL; PROMOTER REGIONS, GENETIC; PROTEIN SORTING SIGNALS; RNA, BACTERIAL; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84883672449     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-616     Document Type: Article

References (78)

1. Pallen MJ, Wren BW. Bacterial pathogenomics. Nature 2007, 449(7164):835-842.
2. Sorek R, Cossart P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat Rev Genet 2009, 11(1):9-16.
3. Raskin DM, Seshadri R, Pukatzki SU, Mekalanos JJ. Bacterial genomics and pathogen evolution. Cell 2006, 124(4):703-714.
4. Boto L. Horizontal gene transfer in evolution: facts and challenges. Proc Biol Sci 2010, 277(1683):819-827.
5. Haugen SP, Ross W, Gourse RL. Advances in bacterial promoter recognition and its control by factors that do not bind DNA. Nat Rev Microbiol 2008, 6(7):507-519.
6. Papenfort K, Vogel J. Regulatory RNA in bacterial pathogens. Cell Host Microbe 2010, 8(1):116-127.
7. Chao Y, Vogel J. The role of Hfq in bacterial pathogens. Curr Opin Microbiol 2010, 13(1):24-33.
8. Deutscher MP. Degradation of RNA in bacteria: comparison of mRNA and stable RNA. Nucl Acids Res 2006, 34(2):659-666.
9. Wurtzel O, Sapra R, Chen F, Zhu Y, Simmons BA, Sorek R. A single-base resolution map of an archaeal transcriptome. Genome Res 2010, 20(1):133-141.
10. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiß S, Sittka A, Chabas S, Reiche K, Hackermüller J, Reinhardt R, et al. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 2010, 464(7286):250-255.
11. Perkins TT, Kingsley RA, Fookes MC, Gardner PP, James KD, Yu L, Assefa SA, He M, Croucher NJ, Pickard DJ, et al. A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella typhi. PLoS Genet 2009, 5(7):e1000569.
12. Guell M, van Noort V, Yus E, Chen WH, Leigh-Bell J, Michalodimitrakis K, Yamada T, Arumugam M, Doerks T, Kuhner S, et al. Transcriptome complexity in a genome-reduced bacterium. Science 2009, 326(5957):1268-1271.
13. van Vliet AHM. Next generation sequencing of microbial transcriptomes: challenges and opportunities. FEMS Microbiol Lett 2010, 302(1):1-7.
14. Eppinger M, Baar C, Raddatz G, Huson DH, Schuster SC. Comparative analysis of four Campylobacterales. Nat Rev Microbiol 2004, 2(11):872-885.
15. Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K. Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA 2007, 104(29):12146-12150.
16. Voordeckers JW, Starovoytov V, Vetriani C. Caminibacter mediatlanticus sp. nov., a thermophilic, chemolithoautotrophic, nitrate-ammonifying bacterium isolated from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge. Int J Syst Evol Microbiol 2005, 55(Pt 2):773-779.
17. Baar C, Eppinger M, Raddatz G, Simon J, Lanz C, Klimmek O, Nandakumar R, Gross R, Rosinus A, Keller H, et al. Complete genome sequence and analysis of Wolinella succinogenes. Proc Natl Acad Sci USA 2003, 100(20):11690-11695.
18. Miller WG, Parker CT, Rubenfield M, Mendz GL, Wosten MM, Ussery DW, Stolz JF, Binnewies TT, Hallin PF, Wang G, et al. The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PLoS One 2007, 2(12):e1358.
19. Gundogdu O, Bentley SD, Holden MT, Parkhill J, Dorrell N, Wren BW. Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 2007, 8:162.
20. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, Chillingworth T, Davies RM, Feltwell T, Holroyd S, et al. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 2000, 403(6770):665-668.
21. Chaudhuri RR, Yu L, Kanji A, Perkins TT, Gardner PP, Choudhary J, Maskell DJ, Grant AJ. Quantitative RNA-seq analysis of the Campylobacter jejuni transcriptome. Microbiology 2011, 157(Pt 10):2922-2932.
22. Reuter M, Mallett A, Pearson BM, van Vliet AHM. Biofilm formation in Campylobacter jejuni is increased under aerobic conditions. Appl Environ Microbiol 2010, 76(7):2122-2128.
23. Holmes K, Mulholland F, Pearson BM, Pin C, McNicholl-Kennedy J, Ketley JM, Wells JM. Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 2005, 151(Pt 1):243-257.
24. Monk CE, Pearson BM, Mulholland F, Smith HK, Poole RK. Oxygen- and NssR-dependent globin expression and enhanced iron acquisition in the response of Campylobacter to nitrosative stress. J Biol Chem 2008, 283(42):28413-28425.
25. Hinton JC, Hautefort I, Eriksson S, Thompson A, Rhen M. Benefits and pitfalls of using microarrays to monitor bacterial gene expression during infection. Curr Opin Microbiol 2004, 7(3):277-282.
