The 3-hydroxy-2-butanone pathway is required for pectobacterium carotovorum pathogenesis

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  del Pilar Marquez Villavicencio, Marial ^a   Weber, Brooke ^a   Witherell, R Andrews ^a   Willis, David K ^a,b   Charkowski, Amy O ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b U S DAIRY FORAGE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 BUTANEDIOL; ACETOIN; ACETOLACTATE SYNTHASE;

ALKALINIZATION; ANAEROBIC CELL CULTURE; ARTICLE; BACTERIAL GROWTH; BACTERIAL PLANT DISEASE; BACTERIAL VIRULENCE; CONTROLLED STUDY; CULTURE MEDIUM; ENTEROBACTERIACEAE INFECTION; GENE EXPRESSION PROFILING; INOCULATION; NONHUMAN; PATHOGENESIS; PECTOBACTERIUM CAROTOVORUM; PH MEASUREMENT; PLANT CELL CULTURE; PLANT GROWTH; PLANT STEM; PLANT TISSUE CULTURE; POTATO; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); HEXAPODA; PECTOBACTERIUM; PECTOBACTERIUM CAROTOVORUM; PECTOBACTERIUM CAROTOVORUM SUBSP. CAROTOVORUM; SOLANUM TUBEROSUM;

EID: 84860411418     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022974     Document Type: Article

References (79)

1. Huang M, Oppermann-Sanio FB, Steinbüchel A, (1999) Biochemical and molecular characterization of the Bacillus subtilis acetoin catabolic pathway. J Bacteriol 181: 3837-3841.
2. Lopez JM, Thoms B, Rehbein H, (1975) Acetoin degradation in Bacillus subtilis by direct oxidative cleavage. Eur J Biochem 57: 425-430.
3. Levine M, (1916) On the significance of the Voges-Proskauer reaction. J Bacteriol 1: 153-164.
4. Xiao Z, Xu P, (2007) Acetoin metabolism in bacteria. Crit Rev Micobiol 33: 127-140.
5. Yoon SS, Mekalanos JJ, (2006) 2,3-butanediol synthesis and the emergence of the Vibrio cholerae El Tor biotype. Infect Immun 74: 6574-6556.
6. Johansen L, Bryn K, Stormer FC, (1975) Physiological and biochemical role of the butanediol pathway in Aerobacter (Enterobacter) aerogenes. J Bacteriol 123: 1124-1130.
7. Mayer D, Schlensog V, Bock A, (1995) Identification of the transcriptional activator controlling the butanediol fermentation pathway in Klebsiella terrigena. J Bacteriol 177: 5261-5269.
8. Grundy FJ, Waters DA, Takova TY, Henkin TM, (1993) Identification of genes involved in utilization of acetate and acetoin in Bacillus subtilis. Mol Microbiol 10: 259-271.
9. Wevers E, Moons P, Van Houdt R, Lurquin I, Aertsen A, et al. (2009) Quorum sensing and butanediol fermentation affect colonization and spoilage of carrot slices by Serratia plymuthica. Int J Food Microbiol 134: 63-69.
10. Hsieh S-C, Lu C-C, Horng Y-T, Soo P-C, Chang Y-L, et al. (2007) The bacterial metabolite 2,3-butanediol ameliorates endotoxin-induced acute lung injury in rats. Microbes Infect 9: 1402-1409.
11. van Rooy FGBGJ, Rooyackers JM, Prokop M, Houba R, Smit LAM, et al. (2007) Bronchiolitis obliterans syndrome in chemical workers producing diacetyl for food flavorings. Amer J Respiratory Crit Care Med 176: 498-504.
12. Nout MJR, Bartelt RJ, (1998) Attraction of a flying nitidulid (Carpophilus humeralis) to volatiles produced by yeasts grown on sweet corn and a corn-based medium. J Chem Ecol 24: 1217-1239.
13. Buttery RG, Kamm JA, Ling LC, (1984) Volatile components of red clover leaves, flowers, and seed pods: possible insect attractants. J Agric Food Chem 32: 254-256.
14. Moore AJ, Moore PJ, (1999) Balancing sexual selection through opposing mate choice and male competition. Proc R Soc Lond B Biol Sci 266: 711-716.
