Dialects of the DNA Uptake Sequence in
In all sexual organisms, adaptations exist that secure the safe reassortment of homologous alleles and prevent the intrusion of potentially hazardous alien DNA. Some bacteria engage in a simple form of sex known as transformation. In the human pathogen Neisseria meningitidis and in related bacterial species, transformation by exogenous DNA is regulated by the presence of a specific DNA Uptake Sequence (DUS), which is present in thousands of copies in the respective genomes. DUS affects transformation by limiting DNA uptake and recombination in favour of homologous DNA. The specific mechanisms of DUS–dependent genetic transformation have remained elusive. Bioinformatic analyses of family Neisseriaceae genomes reveal eight distinct variants of DUS. These variants are here termed DUS dialects, and their effect on interspecies commutation is demonstrated. Each of the DUS dialects is remarkably conserved within each species and is distributed consistent with a robust Neisseriaceae phylogeny based on core genome sequences. The impact of individual single nucleotide transversions in DUS on meningococcal transformation and on DNA binding and uptake is analysed. The results show that a DUS core 5′-CTG-3′ is required for transformation and that transversions in this core reduce DNA uptake more than two orders of magnitude although the level of DNA binding remains less affected. Distinct DUS dialects are efficient barriers to interspecies recombination in N. meningitidis, N. elongata, Kingella denitrificans, and Eikenella corrodens, despite the presence of the core sequence. The degree of similarity between the DUS dialect of the recipient species and the donor DNA directly correlates with the level of transformation and DNA binding and uptake. Finally, DUS–dependent transformation is documented in the genera Eikenella and Kingella for the first time. The results presented here advance our understanding of the function and evolution of DUS and genetic transformation in bacteria, and define the phylogenetic relationships within the Neisseriaceae family.
Vyšlo v časopise:
Dialects of the DNA Uptake Sequence in. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003458
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003458
Souhrn
In all sexual organisms, adaptations exist that secure the safe reassortment of homologous alleles and prevent the intrusion of potentially hazardous alien DNA. Some bacteria engage in a simple form of sex known as transformation. In the human pathogen Neisseria meningitidis and in related bacterial species, transformation by exogenous DNA is regulated by the presence of a specific DNA Uptake Sequence (DUS), which is present in thousands of copies in the respective genomes. DUS affects transformation by limiting DNA uptake and recombination in favour of homologous DNA. The specific mechanisms of DUS–dependent genetic transformation have remained elusive. Bioinformatic analyses of family Neisseriaceae genomes reveal eight distinct variants of DUS. These variants are here termed DUS dialects, and their effect on interspecies commutation is demonstrated. Each of the DUS dialects is remarkably conserved within each species and is distributed consistent with a robust Neisseriaceae phylogeny based on core genome sequences. The impact of individual single nucleotide transversions in DUS on meningococcal transformation and on DNA binding and uptake is analysed. The results show that a DUS core 5′-CTG-3′ is required for transformation and that transversions in this core reduce DNA uptake more than two orders of magnitude although the level of DNA binding remains less affected. Distinct DUS dialects are efficient barriers to interspecies recombination in N. meningitidis, N. elongata, Kingella denitrificans, and Eikenella corrodens, despite the presence of the core sequence. The degree of similarity between the DUS dialect of the recipient species and the donor DNA directly correlates with the level of transformation and DNA binding and uptake. Finally, DUS–dependent transformation is documented in the genera Eikenella and Kingella for the first time. The results presented here advance our understanding of the function and evolution of DUS and genetic transformation in bacteria, and define the phylogenetic relationships within the Neisseriaceae family.
Zdroje
1. ThomasCM, NielsenKM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3: 711–721.
2. JohnsborgO, EldholmV, HavarsteinLS (2007) Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol 158: 767–778.
3. RobertsMS, CohanFM (1993) The effect of DNA sequence divergence on sexual isolation in Bacillus. Genetics 134: 401–408.
4. MajewskiJ (2001) Sexual isolation in bacteria. FEMS Microbiol Lett 199: 161–169.
5. TortosaP, DubnauD (1999) Competence for transformation: a matter of taste. Curr Opin Microbiol 2: 588–592.
6. DannerDB, DeichRA, SiscoKL, SmithHO (1980) An eleven-base-pair sequence determines the specificity of DNA uptake in Haemophilus transformation. Gene 11: 311–318.
