title: Parallel evolution of genome structure and transcriptional landscape in the Epsilonproteobacteria.
abstract: BACKGROUND
  Gene reshuffling, point mutations and horizontal gene transfer contribute to bacterial genome variation, but require the genome to rewire its transcriptional circuitry to ensure that inserted, mutated or reshuffled genes are transcribed at appropriate levels. The genomes of Epsilonproteobacteria display very low synteny, due to high levels of reshuffling and reorganisation of gene order, but still share a significant number of gene orthologs allowing comparison. Here we present the primary transcriptome of the pathogenic Epsilonproteobacterium Campylobacter jejuni, and have used this for comparative and predictive transcriptomics in the Epsilonproteobacteria.
  
  
  RESULTS
  Differential RNA-sequencing using 454 sequencing technology was used to determine the primary transcriptome of C. jejuni NCTC 11168, which consists of 992 transcription start sites (TSS), which included 29 putative non-coding and stable RNAs, 266 intragenic (internal) TSS, and 206 antisense TSS. Several previously unknown features were identified in the C. jejuni transcriptional landscape, like leaderless mRNAs and potential leader peptides upstream of amino acid biosynthesis genes. A cross-species comparison of the primary transcriptomes of C. jejuni and the related Epsilonproteobacterium Helicobacter pylori highlighted a lack of conservation of operon organisation, position of intragenic and antisense promoters or leaderless mRNAs. Predictive comparisons using 40 other Epsilonproteobacterial genomes suggests that this lack of conservation of transcriptional features is common to all Epsilonproteobacterial genomes, and is associated with the absence of genome synteny in this subdivision of the Proteobacteria.
  
  
  CONCLUSIONS
  Both the genomes and transcriptomes of Epsilonproteobacteria are highly variable, both at the genome level by combining and division of multicistronic operons, but also on the gene level by generation or deletion of promoter sequences and 5' untranslated regions. Regulatory features may have evolved after these species split from a common ancestor, with transcriptome rewiring compensating for changes introduced by genomic reshuffling and horizontal gene transfer.
authors.affiliation: Gut Health and Food Safety Programme, Institute of Food Research, Colney Lane, Norwich, NR4 7UA, UK. arnoud.vanvliet@ifr.ac.uk.
authors.forename: Ida
authors.initials: I
authors.lastname: Porcelli
authors.forename: Mark
authors.initials: M
authors.lastname: Reuter
authors.forename: Bruce M
authors.initials: BM
authors.lastname: Pearson
authors.forename: Thomas
authors.initials: T
authors.lastname: Wilhelm
authors.forename: Arnoud H M
authors.initials: AH
authors.lastname: van Vliet
mesh_terms: D020121:5' Untranslated Regions; D001483:Base Sequence; D016123:Campylobacter jejuni / Q000235:genetics*; D055028:Comparative Genomic Hybridization; D017124:Conserved Sequence; D020565:Epsilonproteobacteria / Q000235:genetics; D019143:Evolution, Molecular; D015723:Gene Library; D023061:Gene Order; D016680:Genome, Bacterial; D011401:Promoter Regions, Genetic; D021382:Protein Sorting Signals; D012329:RNA, Bacterial / Q000235:genetics; D022661:RNA, Untranslated / Q000235:genetics; D017423:Sequence Analysis, RNA; D024363:Transcription Initiation Site; D014158:Transcription, Genetic; D059467:Transcriptome
chemical_list: D020121:5' Untranslated Regions; D021382:Protein Sorting Signals; D012329:RNA, Bacterial; D022661:RNA, Untranslated
references.citation: Nature. 2010 Mar 11;464(7286):250-5
references.pmid: 20164839
references.citation: Int J Syst Evol Microbiol. 2005 Mar;55(Pt 2):773-779
references.pmid: 15774661
references.citation: Annu Rev Genet. 2010;44:167-88
references.pmid: 20707673
references.citation: J Bacteriol. 2012 Aug;194(15):3814-23
references.pmid: 22609917
references.citation: Cell Host Microbe. 2010 Jul 22;8(1):116-27
references.pmid: 20638647
references.citation: J Biol Chem. 2004 May 7;279(19):20327-38
references.pmid: 14985343
references.citation: Curr Opin Microbiol. 2008 Apr;11(2):78-86
references.pmid: 18374625
references.citation: PLoS Genet. 2009 Jul;5(7):e1000569
references.pmid: 19609351
references.citation: Mol Microbiol. 2012 Apr;84(2):352-69
references.pmid: 22375824
references.citation: Mol Microbiol. 2002 Jan;43(1):239-46
references.pmid: 11849551
references.citation: Bioinformatics. 2007 Nov 1;23(21):2947-8
references.pmid: 17846036
references.citation: Appl Environ Microbiol. 2010 Apr;76(7):2122-8
references.pmid: 20139307
references.citation: Mol Microbiol. 2007 Sep;65(6):1425-31
references.pmid: 17714443
references.citation: Microbiol Mol Biol Rev. 2011 Mar;75(1):84-132
references.pmid: 21372321
references.citation: Nature. 2000 Feb 10;403(6770):665-8
references.pmid: 10688204
references.citation: J Mol Biol. 2003 Mar 7;326(5):1361-72
references.pmid: 12595250
references.citation: Bioinformatics. 2008 Dec 1;24(23):2672-6
references.pmid: 18845581
