Lack of RsmA-Mediated Control Results in Constant Hypervirulence, Cell Elongation, and Hyperflagellation in Pectobacterium wasabiae

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Kõiv, Viia ^a   Andresen, Liis ^a   Broberg, Martin ^b   Frolova, Jekaterina ^a   Somervuo, Panu ^c   Auvinen, Petri ^c   Pirhonen, Minna ^b   Tenson, Tanel ^a   Mäe, Andres ^a  

^a UNIVERSITY OF TARTU   (Estonia)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BUTANEDIOL; MESSENGER RNA; PLANT CELL WALL DEGRADING ENZYME; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL SECRETION SYSTEM; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL ELONGATION; CELL FUNCTION; CELL MOTILITY; CONTROLLED STUDY; FERMENTATION; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENETIC ASSOCIATION; HYBRID; HYPERFLAGELLATION; HYPERVIRULENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PECTOBACTERIUM; PECTOBACTERIUM WASABIAE; PHENOTYPE; PLANT DISEASE; POTATO; RSMA GENE; TRANSCRIPTION REGULATION; UPREGULATION;

BACTERIAL PROTEINS; CHEMOTAXIS; FLAGELLA; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; METABOLIC NETWORKS AND PATHWAYS; PECTOBACTERIUM; PLANT DISEASES; REPRESSOR PROTEINS; SOLANUM TUBEROSUM; VIRULENCE; VIRULENCE FACTORS;

PECTOBACTERIUM; PECTOBACTERIUM WASABIAE; SOLANUM TUBEROSUM;

EID: 84872766301     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054248     Document Type: Article

References (62)