7. GoodmanSD, ScoccaJJ (1988) Identification and arrangement of the DNA sequence recognized in specific transformation of Neisseria gonorrhoeae. Proc Natl Acad Sci U S A 85: 6982–6986.
8. SmithHO, GwinnML, SalzbergSL (1999) DNA uptake signal sequences in naturally transformable bacteria. Res Microbiol 150: 603–616.
9. DavidsenT, RodlandEA, LagesenK, SeebergE, RognesT, et al. (2004) Biased distribution of DNA uptake sequences towards genome maintenance genes. Nucleic Acids Res 32: 1050–1058.
10. TettelinH, SaundersNJ, HeidelbergJ, JeffriesAC, NelsonKE, et al. (2000) Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287: 1809–1815.
11. TreangenTJ, AmburOH, TønjumT, RochaEP (2008) The impact of the neisserial DNA uptake sequences on genome evolution and stability. Genome Biol 9: R60.
12. ElkinsC, ThomasCE, SeifertHS, SparlingPF (1991) Species-specific uptake of DNA by gonococci is mediated by a 10-base-pair sequence. J Bacteriol 173: 3911–3913.
13. GravesJF, BiswasGD, SparlingPF (1982) Sequence-specific DNA uptake in transformation of Neisseria gonorrhoeae. J Bacteriol 152: 1071–1077.
14. AmburOH, FryeSA, TønjumT (2007) New functional identity for the DNA uptake sequence in transformation and its presence in transcriptional terminators. J Bacteriol 189: 2077–2085.
15. DuffinPM, SeifertHS (2010) DNA uptake sequence-mediated enhancement of transformation in Neisseria gonorrhoeae is strain dependent. J Bacteriol 192: 4436–4444.
16. AasFE, LovoldC, KoomeyM (2002) An inhibitor of DNA binding and uptake events dictates the proficiency of genetic transformation in Neisseria gonorrhoeae: mechanism of action and links to Type IV pilus expression. Mol Microbiol 46: 1441–1450.
17. AasFE, WolfgangM, FryeS, DunhamS, LovoldC, et al. (2002) Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol Microbiol 46: 749–760.
18. CehovinA, SimpsonPJ, McDowellMA, BrownDR, NoscheseR, et al. (2013) Specific DNA recognition mediated by a type IV pilin. Proc Natl Acad Sci U S A
19. GoodmanSD, ScoccaJJ (1991) Factors influencing the specific interaction of Neisseria gonorrhoeae with transforming DNA. J Bacteriol 173: 5921–5923.
20. AmburOH, FryeSA, NilsenM, HovlandE, TonjumT (2012) Restriction and sequence alterations affect DNA uptake sequence-dependent transformation in Neisseria meningitidis. PLoS ONE 7: e39742 doi:10.1371/journal.pone.0039742.
21. RedfieldRJ, FindlayWA, BosseJ, KrollJS, CameronAD, et al. (2006) Evolution of competence and DNA uptake specificity in the Pasteurellaceae. BMC Evol Biol 6: 82.
22. QvarnstromY, SwedbergG (2006) Variations in gene organization and DNA uptake signal sequence in the folP region between commensal and pathogenic Neisseria species. BMC Microbiol 6: 11.
23. HigashiDL, BiaisN, WeyandNJ, AgellonA, SiskoJL, et al. (2011) N. elongata produces type IV pili that mediate interspecies gene transfer with N. gonorrhoeae. PLoS ONE 6: e21373 doi:10.1371/journal.pone.0021373.
24. PazA, KirzhnerV, NevoE, KorolA (2006) Coevolution of DNA-interacting proteins and genome “dialect”. Mol Biol Evol 23: 56–64.
25. BudroniS, SienaE, Dunning HotoppJC, SeibKL, SerrutoD, et al. (2011) Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination. Proc Natl Acad Sci U S A 108: 4494–4499.
26. TurnbaughPJ, LeyRE, HamadyM, Fraser-LiggettCM, KnightR, et al. (2007) The human microbiome project. Nature 449: 804–810.
27. SchoenC, BlomJ, ClausH, Schramm-GluckA, BrandtP, et al. (2008) Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc Natl Acad Sci U S A 105: 3473–3478.
28. MarriPR, PaniscusM, WeyandNJ, RendonMA, CaltonCM, et al. (2010) Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS ONE 5: e11835 doi:10.1371/journal.pone.0011835.
