The Salmonella transcriptome in lettuce and cilantro soft rot reveals a niche overlap with the animal host intestine

Applied and Environmental Microbiology

Volumn 79, Issue 1, 2013, Pages 250-262

  Goudeau, Danielle M ^a   Parker, Craig T ^a   Zhou, Yaguang ^a   Sela, Shlomo ^b   Kroupitski, Yulia ^b   Brandl, Maria T ^a  

^a WESTERN REGIONAL RESEARCH CENTER   (United States)

^b VOLCANI CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC CONDITIONS; ANAEROBIC METABOLISM; CHICKEN INTESTINES; COFACTORS; ETHANOLAMINES; EXPRESSION LEVELS; FRESH VEGETABLES; MULTIPLE GENES; PARENTAL STRAINS; PLANT CELLS; PLANT TISSUES; POPULATION SIZES; POST-HARVEST PLANTS; PROPANEDIOLS; S. TYPHIMURIUM; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SOFT-ROT; TRANSCRIPTOME ANALYSIS; TRANSCRIPTOMES; WILD-TYPE STRAIN;

GENE EXPRESSION; MAMMALS; PLANTS (BOTANY); POPULATION STATISTICS; TISSUE;

SALMONELLA;

TRANSCRIPTOME;

BACTERIUM; DISEASE SPREAD; GENE EXPRESSION; LEAFY VEGETABLE; LESION; NICHE OVERLAP; POPULATION SIZE;

ANAEROBIC GROWTH; ANIMAL; ARTICLE; CATTLE; CHICKEN; COMPARATIVE STUDY; CORIANDRUM; FERMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTESTINE; LETTUCE; METABOLISM; MICROBIOLOGY; MOUSE; SALMONELLA TYPHIMURIUM; SWINE;

ANAEROBIOSIS; ANIMALS; CATTLE; CHICKENS; CORIANDRUM; FERMENTATION; INTESTINES; LETTUCE; METABOLIC NETWORKS AND PATHWAYS; MICE; SALMONELLA TYPHIMURIUM; SWINE; TRANSCRIPTOME;

ANIMALIA; BOVINAE; DICKEYA DADANTII; LACTUCA; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM; SUIDAE;

EID: 84871908950     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02290-12     Document Type: Article

References (79)

