The Erwinia amylovora PhoPQ system is involved in resistance to antimicrobial peptide and suppresses gene expression of two novel type III secretion systems

Microbiological Research

Volumn 165, Issue 8, 2010, Pages 665-673

  Nakka, Sridevi ^a   Qi, Mingsheng ^a   Zhao, Youfu ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Antimicrobial peptide; Fire blight; Two component system; Type III secretion

Indexed keywords

ACIDIC CONDITIONS; ACIDIC PH; ANTIMICROBIAL PEPTIDE; CECROPIN; ERWINIA AMYLOVORA; FIRE BLIGHT; PLANT PATHOGEN; TWO COMPONENT SYSTEMS; TWO-COMPONENT SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM; TYPE III SECRETIONS; WILD TYPES; XANTHOMONAS;

ACID RESISTANCE; ACIDS; MAMMALS; MICROORGANISMS; PATHOGENS; PEPTIDES; POLYPEPTIDES; SIGNAL TRANSDUCTION;

GENE EXPRESSION;

ACID; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; BACTERIAL PROTEIN; CARRIER PROTEIN; CECROPIN A; PHOP PROTEIN, BACTERIA; PHOQ PROTEIN, BACTERIA;

ANTIMICROBIAL ACTIVITY; BACTERIUM; FLORISTICS; GENE EXPRESSION; MAMMAL; PATHOGENICITY; PEPTIDE; PH;

ANTIBIOTIC RESISTANCE; ARTICLE; DRUG EFFECT; ENZYMOLOGY; ERWINIA AMYLOVORA; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; METABOLISM; MICROBIAL VIABILITY; SALMONELLA; SIGNAL TRANSDUCTION; XANTHOMONAS;

ACIDS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; ERWINIA AMYLOVORA; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; MEMBRANE TRANSPORT PROTEINS; MICROBIAL VIABILITY; MUTAGENESIS, INSERTIONAL; SALMONELLA; SIGNAL TRANSDUCTION; XANTHOMONAS;

ERWINIA AMYLOVORA; MAMMALIA; SALMONELLA; XANTHOMONAS;

EID: 78049418323     PISSN: 09445013     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micres.2009.11.013     Document Type: Article

References (42)

