Evolution of the metabolic and regulatory networks associated with oxygen availability in two phytopathogenic enterobacteria

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Babujee, Lavanya ^a   Apodaca, Jennifer ^a   Balakrishnan, Venkatesh ^a   Liss, Paul ^a   Kiley, Patricia J ^a   Charkowski, Amy O ^a   Glasner, Jeremy D ^a   Perna, Nicole T ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN; BACTERIAL PROTEIN;

ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CONTROLLED STUDY; DICKEYA DADANTII; DOWN REGULATION; ENTEROBACTERIACEAE; ESCHERICHIA COLI; FERMENTATION; GENE EXPRESSION; GENE NUMBER; GLYCOLYSIS; NITRATE METABOLISM; NONHUMAN; PECTOBACTERIUM ATROSEPTICUM; STIMULON; TRANSCRIPTION REGULATION; TYPE IV SECRETION SYSTEM; UPREGULATION; ANAEROBIC GROWTH; CLASSIFICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ORDER; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; OXYGEN CONSUMPTION; PHYLOGENY;

ANIMALIA; DICKEYA; DICKEYA DADANTII; ENTEROBACTERIACEAE; ESCHERICHIA COLI; PECTOBACTERIUM; PECTOBACTERIUM ATROSEPTICUM; SALMONELLA ENTERICA;

ANAEROBIOSIS; BACTERIAL PROTEINS; ENTEROBACTERIACEAE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; METABOLIC NETWORKS AND PATHWAYS; OXYGEN CONSUMPTION; PHYLOGENY; TRANSCRIPTION, GENETIC;

EID: 84858731069     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-110     Document Type: Article

References (144)

1. Perombelon MCM. Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol 2002, 51(1):1-12.
2. Lemattre P. 1972, Chimie horticole, Nouvelle éd. edn. Paris,: J.-B. Baillière.
3. Harrison MD, Nielsen LW. Blackleg and bacterial soft rot. Compendium of Potato Diseases 1981, 27-29. American Phytopathological Society, Hooker WJ, St. Paul MN.
4. Ma B, Hibbing ME, Kim HS, Reedy RM, Yedidia I, Breuer J, Glasner JD, Perna NT, Kelman A, Charkowski AO. Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 2007, 97(9):1150-1163. 10.1094/PHYTO-97-9-1150, 18944180.
5. Perombelon MCM, Kelman A. Ecology of the Soft Rot Erwinias. Annu Rev Phytopathol 1980, 18(1):361-387.
6. Kotoujansky A. Molecular Genetics of Pathogenesis by Soft-Rot Erwinias. Annu Rev Phytopathol 1987, 25(1):405-430.
7. Robert-Baudouy J. Molecular biology of Erwinia: from soft-rot to antileukaemics. Trends Biotechnol 1991, 9(1):325-329.
8. Smid EJ, Jansen AH, Tuijn CJ. Anaerobic Nitrate Respiration by Erwinia carotovora subsp. atroseptica during Potato Tuber Invasion. Appl Environ Microbiol 1993, 59(11):3648-3653. 182511, 16349082.
9. Morris CE, Bardin M, Kinkel LL, Moury B, Nicot PC, Sands DC. Expanding the Paradigms of Plant Pathogen Life History and Evolution of Parasitic Fitness beyond Agricultural Boundaries. PLoS Pathog 2009, 5(12):e1000693. 10.1371/journal.ppat.1000693, 2790610, 20041212.
10. Hugouvieux-Cotte-Pattat N, Dominguez H, Robert-Baudouy J. Environmental conditions affect transcription of the pectinase genes of Erwinia chrysanthemi3937. J Bacteriol 1992, 174(23):7807-7818. 207497, 1447147.
11. Salmon KA, Hung SP, Steffen NR, Krupp R, Baldi P, Hatfield GW, Gunsalus RP. Global gene expression profiling in Escherichia coli K12: effects of oxygen availability and ArcA. J Biol Chem 2005, 280(15):15084-15096. 10.1074/jbc.M414030200, 15699038.
12. Kang Y, Weber KD, Qiu Y, Kiley PJ, Blattner FR. Genome-Wide Expression Analysis Indicates that FNR of Escherichia coli K-12 Regulates a Large Number of Genes of Unknown Function. J Bacteriol 2005, 187(3):1135-1160. 10.1128/JB.187.3.1135-1160.2005, 545700, 15659690.
13. Salmon K, Hung SP, Mekjian K, Baldi P, Hatfield GW, Gunsalus RP. Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J Biol Chem 2003, 278(32):29837-29855. 10.1074/jbc.M213060200, 12754220.
14. Cho BK, Knight EM, Palsson BO. Transcriptional regulation of the fad regulon genes of Escherichia coli by ArcA. Microbiology 2006, 152(Pt 8):2207-2219.
15. Constantinidou C, Hobman JL, Griffiths L, Patel MD, Penn CW, Cole JA, Overton TW. A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. J Biol Chem 2006, 281(8):4802-4815.
