Characterizing the effects of inorganic acid and alkaline shock on the Staphylococcus aureus transcriptome and messenger RNA turnover

FEMS Immunology and Medical Microbiology

Volumn 60, Issue 3, 2010, Pages 208-250

  Anderson, Kelsi L ^a   Roux, Christelle M ^a   Olson, Matthew W ^b   Luong, Thanh T ^c   Lee, Chia Y ^c   Olson, Robert ^d,e   Dunman, Paul M ^a,f  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b East Coast Division of Early Development   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^d ARGONNE NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Acid shock; Alkaline shock; MRNA turnover; Staphylococcus aureus; Virulence

Indexed keywords

CELL PROTEIN; INORGANIC ACID; MESSENGER RNA; PROTEIN PPGPP; RIBONUCLEASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ALKALINITY; AMINO ACID SYNTHESIS; ARTICLE; CELL PH; DNA REPAIR; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA DEGRADATION; RNA STABILITY; STAPHYLOCOCCUS AUREUS;

ACIDS; ALKALIES; GENE EXPRESSION PROFILING; RNA STABILITY; RNA, BACTERIAL; RNA, MESSENGER; STAPHYLOCOCCUS AUREUS; STRESS, PHYSIOLOGICAL;

EID: 78349293374     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2010.00736.x     Document Type: Article

References (68)

