Defining the Bacteroides ribosomal binding site

Applied and Environmental Microbiology

Volumn 79, Issue 6, 2013, Pages 1980-1989

  Wegmann, Udo ^a   Horn, Nikki ^a   Carding, Simon R ^a,b  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA; BACTERIAL SPECIES; BACTEROIDES; BACTEROIDETES; CORE REGION; EXPRESSION VECTORS; GASTROINTESTINAL TRACT; GENETIC TOOLS; HUMAN COLON; LACTOBACILLUS DELBRUECKII; PROTEIN EXPRESSIONS; REPORTER GENE; RIBOSOMAL PROTEIN GENES; SEQUENCE LOGOS; TRANSCRIPTION INITIATION; UNTRANSLATED REGIONS;

GENES; PROTEINS; RNA; TRANSCRIPTION;

BACTERIA;

MESSENGER RNA; RIBOSOME RNA;

BACTERIUM; COMMENSAL; GENE; PROTEIN; SIGNAL; STOMACH CONTENT;

5' UNTRANSLATED REGION; ARTICLE; BACTEROIDES; BINDING SITE; GENE EXPRESSION; GENE VECTOR; GENETICS; METABOLISM; METHODOLOGY; MICROBIAL GENETICS; MOLECULAR BIOLOGY; PROTEIN SYNTHESIS; RIBOSOME;

5' UNTRANSLATED REGIONS; BACTEROIDES; BINDING SITES; GENE EXPRESSION; GENETIC VECTORS; GENETICS, MICROBIAL; MOLECULAR BIOLOGY; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, RIBOSOMAL;

EID: 84874805852     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03086-12     Document Type: Article

References (61)