16. Overton TW, Griffiths L, Patel MD, Hobman JL, Penn CW, Cole JA, Constantinidou C. Microarray analysis of gene regulation by oxygen, nitrate, nitrite, FNR, NarL and NarP during anaerobic growth of Escherichia coli : new insights into microbial physiology. Biochem Soc Trans 2006, 34(Pt 1):104-107.
17. Ravcheev DA, Gerasimova AV, Mironov AA, Gelfand MS. Comparative genomic analysis of regulation of anaerobic respiration in ten genomes from three families of gamma-proteobacteria (Enterobacteriaceae, Pasteurellaceae, Vibrionaceae). BMC Genomics 2007, 8:54. 10.1186/1471-2164-8-54, 1805755, 17313674.
18. Kendziorski CM, Newton MA, Lan H, Gould MN. On parametric empirical Bayes methods for comparing multiple groups using replicated gene expression profiles. Stat Med 2003, 22(24):3899-3914. 10.1002/sim.1548, 14673946.
19. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13(9):2178-2189. 10.1101/gr.1224503, 403725, 12952885.
20. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005, 33(17):5691-5702. 10.1093/nar/gki866, 1251668, 16214803.
21. Kiley PJ, Beinert H. Oxygen sensing by the global regulator, FNR: the role of the iron-sulfur cluster. FEMS Microbiol Rev 1998, 22(5):341-352. 10.1111/j.1574-6976.1998.tb00375.x, 9990723.
22. Georgellis D, Kwon O, Lin EC. Quinones as the redox signal for the arc two-component system of bacteria. Science 2001, 292(5525):2314-2316. 10.1126/science.1059361, 11423658.
23. Lynch AS, Lin EC. Transcriptional control mediated by the ArcA two-component response regulator protein of Escherichia coli: characterization of DNA binding at target promoters. J Bacteriol 1996, 178(21):6238-6249. 178496, 8892825.
24. Kwon O, Georgellis D, Lin EC. Phosphorelay as the sole physiological route of signal transmission by the arc two-component system of Escherichia coli. J Bacteriol 2000, 182(13):3858-3862. 10.1128/JB.182.13.3858-3862.2000, 94563, 10851007.
25. Stewart V, Chen LL, Wu HC. Response to culture aeration mediated by the nitrate and nitrite sensor NarQ of Escherichia coli K-12. Mol Microbiol 2003, 50(4):1391-1399. 10.1046/j.1365-2958.2003.03776.x, 14622424.
26. Noriega CE, Schmidt R, Gray MJ, Chen LL, Stewart V. Autophosphorylation and dephosphorylation by soluble forms of the nitrate-responsive sensors NarX and NarQ from Escherichia coli K-12. J Bacteriol 2008, 190(11):3869-3876. 10.1128/JB.00092-08, 2395026, 18375557.
27. Noriega CE, Lin HY, Chen LL, Williams SB, Stewart V. Asymmetric cross-regulation between the nitrate-responsive NarX-NarL and NarQ-NarP two-component regulatory systems from Escherichia coli K-12. Mol Microbiol 2010, 75(2):394-412. 10.1111/j.1365-2958.2009.06987.x, 3034140, 19968795.
28. Unden G, Bongaerts J. Alternative respiratory pathways of Escherichia coli:energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1997, 1320(3):217-234. 10.1016/S0005-2728(97)00034-0, 9230919.
29. Jiang GR, Nikolova S, Clark DP. Regulation of the ldhA gene, encoding the fermentative lactate dehydrogenase of Escherichia coli. Microbiology 2001, 147(Pt 9):2437-2446.
30. Leonhartsberger S, Korsa I, Bock A. The molecular biology of formate metabolism in enterobacteria. J Mol Microbiol Biotechnol 2002, 4(3):269-276.
31. Rossmann R, Sawers G, Bock A. Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. Mol Microbiol 1991, 5(11):2807-2814. 10.1111/j.1365-2958.1991.tb01989.x, 1779767.
32. Axley MJ, Bock A, Stadtman TC. Catalytic properties of an Escherichia coli formate dehydrogenase mutant in which sulfur replaces selenium. Proc Natl Acad Sci USA 1991, 88(19):8450-8454. 10.1073/pnas.88.19.8450, 52526, 1924303.
33. Axley MJ, Grahame DA. Kinetics for formate dehydrogenase of Escherichia coli formate-hydrogenlyase. J Biol Chem 1991, 266(21):13731-13736.
34. Sawers RG, Blokesch M, Böck A. Anaerobic Formate and Hydrogen Metabolism. EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology 2004, Washington: ASM Press, Böck A, Curtiss R III, Kaper JB, Karp PD, Neidhardt FC, Nyström T, Slauch JM, Squires CL, Ussery DA.
35. Mayer D, Schlensog V, Bock A. Identification of the transcriptional activator controlling the butanediol fermentation pathway in Klebsiella terrigena. J Bacteriol 1995, 177(18):5261-5269. 177317, 7665514.