15. Moore AJ, Haynes KF, Preziosi RF, Moore PJ, (2002) The evolution of interacting phenotypes: genetics and evolution of social dominance. Am Nat 160: 5186-5197.
16. Rochat D, Morin JP, Kakul T, Beaudoin-Ollivier L, Prior R, et al. (2002) Activity of male pheromone of Melanesian rhinoceros beetle Scapanes australis. J Chem Ecol 28: 479-500.
17. Bengtsson JM, Wolde-Hawariat Y, Khbaish H, Negash M, Jembere B, et al. (2009) Field attractants for Pachnoda interrupta selected by means of GC-EAD and single sensillum screening. J Chem Ecol 35: 1063-1076.
18. Robacker DC, Lauzon CR, (2002) Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly. J Chem Ecol 28: 1549-1563.
19. Turner SL, Ray A, (2009) Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 461: 277-281.
20. Moore AJ, Gowaty PA, Moore PJ, (2003) Females avoid manipulative males and live longer. J Evol Biol 16: 523-530.
21. Moore AJ, Gowaty PA, Moore PJ, (2001) Sexual conflict and the evolution of female mate choice and male social dominance. Proc R Soc Lond B Biol Sci 268: 517-523.
22. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, et al. (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100: 4927-4932.
23. Ryu CM, Farag AF, Hu C, Reddy MS, Kloepper JW, et al. (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134: 1017-1026.
24. Cho SM, Kang BR, Han SH, Anderson AJ, Park J-Y, et al. (2008) 2R,3R-butandiol, a bacterial volatile produced by Pseudomonas chlororaphis 06, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant-Microbe Interact 21: 1067-1075.
25. Brenner DJ, Krieg NR, Staley JT, Garrity GM, (2004) The Proteobacteria Berlin, New York, London Springer.
26. Ma B, Hibbing ME, Kim H-S, Reedy RM, Yedidia I, et al. (2007) The host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97: 1150-1163.
27. Vikram A, Lui LH, Hossain A, Kushalappa AC, (2006) Metabolic fingerprinting to discriminate disease of stored carrots. Ann Appl Biol 148: 17-26.
28. Lui LH, Vikram A, Abu-Nada Y, Kushalappa AC, Raghavan GSV, et al. (2005) Volatile metabolic profiling for discrimination of potato tubers inoculated with dry and soft rot pathogens. Amer J Potato Res 82: 1-8.
29. Leach JG, (1926) The relation of the seed-corn maggot (Phorbia fuciceps Zett.) to the spread and development of potato blackleg in Minnesota. Phytopathol 16: 149-176.
30. Howard CM, Leach JG, (1963) Relation of the iris borer to bacterial soft rot of iris. Phytopathology 53: 1190-1193.
31. Dalmacio SC, Lugod TR, Serrano EM, Munkvold GP, (2007) Reduced incidence of bacterial rot on transgenic insect-resistant maize in the Philippines. Plant Dis 91: 346-351.
32. Thind BS, Singh N, (1976) Maize borer [Chilo partellus (Swinhoe)] as carrier of Erwinia carotovora var. zeae, tha causal agent of bacterial stalk rot of maize. Curr Sci 45: 117-118.
33. Leach JG, (1931) Further studies on the seed-corn maggot and bacteria with special reference to potato blackleg. Phytopathol 21: 387-406.
34. Leach JG, (1933) The method of survival of bacteria in the puparia of the seed-corn maggot (Hylemyia cilicrura Rond.). Zeitschr fur angewondte Entomologie 20: 150-161.
35. Harrison MD, Quinn CE, Sells A, Graham DC, (1977) Waste potato dumps as sources of insects contaminated with soft rot coliform bacteria in relation to re-contamination of pathogen-free potato stocks. Potato Res 20: 37-52.
36. Kloepper JW, Brewer JW, Harrison MD, (1981) Insect transmission of Erwinia carotovora var. carotovora and Erwinia carotovora var. atroseptica to potato plants in the field. Am Potato J 58: 165-175.
37. Kloepper JW, Harrison MD, Brewer JW, (1979) The association of Erwinia carotovora var. atroseptica and Erwinia carotovora var. carotovora with insects in Colorado. Am Potato J 56: 351-361.