26. Zhang H, Ehrenkaufer GM, Pompey JM, Hackney JA, Singh U. Small RNAs with 5′-polyphosphate termini associate with a Piwi-related protein and regulate gene expression in the single-celled eukaryote Entamoeba histolytica. PLoS Pathog 2008, 4(11):e1000219.
27. Jager D, Sharma CM, Thomsen J, Ehlers C, Vogel J, Schmitz RA. Deep sequencing analysis of the Methanosarcina mazei Go1 transcriptome in response to nitrogen availability. Proc Natl Acad Sci USA 2009, 106(51):21878-21882.
28. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME suite: tools for motif discovery and searching. Nucleic Acids Res 2009, 37(Web Server issue):W202-W208.
29. Dugar G, Herbig A, Forstner KU, Heidrich N, Reinhardt R, Nieselt K, Sharma CM. High-resolution transcriptome maps reveal strain-specific regulatory features of multiple Campylobacter jejuni isolates. PLoS Genet 2013, 9(5):e1003495.
30. Ramachandran VK, Shearer N, Jacob JJ, Sharma CM, Thompson A. The architecture and ppGpp-dependent expression of the primary transcriptome of Salmonella Typhimurium during invasion gene expression. BMC Genomics 2012, 13:25.
31. Kroger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, Chao Y, Sittka A, Hebrard M, Handler K, et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA 2012, 109(20):E1277-E1286.
32. Carrillo CD, Taboada E, Nash JHE, Lanthier P, Kelly J, Lau PC, Verhulp R, Mykytczuk O, Sy J, Findlay WA, et al. Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J Biol Chem 2004, 279(19):20327-20338.
33. Barrero-Tobon AM, Hendrixson DR. Identification and analysis of flagellar coexpressed determinants (Feds) of Campylobacter jejuni involved in colonization. Mol Microbiol 2012, 84(2):352-369.
34. Petersen L, Larsen TS, Ussery DW, On SL, Krogh A. RpoD promoters in Campylobacter jejuni exhibit a strong periodic signal instead of a -35 box. J Mol Biol 2003, 326(5):1361-1372.
35. Friedel M, Nikolajewa S, Suhnel J, Wilhelm T. DiProGB: the dinucleotide properties genome browser. Bioinformatics 2009, 25(19):2603-2604.
36. Friedel M, Nikolajewa S, Suhnel J, Wilhelm T. DiProDB: a database for dinucleotide properties. Nucleic Acids Res 2009, 37(Database issue):D37-D40.
37. Calladine CR, Drew H, Luisi B, Travers A. Understanding DNA, the molecule and how it works 2004, New York: Elsevier Academic Press.
38. Thomason MK, Storz G. Bacterial antisense RNAs: how many are there, and what are they doing?. Annu Rev Genet 2010, 44:167-188.
39. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K, et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459(7249):950-956.
40. Rasmussen S, Nielsen HB, Jarmer H. The transcriptionally active regions in the genome of Bacillus subtilis. Mol Microbiol 2009, 73(6):1043-1057.
41. Raghavan R, Sloan DB, Ochman H. Antisense transcription is pervasive but rarely conserved in enteric bacteria. MBio 2012, 3(4):e00156-12.
42. Gan J, Tropea JE, Austin BP, Court DL, Waugh DS, Ji X. Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell 2006, 124(2):355-366.
43. Giangrossi M, Prosseda G, Tran CN, Brandi A, Colonna B, Falconi M. A novel antisense RNA regulates at transcriptional level the virulence gene icsA of Shigella flexneri. Nucleic Acids Res 2010, 38(10):3362-3375.
44. Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN, Gore J, Wang JX, Lee ER, Block KF, Sudarsan N, et al. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucl Acids Res 2007, 35(14):4809-4819.
45. Valentin-Hansen P, Eriksen M, Udesen C. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 2004, 51(6):1525-1533.
46. Gursinsky T, Grobe D, Schierhorn A, Jager J, Andreesen JR, Sohling B. Factors and selenocysteine insertion sequence requirements for the synthesis of selenoproteins from a gram-positive anaerobe in Escherichia coli. Appl Environ Microbiol 2008, 74(5):1385-1393.
47. Wassarman KM. 6S RNA: a regulator of transcription. Mol Microbiol 2007, 65(6):1425-1431.
48. Barrick JE, Sudarsan N, Weinberg Z, Ruzzo WL, Breaker RR. 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 2005, 11(5):774-784.
49. Wassarman KM, Storz G. 6S RNA regulates E. coli RNA polymerase activity. Cell 2000, 101(6):613-623.
50. Wassarman KM, Saecker RM. Synthesis-mediated release of a small RNA inhibitor of RNA polymerase. Science 2006, 314(5805):1601-1603.
