Functional genomics of probiotic Escherichia coli Nissle 1917 and 83972, and UPEC strain CFT073: Comparison of transcriptomes, growth and biofilm formation

Molecular Genetics and Genomics

Volumn 284, Issue 6, 2010, Pages 437-454

  Hancock, Viktoria ^a   Vejborg, Rebecca Munk ^a   Klemm, Per ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Biofilm formation; Functional genomics; Probiotic E. coli; Urine growth; Uropathogenic E. coli

Indexed keywords

BACTERIAL PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; YBIJ PROTEIN; YHAK PROTEIN; YHCN PROTEIN;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOFILM; CONTROLLED STUDY; DOWN REGULATION; ESCHERICHIA COLI; FUNCTIONAL GENOMICS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC DIFFERENCE; GENETIC SIMILARITY; HOST PATHOGEN INTERACTION; INTESTINE MOTILITY; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; UROPATHOGENIC ESCHERICHIA COLI;

BIOFILMS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; GENOME, BACTERIAL; GENOMICS; HOST-PATHOGEN INTERACTIONS; HUMANS; IRON; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROBIOTICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY; URINARY TRACT INFECTIONS; URINE; VIRULENCE;

ESCHERICHIA COLI; ESCHERICHIA COLI NISSLE 1917;

EID: 78650515414     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-010-0578-8     Document Type: Article

References (61)