1. Pérombelon MCM, (2002) Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathology 51: 1-12.
2. Liu Y, Jiang G, Cui Y, Mukherjee A, Ma WL, et al. (1999) kdgREcc negatively regulates genes for pectinases, cellulase, protease, HarpinEcc, and a global RNA regulator in Erwinia carotovora subsp. carotovora. J Bacteriol 181: 2411-2421.
3. Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, et al. (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS pathogens 4 (6) (): e1000093 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2413422&tool=pmcentrez&rendertype=abstract. Accessed 2012 Mar 9.
4. Põllumaa L, Alamäe T, Mäe A, (2012) Quorum Sensing and Expression of Virulence in Pectobacteria. Sensors 12: 3327-3349.
5. Andresen L, Sala E, Kõiv V, Mäe A, (2010) A role for the Rcs phosphorelay in regulating expression of plant cell wall degrading enzymes in Pectobacterium carotovorum subsp. carotovorum. Microbiology 156: 1323-1334.
6. Cui Y, Chatterjee A, Yang H, Chatterjee AK, (2008) Regulatory network controlling extracellular proteins in Erwinia carotovora subsp. carotovora: FlhDC, the master regulator of flagellar genes, activates rsmB regulatory RNA production by affecting gacA and hexA (lrhA) expression. J Bacteriol 190: 4610-4623.
7. Kõiv V, Mäe A, (2001) Quorum sensing controls the synthesis of virulence factors by modulating rsmA gene expression in Erwinia carotovora subsp. carotovora. Mol Genet Genomics 265: 287-292.
8. Liu Y, Cui Y, Mukherjee A, Chatterjee AK, (1998) Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Mol Microbiol 29: 219-234.
9. Ma W, Cui Y, Liu Y, Dumenyo CK, Mukherjee A, et al. (2001) Molecular characterization of global regulatory RNA species that control pathogenicity factors in Erwinia amylovora and Erwinia herbicola pv. gypsophilae. J Bacteriol 183: 1870-1880.
10. Hugouvieux-Cotte-Pattat N, Condemine G, Nasser W, Reverchon S, (1996) Regulation of pectinolysis in Erwinia chrysanthemi. Ann Rev Microbiol 50: 213-257.
11. Hyytiäinen H, Montesano M, Palva ET, (2001) Global regulators ExpA (GacA) and KdgR modulate extracellular enzyme gene expression through the RsmA-rsmB system in Erwinia carotovora subsp. carotovora. Mol Plant-Microbe Int 14: 931-938.
12. Romeo T, Gong M, Liu MY, Brun-Zinkernagel AM, (1993) Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol 175: 4744-4755.
13. Wei BL, Brun-Zinkernagel AM, Simecka JW, Prüss BM, Babitzke P, et al. (2001) Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40: 245-256.
14. Baker CS, Morozov I, Suzuki K, Romeo T, Babitzke P, (2002) CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 44: 1599-1610.
15. Chao N-X, Wei K, Chen Q, Meng Q-L, Tang D-J, et al. (2008) The rsmA-like gene rsmA(Xcc) of Xanthomonas campestris pv. campestris is involved in the control of various cellular processes, including pathogenesis. Mol Plant-Microbe Interact 21: 411-423.
16. Heeb S, Haas D, (2001) Regulatory roles of the GacS/GacA two-component system in plant-associated and other gram-negative bacteria. Mol Plant-Microbe Interact 14: 1351-1363.
17. Heeb S, Valverde C, Gigot-Bonnefoy C, Haas D, (2005) Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. FEMS Microbiol Lett 243: 251-258.
18. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-301.
19. Altier C, Suyemoto M, Lawhon SD, (2000) Regulation of Salmonella enterica serovar typhimurium invasion genes by csrA. Infect Immun 68: 6790-6797.
20. Liaw S-J, Lai H-C, Ho S-W, Luh K-T, Wang W-B, (2003) Role of RsmA in the regulation of swarming motility and virulence factor expression in Proteus mirabilis. J Med Microbiol 52: 19-28.
21. Timmermans J, Van Melderen L, (2009) Conditional essentiality of the csrA gene in Escherichia coli. J Bacteriol 191: 1722-1724.
22. Ang S, Horng YT, Shu JC, Soo PC, Liu JH, et al. (2001) The role of RsmA in the regulation of swarming motility in Serratia marcescens. J Biomed Sci 8: 160-169.
23. Chatterjee A, Cui Y, Liu Y, Dumenyo CK, Chatterjee AK, (1995) Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl Environ Microbiol 61: 1959-1967.
24. Nykyri J, Niemi O, Koskinen P, Nokso-Koivisto J, Pasanen M, et al. (2012) Revised Phylogeny and Novel Horizontally Acquired Virulence Determinants of the Model Soft Rot Phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog 8 (11) (): e1003013 doi:10.1371/journal.ppat.1003013.
25. Kõiv V, Andresen L, Mäe A, (2010) AepA of Pectobacterium is not involved in the regulation of extracellular plant cell wall degrading enzymes production. Mol Genet Genomics 283: 541-549.
26. Pirhonen M, Heino P, Helander I, Harju P, Palva ET, (1988) Bacteriophage T4 resistant mutants of the plant pathogen Erwinia carotovora. Microb Pathog 4: 359-367.
27. Herrero M, de Lorenzo V, Timmis KN, (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172: 6557-6567.
28. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
29. Sambrook J, Russell D (2001) Molecular Cloning: A Laboratory Manual. 3rd ed. Cold Spring Harbor Laboratory Press. p.
30. Bauchop T, Elsden SR, (1960) The growth of micro-organisms in relation to their energy supply. J Gen Microbiol 23: 457-469.