36. Marquez-Villavicencio M, Weber B, Witherell RA, Willis DK, Charkowski AO. The 3-Hydroxy-2-Butanone Pathway Is Required for Pectobacterium carotovorum Pathogenesis. PLoS One 2011, 6(8):e22974. doi:doi:10.1371/journal.pone.0022974, 10.1371/journal.pone.0022974, 3158072, 21876734.
37. Blomqvist K, Nikkola M, Lehtovaara P, Suihko ML, Airaksinen U, Straby KB, Knowles JK, Penttila ME. Characterization of the genes of the 2,3-butanediol operons from Klebsiella terrigena and Enterobacter aerogenes. J Bacteriol 1993, 175(5):1392-1404. 193226, 8444801.
38. Turner SL, Ray A. Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 2009, 461:277-281. 10.1038/nature08295, 19710651.
39. Rochat D, Morin JP, Kakul T, Beaudoin-Ollivier L, Prior R, Renou M, Malosse I, Stathers T, Embupa S, Laup S. Activity of male pheromone of Melanesian rhinoceros beetle Scapanes australis. J Chem Ecol 2002, 28(3):479-500. 10.1023/A:1014531810037, 11944826.
40. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 2004, 134(3):1017-1026. 10.1104/pp.103.026583, 389924, 14976231.
41. Hsieh SC, Lu CC, Horng YT, Soo PC, Chang YL, Tsai YH, Lin CS, Lai HC. The bacterial metabolite 2,3-butanediol ameliorates endotoxin-induced acute lung injury in rats. Microbes Infect 2007, 9(12-13):1402-1409. 10.1016/j.micinf.2007.07.004, 17913548.
42. Dickey RS. Erwinia chrysanthemi: A Comparative Study of Phenotypic Properties of Strains from Several Hosts and Other Erwinia Species. Phytopathology 1979, 69:324-329.
43. Darwin AJ, Li J, Stewart V. Analysis of nitrate regulatory protein NarL-binding sites in the fdnG and narG operon control regions of Escherichia coli K-12. Mol Microbiol 1996, 20(3):621-632. 10.1046/j.1365-2958.1996.5491074.x, 8736541.
44. Melville SB, Gunsalus RP. Isolation of an oxygen-sensitive FNR protein of Escherichia coli: interaction at activator and repressor sites of FNR-controlled genes. Proc Natl Acad Sci USA 1996, 93(3):1226-1231. 10.1073/pnas.93.3.1226, 40061, 8577745.
45. Nikkila H, Gennis RB, Sligar SG. Cloning and expression of the gene encoding the soluble cytochrome b562 of Escherichia coli. Eur J Biochem 1991, 202(2):309-13. 10.1111/j.1432-1033.1991.tb16377.x, 1761034.
46. Unden G, Dünnwald P. The Aerobic and Anaerobic Respiratory Chain of Escherichia coli and Salmonella enterica: Enzymes and Energetics. EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology 2004, Washington: ASM Press, Böck A, III RC, Kaper JB, Karp PD, Neidhardt FC, Nyström T, Slauch JM, Squires CL, Ussery DA.
47. Abaibou H, Pommier J, Benoit S, Giordano G, Mandrand-Berthelot MA. Expression and characterization of the Escherichia coli fdo locus and a possible physiological role for aerobic formate dehydrogenase. J Bacteriol 1995, 177(24):7141-7149. 177593, 8522521.
48. Andrews BJ, Lehman JA, Turchi JJ. Kinetic analysis of the Ku-DNA binding activity reveals a redox-dependent alteration in protein structure that stimulates dissociation of the Ku-DNA complex. J Biol Chem 2006, 281(19):13596-13603. 10.1074/jbc.M512787200, 2432111, 16537541.
49. Gort AS, Ferber DM, Imlay JA. The regulation and role of the periplasmic copper, zinc superoxide dismutase of Escherichia coli. Mol Microbiol 1999, 32(1):179-191. 10.1046/j.1365-2958.1999.01343.x, 10216871.
50. Battistoni A, Pacello F, Folcarelli S, Ajello M, Donnarumma G, Greco R, Ammendolia MG, Touati D, Rotilio G, Valenti P. Increased expression of periplasmic Cu, Zn superoxide dismutase enhances survival of Escherichia coli invasive strains within nonphagocytic cells. Infect Immun 2000, 68(1):30-37. 10.1128/IAI.68.1.30-37.2000, 97098, 10603365.
51. Uzzau S, Bossi L, Figueroa-Bossi N. Differential accumulation of Salmonella[Cu, Zn] superoxide dismutases SodCI and SodCII in intracellular bacteria: correlation with their relative contribution to pathogenicity. Mol Microbiol 2002, 46(1):147-156. 10.1046/j.1365-2958.2002.03145.x, 12366838.
52. Abremski K, Gottesman S. The form of the DNA substrate required for excisive recombination of bacteriophage lambda. J Mol Biol 1979, 131(3):637-649. 10.1016/0022-2836(79)90012-3, 229232.