1. Abranches J, Martinez AR, Kajfasz JK et al. (2009) The molecular alarmone (p)ppGpp mediates stress responses, vancomycin tolerance, and virulence in Enterococcus faecalis. J Bacteriol 191: 2248-2256.
2. Abu-Qatouseh LF, Chinni SV, Seggewiss J et al. (2010) Identification of differentially expressed small non-protein-coding RNAs in Staphylococcus aureus displaying both the normal and the small-colony variant phenotype. J Mol Med 88: 565-575.
3. Anderson KL & Dunman PM (2009) Messenger RNA turnover processes in Escherichia coli, Bacillus subtilis, and emerging studies in Staphylococcus aureus. Int J Microbiol 2009: 525491.
4. Anderson KL, Roberts C, Disz T et al. (2006) Characterization of the Staphylococcus aureus heat-shock, cold-shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J Bacteriol 188: 6739-6756.
5. Appelbe OK & Sedgley CM (2007) Effects of prolonged exposure to alkaline pH on Enterococcus faecalis survival and specific gene transcripts. Oral Microbiol Immun 22: 169-174.
6. Beaume M, Hernandez D, Farinelli L et al. (2010) Cartography of methicillin-resistant S. aureus transcripts: detection, orientation and temporal expression during growth phase and stress conditions. PLoS One 5: e10725.
7. Beenken KE, Dunman PM, McAleese F et al. (2004) Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 186: 4665-4684.
8. Bernstein JA, Khodursky AB, Lin PH, Lin-Chao S & Cohen SN (2002) Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. P Natl Acad Sci USA 99: 9697-9702. Epub July 2002.
9. Bhagat N & Virdi JS (2009) Molecular and biochemical characterization of urease and survival of Yersinia enterocolitica biovar 1A in acidic pH in vitro. BMC Microbiol 9: 262.
10. Bischoff M, Dunman P, Kormanec J et al. (2004) Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J Bacteriol 186: 4085-4099.
11. Boes N, Schreiber K & Schobert M (2008) SpoT-triggered stringent response controls usp gene expression in Pseudomonas aeruginosa. J Bacteriol 190: 7189-7199.
12. Bohn C, Rigoulay C, Chabelskaya S et al. (2010) Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism. Nucleic Acids Res 2010: 28. DOI: DOI: 10.1093/nar/gkq462.
13. Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49: 359-378.
14. Bore E, Langsrud S, Langsrud O, Rode TM & Holck A (2007) Acid-shock responses in Staphylococcus aureus investigated by global gene expression analysis. Microbiology 153 (Part 7): 2289-2303.
15. Boucher HW & Corey GR (2008) Epidemiology of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 46 (suppl 5): S344-S349.
16. Bronner S, Monteil H & Prevost G (2004) Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol Rev 28: 183-200.
17. Cassat J, Dunman PM, Murphy E et al. (2006) Transcriptional profiling of a Staphylococcus aureus clinical isolate and its isogenic agr and sarA mutants reveals global differences in comparison to the laboratory strain RN6390. Microbiology 152 (Part 10): 3075-3090.
18. Cassat JE, Dunman PM, McAleese F et al. (2005) Comparative genomics of Staphylococcus aureus musculoskeletal isolates. J Bacteriol 187: 576-592.
19. Crosse AM, Greenway DL & England RR (2000) Accumulation of ppGpp and ppGp in Staphylococcus aureus 8325-4 following nutrient starvation. Lett Appl Microbiol 31: 332-337.
20. Dunman PM, Murphy E, Haney S et al. (2001) Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 183: 7341-7353.
21. Fang L, Jiang W, Bae W & Inouye M (1997) Promoter-independent cold-shock induction of cspA and its derepression at 37 degrees C by mRNA stabilization. Mol Microbiol 23: 355-364.
22. Fang L, Xia B & Inouye M (1999) Transcription of cspA, the gene for the major cold-shock protein of Escherichia coli, is negatively regulated at 37 degrees C by the 5'-untranslated region of its mRNA. FEMS Microbiol Lett 176: 39-43.
23. Ferrero RL, Cussac V, Courcoux P & Labigne A (1992) Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J Bacteriol 174: 4212-4217.
24. Gaynor EC, Wells DH, MacKichan JK & Falkow S (2005) The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol Microbiol 56: 8-27.
25. Geiger T, Goerke C, Fritz M et al. (2010) Role of the (p)ppGpp synthase RSH, a RelA/SpoT homolog, in stringent response and virulence of Staphylococcus aureus. Infect Immun 78: 1873-1883.
26. Gentry D, Li T, Rosenberg M & McDevitt D (2000) The rel gene is essential for in vitro growth of Staphylococcus aureus. J Bacteriol 182: 4995-4997.
27. Gillaspy AF, Hickmon SG, Skinner RA et al. (1995) Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect Immun 63: 3373-3380.
28. Gillaspy AF, Lee CY, Sau S, Cheung AL & Smeltzer MS (1998) Factors affecting the collagen binding capacity of Staphylococcus aureus. Infect Immun 66: 3170-3178.
29. Goldenberg D, Azar I & Oppenheim AB (1996) Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol Microbiol 19: 241-248.
30. Goldstein J, Pollitt NS & Inouye M (1990) Major cold shock protein of Escherichia coli. P Natl Acad Sci USA 87: 283-287.
31. Gordon RJ & Lowy FD (2008) Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis 46 (suppl 5): S350-S359.
32. Greenway DL & England RR (1999) The intrinsic resistance of Escherichia coli to various antimicrobial agents requires ppGpp and sigma s. Lett Appl Microbiol 29: 323-326.
33. Hiramatsu T, Kodama K, Kuroda T, Mizushima T & Tsuchiya T (1998) A putative multisubunit Na+/H+ antiporter from Staphylococcus aureus. J Bacteriol 180: 6642-6648.
