A novel manganese efflux system, YebN, is required for virulence by xanthomonas oryzae pv. oryzae

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Li, Chunxia ^a,b   Tao, Jun ^a,c   Mao, Daqing ^d   He, Chaozu ^a,e  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF MICROBIOLOGY   (China)

^d TSINGHUA UNIVERSITY   (China)

^e HAINAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MANGANESE; PROTEIN YEBN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; MNTR PROTEIN, BACTERIA; REPRESSOR PROTEIN;

ARTICLE; BACTERIAL LEAF BLIGHT; BACTERIAL VIRULENCE; CONTROLLED STUDY; DETOXIFICATION; ESCHERICHIA COLI; GENE DELETION; GENE MUTATION; HOMEOSTASIS; HOST PATHOGEN INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; WILD TYPE; XANTHOMONAS; XANTHOMONAS ORYZAE; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; OSMOTIC PRESSURE; PATHOGENICITY; PROTEIN TERTIARY STRUCTURE; RICE; TRANSPORT AT THE CELLULAR LEVEL; UPREGULATION; VIRULENCE;

BACTERIA (MICROORGANISMS); XANTHOMONAS ORYZAE PV. ORYZAE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CONSERVED SEQUENCE; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; MANGANESE; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; ORYZA SATIVA; OSMOTIC PRESSURE; OXIDATIVE STRESS; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; UP-REGULATION; VIRULENCE; XANTHOMONAS;

EID: 79960323472     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021983     Document Type: Article

References (54)