1. Brandl MT, Amundson R. 2008. Leaf age as a risk factor in contamination of lettuce with Escherichia coli O157:H7 and Salmonella enterica. Appl. Environ. Microbiol. 74:2298-2306.
2. Brandl MT, Mandrell RE. 2002. Fitness of Salmonella enterica serovar Thompson in the cilantro phyllosphere. Appl. Environ. Microbiol. 68: 3614-3621.
3. Brandl MT. 2006. Fitness of human enteric pathogens on plants and implications for food safety. Annu. Rev. Phytopathol. 44:367-392.
4. Aruscavage D, Miller SA, Ivey ML, Lee K, LeJeune JT. 2008. Survival and dissemination of Escherichia coli O157:H7 on physiologically and biologically damaged lettuce plants. J. Food Prot. 71:2384-2388.
5. Brandl MT. 2008. Plant lesions promote the rapid multiplication of Escherichia coli O157:H7 on postharvest lettuce. Appl. Environ. Microbiol. 74:5285-5289.
6. Kyle JL, Parker CT, Goudeau D, Brandl MT. 2010. Transcriptome analysis of Escherichia coli O157:H7 exposed to lysates of lettuce leaves. Appl. Environ. Microbiol. 76:1375-1387.
7. Wells JM, Butterfield JE. 1999. Incidence of Salmonella on fresh fruits and vegetables affected by fungal rots and physical injury. Plant Dis. 83: 722-726.
8. 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.
9. Yamazaki A, Li J, Hutchins WC, Wang L, Ma J, Ibekwe AM, Yang CH. 2011. Commensal effect of pectate lyases secreted from Dickeya dadantii on proliferation of Escherichia coli O157:H7 EDL933 on lettuce leaves. Appl. Environ. Microbiol. 77:156-162.
10. Noel JT, Joy J, Smith JN, Fatica M, Schneider KR, Ahmer BM, Teplitski M. 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.
11. Carlin F, Nguyen-the C, Da Silva AA. 1995. Factors affecting the growth of Listeria monocytogenes on minimally processed fresh endive. J. Appl. Microbiol. 78:636-646.
12. Liao CH, Sapers GM. 1999. Influence of soft rot bacteria on growth of Listeria monocytogenes on potato tuber slices. J. Food Prot. 62:343-348.
13. Conway WS, Leverentz B, Saftner RA, Janisiewicz WJ, Sams CE, Leblanc E. 2000. Survival and growth of Listeria monocytogenes on fresh-cut apple slices and its interaction with Glomerella cingulata and Penicillium expansum. Plant Dis. 84:177-181.
14. Riordan DC, Sapers GM, Annous BA. 2000. The survival of Escherichia coli O157:H7 in the presence of Penicillium expansum and Glomerella cingulata in wounds on apple surfaces. J. Food Prot. 63:1637-1642.
15. Wade WN, Beuchat LR. 2003. Metabiosis of proteolytic moulds and Salmonella in raw, ripe tomatoes. J. Appl. Microbiol. 95:437-450.
16. Hoiseth SK, Stocker BA. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238-239.
17. 12-dependent anaerobic growth of Salmonella enterica serovar Typhimurium on ethanolamine or 1,2- propanediol. J. Bacteriol. 183:2463-2475.
18. Lemattre M, Narcy JP. 1972. A new bacterial infection of Saintpaulia ionantha by Erwinia chrysanthemi. C. R. Acad. Agric. Fr. 58:227-231.
19. 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.
20. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, II, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
21. Kofoid E, Rappleye C, Stojiljkovic I, Roth J. 1999. The 17-gene ethanolamine (eut) operon of Salmonella typhimurium encodes five homologues of carboxysome shell proteins. J. Bacteriol. 181:5317-5329.
22. Walter D, Ailion M, Roth J. 1997. Genetic characterization of the pdu operon: use of 1,2-propanediol in Salmonella typhimurium. J. Bacteriol. 179:1013-1022.
23. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. doi:10.1093/nar/29.9.e45.
24. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC. 2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103-118.
25. Rehfuss MYM, Parker CT, Brandl MT. 2011. Salmonella transcriptional signature in Tetrahymena phagosomes and role of acid tolerance in passage through the protist. ISME J. 5:262-273.
26. Dixon WJ. 1950. Analysis of extreme values. Ann. Math. Stat. 21:488-506.
27. Okinaka Y, Yang CH, Perna NT, Keen NT. 2002. Microarray profiling of Erwinia chrysanthemi 3937 genes that are regulated during plant infection. Mol. Plant Microbe Interact. 15:619-629.
28. Thony-Meyer L, Fischer F, Kunzler P, Ritz D, Hennecke H. 1995. Escherichia coli genes required for cytochrome c maturation. J. Bacteriol. 177:4321-4326.
29. Gilberthorpe NJ, Poole RK. 2008. Nitric oxide homeostasis in Salmonella Typhimurium. J. Biol. Chem. 283:11146-11154.
30. Mills PC, Rowley G, Spiro S, Hinton JCD, Richardson DJ. 2008. A combination of cytochrome c nitrite reductase (NrfA) and flavorubredoxin (NorV) protects Salmonella enterica serovar Typhimurium against killing by NO in anoxic environments. Microbiology 154:1218-1228.
31. Tseng CP, Albrecht J, Gunsalus RP. 1996. Effect of microaerophilic cell growth conditions on expression of the aerobic (cyoABCDE and cydAB) and anaerobic (narGHJI, frdABCD, and dmsABC) respiratory pathway genes in Escherichia coli. J. Bacteriol. 178:1094-1098.
32. Soo P-C, Horng Y-T, Lai M-J, Wei J-R, Hsieh S-C, Chang Y-L, Tsai Y-H, Lai H-C. 2007. Pirin regulates pyruvate catabolism by interacting with the pyruvate dehydrogenase E1 subunit and modulating pyruvate dehydrogenase activity. J. Bacteriol. 189:109-118.
33. Subramoni S, Gonzalez JF, Johnson A, Pechy-Tarr M, Rochat L, Paulsen I, Loper JE, Keel C, Venturi V. 2011. Bacterial subfamily of LuxR regulators that respond to plant compounds. Appl. Environ. Microbiol. 77:4579-4588.
34. Seim H, Löster H, Claus R, Kleber HP, Strack E. 1982. Stimulation of the anaerobic growth of Salmonella typhimurium by reduction of L-carnitine, carnitine derivatives and structure-related trimethylammonium compounds. Arch. Microbiol. 132:91-95.
35. Fraenkel G. 1953. Studies on the distribution of vitamin Bt (carnitine). Biol. Bull. 104:359-371.
36. Bourdin B, Adenier H, Perrin Y. 2007. Carnitine is associated with fatty acid metabolism in plants. Plant Physiol. Biochem. 45:926-931.
37. Bott M. 1997. Anaerobic citrate metabolism and its regulation in enterobacteria. Arch. Microbiol. 167:78-88.
38. Chen Y-T, Liao T-L, Wu K-M, Lauderdale T-L, Yan J-J, Huang IW, Lu M-C, Lai Y-C, Liu Y-M, Shu H-Y, Wang J-T, Su I-J, Tsai S-F. 2009. Genomic diversity of citrate fermentation in Klebsiella pneumoniae. BMC Microbiol. 9:168. doi:110.1186/1471-2180-1189-1168.
39. Roth JR, Lawrence JG, Bobik TA. 1996. Cobalamin (coenzyme B12): synthesis and biological significance. Annu. Rev. Microbiol. 50:137-181.
40. Chapman KD. 2004. Occurrence, metabolism, and prospective functions of N-acylethanolamines in plants. Prog. Lipid Res. 43:302-327.
41. Badia J, Ros J, Aguilar J. 1985. Fermentation mechanism of fucose and rhamnose in Salmonella typhimurium and Klebsiella pneumoniae. J. Bacteriol. 161:435-437.
42. Laatu M, Condemine G. 2003. Rhamnogalacturonate lyase RhiE is secreted by the Out system in Erwinia chrysanthemi. J. Bacteriol. 185:1642-1649.
43. Reiter W-D. 2002. Biosynthesis and properties of the plant cell wall. Curr. Opin. Plant Biol. 5:536-542.