31. Karlsson MB, Pirhonen M, Saarilahti HT, Palva ET, (1991) Molecular cloning of ompRS, a regulatory locus controlling production of outer membrane proteins in Erwinia carotovora subsp. carotovora. Mol Gen genet 226: 353-360.
32. Marits R, Tshuikina M, Pirhonen M, Laasik E, Mäe A, (2002) gusA fusions in Erwinia carotovora subsp. carotovora. Microbiology 148: 835-842.
33. West M, Burdash NM, Freimuth F, (1977) Simplified silver-plating stain for flagella. J Clinic Microbiol 6: 414-419.
34. MacFaddin JF (1980) Biochemical tests for identification of medical bacteria. 2nd ed. Philadelphia, PA.: Lippincott Williams & Wilkins.
35. Sjöblom S, Brader G, Koch G, Palva ET, (2006) Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol Microbiol 60: 1474-1489.
36. Mukherjee A, Cui Y, Liu Y, Dumenyo CK, Chatterjee AK, (1996) Global regulation in Erwinia species by Erwinia carotovora rsmA, a homologue of Escherichia coli csrA: repression of secondary metabolites, pathogenicity and hypersensitive reaction. Microbiology 142: 427-434.
37. Chatterjee A, Cui Y, Chakrabarty P, Chatterjee AK, (2010) Regulation of motility in Erwinia carotovora subsp. carotovora: quorum-sensing signal controls FlhDC, the global regulator of flagellar and exoprotein genes, by modulating the production of RsmA, an RNA-binding protein. Mol Plant-Microbe Interact 23: 1316-1323.
38. Kearns DB, (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8: 634-644.
39. Chen BG, Turner L, Berg HC, (2007) The wetting agent required for swarming in Salmonella enterica serovar typhimurium is not a surfactant. J Bacteriol 189: 8750-8753.
40. Gygi D, Rahman MM, Lai HC, Carlson R, Guard-Petter J, et al. (1995) A cell-surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol Microbiol 17: 1167-1175.
41. Lindum PW, Anthoni U, Christophersen C, Eberl L, Molin S, et al. (1998) N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J Bacteriol 180: 6384-6388.
42. Neu TR, (1996) Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev 60: 151-166.
43. Effantin G, Rivasseau C, Gromova M, Bligny R, Hugouvieux-Cotte-Pattat N, (2011) Massive production of butanediol during plant infection by phytopathogenic bacteria of the genera Dickeya and Pectobacterium. Mol Microbiol 82: 988-997.
44. Marquez-Villavicencio M delP, Weber B, Witherell RA, Willis DK, Charkowski AO, (2011) The 3-hydroxy-2-butanone pathway is required for Pectobacterium carotovorum pathogenesis. PloS one 6: e22974 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3158072&tool=pmcentrez&rendertype=abstract. Accessed 2012 May 25.
45. Kania A, Langlade N, Martinoia E, Neumann G, (2003) Phosphorus deficiency-induced modifications in citrate catabolism and in cytosolic pH as related to citrate exudation in cluster roots of white lupin. Plant Soil 248: 117-127.
46. Urbany C, Neuhaus HE, (2008) Citrate uptake into Pectobacterium atrosepticum is critical for bacterial virulence. Mol Plant-Microbe Interact 21: 547-554.
47. Mattinen L, Somervuo P, Nykyri J, Nissinen R, Kouvonen P, et al. (2008) Microarray profiling of host-extract-induced genes and characterization of the type VI secretion cluster in the potato pathogen Pectobacterium atrosepticum. Microbiology 154: 2387-2396.
48. Kurland CG, Dong H, (1996) Bacterial growth inhibition by overproduction of protein. Mol Microbiol 21: 1-4.
49. Stoebel DM, Dean AM, Dykhuizen DE, (2008) The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178: 1653-1660.
50. Cronan JEJ, Laporte D (2006) Tricarboxylic acid cycle and glyoxylate bypass. In: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, et al., editors. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Washington, D.C.: ASM PRESS. pp. 206-216.
51. Kim W, Surette MG, (2004) Metabolic differentiation in actively swarming Salmonella. Mol Microbiol 54: 702-714.
52. Overhage J, Bains M, Brazas MD, Hancock REW, (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190: 2671-2679.
53. Pearson MM, Rasko DA, Smith SN, Mobley HLT, (2010) Transcriptome of swarming Proteus mirabilis. Infect Immun 78: 2834-2845.
54. Wang Q, Frye JG, McClelland M, Harshey RM, (2004) Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol Microbiol 52: 169-187.
55. Inoue T, Shingaki R, Hirose S, Waki K, Mori H, et al. (2007) Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. J Bacteriol 189: 950-957.
56. Patrick JE, Kearns DB, (2012) Swarming motility and the control of master regulators of flagellar biosynthesis. Mol Microbiol 83: 14-23.
57. Felix G, Duran JD, Volko S, Boller T, (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J Cell Mol Biol 18: 265-276.
58. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, et al. (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. The Plant Cell 16: 3496-3507.
59. Ausubel FM, (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immun 6: 973-979.
60. Chisholm ST, Coaker G, Day B, Staskawicz BJ, (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
61. Nürnberger T, Brunner F, Kemmerling B, Piater L, (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immun Rev 198: 249-266.
62. Hématy K, Cherk C, Somerville S, (2009) Host-pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12: 406-413.