53. Piddington DL, Fang FC, Laessig T, Cooper AM, Orme IM, Buchmeier NA. Cu, Zn superoxide dismutase of Mycobacterium tuberculosis contributes to survival in activated macrophages that are generating an oxidative burst. Infect Immun 2001, 69(8):4980-4987. 10.1128/IAI.69.8.4980-4987.2001, 98590, 11447176.
54. Mitchell A, Romano GH, Groisman B, Yona A, Dekel E, Kupiec M, Dahan O, Pilpel Y. Adaptive prediction of environmental changes by microorganisms. Nature 2009, 460(7252):220-224. 10.1038/nature08112, 19536156.
55. Hommais F, Oger-Desfeux C, Van Gijsegem F, Castang S, Ligori S, Expert D, Nasser W, Reverchon S. PecS is a global regulator of the symptomatic phase in the phytopathogenic bacterium Erwinia chrysanthemi3937. J Bacteriol 2008, 190(22):7508-7522. 10.1128/JB.00553-08, 2576657, 18790868.
56. Ritz D, Patel H, Doan B, Zheng M, Aslund F, Storz G, Beckwith J. Thioredoxin 2 is involved in the oxidative stress response in Escherichia coli. J Biol Chem 2000, 275(4):2505-2512. 10.1074/jbc.275.4.2505, 10644706.
57. Tang Y, Quail MA, Artymiuk PJ, Guest JR, Green J. Escherichia coli aconitases and oxidative stress: post-transcriptional regulation of sodA expression. Microbiology 2002, 148(4):1027-1037.
58. Nachin L, Nannmark U, Nystrom T. Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J Bacteriol 2005, 187(18):6265-6272. 10.1128/JB.187.18.6265-6272.2005, 1236625, 16159758.
59. Liu WT, Karavolos MH, Bulmer DM, Allaoui A, Hormaeche RD, Lee JJ, Khan CM. Role of the universal stress protein UspA of Salmonella in growth arrest, stress and virulence. Microb Pathog 2007, 42(1):2-10. 10.1016/j.micpath.2006.09.002, 17081727.
60. Farewell A, Kvint K, Nystrom T. uspB, a new σS-regulated gene in Escherichia coli which is required for stationary-phase resistance to ethanol. J Bacteriol 1998, 180(23):6140-6147. 107697, 9829921.
61. Phadtare S, Inouye M. Role of CspC and CspE in regulation of expression of RpoS and UspA, the stress response proteins in Escherichia coli. J Bacteriol 2001, 183(4):1205-1214. 10.1128/JB.183.4.1205-1214.2001, 94993, 11157932.
62. Yamanaka K, Zheng W, Crooke E, Wang YH, Inouye M. CspD, a novel DNA replication inhibitor induced during the stationary phase in Escherichia coli. Mol Microbiol 2001, 39(6):1572-1584. 10.1046/j.1365-2958.2001.02345.x, 11260474.
63. Outten FW, Huffman DL, Hale JA, O'Halloran TV. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 2001, 276(33):30670-30677. 10.1074/jbc.M104122200, 11399769.
64. Franza T, Expert D. Iron Uptake in Soft Rot Erwinia. Iron Uptake and Homeostasis in Microorganisms 2010, 292. Norfolk, UK: Caister Academic Press, Cornelis P, Andrews SC.
65. Rauscher L, Expert D, Matzanke BF, Trautwein AX. Chrysobactin-dependent iron acquisition in Erwinia chrysanthemi. Functional study of a homolog of the Escherichia coli ferric enterobactin esterase. J Biol Chem 2002, 277(4):2385-2395. 10.1074/jbc.M107530200, 11694506.
66. Mahe B, Masclaux C, Rauscher L, Enard C, Expert D. Differential expression of two siderophore-dependent iron-acquisition pathways in Erwinia chrysanthemi 3937: characterization of a novel ferrisiderophore permease of the ABC transporter family. Mol Microbiol 1995, 18(1):33-43. 10.1111/j.1365-2958.1995.mmi_18010033.x, 8596459.
67. Braun V, Killmann H. Bacterial solutions to the iron-supply problem. Trends Biochem Sci 1999, 24(3):104-109. 10.1016/S0968-0004(99)01359-6, 10203757.
68. Boughammoura A, Matzanke BF, Bottger L, Reverchon S, Lesuisse E, Expert D, Franza T. Differential role of ferritins in iron metabolism and virulence of the plant-pathogenic bacterium Erwinia chrysanthemi3937. J Bacteriol 2008, 190(5):1518-1530. 10.1128/JB.01640-07, 2258672, 18165304.
69. Gloux K, Touze T, Pagot Y, Jouan B, Blanco C. Mutations of ousA alter the virulence of Erwinia chrysanthemi. Mol Plant Microbe Interact 2005, 18:150-157. 10.1094/MPMI-18-0150, 15720084.