1. Papp-Wallace KM, Maguire ME, (2006) Manganese Transport and the Role of Manganese in Virulence. Annu Rev Microbiol 60: 187-209.
2. Nelson N, (1999) Metal ion transporters and homeostasis. EMBO J 18: 4361-4371.
3. Anderson ES, Paulley JT, Gaines JM, Valderas MW, Martin DW, et al. (2009) The manganese transporter MntH is a critical virulence determinant for Brucella abortus 2308 in experimentally infected mice. Infect Immun 77: 3466-3474.
4. Anjem A, Varghese S, Imlay JA, (2009) Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol Microbiol 72: 844-858.
5. Janulczyk R, Ricci S, Bjorck L, (2003) MtsABC is important for manganese and iron transport, oxidative stress resistance, and virulence of Streptococcus pyogenes. Infect Immun 71: 2656-2664.
6. Hohle TH, O'Brian MR, (2009) The mntH gene encodes the major Mn(2+) transporter in Bradyrhizobium japonicum and is regulated by manganese via the Fur protein. Mol Microbiol 72: 399-409.
7. Kehres DG, Zaharik ML, Finlay BB, Maguire ME, (2000) The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol 36: 1085-1100.
8. Kolenbrander PE, Andersen RN, Baker RA, Jenkinson HF, (1998) The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J Bacteriol 180: 290-295.
9. Hao Z, Chen S, Wilson DB, (1999) Cloning, expression, and characterization of cadmium and manganese uptake genes from Lactobacillus plantarum. Appl Environ Microbiol 65: 4746-4752.
10. Ouyang Z, He M, Oman T, Yang XF, Norgard MV, (2009) A manganese transporter, BB0219 (BmtA), is required for virulence by the Lyme disease spirochete, Borrelia burgdorferi. Proc Natl Acad Sci USA 106: 3449-3454.
11. Jakubovics NS, Valentine RA, (2009) A new direction for manganese homeostasis in bacteria: identification of a novel efflux system in Streptococcus pneumoniae. Mol Microbiol 72: 1-4.
12. Rosch JW, Gao G, Ridout G, Wang YD, Tuomanen EI, (2009) Role of the manganese efflux system mntE for signalling and pathogenesis in Streptococcus pneumoniae. Mol Microbiol 72: 12-25.
13. Ferluga S, Bigirimana J, Hofte M, Venturi V, (2007) A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence. Mol Plant Pathol 8: 529-538.
14. Aparna G, Chatterjee A, Sonti RV, Sankaranarayanan R, (2009) A cell wall-degrading esterase of Xanthomonas oryzae requires a unique substrate recognition module for pathogenesis on rice. Plant Cell 21: 1860-1873.
15. Yang W, Liu Y, Chen L, Gao T, Hu B, et al. (2007) Zinc uptake regulator (zur) gene involved in zinc homeostasis and virulence of Xanthomonas oryzae pv. oryzae in rice. Curr Microbiol 54: 307-314.
16. Pandey A, Sonti RV, (2010) Role of the FeoB protein and siderophore in promoting virulence of Xanthomonas oryzae pv. oryzae on rice. J Bacteriol 192: 3187-3203.
17. Sun Q, Wu W, Qian W, Hu J, Fang R, et al. (2003) High-quality mutant libraries of Xanthomonas oryzae pv. oryzae and X. campestris pv. campestris generated by an efficient transposon mutagenesis system. FEMS Microbiol Lett 226: 145-150.
18. Salzberg SL, Sommer DD, Schatz MC, Phillippy AM, Rabinowicz PD, et al. (2008) Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9: 204.
19. Jakubovics NS, Smith AW, Jenkinson HF, (2002) Oxidative stress tolerance is manganese (Mn(2+)) regulated in Streptococcus gordonii. Microbiology 148: 3255-3263.
20. Tseng HJ, Srikhanta Y, McEwan AG, Jennings MP, (2001) Accumulation of manganese in Neisseria gonorrhoeae correlates with resistance to oxidative killing by superoxide anion and is independent of superoxide dismutase activity. Mol Microbiol 40: 1175-1186.
21. Niven DF, Ekins A, al-Samaurai AA, (1999) Effects of iron and manganese availability on growth and production of superoxide dismutase by Streptococcus suis. Can J microbiol 45: 1027-1032.
22. Moore RA, Tuanyok A, Woods DE, (2008) Survival of Burkholderia pseudomallei in water. BMC Res Notes 1: 11.
23. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
24. Subramoni S, Sonti RV, (2005) Growth deficiency of a Xanthomonas oryzae pv. oryzae fur mutant in rice leaves is rescued by ascorbic acid supplementation. Mol Plant Microbe Interact 18: 644-651.
25. Kehres DG, Maguire ME, (2003) Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol Rev 27: 263-290.
26. Levina N, Totemeyer S, Stokes NR, Louis P, Jones MA, et al. (1999) Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18: 1730-1737.
27. Schumann U, Edwards MD, Rasmussen T, Bartlett W, van West P, et al. (2010) YbdG in Escherichia coli is a threshold-setting mechanosensitive channel with MscM activity. Proc Natl Acad Sci U S A 107: 12664-12669.
28. Wood JM, (1999) Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev 63: 230-262.
