Characterization of a novel riboswitch-regulated lysine transporter in Aggregatibacter actinomycetemcomitans

Journal of Bacteriology

Volumn 192, Issue 23, 2010, Pages 6240-6250

  Jorth, Peter ^a   Whiteley, Marvin ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; BACTERIAL RNA; LYSINE;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BIOFILM; BIOINFORMATICS; CONTROLLED STUDY; GENETIC CONSERVATION; HAEMOPHILUS INFLUENZAE; LYST GENE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY RNA SEQUENCE; RIBOSWITCH; SPECIES DIFFERENCE; TRANSCRIPTION INITIATION SITE;

COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION, BACTERIAL; HAEMOPHILUS INFLUENZAE; LYSINE; MEMBRANE TRANSPORT PROTEINS; PASTEURELLACEAE; RIBOSWITCH;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; MAMMALIA;

EID: 78649341146     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00935-10     Document Type: Article

References (61)

1. Abe, N., A. Baba, R. Takii, K. Nakayama, A. Kamaguchi, Y. Shibata, Y. Abiko, K. Okamoto, T. Kadowaki, and K. Yamamoto. 2004. Roles of Argand Lys-gingipains in coaggregation of Porphyromonas gingivalis: identification of its responsible molecules in translation products of rgpA, kgp, and hagA genes. Biol. Chem. 385:1041-1047.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Altschul, S. F., J. C. Wootton, E. M. Gertz, R. Agarwala, A. Morgulis, A. A. Schaffer, and Y. K. Yu. 2005. Protein database searches using compositionally adjusted substitution matrices. FEBS J. 272:5101-5109.
4. Ausubel, F. M. 2002. Short protocols in molecular biology: a compendium of methods from Current Protocols in Molecular Biology, 5th ed. Wiley, New York, NY.
5. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K. A. Datsenko, M. Tomita, B. L. Wanner, and H. Mori. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
6. Baehni, P., C. C. Tsai, W. P. McArthur, B. F. Hammond, and N. S. Taichman. 1979. Interaction of inflammatory cells and oral microorganisms. VIII. Detection of leukotoxic activity of a plaque-derived gram-negative microorganism. Infect. Immun. 24:233-243.
7. Bakaletz, L. O., B. M. Tallan, T. Hoepf, T. F. DeMaria, H. G. Birck, and D. J. Lim. 1988. Frequency of fimbriation of nontypable Haemophilus influenzae and its ability to adhere to chinchilla and human respiratory epithelium. Infect. Immun. 56:331-335.
8. Bernstein, J. A., P. H. Lin, S. N. Cohen, and S. Lin-Chao. 2004. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc. Natl. Acad. Sci. U. S. A. 101:2758-2763.
9. Blouin, S., and D. A. Lafontaine. 2007. A loop loop interaction and a K-turn motif located in the lysine aptamer domain are important for the riboswitch gene regulation control. RNA 13:1256-1267.
10. Blount, K. F., J. X. Wang, J. Lim, N. Sudarsan, and R. R. Breaker. 2007. Antibacterial lysine analogs that target lysine riboswitches. Nat. Chem. Biol. 3:44-49.
11. Brown, S. A., and M. Whiteley. 2007. A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J. Bacteriol. 189:6407-6414.
12. Chang, T. H., H. D. Huang, L. C. Wu, C. T. Yeh, B. J. Liu, and J. T. Horng. 2009. Computational identification of riboswitches based on RNA conserved functional sequences and conformations. RNA 15:1426-1430.
13. Danner, D. B., R. A. Deich, K. L. Sisco, and H. O. Smith. 1980. An eleven-base-pair sequence determines the specificity of DNA uptake in Haemophilus transformation. Gene 11:311-318.
14. de Soet, J. J., B. Nyvad, and M. Kilian. 2000. Strain-related acid production by oral streptococci. Caries Res. 34:486-490.
15. Ellis, J., A. Carlin, C. Steffes, J. Wu, J. Liu, and B. P. Rosen. 1995. Topological analysis of the lysine-specific permease of Escherichia coli. Microbiology 141(pt. 8):1927-1935.