70. Hugouvieux-Cotte-Pattat N, Condemine G, Nasser W, Reverchon S. Regulation of pectinolysis in Erwinia chrysanthemi. Annu Rev Microbiol 1996, 50(1):213-257. 10.1146/annurev.micro.50.1.213, 8905080.
71. Shevchik VE, Kester HCM, Benen JAE, Visser J, Robert-Baudouy J, Hugouvieux-Cotte-Pattat N. Characterization of the exopolygalacturonate lyase PelX of Erwinia chrysanthemi3937. J Bacteriol 1999, 181(5):1652-1663. 93558, 10049400.
72. Keen NT, Boyd C, Henrissat B. Cloning and characterization of a xylanase gene from corn strains of Erwinia chrysanthemi. Mol Plant Microbe Interact 1996, 9(7):651-657. 10.1094/MPMI-9-0651, 8810080.
73. Mattinen L, Somervuo P, Nykyri J, Nissinen R, Kouvonen P, Corthals G, Auvinen P, Aittamaa M, Valkonen JP, Pirhonen M. Microarray profiling of host-extract-induced genes and characterization of the type VI secretion cluster in the potato pathogen Pectobacterium atrosepticum. Microbiology 2008, 154(Pt 8):2387-2396.
74. Mattinen L, Nissinen R, Riipi T, Kalkkinen N, Pirhonen M. Host-extract induced changes in the secretome of the plant pathogenic bacterium Pectobacterium atrosepticum. Proteomics 2007, 7(19):3527-3537. 10.1002/pmic.200600759, 17726675.
75. Kazemi-Pour N, Condemine G, Hugouvieux-Cotte-Pattat N. The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics 2004, 4(10):3177-3186. 10.1002/pmic.200300814, 15378709.
76. Douet V, Expert D, Barras F, Py B. Erwinia chrysanthemi iron metabolism: the unexpected implication of the inner membrane platform within the type II secretion system. J Bacteriol 2009, 191(3):795-804. 10.1128/JB.00845-08, 2632095, 18978048.
77. Francetic O, Belin D, Badaut C, Pugsley AP. Expression of the endogenous type II secretion pathway in Escherichia coli leads to chitinase secretion. EMBO J 2000, 19(24):6697-6703. 10.1093/emboj/19.24.6697, 305903, 11118204.
78. Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, Humphris S, Burr T, Takle G, Brurberg MB, Birch PR, et al. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 2008, 4(6):e1000093. 10.1371/journal.ppat.1000093, 2413422, 18566662.
79. Yang CH, Gavilanes-Ruiz M, Okinaka Y, Vedel R, Berthuy I, Boccara M, Chen JW, Perna NT, Keen NT. hrp genes of Erwinia chrysanthemi 3937 are important virulence factors. Mol Plant Microbe Interact 2002, 15(5):472-480. 10.1094/MPMI.2002.15.5.472, 12036278.
80. Bell KS, Sebaihia M, Pritchard L, Holden MT, Hyman LJ, Holeva MC, Thomson NR, Bentley SD, Churcher LJ, Mungall K, et al. Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci USA 2004, 101(30):11105-11110. 10.1073/pnas.0402424101, 503747, 15263089.
81. Kim HS, Ma B, Perna NT, Charkowski AO. Phylogeny and virulence of naturally occurring type III secretion system-deficient Pectobacterium strains. Appl Environ Microbiol 2009, 75(13):4539-4549. 10.1128/AEM.01336-08, 2704834, 19411432.
82. Yap MN, Yang CH, Barak JD, Jahn CE, Charkowski AO. The Erwinia chrysanthemi type III secretion system is required for multicellular behavior. J Bacteriol 2005, 187(2):639-648. 10.1128/JB.187.2.639-648.2005, 543537, 15629935.
83. Rojas CM, Ham JH, Deng WL, Doyle JJ, Collmer A. HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc Natl Acad Sci USA 2002, 99(20):13142-13147. 10.1073/pnas.202358699, 130600, 12271135.
84. Wuichet K, Alexander RP, Zhulin IB. Comparative genomic and protein sequence analyses of a complex system controlling bacterial chemotaxis. Methods Enzymol 2007, 422:1-31. 2754700, 17628132.
85. Bibikov SI, Biran R, Rudd KE, Parkinson JS. A signal transducer for aerotaxis in Escherichia coli. J Bacteriol 1997, 179(12):4075-4079. 179224, 9190831.
86. Evans AA, Lauga E. Propulsion by passive filaments and active flagella near boundaries. Phys Rev E Stat Nonlin Soft Matter Phys 2010, 82(4 Pt 1):041915.
87. Mulholland V, Hinton JC, Sidebotham J, Toth IK, Hyman LJ, Perombelon MC, Reeves PJ, Salmond GP. A pleiotropic reduced virulence (Rvi-) mutant of Erwinia carotovora subspecies atroseptica is defective in flagella assembly proteins that are conserved in plant and animal bacterial pathogens. Mol Microbiol 1993, 10(5):1154. 10.1111/j.1365-2958.1993.tb00986.x, 7934865.