1. Aguirre A, Cabeza ML, Spinelli SV, McClelland M, Vescovi EG, Soncini FC. PhoP-induced genes with Salmonella pathogenicity island 1. J Bacteriol 2006, 188:6889-6898.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
3. Andreu D, Ubach J, Boman A, Wahlin B, Wade D, Merrifield RB, et al. Shortened cecropin A-melittin hybrids. Significant size reduction retains potent antibiotic activity. FEBS Lett 1992, 296:190-194.
4. Bader MW, Sanowar S, Daley ME, Schneider AR, Cho U, Xu W, et al. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 2005, 122:461-472.
5. Bearson BL, Wilson L, Foster JW. A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 1998, 180:2409-2417.
6. Bocsanczy AM, Perna NT, Biehl B, Glasner JD, Cartinhour SW, Schneider DJ, et al. Contributions of the genome sequence of Erwinia amylovora to the fire blight community. Acta Hort 2008, 793:163-170.
7. Brodsky IE, Gunn JS. A bacterial sensory system that activates resistance to innate immune defenses: potential targets for antimicrobial therapeutics. Mol Int 2005, 5:335-337.
8. Burse A, Weingart H, Ullrich MS NorM, an Erwinia amylovora multidrug efflux pump involved in in vitro competition with other epiphytic bacteria. Appl Environ Microbiol 2004, 70:693-703.
9. Castanie-Cornet MP, Penfound TA, Smith D, Elliott JF, Foster JW. Control of acid resistance in Escherichia coli. J Bacteriol 1999, 181:3525-3535.
10. Correa VR, Majerczak DR, Ammar E, Merighi M, Coplin DL, Pratt RC, et al. Characterization of a Pantoea stewartii TTSS gene required for persistence in its flea beetle vector. Phytopathology 2008, 98:S41.
11. Dale C, Moran NA. Molecular interactions between bacterial symbionts and their hosts. Cell 2006, 126:453-465.
12. Dale C, Young SA, Haydon DT, Welburn SC. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci USA 2001, 98:1883-1888.
13. Derzelle S, Turlin E, Duchaud E, Pages S, Kunst F, Givaudan A, et al. The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 2004, 186:1270-1279.
14. Fields PI, Groisman EA, Heffron F. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 1989, 243:1059-1062.
15. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 1996, 84:165-174.
16. Grignon C, Sentenac H. pH and ionic conditions in the apoplast. Annu Rev Plant Physiol 1991, 42:103-128.
17. Groisman EA. The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 2001, 183:1835-1842.
18. Groisman EA, Mouslim C. Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 2006, 4:705-709.
19. Gunn JS, Miller SI. PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J Bacteriol 1996, 178:6857-6864.
20. Gunn JS, Richards SM. Recognition and intergration of multiple environmental signals by the bacterial sensor kinase PhoQ. Cell Host & Microbe 2007, 1:163-165.
21. Guo L, Lim KB, Poduje CM, Daniel M, Gunn JS, Hackett M, et al. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 1998, 95:189-198.
22. Haque MM, Tsuyumu S. Virulence, resistance to magainin II, and expression of pectate lyase are controlled by the PhoP-PhoQ two-component regulatory system responding to pH and magnesium in Erwinia chrysanthemi 3937. J Gen Plant Pathol 2005, 71:47-53.
23. Hoch JA Two-component and phosphorelay signal transduction. Curr Opin Microbiol 2000, 3:165-170.
24. Hoch JA, Silhavy TJ. Two-component signal transduction 1995, ASM Press, Washington DC.
25. Lee SW, Jeong KS, Han SW, Lee SE, Phee BK, Hahn TR, et al. The Xanthomonas oryzae pv. oryzae PhoPQ two-component system is required for AvrXA21 activity, hrpG expression, and virulence. J Bacteriol 2008, 190:2138-2197.
26. Llama-Palacios A, Lopez-Solanilla E, Poza-Carrion C, Garcia-Olmedo F, Rodriguez-Palenzuela P. The Erwinia chrysanthemi phoP-phoQ operon plays an important role in growth at low pH, virulence and bacterial survival in plant tissue. Mol Microbiol 2003, 49:347-357.
27. Llama-Palacios A, Lopez-Solanilla E, Rodriguez-Palenzuela P. Role of the PhoP-PhoQ system in the virulence of Erwinia chrysanthemi strain 3937: involvement in sensitivity to plant antimicrobial peptides, survival at acid pH, and regulation of pectolytic enzymes. J Bacteriol 2005, 187:2157-2162.
28. Miller SI, Pulkkinen WS, Selsted ME, Mekalanos JJ. Characterization of defensin resistance phenotypes associated with mutations in the phoP virulence regulon of Salmonella typhimurium. Infect Immun 1990, 58:3706-3710.
29. Oh CS, Beer SV. Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiol Lett 2005, 253:185-192.
30. Oyston PC, Dorrell N, Williams K, Li SR, Green M, Titball RW, et al. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 2000, 68:3419-3425.
31. Perez JC, Groisman EA. Acid pH activation of the PmrA/PmrB two-component regulatory system of Salmonella enterica. Mol Microbiol 2007, 63:283-293.
32. Perez JC, Groisman EA. Transcription factor function and promoter architecture govern the evolution of bacterial regulons. Proc Natl Acad Sci USA 2009, 106:4319-4324.
33. Prost LR, Daley ME, Le Sage V, Bader MW, Moual HL, Klevit RE, et al. Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell 2007, 26:165-174.
34. Sambrook J, Russell DW. Molecular cloning: a laboratory manual 2001, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 3rd ed.
35. Soncini FC, Garcia Vescovi E, Solomon F, Groisman EA. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 1996, 178:5092-5099.
36. Torriani A. Influence of inorganic phosphate in the formation of phosphatases by Escherichia coli. Biochim Biophys Acta 1960, 38:460-469.
37. Valdivia RH, Falkow S. Fluorescence-based isolation of bacterial genes expressed within host cells. Science 1997, 277:2007-2011.
38. Walker KA, Miller VL. Regulation of the Ysa type III secretion system of Yersinia enterocolitica by YsaE/sycB and YsrS/YsrR. J Bacteriol 2004, 186:4056-4066.
39. Wang DP, Korban SS, Zhao YF. The Rcs phosphorelay system is essential for pathogenicity in Erwinia amylovora. Mol Plant Path 2009, 10:277-290.
40. Zhao YF, Sundin GW, Wang DP. Construction and analysis of pathogenicity island deletion mutants Erwinia amylovora. Can J Microbiol 2009, 55:457-464.
41. Zhao YF, Wang DP, Nakka S, Sundin GW, Korban SS. Systems level analysis of two component signal transduction systems in Erwinia amylovora: role in virulence, regulation of amylovoran biosynthesis and swarming motility. BMC Genomics 2009, 10:245.
42. Zwir I, Shin DW, Kato A, Nishino K, Latifi T, Solomon F, et al. Dissecting the PhoP regulatory network of Eschrichia coli and Salmonella enterica. Proc Natl Acad Sci USA 2005, 102:2862-2867.