16. Foxwell, A. R., J. M. Kyd, and A. W. Cripps. 1998. Nontypeable Haemophilus influenzae: pathogenesis and prevention. Microbiol. Mol. Biol. Rev. 62:294-308.
17. Garst, A. D., A. Heroux, R. P. Rambo, and R. T. Batey. 2008. Crystal structure of the lysine riboswitch regulatory mRNA element. J. Biol. Chem. 283:22347-22351.
18. Gottesman, S. 2005. Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet. 21:399-404. (Pubitemid 40835726)
19. Gregory, R. L., D. E. Kim, J. C. Kindle, L. C. Hobbs, and D. R. Lloyd. 1992. Immunoglobulin-degrading enzymes in localized juvenile periodontitis. J. Periodontal Res. 27:176-183.
20. Grundy, F. J., S. C. Lehman, and T. M. Henkin. 2003. The L box regulon: lysine sensing by leader RNAs of bacterial lysine biosynthesis genes. Proc. Natl. Acad. Sci. U. S. A. 100:12057-12062.
21. Hayes, W. 1952. Genetic recombination in Bact. coli K12; analysis of the stimulating effect of ultra-violet light. Nature 169:1017-1018.
22. Henderson, B., M. Wilson, L. Sharp, and J. M. Ward. 2002. Actinobacillus actinomycetemcomitans. J. Med. Microbiol. 51:1013-1020.
23. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
24. + antiporter of alkaliphilic Bacillus firmus OF4. J. Bacteriol. 179:3851-3857.
25. Kang, C. H., W. C. Shin, Y. Yamagata, S. Gokcen, G. F. Ames, and S. H. Kim. 1991. Crystal structure of the lysine-, arginine-, ornithine-binding protein (LAO) from Salmonella typhimurium at 2.7-A resolution. J. Biol. Chem. 266:23893-23899.
26. Kelley, L. A., and M. J. Sternberg. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371.
27. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
28. Kwon, M., and S. A. Strobel. 2008. Chemical basis of glycine riboswitch cooperativity. RNA 14:25-34.
29. Lamster, I. B., and M. J. Novak. 1992. Host mediators in gingival crevicular fluid: implications for the pathogenesis of periodontal disease. Crit. Rev. Oral Biol. Med. 3:31-60.
30. Legewie, S., D. Dienst, A. Wilde, H. Herzel, and I. M. Axmann. 2008. Small RNAs establish delays and temporal thresholds in gene expression. Biophys. J. 95:3232-3238.
31. Lloyd, A. L., B. J. Marshall, and B. J. Mee. 2005. Identifying cloned Helicobacter pylori promoters by primer extension using a FAM-labelled primer and GeneScan analysis. J. Microbiol. Methods. 60:291-298.
32. Loesche, W. J., F. Gusberti, G. Mettraux, T. Higgins, and S. Syed. 1983. Relationship between oxygen tension and subgingival bacterial flora in untreated human periodontal pockets. Infect. Immun. 42:659-667.
33. Loh, E., O. Dussurget, J. Gripenland, K. Vaitkevicius, T. Tiensuu, P. Mandin, F. Repoila, C. Buchrieser, P. Cossart, and J. Johansson. 2009. A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139:770-779.
34. MacLeod, P. R., and R. A. MacLeod. 1992. Identification and sequence of a Na(+)-linked gene from the marine bacterium Alteromonas haloplanktis which functionally complements the dagA gene of Escherichia coli. Mol. Microbiol. 6:2673-2681.
35. Marchler-Bauer, A., J. B. Anderson, F. Chitsaz, M. K. Derbyshire, C. DeWeese-Scott, J. H. Fong, L. Y. Geer, R. C. Geer, N. R. Gonzales, M. Gwadz, S. He, D. I. Hurwitz, J. D. Jackson, Z. Ke, C. J. Lanczycki, C. A. Liebert, C. Liu, F. Lu, S. Lu, G. H. Marchler, M. Mullokandov, J. S. Song, A. Tasneem, N. Thanki, R. A. Yamashita, D. Zhang, N. Zhang, and S. H. Bryant. 2009. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37:D205-D210.
36. Mesbah, N. M., G. M. Cook, and J. Wiegel. 2009. The halophilic alkalithermophile Natranaerobius thermophilus adapts to multiple environmental extremes using a large repertoire of Na(K)/H antiporters. Mol. Microbiol. 74:270-281.
37. Mintz, K. P., and P. M. Fives-Taylor. 2000. impA, a gene coding for an inner membrane protein, influences colonial morphology of Actinobacillus actinomycetemcomitans. Infect. Immun. 68:6580-6586.