29. Miller KJ, Wood JM, (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50: 101-136.
30. Matsumoto TK, Ellsmore AJ, Cessna SG, Low PS, Pardo JM, et al. (2002) An osmotically induced cytosolic Ca2+ transient activates calcineurin signaling to mediate ion homeostasis and salt tolerance of Saccharomyces cerevisiae. J Biol Chem 277: 33075-33080.
31. Knight H, Trewavas AJ, Knight MR, (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12: 1067-1078.
32. Trischitta F, Denaro MG, Faggio C, (2005) Cell volume regulation following hypotonic stress in the intestine of the eel, Anguilla anguilla, is Ca2+-dependent. Comp Biochem Physiol 140: 359-367.
33. Park SY, Cromie MJ, Lee EJ, Groisman EA, (2010) A bacterial mRNA leader that employs different mechanisms to sense disparate intracellular signals. Cell 142: 737-748.
34. Van Dort HM, Knowles DW, Chasis JA, Lee G, Mohandas N, et al. (2001) Analysis of integral membrane protein contributions to the deformability and stability of the human erythrocyte membrane. J Biol Chem 276: 46968-46974.
35. Cartee RT, Forsee WT, Schutzbach JS, Yother J, (2000) Mechanism of type 3 capsular polysaccharide synthesis in Streptococcus pneumoniae. J Biol Chem 275: 3907-3914.
36. Dillon DA, Wu WI, Riedel B, Wissing JB, Dowhan W, et al. (1996) The Escherichia coli pgpB gene encodes for a diacylglycerol pyrophosphate phosphatase activity. J Biol Chem 271: 30548-30553.
37. Sueyoshi N, Kita K, Okino N, Sakaguchi K, Nakamura T, et al. (2002) Molecular Cloning and Expression of Mn2+-Dependent Sphingomyelinase/Hemolysin of an Aquatic Bacterium, Pseudomonas sp. Strain TK4. J Bacteriol 184: 540-546.
38. Haskew-Layton RE, Mongin AA, Kimelberg HK, (2005) Hydrogen peroxide potentiates volume-sensitive excitatory amino acid release via a mechanism involving Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 280: 3548-3554.
39. Deng W, Baki L, Baumgarten CM, (2010) Endothelin signalling regulates volume-sensitive Cl- current via NADPH oxidase and mitochondrial reactive oxygen species. Cardiovasc Res 88: 93-100.
40. Wu HJ, Seib KL, Srikhanta YN, Edwards J, Kidd SP, et al. (2009) Manganese regulation of virulence factors and oxidative stress resistance in Neisseria gonorrhoeae. J Proteomics 73: 899-916.
41. Bayer AS, Coulter SN, Stover CK, Schwan WR, (1999) Impact of the high-affinity proline permease gene (putP) on the virulence of Staphylococcus aureus in experimental endocarditis. Infect Immun 67 (2): 740-744.
42. Bernardini ML, Fontaine A, Sansonetti PJ, (1990) The two-component regulatory system ompR-envZ controls the virulence of Shigella flexneri. J Bacteriol 172: 6274-6281.
43. Sleator RD, Hill C, (2002) Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26: 49-71.
44. NiÑO-Liu DO, Ronald PC, Bogdanove AJ, (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7: 303-324.
45. Shen Y, Sharma P, da Silva FG, Ronald P, (2002) The Xanthomonas oryzae pv. lozengeoryzae raxP and raxQ genes encode an ATP sulphurylase and adenosine-5′-phosphosulphate kinase that are required for AvrXa21 avirulence activity. Mol Microbiol 44: 37-48.
46. Schafer A, Tauch A, Jager W, Kalinowski J, Thierbach G, et al. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145: 69-73.
47. Huynh TV, Dahlbeck D, Staskawicz BJ, (1989) Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245: 1374-1377.
48. Wang L, Rong W, He C, (2008) Two Xanthomonas Extracellular Polygalacturonases, PghAxc and PghBxc, Are Regulated by Type III Secretion Regulators HrpX and HrpG and Are Required for Virulence. Mol Plant Microbe Interact 21: 555-563.
49. Kuo MM, Saimi Y, Kung C, Choe S, (2007) Patch clamp and phenotypic analyses of a prokaryotic cyclic nucleotide-gated K+ channel using Escherichia coli as a host. J Biol Chem 282: 24294-24301.
50. Kuo MM, Saimi Y, Kung C, (2003) Gain-of-function mutations indicate that Escherichia coli Kch forms a functional K+ conduit in vivo. EMBO J 22: 4049-4058.
51. Outten CE, O'Halloran TV, (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292: 2488-2492.
52. Mongkolsuk S, Loprasert S, Vattanaviboon P, Chanvanichayachai C, Chamnongpol S, et al. (1996) Heterologous growth phase- and temperature-dependent expression and H2O2 toxicity protection of a superoxide-inducible monofunctional catalase gene from Xanthomonas oryzae pv. oryzae. J Bacteriol 178: 3578-3584.
53. Jefferson RA, Kavanagh TA, Bevan MW, (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
54. Qi H-Y, Bernstein HD, (1999) SecA is required for the insertion of inner membrane proteins targeted by the Escherichia coli signal recognition particle. J Biol Chem 274: 8993-8997.