references.citation: Nat Rev Microbiol. 2006 Jun;4(6):458-68
references.pmid: 16652138
references.citation: Nucleic Acids Res. 2006 Feb 01;34(2):659-66
references.pmid: 16452296
references.citation: Nat Rev Genet. 2010 Jan;11(1):9-16
references.pmid: 19935729
references.citation: Proc Biol Sci. 2010 Mar 22;277(1683):819-27
references.pmid: 19864285
references.citation: Science. 2009 Nov 27;326(5957):1268-71
references.pmid: 19965477
references.citation: BMC Res Notes. 2010 Feb 23;3:41
references.pmid: 20178631
references.citation: Nucleic Acids Res. 2010 Jun;38(10):3362-75
references.pmid: 20129941
references.citation: Bioinformatics. 2009 Oct 15;25(20):2730-1
references.pmid: 19654113
references.citation: Nucleic Acids Res. 2009 Jan;37(Database issue):D37-40
references.pmid: 18805906
references.citation: Genome Biol. 2007;8(7):R130
references.pmid: 17615063
references.citation: J Bacteriol. 1996 Apr;178(8):2272-8
references.pmid: 8636028
references.citation: Trends Genet. 2000 Jun;16(6):276-7
references.pmid: 10827456
references.citation: Proc Natl Acad Sci U S A. 2012 May 15;109(20):E1277-86
references.pmid: 22538806
references.citation: Curr Opin Microbiol. 2010 Feb;13(1):24-33
references.pmid: 20080057
references.citation: Genome Dyn. 2009;6:91-109
references.pmid: 19696496
references.citation: Nature. 2007 Oct 18;449(7164):835-42
references.pmid: 17943120
references.citation: Environ Microbiol. 2010 Mar;12(3):576-91
references.pmid: 19919540
references.citation: Mol Microbiol. 2004 Mar;51(6):1525-33
references.pmid: 15009882
references.citation: BMC Genomics. 2013 Mar 07;14:156
references.pmid: 23497287
references.citation: FEMS Microbiol Lett. 2010 Jan;302(1):1-7
references.pmid: 19735299
references.citation: Nature. 1997 Aug 7;388(6642):539-47
references.pmid: 9252185
references.citation: PLoS Genet. 2006 Jul;2(7):e120
references.pmid: 16789826
references.citation: Nucleic Acids Res. 2010 Mar;38(5):1504-14
references.pmid: 19969537
references.citation: BMC Genomics. 2012 Jan 17;13:25
references.pmid: 22251276
references.citation: Nature. 2009 Jun 18;459(7249):950-6
references.pmid: 19448609
references.citation: Mol Cell. 2009 Jan 30;33(2):227-36
references.pmid: 19187763
references.citation: Nat Rev Microbiol. 2008 Jul;6(7):507-19
references.pmid: 18521075
references.citation: Microbiology (Reading). 2011 Oct;157(Pt 10):2922-2932
references.pmid: 21816880
references.citation: Genome Res. 2004 Jun;14(6):1188-90
references.pmid: 15173120
references.citation: RNA. 2005 May;11(5):774-84
references.pmid: 15811922
references.citation: Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11690-5
references.pmid: 14500908
references.citation: Cell. 2006 Jan 27;124(2):355-66
references.pmid: 16439209
references.citation: mBio. 2012 Aug 07;3(4):
references.pmid: 22872780
references.citation: J Biol Chem. 2008 Oct 17;283(42):28413-25
references.pmid: 18682395
references.citation: Genome Res. 2010 Jan;20(1):133-41
references.pmid: 19884261
references.citation: Nat Rev Microbiol. 2004 Nov;2(11):872-85
references.pmid: 15494744
references.citation: PLoS One. 2007 Dec 26;2(12):e1358
references.pmid: 18159241
references.citation: Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):12146-50
references.pmid: 17615243
references.citation: Microbiology (Reading). 2005 Jan;151(Pt 1):243-257
references.pmid: 15632442
references.citation: Proc Natl Acad Sci U S A. 2009 Dec 22;106(51):21878-82
references.pmid: 19996181
references.citation: RNA. 2008 Oct;14(10):2159-69
references.pmid: 18755843
references.citation: Nucleic Acids Res. 2007;35(14):4809-19
references.pmid: 17621584
references.citation: Cell. 2006 Feb 24;124(4):703-14
references.pmid: 16497582
references.citation: PLoS Biol. 2005 Jan;3(1):e15
references.pmid: 15660156
references.citation: Curr Opin Microbiol. 2004 Jun;7(3):277-82
references.pmid: 15196496
references.citation: J Bacteriol. 2006 May;188(10):3726-9
references.pmid: 16672627
references.citation: BMC Genomics. 2007 Jun 12;8:162
references.pmid: 17565669
references.citation: Science. 2006 Dec 8;314(5805):1601-3
references.pmid: 17158328
references.citation: Cell. 2000 Jun 9;101(6):613-23
references.pmid: 10892648
references.citation: PLoS Genet. 2013 May;9(5):e1003495
references.pmid: 23696746
references.citation: PLoS Comput Biol. 2009 Sep;5(9):e1000502
references.pmid: 19750212
references.citation: Infect Immun. 2011 Nov;79(11):4286-98
references.pmid: 21896772
references.citation: PLoS Pathog. 2008 Nov;4(11):e1000219
references.pmid: 19043551
references.citation: Mol Microbiol. 2005 Apr;56(1):8-27
references.pmid: 15773975
references.citation: Bioinformatics. 2009 Oct 1;25(19):2603-4
references.pmid: 19605418
references.citation: J Mol Biol. 1990 Oct 5;215(3):403-10
references.pmid: 2231712
references.citation: Appl Environ Microbiol. 2008 Mar;74(5):1385-93
references.pmid: 18165360
references.citation: Nucleic Acids Res. 2009 Jul;37(Web Server issue):W202-8
references.pmid: 19458158
references.citation: Mol Microbiol. 2009 Sep;73(6):1043-57
references.pmid: 19682248