1. Berg RD. 1996. The indigenous gastrointestinal microflora. Trends Microbiol. 4:430-435.
2. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. 2005. Diversity of the human intestinal microbial flora. Science 308:1635-1638.
3. Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, Dore J. 1999. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 65:4799-4807.
4. Tap J, Mondot S, Levenez F, Pelletier E, Caron C, Furet JP, Ugarte E, Munoz-Tamayo R, Paslier DLE, Nalin R, Dore J, Leclerc M. 2009. Towards the human intestinal microbiota phylogenetic core. Environ. Microbiol. 11:2574 -2584.
5. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze XL, Brown D, Stares MD, Scott P, Bergerat A, Louis P, McIntosh F, Johnstone AM, Lobley GE, Parkhill J, Flint HJ. 2011. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 5:220 -230.
6. Flint H, Scott K, Duncan S, Louis P, Forano E. 2012. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3:289 -306.
7. Cebra JJ. 1999. Influences of microbiota on intestinal immune system development. Am. J. Clin. Nutr. 69:1046S-1051S.
8. Xavier RJ, Podolsky DK. 2007. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448:427- 434.
9. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. 2006. Microbial ecology: human gut microbes associated with obesity. Nature 444:1022-1023.
10. Qin JJ, Li RQ, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li JH, Xu JM, Li SC, Li DF, Cao JJ, Wang B, Liang HQ, Zheng HS, Xie YL, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu HM, Yu C, Li ST, Jian M, Zhou Y, Li YR, Zhang XQ, Li SG, Qin N, Yang HM, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Bork P, Ehrlich SD, Wang J, MetaHIT Consortium. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59-65.
11. Woese CR. 1987. Bacterial evolution. Microbiol. Rev. 51:221-271.
12. Kunsman JE, Caldwell DR. 1974. Comparison of the sphingolipid content of rumen Bacteroides species. Appl. Microbiol. 28:1088 -1089.
13. Bayley DP, Rocha ER, Smith CJ. 2000. Analysis of cepA and other Bacteroides fragilis genes reveals a unique promoter structure. FEMS Microbiol. Lett. 193:149 -154.
14. Vingadassalom D, Kolb A, Mayer C, Rybkine T, Collatz E, Podglajen I. 2005. An unusual primary sigma factor in the Bacteroidetes phylum. Mol. Microbiol. 56:888 -902.
15. Smith CJ, Rogers MB, McKee ML. 1992. Heterologous gene expression in Bacteroides fragilis. Plasmid 27:141-154.
16. Shine J, Dalgarno L. 1975. Determinant of cistron specificity in bacterial ribosomes. Nature 254:34 -38.
17. Mastropaolo MD, Thorson ML, Stevens AM. 2009. Comparison of Bacteroides thetaiotaomicron and Escherichia coli 16S rRNA gene expression signals. Microbiology 155:2683-2693.
18. Tribble GD, Parker AC, Smith CJ. 1999. Genetic structure and transcriptional analysis of a mobilizable, antibiotic resistance transposon from Bacteroides. Plasmid 42:1-12.
19. Band L, Henner DJ. 1984. Bacillus subtilis requires a "stringent" Shine- Dalgarno region for gene expression. DNA 3:17-21.
20. Accetto T, Avgustin G. 2011. Inability of Prevotella bryantii to form a functional Shine-Dalgarno interaction reflects unique evolution of ribosome binding sites in Bacteroidetes. PLoS One 6:e22914. doi:10.1371 /journal.pone.0022914.
21. Klein JR, Schmidt U, Plapp R. 1994. Cloning, heterologous expression, and sequencing of a novel proline iminopeptidase gene, pepI, from Lactobacillus delbrueckii subsp. lactis DSM 7290. Microbiology 140:1133-1139.
22. Yaron A, Naider F. 1993. Proline-dependent structural and biological properties of peptides and proteins. Crit. Rev. Biochem. Mol. Biol. 28:31- 81.
23. Shoemaker NB, Getty C, Gardner JF, Salyers AA. 1986. Tn4351 transposes in Bacteroides spp. and mediates the integration of plasmid R751 into the Bacteroides chromosome. J. Bacteriol. 165:929 -936.
24. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16:276 -277.
25. Feldhaus MJ, Hwa V, Cheng Q, Salyers AA. 1991. Use of an Escherichia coli B-glucuronidase gene as a reporter gene for investigation of Bacteroides promoters. J. Bacteriol. 173:4540-4543.
26. Tancula E, Feldhaus MJ, Bedzyk LA, Salyers AA. 1992. Location and characterization of genes involved in binding of starch to the surface of Bacteroides thetaiotaomicron. J. Bacteriol. 174:5609 -5616.
27. Wegmann U, Klein JR, Drumm I, Kuipers OP, Henrich B. 1999. Introduction of peptidase genes from Lactobacillus delbrueckii subsp. lactis into Lactococcus lactis and controlled expression. Appl. Environ. Microbiol. 65:4729-4733.
28. Smith CJ, Rollins LA, Parker AC. 1995. Nucleotide sequence determination and genetic analysis of the Bacteroides plasmid, pBI143. Plasmid 34:211-222.
29. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI. 2003. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299:2074 -2076.
30. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P, Cordum H, Van Brunt A, Kim K, Fulton RS, Fulton LA, Clifton SW, Wilson RK, Knight RD, Gordon JI. 2007. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol. 5:e156. doi:10.1371/journal.pbio.0050156.
31. Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, Coutinho PM, Henrissat B, Nelson KE, Bacteria NACR. 2010. Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb. Ecol. 60:721-729.
32. Brosius J, Palmer ML, Kennedy PJ, Noller HF. 1978. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 75:4801- 4805.
33. Ehresmann C, Stiegler P, Mackie GA, Zimmermann RA, Ebel JP, Fellner P. 1975. Primary sequence of the 16S ribosomal RNA of Escherichia coli. Nucleic Acids Res. 2:265-278.
34. Murray CL, Rabinowitz JC. 1982. Nucleotide sequences of transcription and translation initiation regions in Bacillus phage phi-29 early genes. J. Biol. Chem. 257:1053-1062.
35. Van Charldorp R, Van Kimmenade AM, Van Knippenberg PH. 1981. Sequence and secondary structure of the colicin fragment of Bacillus stearothermophilus 16S ribosomal RNA. Nucleic Acids Res. 9:4909-4917.