88. Jahn CE, Willis DK, Charkowski AO. The flagellar sigma factor fliA is required for Dickeya dadantii virulence. Mol Plant Microbe Interact 2008, 21(11):1431-1442. 10.1094/MPMI-21-11-1431, 18842093.
89. Bouchart F, Boussemart G, Prouvost AF, Cogez V, Madec E, Vidal O, Delrue B, Bohin JP, Lacroix JM. The virulence of a Dickeya dadantii3937 mutant devoid of osmoregulated periplasmic glucans is restored by inactivation of the RcsCD-RcsB phosphorelay. J Bacteriol 2010, 192(13):3484-3490. 10.1128/JB.00143-10, 2897653, 20418397.
90. Evans TJ, Ind A, Komitopoulou E, Salmond GP. Phage-selected lipopolysaccharide mutants of Pectobacterium atrosepticum exhibit different impacts on virulence. J Appl Microbiol 2010, 109(2):505-514.
91. Toth IK, Thorpe CJ, Bentley SD, Mulholland V, Hyman LJ, Perombelon MC, Salmond GP. Mutation in a gene required for lipopolysaccharide and enterobacterial common antigen biosynthesis affects virulence in the plant pathogen Erwinia carotovora subsp. atroseptica. Mol Plant Microbe Interact 1999, 12(6):499-507. 10.1094/MPMI.1999.12.6.499, 10356801.
92. Kotoujansky A, Diolez A, Boccara M, Bertheau Y, Andro T, Coleno A. Molecular cloning of Erwinia chrysanthemi pectinase and cellulase structural genes. EMBO J 1985, 4(3):781-785. 554256, 16453606.
93. Page F, Altabe S, Hugouvieux-Cotte-Pattat N, Lacroix JM, Robert-Baudouy J, Bohin JP. Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity. J Bacteriol 2001, 183(10):3134-3141. 10.1128/JB.183.10.3134-3141.2001, 95214, 11325942.
94. Bender CL, Alarcon-Chaidez F, Gross DC. Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 1999, 63(2):266-292. 98966, 10357851.
95. Bignell DR, Seipke RF, Huguet-Tapia JC, Chambers AH, Parry RJ, Loria R. Streptomyces scabies 87-22 contains a coronafacic acid-like biosynthetic cluster that contributes to plant-microbe interactions. Mol Plant Microbe Interact 2010, 23(2):161-175. 10.1094/MPMI-23-2-0161, 20064060.
96. Grenier AM, Duport G, Pages S, Condemine G, Rahbe Y. The phytopathogen Dickeya dadantii(Erwinia chrysanthemi3937) is a pathogen of the pea aphid. Appl Environ Microbiol 2006, 72(3):1956-1965. 10.1128/AEM.72.3.1956-1965.2006, 1393189, 16517643.
97. Costechareyre D, Dridi B, Rahbe Y, Condemine G. Cyt toxin expression reveals an inverse regulation of insect and plant virulence factors of Dickeya dadantii. Environ Microbiol 2010, 12(12):3290-3301. 10.1111/j.1462-2920.2010.02305.x, 20649641.
98. Nasser W, Faelen M, Hugouvieux-Cotte-Pattat N, Reverchon S. Role of the nucleoid-associated protein H-NS in the synthesis of virulence factors in the phytopathogenic bacterium Erwinia chrysanthemi. Mol Plant Microbe Interact 2001, 14(1):10-20. 10.1094/MPMI.2001.14.1.10, 11194867.
99. Nasser W, Robert-Baudouy J, Reverchon S. Antagonistic effect of CRP and KdgR in the transcription control of the Erwinia chrysanthemi pectinolysis genes. Mol Microbiol 1997, 26(5):1071-1082. 10.1046/j.1365-2958.1997.6472020.x, 9426143.
100. Nasser W, Reverchon S. H-NS-dependent activation of pectate lyases synthesis in the phytopathogenic bacterium Erwinia chrysanthemi is mediated by the PecT repressor. Mol Microbiol 2002, 43(3):733-748. 10.1046/j.1365-2958.2002.02782.x, 11929528.
101. Reverchon S, Expert D, Robert-Baudouy J, Nasser W. The cyclic AMP receptor protein is the main activator of pectinolysis genes in Erwinia chrysanthemi. J Bacteriol 1997, 179(11):3500-3508. 179141, 9171393.
102. Sepulchre JA, Reverchon S, Nasser W. Modeling the onset of virulence in a pectinolytic bacterium. J Theor Biol 2007, 244(2):239-257. 10.1016/j.jtbi.2006.08.010, 17005207.
103. Lebeau A, Reverchon S, Gaubert S, Kraepiel Y, Simond-Cote E, Nasser W, Van Gijsegem F. The GacA global regulator is required for the appropriate expression of Erwinia chrysanthemi3937 pathogenicity genes during plant infection. Environ Microbiol 2008, 10(3):545-559. 10.1111/j.1462-2920.2007.01473.x, 18177376.