44. Palacios S, Starai VJ, Escalante-Semerena JC. 2003. Propionyl coenzyme A is a common intermediate in the 1,2-propanediol and propionate catabolic pathways needed for expression of the prpBCDE operon during growth of Salmonella enterica on 1,2-propanediol. J. Bacteriol. 185:2802-2810.
45. Hensel M, Hinsley AP, Nikolaus T, Sawers G, Berks BC. 1999. The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol. Microbiol. 32:275-287.
46. Yang S, Perna NT, Cooksey DA, Okinaka Y, Lindow SE, Ibekwe AM, Keen NT, Yang C-H. 2004. Genome-wide identification of plantupregulated genes of Erwinia chrysanthemi 3937 using a GFP-based IVET leaf array. Mol. Plant Microbe Interact. 17:999-1008.
47. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC. 2006. Feo-transport of ferrous iron into bacteria. Biometals 19:143-157.
48. Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M, Kehl-Fie TE, Restrepo NA, Hosking MP, Edwards RA, Battistoni A, Pasquali P, Lane TE, Chazin WJ, Vogl T, Roth J, Skaar EP, Raffatellu M. 2012. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11:227-239.
49. Adams M, Jia Z. 2005. Structural and biochemical analysis reveal pirins to possess quercetinase activity. J. Biol. Chem. 280:28675-28682.
50. Fuchs G, Boll M, Heider J. 2011. Microbial degradation of aromatic compounds-from one strategy to four. Nat. Rev. Microbiol. 9:803-816.
51. Allocati N, Federici L, Masulli M, Di Ilio C. 2009. Glutathione transferases in bacteria. FEBS J. 276:58-75.
52. Gilberthorpe NJ, Lee ME, Stevanin TM, Read RC, Poole RK. 2007. NsrR: a key regulator circumventing Salmonella enterica serovar Typhimurium oxidative and nitrosative stress in vitro and in IFN-gammastimulated J774.2 macrophages. Microbiology 153:1756-1771.
53. Etsuko H, Mitsuoki M, Kazuei M, Isamu M, Hiroko Hideo H-IT, Sachiko I, Yutaka N. 1994. The methyl viologen-resistance-encoding gene smvA of Salmonella Typhimurium. Gene 148:173-174.
54. Deng K, Wang S, Rui X, Zhang W, Tortorello ML. 2011. Functional analysis of ycfR and ycfQ in Escherichia coli O157:H7 linked to outbreaks of illness associated with fresh produce. Appl. Environ. Microbiol. 77:3952-3959.
55. Dhawi AA, Elazomi A, Jones MA, Lovell MA, Li H, Emes RD, Barrow PA. 2011. Adaptation to the chicken intestine in Salmonella Enteritidis PT4 studied by transcriptional analysis. Vet. Microbiol. 153:198-204.
56. Wilson M, Lindow SE. 1994. Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl. Environ. Microbiol. 60:4468-4477.
57. Hugouvieux-Cotte-Pattat N, Condemine G, Nasser W, Reverchon S. 1996. Regulation of pectinolysis in Erwinia chrysanthemi. Annu. Rev. Microbiol. 50:213-257.
58. Smid EJ, Jansen AHJ, Tuijn CJ. 1993. Anaerobic nitrate respiration by Erwinia carotovora subsp. atroseptica during potato tuber invasion. Appl. Environ. Microbiol. 59:3648-3653.
59. Fagard M, Dellagi A, Roux C, Perino C, Rigault M, Boucher V, Shevchik VE, Expert D. 2007. Arabidopsis thaliana expresses multiple lines of defense to counterattack Erwinia chrysanthemi. Mol. Plant Microbe Interact. 20:794-805.
60. Mole B, Habibi S, Dangl JL, Grant SR. 2010. Gluconate metabolism is required for virulence of the soft-rot pathogen Pectobacterium carotovorum. Mol. Plant Microbe Interact. 23:1335-1344.
61. Truesdell SJ, Sims JC, Boerman PA, Seymour JL, Lazarus RA. 1991. Pathways for metabolism of ketoaldonic acids in an Erwinia sp. J. Bacteriol. 173:6651-6656.
62. Bakovic M, Fullerton MD, Michel V. 2007. Metabolic and molecular aspects of ethanolamine phospholipid biosynthesis: the role of CTP: phosphoethanolamine cytidylyltransferase (Pcyt2). Biochem. Cell Biol. 85:283-300.
63. Miedema E, Richardson KE. 1966. Ethanolamine metabolism in plant tissues. Plant Physiol. 41:1026-1030.