29. HaoW, MaJH, WarrenK, TsangRS, LowDE, et al. (2011) Extensive genomic variation within clonal complexes of Neisseria meningitidis. Genome Biol Evol 3: 1406–1418.
30. BennettJS, JolleyKA, EarleSG, CortonC, BentleySD, et al. (2012) A genomic approach to bacterial taxonomy: an examination and proposed reclassification of species within the genus Neisseria. Microbiology 158: 1570–1580.
31. YiH, ChoYJ, YoonSH, ParkSC, ChunJ (2011) Comparative genomics of Neisseria weaveri clarifies the taxonomy of this species and identifies genetic determinants that may be associated with virulence. FEMS Microbiol Lett
32. Fitz-GibbonST, HouseCH (1999) Whole genome-based phylogenetic analysis of free-living microorganisms. Nucleic Acids Res 27: 4218–4222.
33. SnelB, BorkP, HuynenMA (1999) Genome phylogeny based on gene content. Nat Genet 21: 108–110.
34. KovacsAT, SmitsWK, MironczukAM, KuipersOP (2009) Ubiquitous late competence genes in Bacillus species indicate the presence of functional DNA uptake machineries. Environ Microbiol 11: 1911–1922.
35. DubnauD (1999) DNA uptake in bacteria. Annu Rev Microbiol 53: 217–244.
36. LorenzMG, WackernagelW (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58: 563–602.
37. ClaverysJP, MartinB (2003) Bacterial “competence” genes: signatures of active transformation, or only remnants? Trends Microbiol 11: 161–165.
38. VosM (2009) Why do bacteria engage in homologous recombination? Trends Microbiol 17: 226–232.
39. BurgeC, CampbellAM, KarlinS (1992) Over- and under-representation of short oligonucleotides in DNA sequences. Proc Natl Acad Sci U S A 89: 1358–1362.
40. CoenyeT, VandammeP (2004) Use of the genomic signature in bacterial classification and identification. Syst Appl Microbiol 27: 175–185.
41. HalpernD, ChiapelloH, SchbathS, RobinS, Hennequet-AntierC, et al. (2007) Identification of DNA motifs implicated in maintenance of bacterial core genomes by predictive modeling. PLoS Genet 3: e153 doi:10.1371/journal.pgen.0030153.
42. SouriceS, BiaudetV, El KarouiM, EhrlichSD, GrussA (1998) Identification of the Chi site of Haemophilus influenzae as several sequences related to the Escherichia coli Chi site. Mol Microbiol 27: 1021–1029.
43. KingsfordCL, AyanbuleK, SalzbergSL (2007) Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 8: R22.
44. SprattBG, BowlerLD, ZhangQY, ZhouJ, SmithJM (1992) Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species. J Mol Evol 34: 115–125.
45. SprattBG, ZhangQY, JonesDM, HutchisonA, BranniganJA, et al. (1989) Recruitment of a penicillin-binding protein gene from Neisseria flavescens during the emergence of penicillin resistance in Neisseria meningitidis. Proc Natl Acad Sci U S A 86: 8988–8992.
46. ZhouJ, BowlerLD, SprattBG (1997) Interspecies recombination, and phylogenetic distortions, within the glutamine synthetase and shikimate dehydrogenase genes of Neisseria meningitidis and commensal Neisseria species. Mol Microbiol 23: 799–812.
47. SmithNH, HolmesEC, DonovanGM, CarpenterGA, SprattBG (1999) Networks and groups within the genus Neisseria: analysis of argF, recA, rho, and 16S rRNA sequences from human Neisseria species. Mol Biol Evol 16: 773–783.
48. FeilEJ, MaidenMC, AchtmanM, SprattBG (1999) The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis. Mol Biol Evol 16: 1496–1502.
49. LinzB, SchenkerM, ZhuP, AchtmanM (2000) Frequent interspecific genetic exchange between commensal Neisseriae and Neisseria meningitidis. Mol Microbiol 36: 1049–1058.
50. HolmesB, CostasM, OnSL, VandammeP, FalsenE, et al. (1993) Neisseria weaveri sp. nov. (formerly CDC group M-5), from dog bite wounds of humans. Int J Syst Bacteriol 43: 687–693.