38. Kloepper JW, Harrison MD, Brewer JW, (1981) Effect of temperature on differential persistence and insect transmission of Erwinia carotovora var. Atroseptica and Erwinia carotovora var. Carotovora. The American Potato Journal 58: 585-592.
39. Phillips JA, Kelman A, (1982) Direct fluorescent antibody stain procedure applied to insect transmission of Erwinia carotovora. Phytopathology 72: 898-901.
40. Grenier AM, Duport G, Pages S, Condemine G, Rahbe Y, (2006) The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. Appl Environ Microbiol 72: 1956-1965.
41. Molina JM, Harrison D, Brewer JW, (1974) Transmission of Erwinia carotovora var. atroseptica by Drosophila melanogaster Meig. I. Acquisition and transmission of the bacterium. Am Potato J 51: 245-250.
42. Toth IK, Bell KS, Holeva MC, Birch PRJ, (2003) Soft rot erwiniae: from genes to genomes. Mol Plant Pathol 4: 17-30.
43. Barras F, Van Gijsegem F, Chatterjee AK, (1994) Extracellular enzymes and pathogenesis of soft rot Erwinia. Annu Rev Phytopathol 32: 210-234.
44. Lei S-P, Lin H-C, Wang S-S, Callaway J, Wilcox G, (1987) Characterization of the Erwinia carotovora pelB gene and its product pectate lyase. J Bacteriol 169: 4379-4383.
45. Lei S-P, Lin H-C, Wang S-S, Wilcox G, (1988) Characterization of the Erwinia carotovora pelA gene and its product pectate lyase A. Gene 62: 159-164.
46. Grignon C, Sentenac H, (1991) pH and ionic conditions in the apoplast. Ann Rev Plant Physiol 42: 103-128.
47. Nachin L, Barras F, (2000) External pH: an environmental signal that helps to rationalize pel gene duplication in Erwinia chrysanthemi. Mol Plant Microbe Interact 13: 882-886.
48. Jahn CE, Charkowski AO, Willis DK, (2008) Evaluation of isolation methods and RNA integrity for bacterial RNA quantitation. Jounal of Microbiological Methods 75: 318-324.
49. Linchao S, Bremer H, (1986) Effect of the bacterial-growth rate on replication control of plasmid pBR322 in Escherichia coli. Mol Gen Genet 203: 143-149.
50. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622.
51. Ried JL, Collmer A, (1986) Comparison of pectic enzymes produced by Erwinia chrysanthemi, Erwinia carotovora subsp. carotovora, and Erwinia carotovora subsp. atroseptica. Appl Environ Microbiol 52: 305-310.
52. Sambrook J, Russell DW, (2001) Molecular Cloning. A Laboratory Manual Cold Spring Harbor Cold Spring Harbor Laboratory Press.
53. Llama-Palacios A, Lopez-Solanilla E, Rodriguez-Palenzuela P, (2002) The ybiT gene of Erwinia chrysanthemi codes for a putative ABC transporter and is involved in competitiveness against endophytic bacteria during infection. Applied and Environmental Microbiology 68: 1624-1630.
54. Haberlach GT, Cohen BA, Reichert NA, Baer MA, Towill LE, et al. (1985) Isolation, culture and regeneration of protoplasts from potato and several related Solanum species. Plant Sci 39: 67-74.
55. Rotenberg DT, Thompson TS, German TL, Willis DK, (2006) Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. Virological Methods pp. 1-11.
56. Renna MC, Najimudin N, Winik LR, Zahler SA, (1993) Regulation of the Bacillus subtilis alsS, alsD, and alsR genes involved in post-exponential-phase production of acetoin. J Bacteriol 175: 3863-3875.
57. Blomqvist K, Nikkola M, Lehtovaara P, Suihko ML, Airaksinen U, et al. (1993) Characterization of genes of the 2,3-butanediol operons from Klebsiella terrigena and Enterobacter aerogenes. J Bacteriol 175: 1392-1404.
58. Mayer D, Schlensog V, Böck A, (1995) Identification of the transcriptional activator controlling the butanediol fermentation pathway in Klebsiella terrigena. J Bacteriol 177: 5261-5269.