51. Guccione E, Hitchcock A, Hall SJ, Mulholland F, Shearer N, van Vliet AHM, Kelly DJ. Reduction of fumarate, mesaconate and crotonate by Mfr, a novel oxygen-regulated periplasmic reductase in Campylobacter jejuni. Environ Microbiol 2010, 12(3):576-591.
52. Livny J, Waldor MK. Mining regulatory 5′ UTRs from cDNA deep sequencing datasets. Nucl Acids Res 2010, 38(5):1504-1514.
53. Merino E, Jensen RA, Yanofsky C. Evolution of bacterial trp operons and their regulation. Curr Opin Microbiol 2008, 11:78-86.
54. Gaskin DJ, Reuter M, Shearer N, Mulholland F, Pearson BM, van Vliet AHM. Genomics of thermophilic Campylobacter species. Genome Dyn 2009, 6:91-109.
55. Moll I, Grill S, Gualerzi CO, Blasi U. Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 2002, 43(1):239-246.
56. Kaberdina AC, Szaflarski W, Nierhaus KH, Moll I. An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis?. Mol Cell 2009, 33(2):227-236.
57. Gaynor EC, Wells DH, MacKichan JK, Falkow S. The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol Microbiol 2005, 56(1):8-27.
58. Wells DH, Gaynor EC. Helicobacter pylori initiates the stringent response upon nutrient and pH downshift. J Bacteriol 2006, 188(10):3726-3729.
59. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997, 388(6642):539-547.
60. Carver T, Berriman M, Tivey A, Patel C, Bohme U, Barrell BG, Parkhill J, Rajandream MA. Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 2008, 24(23):2672-2676.
61. Brock JE, Pourshahian S, Giliberti J, Limbach PA, Janssen GR. Ribosomes bind leaderless mRNA in Escherichia coli through recognition of their 5′-terminal AUG. RNA 2008, 14(10):2159-2169.
62. Parrish JR, Yu J, Liu G, Hines JA, Chan JE, Mangiola BA, Zhang H, Pacifico S, Fotouhi F, DiRita VJ, et al. A proteome-wide protein interaction map for Campylobacter jejuni. Genome Biol 2007, 8(7):R130.
63. Schluter JP, Reinkensmeier J, Barnett MJ, Lang C, Krol E, Giegerich R, Long SR, Becker A. Global mapping of transcription start sites and promoter motifs in the symbiotic alpha-proteobacterium Sinorhizobium meliloti 1021. BMC Genomics 2013, 14:156.
64. Gilbreath JJ, Cody WL, Merrell DS, Hendrixson DR. Change is good: variations in common biological mechanisms in the epsilonproteobacterial genera Campylobacter and Helicobacter. Microbiol Mol Biol Rev 2011, 75(1):84-132.
65. Campbell BJ, Engel AS, Porter ML, Takai K. The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 2006, 4(6):458-468.
66. Fouts DE, Mongodin EF, Mandrell RE, Miller WG, Rasko DA, Ravel J, Brinkac LM, DeBoy RT, Parker CT, Daugherty SC, et al. Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 2005, 3(1):e15.
67. Eppinger M, Baar C, Linz B, Raddatz G, Lanz C, Keller H, Morelli G, Gressmann H, Achtman M, Schuster SC. Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet 2006, 2(7):e120.
68. Mattatall NR, Sanderson KE. Salmonella typhimurium LT2 possesses three distinct 23S rRNA intervening sequences. J Bacteriol 1996, 178(8):2272-2278.
69. Hoffmann S, Otto C, Kurtz S, Sharma CM, Khaitovich P, Vogel J, Stadler PF, Hackermuller J. Fast mapping of short sequences with mismatches, insertions and deletions using index structures. PLoS Comput Biol 2009, 5(9):e1000502.
70. Nicol JW, Helt GA, Blanchard SG, Raja A, Loraine AE. The integrated genome browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 2009, 25(20):2730-2731.
71. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14(6):1188-1190.
72. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
73. Felsenstein J. PHYLIP - phylogeny inference package (Version 3.2). Cladistics 1989, 5:164-166.
74. Gillespie JJ, Wattam AR, Cammer SA, Gabbard JL, Shukla MP, Dalay O, Driscoll T, Hix D, Mane SP, Mao C, et al. PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect Immun 2011, 79(11):4286-4298.
75. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet 2000, 16(6):276-277.
76. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
77. Mahadevan P, Seto D. Rapid pair-wise synteny analysis of large bacterial genomes using web-based GeneOrder4.0. BMC Res Notes 2010, 3:41.
78. Shaw FL, Mulholland F, Le Gall G, Porcelli I, Hart DJ, Pearson BM, van Vliet AHM. Selenium-dependent biogenesis of formate dehydrogenase in Campylobacter jejuni is controlled by the fdhTU accessory genes. J Bacteriol 2012, 194(15):3814-3823.