51. AndersenBM, SteigerwaltAG, O'ConnorSP, HollisDG, WeyantRS, et al. (1993) Neisseria weaveri sp. nov., formerly CDC group M-5, a gram-negative bacterium associated with dog bite wounds. J Clin Microbiol 31: 2456–2466.
52. HanageWP, FraserC, SprattBG (2005) Fuzzy species among recombinogenic bacteria. BMC Biol 3: 6.
53. BakkaliM (2007) Genome dynamics of short oligonucleotides: the example of bacterial DNA uptake enhancing sequences. PLoS ONE 2: e741 doi:10.1371/journal.pone.0000741.
54. MaughanH, WilsonLA, RedfieldRJ (2010) Bacterial DNA uptake sequences can accumulate by molecular drive alone. Genetics 186: 613–627.
55. BowlerLD, ZhangQY, RiouJY, SprattBG (1994) Interspecies recombination between the penA genes of Neisseria meningitidis and commensal Neisseria species during the emergence of penicillin resistance in N. meningitidis: natural events and laboratory simulation. J Bacteriol 176: 333–337.
56. KrollJS, WilksKE, FarrantJL, LangfordPR (1998) Natural genetic exchange between Haemophilus and Neisseria: intergeneric transfer of chromosomal genes between major human pathogens. Proc Natl Acad Sci U S A 95: 12381–12385.
57. AlbrittonWL, SetlowJK, ThomasML, SottnekFO (1986) Relatedness within the Family Pasteurellaceae as Determined by Genetic Transformation. International Journal of Systematic Bacteriology 36: 103–106.
58. TønjumT, HagenN, BøvreK (1985) Identification of Eikenella corrodens and Cardiobacterium hominis by genetic transformation. Acta Pathol Microbiol Immunol Scand B 93: 389–394.
59. BøvreK (1964) Studies on Transformation in Moraxella and Organisms Assumed to Be Related to Moraxella. 1. a Method for Quantitative Transformation in Moraxella and Neisseria, with Streplomycin Resistance as the Genetic Marker. Acta Pathol Microbiol Scand 61: 457–473.
60. RiceP, LongdenI, BleasbyA (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276–277.
61. CrooksGE, HonG, ChandoniaJ-M, BrennerSE (2004) WebLogo: A Sequence Logo Generator. Genome Res 14: 1188–1190.
62. MeyerF, GoesmannA, McHardyAC, BartelsD, BekelT, et al. (2003) GenDB–an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31: 2187–2195.
63. LaingC, BuchananC, TaboadaEN, ZhangY, KropinskiA, et al. (2010) Pan-genome sequence analysis using Panseq: an online tool for the rapid analysis of core and accessory genomic regions. BMC Bioinformatics 11: 461.
64. KorbelJO, SnelB, HuynenMA, BorkP (2002) SHOT: a web server for the construction of genome phylogenies. Trends Genet 18: 158–162.
65. DarlingAE, MauB, PernaNT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147 doi:10.1371/journal.pone.0011147.
66. TreangenTJ, MesseguerX (2006) M-GCAT: interactively and efficiently constructing large-scale multiple genome comparison frameworks in closely related species. BMC Bioinformatics 7: 433.
67. BlomJ, AlbaumSP, DoppmeierD, PuhlerA, VorholterFJ, et al. (2009) EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10: 154.
68. HenriksenSD, HoltenE (1976) Neisseria elongata subsp. glycolytica subsp. nov. International Journal of Systematic Bacteriology October 1976: 478–481.
69. BøvreK, FrøholmLO, HenriksenSD, HoltenE (1977) Relationship of Neisseria elongata subsp. glycolytica to other members of the family Neisseriaceae. Acta Pathol Microbiol Scand B 85B: 18–26.
70. ToriiN, NozakiT, MasutaniM, NakagamaH, SugiyamaT, et al. (2003) Spontaneous mutations in the Helicobacter pylori rpsL gene. Mutat Res 535: 141–145.
71. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 4
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- The G4 Genome
- Neutral Genomic Microevolution of a Recently Emerged Pathogen, Serovar Agona
- The Histone Demethylase Jarid1b Ensures Faithful Mouse Development by Protecting Developmental Genes from Aberrant H3K4me3
- The Tissue-Specific RNA Binding Protein T-STAR Controls Regional Splicing Patterns of Pre-mRNAs in the Brain