1. P Andersson I Engberg G Lidin-Janson K Lincoln R Hull S Hull C Svanborg 1991 Persistence of Escherichia coli bacteriuria is not determined by bacterial adherence Infect Immun 59 2915 2921 1:CAS:528:DyaK3MXlvVSmtLo%3D 1879917
2. C Beloin J Valle P Latour-Lambert P Faure M Kzreminski D Balestrino JA Haagensen S Molin G Prensier B Arbeille JM Ghigo 2004 Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression Mol Microbiol 51 659 674 1:CAS:528:DC%2BD2cXhtlWitLo%3D 10.1046/j.1365-2958.2003.03865.x 14731270 (Pubitemid 38233935)
3. E Brzuszkiewicz H Brüggemann H Liesegang M Emmerth T Ölschläger G Nagy K Albermann C Wagner C Buchrieser L Emody G Gottschalk J Hacker U Dobrindt 2006 How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains Proc Natl Acad Sci USA 103 12879 12884 10.1073/pnas.0603038103 16912116 (Pubitemid 44298655)
4. SL Chen CS Hung J Xu CS Reigstad V Magrini A Sabo D Blasiar T Bieri RR Meyer P Ozersky JR Armstrong RS Fulton JP Latreille J Spieth TM Hooton ER Mardis SJ Hultgren JI Gordon 2006 Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach Proc Natl Acad Sci USA 103 5977 5982 1:CAS:528:DC%2BD28XktFaitb0%3D 10.1073/pnas.0600938103 16585510
5. I Chouikha P Germon A Brée P Gilot M Moulin-Schouleur C Schouler 2006 A selC-associated genomic island of the extraintestinal avian pathogenic Escherichia coli strain BEN2908 is involved in carbohydrate uptake and virulence J Bacteriol 188 977 987 1:CAS:528:DC%2BD28XhtVOis7s%3D 10.1128/JB.188.3.977- 987.2006 16428402 (Pubitemid 43146414)
6. BB Christensen C Sternberg JB Andersen RJ Palmer Jr AT Nielsen M Givskov S Molin 1999 Molecular tools for study of biofilm physiology Methods Enzymol 310 20 42 1:CAS:528:DC%2BD3cXnt1Wgug%3D%3D 10.1016/S0076-6879(99)10004-1 10547780 (Pubitemid 29504266)
7. JW Costerton Z Lewandowski DE Caldwell DR Korber HM Lappin-Scott 1995 Microbial biofilms Annu Rev Microbiol 49 711 745 1:CAS:528:DyaK2MXovVWjtbg%3D 10.1146/annurev.mi.49.100195.003431 8561477
8. JW Costerton PS Stewart EP Greenberg 1999 Bacterial biofilms: a common cause of persistent infections Science 284 1318 1322 1:CAS:528: DyaK1MXjs1Squ78%3D 10.1126/science.284.5418.1318 10334980 (Pubitemid 29289651)
9. KA Datsenko BL Wanner 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc Natl Acad Sci USA 97 6640 6645 1:CAS:528:DC%2BD3cXktFais7c%3D 10.1073/pnas.120163297 10829079 (Pubitemid 30412767)
10. J Domka J Lee TK Wood 2006 YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling Appl Environ Microbiol 72 2449 2459 1:CAS:528:DC%2BD28XktFagtLY%3D 10.1128/AEM.72.4.2449-2459.2006 16597943
11. L Ferrières V Hancock P Klemm 2007 Biofilm exclusion of uropathogenic bacteria by selected asymptomatic bacteriuria Escherichia coli strains Microbiology 153 1711 1719 10.1099/mic.0.2006/004721-0 17526829 (Pubitemid 46952503)
12. L Grozdanov C Raasch J Schulze U Sonnenborn G Gottschalk J Hacker U Dobrindt 2004 Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917 J Bacteriol 186 5432 5441 1:CAS:528:DC%2BD2cXmvVKhu74%3D 10.1128/JB.186.16.5432-5441.2004 15292145 (Pubitemid 39038145)
13. D Gurmu J Lu KA Johnson P Nordlund A Holmgren H Erlandsen 2009 The crystal structure of the protein YhaK from Escherichia coli reveals a new subclass of redox sensitive enterobacterial bicupins Proteins 74 18 31 1:CAS:528:DC%2BD1MXhsVSiug%3D%3D 10.1002/prot.22128 18561187
14. EC Hagan HL Mobley 2007 Uropathogenic Escherichia coli outer membrane antigens expressed during urinary tract infection Infect Immun 75 3941 3949 1:CAS:528:DC%2BD2sXoslShtLs%3D 10.1128/IAI.00337-07 17517861 (Pubitemid 47206292)
15. V Hancock P Klemm 2007 Global gene expression profiling of asymptomatic bacteriuria Escherichia coli during biofilm growth in human urine Infect Immun 75 966 976 1:CAS:528:DC%2BD2sXhs1ahsbw%3D 10.1128/IAI.01748-06 17145952 (Pubitemid 46203462)
16. V Hancock L Ferrières P Klemm 2007 Biofilm formation by asymptomatic and virulent urinary tract infectious Escherichia coli strains FEMS Microbiol Lett 267 30 37 1:CAS:528:DC%2BD2sXhtVWksbs%3D 10.1111/j.1574-6968. 2006.00507.x 17166230 (Pubitemid 46066536)