36. Chiaruttini C, Milet M. 1993. Gene organization, primary structure and RNA processing analysis of a ribosomal RNA operon in Lactococcus lactis. J. Mol. Biol. 230:57-76.
37. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessieres P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Codani JJ, Connerton IF, Cummings NJ, Daniel RA, Denizot F, Devine KM, Dusterhoft A, Ehrlich SD, Emmerson PT, Entian KD, Errington J, Fabret C, Ferrari E, Foulger D, Fritz C, Fujita M, Fujita Y, Fuma S, Galizzi A, Galleron N, Ghim SY, Glaser P, Goffeau A, Golightly EJ, Grandi G, Guiseppi G, Guy BJ, Haga K, Haiech J, Harwood CR, Henaut A, Hilbert H, Holsappel S, Hosono S, Hullo MF, Itaya M, Jones L, Joris B, Karamata D, Kasahara Y, Klaerr-Blanchard M, Klein C, Kobayashi Y, Koetter P, Koningstein G, Krogh S, Kumano M, Kurita K, Lapidus A, Lardinois S, Lauber J, Lazarevic V, Lee SM, Levine A, Liu H, Masuda S, Mauel C, Medigue C, Medina N, Mellado RP, Mizuno M, Moestl D, Nakai S, Noback M, Noone D, O'Reilly M, Ogawa K, Ogiwara A, Oudega B, Park SH, Parro V, Pohl TM, Portetelle D, Porwollik S, Prescott AM, Presecan E, Pujic P, Purnelle B, Rapoport G, Rey M, Reynolds S, Rieger M, Rivolta C, Rocha E, Roche B, Rose M, Sadaie Y, Sato T, Scanlan E, Schleich S, Schroeter R, Scoffone F, Sekiguchi J, Sekowska A, Seror SJ, Serror P, Shin B-S, Soldo B, Sorokin A, Tacconi E, Takagi T, Takahashi H, Takemaru K, Takeuchi M, Tamakoshi A, Tanaka T, Terpstra P, Tognoni A, Tosato V, Uchiyama S, Vandenbol M, Vannier F, Vassarotti A, Viari A, Wambutt R, Wedler E, Wedler H, Weitzenegger T, Winters P, Wipat A, Yamamoto H, Yamane K, Yasumoto K, Yata K, Yoshida K, Yoshikawa H-F, Zumstein E, Yoshikawa H, Danchin A. 1997. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249 -256.
38. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453- 1462.
39. Wegmann U, O'Connell-Motherway M, Zomer AL, Buist G, Shearman C, Canchaya C, Ventura M, Goesmann A, Gasson M, Kuipers O, van Sinderen D, Kok J. 2007. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol. 189:3256 -3270.
40. Ma J, Campbell A, Karlin S. 2002. Correlations between Shine-Dalgarno sequences and gene features such as predicted expression levels and operon structures. J. Bacteriol. 184:5733-5745.
41. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188 -1190.
42. Schneider TD, Stephens RM. 1990. Sequence Logos: a new way to display consensus sequences. Nucleic Acids Res. 18:6097- 6100.
43. Kuipers OP, Beerthuyzen MM, Siezen RJ, Devos WM. 1993. Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis: requirement of expression of the nisA and nisI genes for development of immunity. Eur. J. Biochem. 216:281-291.
44. Sorensen MA, Fricke J, Pedersen S. 1998. Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J. Mol. Biol. 280:561-569.
45. Nakagawa S, Niimura Y, Miura K, Gojobori T. 2010. Dynamic evolution of translation initiation mechanisms in prokaryotes. Proc. Natl. Acad. Sci. U. S. A. 107:6382- 6387.
46. Boni IV, Isaeva DM, Musychenko ML, Tzareva NV. 1991. Ribosomemessenger recognition: mRNA target sites for ribosomal protein S1. Nucleic Acids Res. 19:155-162.
47. Gallie DR, Kado CI. 1989. A translational enhancer derived from tobacco mosaic virus is functionally equivalent to a Shine-Dalgarno sequence. Proc. Natl. Acad. Sci. U. S. A. 86:129 -132.
48. Lim K, Furuta Y, Kobayashi I. 2012. Large variations in bacterial ribosomal RNA genes. Mol. Biol. Evol. 29:2937-2948.
49. Moll I, Grill S, Gualerzi CO, Blasi U. 2002. Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol. Microbiol. 43:239 -246.
50. Chen HY, Bjerknes M, Kumar R, Jay E. 1994. Determination of the optimal aligned spacing between the Shine-Dalgarno sequence and the translation initiation codon of Escherichia coli messenger RNAs. Nucleic Acids Res. 22:4953- 4957.
51. He JL, Sakaguchi K, Suzuki T. 2012. Determination of the ribosome binding sequence and spacer length between binding site and initiation codon for efficient protein expression in Bifidobacterium longum 105-A. J. Biosci. Bioeng. 113:442- 444.
52. Vellanoweth RL, Rabinowitz JC. 1992. The influence of ribosome binding site elements on translational efficiency in Bacillus subtilis and Escherichia coli in vivo. Mol. Microbiol. 6:1105-1114.
53. Kozak M. 2005. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361:13-37.
54. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406 -3415.
55. Higo K, Otaka E, Osawa S. 1982. Purification and characterization of 30S ribosomal proteins from Bacillus subtilis: correlation to Escherichia coli 30S proteins. Mol. Gen. Genet. 185:239 -244.
56. Kleerebezem M, Beerthuyzen MM, Vaughan E, de Vos WM, Kuipers OP. 1997. Controlled gene expression systems for lactic acid bacteria: transferable nisin-inducible expression cassettes for Lactococcus, Leuconostoc, and Lactobacillus spp. Appl. Environ. Microbiol. 63:4581- 4584.
57. Roberts MW, Rabinowitz JC. 1989. The effect of Escherichia coli ribosomal protein S1 on the translational specificity of bacterial ribosomes. J. Biol. Chem. 264:2228 -2235.
58. Sorokin A, Serror P, Pujic P, Azevedo V, Ehrlich SD. 1995. The Bacillus subtilis chromosome region encoding homologs of the Escherichia coli mssA and rpsA gene products. Microbiology 141:311-319.
59. Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A. 2001. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res. 11:731- 753.
60. Salah P, Bisaglia M, Aliprandi P, Uzan M, Sizun C, Bontems F. 2009. Probing the relationship between Gram-negative and Gram-positive S1 proteins by sequence analysis. Nucleic Acids Res. 37:5578 -5588.
61. Whitehead TR. 1997. Development of a bifunctional xylosidase/ arabinosidase gene as a reporter gene for the Gram-negative anaerobes Bacteroides and Porphyromonas, and Escherichia coli. Curr. Microbiol. 35: 282-286.