38. Palmer, G. C., K. L. Palmer, P. A. Jorth, and M. Whiteley. 2010. Characterization of the Pseudomonas aeruginosa transcriptional response to phenylalanine and tyrosine. J. Bacteriol. 192:2722-2728.
39. Paster, B. J., I. Olsen, J. A. Aas, and F. E. Dewhirst. 2006. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol. 2000 42:80-87.
40. Phan, T. T., and W. Schumann. 2009. Transcriptional analysis of the lysine-responsive and riboswitch-regulated lysC gene of Bacillus subtilis. Curr. Microbiol. 59:463-468.
41. Pulvermacher, S. C., L. T. Stauffer, and G. V. Stauffer. 2009. Role of the sRNA GcvB in regulation of cycA in Escherichia coli. Microbiology 155:106-114.
42. Pulvermacher, S. C., L. T. Stauffer, and G. V. Stauffer. 2009. The small RNA GcvB regulates sstT mRNA expression in Escherichia coli. J. Bacteriol. 191:238-248.
43. Ramsey, M. M., and M. Whiteley. 2009. Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc. Natl. Acad. Sci. U. S. A. 106:1578-1583.
44. Repoila, F., N. Majdalani, and S. Gottesman. 2003. Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol. Microbiol. 48:855-861.
45. Rodionov, D. A., A. G. Vitreschak, A. A. Mironov, and M. S. Gelfand. 2003. Regulation of lysine biosynthesis and transport genes in bacteria: yet another RNA riboswitch? Nucleic Acids Res. 31:6748-6757.
46. Rosen, B. P. 1971. Basic amino acid transport in Escherichia coli. J. Biol. Chem. 246:3653-3662.
47. Seep-Feldhaus, A. H., J. Kalinowski, and A. Puhler. 1991. Molecular analysis of the Corynebacterium glutamicum lysl gene involved in lysine uptake. Mol. Microbiol. 5:2995-3005.
48. Serganov, A., L. Huang, and D. J. Patel. 2008. Structural insights into amino acid binding and gene control by a lysine riboswitch. Nature 455:1263-1267.
49. Sharma, C. M., F. Darfeuille, T. H. Plantinga, and J. Vogel. 2007. A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev. 21:2804-2817.
50. Smith, H. O., D. B. Danner, and R. A. Deich. 1981. Genetic transformation. Annu. Rev. Biochem. 50:41-68.
51. Socransky, S. S., J. L. Dzink, and C. M. Smith. 1985. Chemically defined medium for oral microorganisms. J. Clin. Microbiol. 22:303-305.
52. Spurio, R., M. Falconi, A. Brandi, C. L. Pon, and C. O. Gualerzi. 1997. The oligomeric structure of nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA bending. EMBO J. 16:1795-1805.
53. Steffes, C., J. Ellis, J. Wu, and B. P. Rosen. 1992. The lysP gene encodes the lysine-specific permease. J. Bacteriol. 174:3242-3249.
54. Sudarsan, N., J. K. Wickiser, S. Nakamura, M. S. Ebert, and R. R. Breaker. 2003. An mRNA structure in bacteria that controls gene expression by binding lysine. Genes Dev. 17:2688-2697.
55. Thompson, J. D., T. J. Gibson, and D. G. Higgins. 2002. Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics Chapter 2:Unit 2.3.
56. Urbanowski, M. L., L. T. Stauffer, and G. V. Stauffer. 2000. The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol. Microbiol. 37:856-868.
57. Walters, M. C., III, F. Roe, A. Bugnicourt, M. J. Franklin, and P. S. Stewart. 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47:317-323.
58. Wei, Y., A. A. Guffanti, M. Ito, and T. A. Krulwich. 2000. Bacillus subtilis YqkI is a novel malic/Na+-lactate antiporter that enhances growth on malate at low protonmotive force. J. Biol. Chem. 275:30287-30292.
59. Winkler, W. C., and R. R. Breaker. 2005. Regulation of bacterial gene expression by riboswitches. Annu. Rev. Microbiol. 59:487-517.
60. Zhai, Y., J. Tchieu, and M. H. Saier, Jr. 2002. A Web-based Tree View (TV) program for the visualization of phylogenetic trees. J. Mol. Microbiol. Biotechnol. 4:69-70.
61. Zuker, M. 2003. Mfold Web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.