17. V Hancock L Ferrières P Klemm 2008 The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine Microbiology 154 167 175 1:CAS:528:DC%2BD1cXhtFOksLs%3D 10.1099/mic.0.2007/011981-0 18174135 (Pubitemid 351201396)
18. V Hancock AS Seshasayee DW Ussery NM Luscombe P Klemm 2008 Transcriptomics and adaptive genomics of the asymptomatic bacteriuria Escherichia coli strain 83972 Mol Gen Genet 279 523 534 1:CAS:528: DC%2BD1cXkvFWksrs%3D
19. V Hancock M Dahl P Klemm 2010 Probiotic Escherichia coli strain Nissle 1917 out-competes intestinal pathogens during biofilm formation J Med Microbiol 59 392 399 10.1099/jmm.0.008672-0 20110388
20. R Hull D Rudy W Donovan C Svanborg I Wieser C Stewart R Darouiche 2000 Urinary tract infection prophylaxis using Escherichia coli 83972 in spinal cord injured patients J Urol 163 872 877 1:STN:280:DC%2BD3c7ltVOjtg%3D%3D 10.1016/S0022-5347(05)67823-8 10687996
21. JR Johnson P Delavari M Kuskowski AL Stell 2001 Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli J Infect Dis 183 78 88 1:CAS:528:DC%2BD3MXot1GmsQ%3D%3D 10.1086/317656 11106538 (Pubitemid 32043044)
22. LM Junker JE Peters AG Hay 2006 Global analysis of candidate genes important for fitness in a competitive biofilm using DNA-array-based transposon mapping Microbiology 152 2233 2245 1:CAS:528:DC%2BD28XosVeltbk%3D 10.1099/mic.0.28767-0 16849790 (Pubitemid 44219633)
23. T-J Kim BM Young GM Young 2008 Effect of flagellar mutations on Yersinia enterocolitica biofilm formation Appl Environ Microbiol 74 5466 5474 1:CAS:528:DC%2BD1cXhtV2ru7jM 10.1128/AEM.00222-08 18606789
24. SM Kirov M Castrisios JG Shaw 2004 Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces Infect Immun 72 1939 1945 1:CAS:528:DC%2BD2cXjt1eksbw%3D 10.1128/IAI.72.4.1939-1945. 2004 15039313 (Pubitemid 38419904)
25. P Klemm V Roos GC Ulett C Svanborg MA Schembri 2006 Molecular characterization of the Escherichia coli asymptomatic bacteriuria strain 83972: the taming of a pathogen Infect Immun 74 781 785 1:CAS:528: DC%2BD28XitlOjuw%3D%3D 10.1128/IAI.74.1.781-785.2006 16369040 (Pubitemid 43023139)
26. P Klemm V Hancock MA Schembri 2007 Mellowing out: adaptation to commensalism by Escherichia coli asymptomatic bacteriuria strain 83972 Infect Immun 75 3688 3695 1:CAS:528:DC%2BD2sXoslShsbg%3D 10.1128/IAI.01730-06 17502385 (Pubitemid 47206264)
27. MA Lasaro N Salinger J Zhang Y Wang Z Zhong M Goulian J Zhu 2009 F1C fimbriae play an important role in biofilm formation and intestinal colonization by the Escherichia coli commensal strain Nissle 1917 Appl Environ Microbiol 75 246 251 1:CAS:528:DC%2BD1MXktlejur4%3D 10.1128/AEM.01144-08 18997018
28. KP Lemon DE Higgins R Kolter 2007 Flagellar motility is critical for Listeria monocytogenes biofilm formation J Bacteriol 189 4418 4424 1:CAS:528:DC%2BD2sXms1alt7k%3D 10.1128/JB.01967-06 17416647 (Pubitemid 46919628)
29. C Li WH Wong 2001 Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application Genome Biol 2 1
30. U Lindberg LA Hanson U Jodal G Lidin-Janson K Lincoln S Olling 1975 Asymptomatic bacteriuria in schoolgirls. II. Differences in Escherichia coli causing asymptomatic bacteriuria Acta Paediatr Scand 64 432 436 1:STN:280:DyaE2M3itFOitw%3D%3D 10.1111/j.1651-2227.1975.tb03860.x 1098383
31. AL Lloyd TA Henderson PD Vigil HLT Mobley 2009 Genomic islands of uropathogenic Escherichia coli contribute to virulence J Bacteriol 191 3469 3481 1:CAS:528:DC%2BD1MXms1eisLk%3D 10.1128/JB.01717-08 19329634
32. R Lodinova-Zadnikova U Sonnenborn 1997 Effect of preventive administration of a nonpathogenic Escherichia coli strain on the colonization of the intestine with microbial pathogens in newborn infants Biol Neonate 71 224 232 1:STN:280:DyaK2s3ns1Sgug%3D%3D 10.1159/000244421 9129791
33. R Lodinova-Zadnikova Z Bartakova H Tlaskalova 1992 The effect of oral colonization by non-pathogenic E. coli on the immune response in neonates and possibilities of its use in the prevention of nosocomial infections in children at risk Cesk Epidemiol Mikrobiol Imunol 42 126 132 1:STN:280: DyaK2c%2Fgs1Khsw%3D%3D 1339604