64. Glasner JD, Yang Reverchon C-HS, Hugouvieux-Cotte-Pattat N, Condemine G, Bohin JP, Van Gijsegem F, Yang S, Franza T, Expert D, Plunkett G, San Francisco MJ, Charkowski AO, Py B, Bell K, Rauscher L, Rodriguez-Palenzuela P, Toussaint A, Holeva MC, He SY, Douet V, Boccara M, Blanco C, Toth I, Anderson BD, Biehl BS, Mau B, Flynn SM, Barras F, Lindeberg M, Birch PRJ, Tsuyumu S, Shi X, Hibbing M, Yap MN, Carpentier M, Dassa E, Umehara M, Kim JF, Rusch M, Soni P, Mayhew GF, Fouts DE, Gill SR, Blattner FR, Keen NT, Perna NT. 2011. Genome sequence of the plant-pathogenic bacterium Dickeya dadantii 3937. J. Bacteriol. 193:2076-2077.
65. Jeter RM, Olivera BM, Roth JR. 1984. Salmonella typhimurium synthesizes cobalamin (vitamin B12) de novo under anaerobic growth conditions. J. Bacteriol. 159:206-213.
66. Becker D, Selbach M, Rollenhagen C, Ballmaier M, Meyer TF, Mann M, Bumann D. 2006. Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 440:303-307.
67. Jarvik T, Smillie C, Groisman EA, Ochman H. 2010. Short-term signatures of evolutionary change in the Salmonella enterica serovar Typhimurium 14028 genome. J. Bacteriol. 192:560-567.
68. Chen P, Ailion M, Bobik T, Stormo G, Roth J. 1995. Five promoters integrate control of the cob/pdu regulon in Salmonella typhimurium. J. Bacteriol. 177:5401-5410.
69. Lawhon SD, Frye JG, Suyemoto M, Porwollik S, McClelland M, Altier C. 2003. Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol. 48:1633-1645.
70. Wesley A, Mantle M, Man D, Qureshi R, Forstner G, Forstner J. 1985. Neutral and acidic species of human intestinal mucin. Evidence for different core peptides. J. Biol. Chem. 260:7955-7959.
71. Kawai K, Fujita M, Nakao M. 1974. Lipid components of two different regions of an intestinal epithelial cell membrane of mouse. Biochim. Biophys. Acta 369:222-233.
72. Harvey PC, Watson M, Hulme S, Jones MA, Lovell M, Berchieri A, Young J, Bumstead N, Barrow P. 2011. Salmonella enterica serovar Typhimurium colonizing the lumen of the chicken intestine grows slowly and upregulates a unique set of virulence and metabolism genes. Infect. Immun. 79:4105-4121.
73. Sheikh A, Charles RC, Rollins SM, Harris JB, Bhuiyan MS, Khanam F, Bukka A, Kalsy A, Porwollik S, Brooks WA, LaRocque RC, Hohmann EL, Cravioto A, Logvinenko T, Calderwood SB, McClelland M, Graham JE, Qadri F, Ryan ET. 2010. Analysis of Salmonella enterica serotype Paratyphi A gene expression in the blood of bacteremic patients in Bangladesh. PLoS Negl. Trop. Dis. 4:e908. doi:10.1371/journal.pntd.0000908.
74. Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Baumler AJ. 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl. Acad. Sci. U. S. A. 108:17480-17485.
75. Bertin Y, Girardeau JP, Chaucheyras-Durand F, Lyan B, Pujos-Guillot E, Harel J, Martin C. 2011. Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ. Microbiol. 13:365-377.
76. Klumpp J, Fuchs TM. 2007. Identification of novel genes in genomic islands that contribute to Salmonella typhimurium replication in macrophages. Microbiology 153:1207-1220.
77. Maier RJ, Olczak A, Maier S, Soni S, Gunn J. 2004. Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect. Immun. 72:6294-6299.
78. Sweeney NJ, Laux DC, Cohen PS. 1996. Escherichia coli F-18 and E. coli K-12 eda mutants do not colonize the streptomycin-treated mouse large intestine. Infect. Immun. 64:3504-3511.
79. Tsolis RM, Baumler AJ, Heffron F, Stojiljkovic I. 1996. Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect. Immun. 64:4549-4556.