104. Praillet T, Reverchon S, Robert-Baudouy J, Nasser W. The PecM protein is necessary for the DNA-binding capacity of the PecS repressor, one of the regulators of virulence-factor synthesis in Erwinia chrysanthemi. FEMS Microbiol Lett 1997, 154(2):265-270. 10.1111/j.1574-6968.1997.tb12654.x, 9311123.
105. Perera IC, Grove A. Urate is a ligand for the transcriptional regulator PecS. J Mol Biol 2010, 402(3):539-551. 10.1016/j.jmb.2010.07.053, 20678501.
106. Praillet T, Reverchon S, Nasser W. Mutual control of the PecS/PecM couple, two proteins regulating virulence-factor synthesis in Erwinia chrysanthemi. Mol Microbiol 1997, 24(4):803-814. 10.1046/j.1365-2958.1997.3901755.x, 9194707.
107. Glasner JD, Marquez-Villavicencio M, Kim HS, Jahn CE, Ma B, Biehl BS, Rissman AI, Mole B, Yi X, Yang CH, et al. Niche-specificity and the variable fraction of the Pectobacterium pan-genome. Mol Plant Microbe Interact 2008, 21(12):1549-1560. 10.1094/MPMI-21-12-1549, 18986251.
108. Liu Y, Chatterjee A, Chatterjee AK. Nucleotide sequence, organization and expression of rdgA and rdgB genes that regulate pectin lyase production in the plant pathogenic bacterium Erwinia carotovora subsp. carotovora in response to DNA-damaging agents. Mol Microbiol 1994, 14(5):999-1010. 10.1111/j.1365-2958.1994.tb01334.x, 7715460.
109. Nguyen HA, Kaneko J, Kamio Y. Temperature-dependent production of carotovoricin Er and pectin lyase in phytopathogenic Erwinia carotovora subsp. carotovora Er. Biosci Biotechnol Biochem 2002, 66(2):444-447. 10.1271/bbb.66.444, 11999425.
110. Reverchon S, Chantegrel B, Deshayes C, Doutheau A, Cotte-Pattat N. New synthetic analogues of N-acyl homoserine lactones as agonists or antagonists of transcriptional regulators involved in bacterial quorum sensing. Bioorg Med Chem Lett 2002, 12(8):1153-1157. 10.1016/S0960-894X(02)00124-5, 11934577.
111. Rodionov DA, Gelfand MS, Hugouvieux-Cotte-Pattat N. Comparative genomics of the KdgR regulon in Erwinia chrysanthemi3937 and other gamma-proteobacteria. Microbiology 2004, 150(Pt 11):3571-3590.
112. Hugouvieux-Cotte-Pattat N, Robert-Baudouy J. Isolation of Erwinia chrysanthemi mutants altered in pectinolytic enzyme production. Mol Microbiol 1989, 3(11):1587-1597. 10.1111/j.1365-2958.1989.tb00144.x, 2693903.
113. Boysen A, Moller-Jensen J, Kallipolitis B, Valentin-Hansen P, Overgaard M. Translational regulation of gene expression by an anaerobically induced small non-coding RNA in Escherichia coli. J Biol Chem 2010, 285(14):10690-10702. 10.1074/jbc.M109.089755, 2856277, 20075074.
114. Durand S, Storz G. Reprogramming of anaerobic metabolism by the FnrS small RNA. Mol Microbiol 2010, 75(5):1215-1231. 10.1111/j.1365-2958.2010.07044.x, 2941437, 20070527.
115. Mandin P, Gottesman S. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 2010, 29(18):3094-3107. 10.1038/emboj.2010.179, 2944060, 20683441.
116. Gottesman S. Small RNAs shed some light. Cell 2004, 118(1):1-2. 10.1016/j.cell.2004.06.024, 15242637.
117. Brown S, Fournier MJ. The 4.5 S RNA gene of Escherichia coli is essential for cell growth. J Mol Biol 1984, 178(3):533-550. 10.1016/0022-2836(84)90237-7, 6208371.
118. Wickstrom D, Wagner S, Baars L, Ytterberg AJ, Klepsch M, van Wijk KJ, Luirink J, de Gier JW. Consequences of depletion of the signal recognition particle in Escherichia coli. J Biol Chem 2011, 286(6):4598-4609. 10.1074/jbc.M109.081935, 3039323, 20923772.
119. Gopel Y, Luttmann D, Heroven AK, Reichenbach B, Dersch P, Gorke B. Common and divergent features in transcriptional control of the homologous small RNAs GlmY and GlmZ in Enterobacteriaceae. Nucleic Acids Res 2011, 39(4):1294-1309. 10.1093/nar/gkq986, 3045617, 20965974.
120. Urban JH, Vogel J. Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 2008, 6(3):e64. 10.1371/journal.pbio.0060064, 2267818, 18351803.
121. Urban JH, Vogel J. Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 2007, 35(3):1018-1037. 10.1093/nar/gkl1040, 1807950, 17264113.