34. Hiron A, Borezee-Durant E, Piard JC & Juillard V (2007) Only one of four oligopeptide transport systems mediates nitrogen nutrition in Staphylococcus aureus. J Bacteriol 189: 5119-5129.
35. Hornbaek T, Jakobsen M, Dynesen J & Nielsen AK (2004) Global transcription profiles and intracellular pH regulation measured in Bacillus licheniformis upon external pH upshifts. Arch Microbiol 182: 467-474.
36. Hu Y, Lu P, Wang Y et al. (2009) OmpR positively regulates urease expression to enhance acid survival of Yersinia pseudotuberculosis. Microbiology 155 (Part 8): 2522-2531.
37. Jarry TM & Cheung AL (2006) Staphylococcus aureus escapes more efficiently from the phagosome of a cystic fibrosis bronchial epithelial cell line than from its normal counterpart. Infect Immun 74: 2568-2577.
38. Jiang W, Hou Y & Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272: 196-202.
39. Jones PG, Mitta M, Kim Y, Jiang W & Inouye M (1996) Cold shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli. P Natl Acad Sci USA 93: 76-80.
40. Joseleau-Petit D, Thevenet D & D'Ari R (1994) ppGpp concentration, growth without PBP2 activity, and growth-rate control in Escherichia coli. Mol Microbiol 13: 911-917.
41. Kim S, Watanabe K, Suzuki H & Watarai M (2005) Roles of Brucella abortus SpoT in morphological differentiation and intramacrophagic replication. Microbiology 151 (Part 5): 1607-1617.
42. Kinsinger RF, Kearns DB, Hale M & Fall R (2005) Genetic requirements for potassium ion-dependent colony spreading in Bacillus subtilis. J Bacteriol 187: 8462-8469.
43. Klevens RM, Morrison MA, Nadle J et al. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. Journal of American Medical Association 298: 1763-1771.
44. Kuroda M, Ohta T & Hayashi H (1995) Isolation and the gene cloning of an alkaline shock protein in methicillin resistant Staphylococcus aureus. Biochem Bioph Res Co 207: 978-984.
45. Lemos JA, Brown TA Jr & Burne RA (2004) Effects of RelA on key virulence properties of planktonic and biofilm populations of Streptococcus mutans. Infect Immun 72: 1431-1440.
46. Luong T, Sau S, Gomez M, Lee JC & Lee CY (2002) Regulation of Staphylococcus aureus capsular polysaccharide expression by agr and sarA. Infect Immun 70: 444-450.
47. Luong TT, Newell SW & Lee CY (2003) Mgr, a novel global regulator in Staphylococcus aureus. J Bacteriol 185: 3703-3710.
48. Manka W, Adrianowicz L, Wesolek Z & Adrianowicz K (2002) The value of determining vaginal secretion reaction (pH) as a screening test of bacterial vaginosis. Wiad Lek 55: 51-55.
49. Mols M & Abee T (2008) Role of ureolytic activity in Bacillus cereus nitrogen metabolism and acid survival. Appl Environ Microb 74: 2370-2378.
50. Morfeldt E, Taylor D, Von Gabain A & Arvidson S (1995) Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 14: 4569-4577.
51. Musarrat J & Ahmad M (1991) Damage and mutagenesis of bacteriophage lambda induced by high pH. Mutagenesis 6: 207-211.
52. Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48: 1429-1449.
53. Padan E, Bibi E, Ito M & Krulwich TA (2005) Alkaline pH homeostasis in bacteria: new insights. Biochim Biophys Acta 1717: 67-88.
54. Pané-Farré J, Jonas B, Forstner K, Engelmann S & Hecker M (2006) The sigmaB regulon in Staphylococcus aureus and its regulation. Int J Med Microbiol 296: 237-258.
55. Pichon C & Felden B (2005) Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains. P Natl Acad Sci USA 102: 14249-14254.
56. Pomares MF, Vincent PA, Farias RN & Salomon RA (2008) Protective action of ppGpp in microcin J25-sensitive strains. J Bacteriol 190: 4328-4334.
57. Regassa LB & Betley MJ (1992) Alkaline pH decreases expression of the accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 174: 5095-5100.
58. Reid AN, Pandey R, Palyada K et al. (2008) Identification of Campylobacter jejuni genes contributing to acid adaptation by transcriptional profiling and genome-wide mutagenesis. Appl Environ Microb 74: 1598-1612.
59. Roberts C, Anderson KL, Murphy E et al. (2006) Characterizing the effect of the Staphylococcus aureus virulence factor regulator, SarA, on log-phase mRNA half-lives. J Bacteriol 188: 2593-2603.
60. Schilling O, Frick O, Herzberg C et al. (2007) Transcriptional and metabolic responses of Bacillus subtilis to the availability of organic acids: transcription regulation is important but not sufficient to account for metabolic adaptation. Appl Environ Microb 73: 499-507.
61. Schneider LA, Korber A, Grabbe S & Dissemond J (2007) Influence of pH on wound-healing: a new perspective for wound-therapy? Arch Dermatol Res 298: 413-420.
62. Shang F, Xue T, Sun H et al. (2009) The Staphylococcus aureus GGDEF domain-containing protein, GdpS, influences protein A gene expression in a cyclic diguanylic acid-independent manner. Infect Immun 77: 2849-2856.
63. Sleator RD & Hill C (2002) Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26: 49-71.
64. Stolyar S, He Q, Joachimiak MP et al. (2007) Response of Desulfovibrio vulgaris to alkaline stress. J Bacteriol 189: 8944-8952.
65. Takayama K & Kjelleberg S (2000) The role of RNA stability during bacterial stress responses and starvation. Environ Microbiol 2: 355-365.
66. Voyich JM, Braughton KR, Sturdevant DE et al. (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175: 3907-3919.
67. Weinrick B, Dunman PM, McAleese F et al. (2004) Effect of mild acid on gene expression in Staphylococcus aureus. J Bacteriol 186: 8407-8423.
68. Wilks JC, Kitko RD, Cleeton SH et al. (2009) Acid and base stress and transcriptomic responses in Bacillus subtilis. Appl Environ Microb 75: 981-990.