59. Geraats BP, Bakker PA, Lawrence CB, Achuo EA, Höfte M, et al. (2003) Ethylene-insensitive tobacco shows differentially altered susceptibility to different pathogens. Phytopathology 93: 813-821.
60. 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: e1000093 doi:1000010.1001371/journal.ppat.1000093.
61. Moons P, Van Houdt R, Vivijs B, Michiels CM, Aertsen A, (2011) Integrated regulation of acetoin fermentation by quorum sensing and pH in Serratia plymuthica RVH1. Appl Environ Microbiol.
62. Kovacikova G, Lin W, Skorupski K, (2005) Dual regulation of genes involved in acetoin biosynthesis and motility/biofilm formation by the virulence activator AphA and the acetate-responsive LysR-type regulator AlsR in Vibrio cholerae. Mol Microbiol 57: 420-433.
63. Kovacikova G, Lin W, Skorupsk iK, (2010) The LysR-type virulence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobiosis. J Bacteriol 192: 4181-4191.
64. Kramer-Haimovich H, Servi E, Katan T, Rollins J, Okon Y, et al. (2006) Effect of ammonia production by Colletotrichum gloeosporioides on pelB activation, pectate lyase secretion, and fruit pathogenicity. Appl Environ Microbiol 72: 1034-1039.
65. Glasner JD, Liss P, Plunkett G, Darling A, Prasad T, et al. (2003) ASAP, a systematic annotation package for community analysis of genomes. Nucl Acids Res 31: 147-151.
66. Glasner JD, Rusch M, Liss P, Plunkett G 3rd, Cabot EL, et al. (2006) ASAP: a resource for annotating, curating, comparing, and disseminating genomic data. Nucl Acids Res 34: D41-45.
67. Fründ C, Priefert H, Steinbüchel A, Schlegel HG, (1989) Biochemical and genetic analyses of acetoin catabolism in Alcaligenes eutrophus. J Bacteriol 171: 6539-6548.
68. Wells JM, Butterfield JE, (1997) Salmonella contamination associated with bacterial soft rot of fresh fruits and vegetables in the marketplace. Plant Dis 81: 867-872.
69. Brandl MT, (2008) Plant lesions promote the rapid multiplication of Escherichia coli O157:H7 on postharvest lettuce. Appl Environ Microbiol 74: 5285-5289.
70. Noel JT, Joy J, Smith JN, Fatica M, Schneider KR, et al. (2010) Salmonella SdiA recognizes N-acyl homoserine lactone signals from Pectobacterium carotovorum in vitro, but not in a bacterial soft rot. Mol Plant-Microbe Interact 23: 273-282.
71. Pérombelon MCM, Gullings-Handley J, Kelman A, (1979) Population dynamics of Erwinia carotovora and pectolytic Clostridium spp. in relation to decay of potatoes. Phytopathol 69: 167-173.
72. Byers JT, Lucas C, Salmond GPC, Welch M, (2002) Nonenzymatic turnover of an Erwinia carotovora quorum-sensing signaling molecule. J Bacteriol 184: 1163-1171.
73. Dindonis LL, Miller JR, (1980) Host-finding responses of onion and seedcorn flies to healthy and decomposing onions and several synthetic constituents of onion. Environ Entomol 9: 467-472.
74. Purcell AH, (1982) Insect vector relationships with procaryotic plant pathogens. Ann Rev Phytopathol 20: 397-417.
75. Yap M-N, Barak JD, Charkowski AO, (2004) Genomic diversity of Erwinia carotovora subsp. carotovora and its correlation with virulence. Appl Environ Microbiol 70: 3013-3023.
76. Glasner JD, Marquez-Villavicencio M, Kim H-S, Jahn CE, Ma B, et al. (2008) Niche-specificity and the variable fraction of the Pectobacterium pan-genome. Mol Plant-Microbe Interact 21: 1549-1560.
77. Bogdanove AJ, Bauer DW, Beer SV, (1998) Erwinia amylovora secretes DspE, a pathogenicity factor and functional AvrE homolog, through the Hrp (type III secretion) pathway. J Bacteriol 180: 2244-2247.
78. Fellay R, Frey J, Krisch H, (1987) Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 52: 147-154.
79. 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.