122. Reichenbach B, Maes A, Kalamorz F, Hajnsdorf E, Gorke B. The small RNA GlmY acts upstream of the sRNA GlmZ in the activation of glmS expression and is subject to regulation by polyadenylation in Escherichia coli. Nucleic Acids Res 2008, 36(8):2570-2580. 10.1093/nar/gkn091, 2377431, 18334534.
123. Gorke B, Vogel J. Noncoding RNA control of the making and breaking of sugars. Genes Dev 2008, 22(21):2914-2925. 10.1101/gad.1717808, 18981470.
124. Liu Y, Cui Y, Mukherjee A, Chatterjee AK. Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Mol Microbiol 1998, 29(1):219-234. 10.1046/j.1365-2958.1998.00924.x, 9701816.
125. Mukherjee A, Cui Y, Ma W, Liu Y, Chatterjee AK. hexA of Erwinia carotovora ssp. carotovora strain Ecc71 negatively regulates production of RpoS and rsmB RNA, a global regulator of extracellular proteins, plant virulence and the quorum-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. 215 2000, 2(2):203.
126. Yang S, Peng Q, Zhang Q, Yi X, Choi CJ, Reedy RM, Charkowski AO, Yang CH. Dynamic regulation of GacA in type III secretion, pectinase gene expression, pellicle formation, and pathogenicity of Dickeya dadantii(Erwinia chrysanthemi3937). Mol Plant Microbe Interact 2008, 21(1):133-142. 10.1094/MPMI-21-1-0133, 18052890.
127. Vogel J, Bartels V, Tang TH, Churakov G, Slagter Jager JG, Huttenhofer A, Wagner EGH. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 2003, 31(22):6435-6443. 10.1093/nar/gkg867, 275561, 14602901.
128. Hayes ET, Wilks JC, Sanfilippo P, Yohannes E, Tate DP, Jones BD, Radmacher MD, BonDurant SS, Slonczewski JL. Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12. BMC Microbiol 2006, 6:89. 10.1186/1471-2180-6-89, 1626474, 17026754.
129. Guillier M, Gottesman S. The 5' end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res 2008, 36(21):6781-6794. 10.1093/nar/gkn742, 2588501, 18953042.
130. Guillier M, Gottesman S. Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 2006, 59(1):231-247. 10.1111/j.1365-2958.2005.04929.x, 16359331.
131. Adhya S. Suboperonic regulatory signals. Sci STKE 2003 2003, (185):pe22.
132. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 2001, 11(12):941-950. 10.1016/S0960-9822(01)00270-6, 11448770.
133. Geissen R, Steuten B, Polen T, Wagner R. E. coli 6S RNA: A universal transcriptional regulator within the centre of growth adaptation. RNA Biol 2010, 7(5):564-568. 10.4161/rna.7.5.12969, 20930516.
134. Rivas E, Klein RJ, Jones TA, Eddy SR. Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol 2001, 11(17):1369-1373. 10.1016/S0960-9822(01)00401-8, 11553332.
135. Moller T, Franch T, Udesen C, Gerdes K, Valentin-Hansen P. Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 2002, 16(13):1696-1706. 10.1101/gad.231702, 186370, 12101127.
136. Polayes DA, Rice PW, Dahlberg JE. DNA polymerase I activity in Escherichia coli is influenced by spot 42 RNA. J Bacteriol 1988, 170(5):2083-2088. 211090, 2452153.
137. Sutton VR, Kiley PJ. Techniques for studying the oxygen-sensitive transcription factor FNR from Escherichia coli. Methods Enzymol 2003, 370:300-312.
138. Bernstein JA, Lin P-H, Cohen SN, Lin-Chao S. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. PNAS 2004, 101(9):2758-2763. 10.1073/pnas.0308747101, 365694, 14981237.
139. Dufour YS, Wesenberg GE, Tritt AJ, Glasner JD, Perna NT, Mitchell JC, Donohue TJ. chipD: a web tool to design oligonucleotide probes for high-density tiling arrays. Nucleic Acids Res 2010, 38(Suppl):W321-325. 2896189, 20529880.
140. Team RDC R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing 2011, Team RDC.
141. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5(10):R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
142. Sathesh-Kumar S, Sridhar J, Rafi ZA. sRNAbase: A web resource for small RNAs in Enterobacteriaceae. Silico Biol 2009, (9):35.
143. Glasner JD, Liss P, Plunkett G, Darling A, Prasad T, Rusch M, Byrnes A, Gilson M, Biehl B, Blattner FR, et al. ASAP, a systematic annotation package for community analysis of genomes. Nucleic Acids Res 2003, 31(1):147-151. 10.1093/nar/gkg125, 165572, 12519969.
144. Keseler IM, Collado-Vides J, Gama-Castro S, Ingraham J, Paley S, Paulsen IT, Peralta-Gil M, Karp PD. EcoCyc: a comprehensive database resource for Escherichia coli. Nucleic Acids Res 2005, (33 Database):D334-D337.