34. AN Mabbett GC Ulett RE Watts JJ Tree M Totsika CL Ong JM Wood W Monaghan DF Looke GR Nimmo C Svanborg MA Schembri 2009 Virulence properties of asymptomatic bacteriuria Escherichia coli Int J Med Microbiol 299 53 63 1:CAS:528:DC%2BD1MXivVKisr0%3D 10.1016/j.ijmm.2008.06.003 18706859
35. S Macfarlane JF Dillon 2007 Microbial biofilms in the human gastrointestinal tract J Appl Microbiol 102 1187 1196 1:STN:280: DC%2BD2s3ktVKhtA%3D%3D 10.1111/j.1365-2672.2007.03287.x 17448154 (Pubitemid 46633431)
36. PM Merritt T Danhorn C Fuqua 2007 Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation J Bacteriol 189 8005 8014 1:CAS:528:DC%2BD2sXhtlyht7zF 10.1128/JB.00566-07 17766409 (Pubitemid 350178911)
37. HLT Mobley DM Green AL Trifillis DE Johnson GR Chippendale CV Lockatell BD Jones JW Warren 1990 Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains Infect Immun 58 1281 1289 1:CAS:528:DyaK3cXktVehsrg%3D 2182540
38. FC Neidhardt PL Bloch DF Smith 1974 Culture Medium for Enterobacteria J Bacteriol 119 736 747 1:CAS:528:DyaE2cXlsVygu7k%3D 4604283
39. GA O'Toole R Kolter 1998 Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development Mol Microbiol 30 295 304 10.1046/j.1365-2958.1998.01062.x 9791175 (Pubitemid 28480181)
40. G O'Toole HB Kaplan R Kolter 2000 Biofilm formation as microbial development Annu Rev Microbiol 54 49 79 10.1146/annurev.micro.54.1.49 11018124
41. J Oscarsson Y Mizunoe BE Uhlin DJ Haydon 1996 Induction of haemolytic activity in Escherichia coli by the slyA gene product Mol Microbiol 20 191 199 1:CAS:528:DyaK28XisFaqu74%3D 10.1111/j.1365-2958.1996.tb02500.x 8861216 (Pubitemid 26124796)
42. D Ren LA Bedzyk SM Thomas RW Ye TK Wood 2004 Gene expression in Escherichia coli biofilms Appl Microbiol Biotechnol 64 515 524 1:CAS:528:DC%2BD2cXjtFyisrk%3D 10.1007/s00253-003-1517-y 14727089 (Pubitemid 38686161)
43. V Roos P Klemm 2006 Global gene expression profiling of the asymptomatic bacteriuria Escherichia coli strain 83972 in the human urinary tract Infect Immun 74 3565 3575 1:CAS:528:DC%2BD28Xlt1Cns7w%3D 10.1128/IAI.01959-05 16714589 (Pubitemid 43794548)
44. V Roos MA Schembri GC Ulett P Klemm 2006 Asymptomatic bacteriuria Escherichia coli strain 83972 carries mutations in the foc locus and is unable to express F1C fimbriae Microbiology 152 1799 1806 1:CAS:528: DC%2BD28Xmt1ert7o%3D 10.1099/mic.0.28711-0 16735742
45. V Roos GC Ulett MA Schembri P Klemm 2006 The asymptomatic bacteriuria Escherichia coli strain 83972 out-competes UPEC strains in human urine Infect Immun 74 615 624 1:CAS:528:DC%2BD28XitlKrtQ%3D%3D 10.1128/IAI.74.1.615-624.2006 16369018 (Pubitemid 43023117)
46. KE Rudd H-S Ian CW Valerie B Amos 1998 Low molecular weight proteins: a challenge for post-genomic research Electrophoresis 19 536 544 1:CAS:528:DyaK1cXisVentrs%3D 10.1002/elps.1150190413 9588799 (Pubitemid 28179957)
47. TA Russo UB Carlino JR Johnson 2001 Identification of a new iron-regulated virulence gene, ireA, in an extraintestinal pathogenic isolate of Escherichia coli Infect Immun 69 6209 6216 1:CAS:528:DC%2BD3MXntFCjsbo%3D 10.1128/IAI.69.10.6209-6216.2001 11553562 (Pubitemid 32885184)
48. MA Schembri K Kjaergaard P Klemm 2003 Global gene expression in Escherichia coli biofilms Mol Microbiol 48 253 267 1:CAS:528: DC%2BD3sXislOrtr8%3D 10.1046/j.1365-2958.2003.03432.x 12657059 (Pubitemid 36411481)
49. M Schultz 2008 Clinical use of E. coli Nissle 1917 in inflammatory bowel disease Inflamm Bowel Dis 14 1012 1018 10.1002/ibd.20377 18240278
50. J Schulze U Sonnenborn 1995 Oral administration of a certain strain of live Escherichia coli for intestinal disorders? Infection 23 184 188 1:STN:280:DyaK287itFyiuw%3D%3D 10.1007/BF01793863 7499010
51. JA Snyder BJ Haugen EL Buckles CV Lockatell DE Johnson MS Donnenberg RA Welch HL Mobley 2004 Transcriptome of uropathogenic Escherichia coli during urinary tract infection Infect Immun 72 6373 6381 1:CAS:528:DC%2BD2cXpsFeks70%3D 10.1128/IAI.72.11.6373-6381.2004 15501767 (Pubitemid 39425418)
52. U Sonnenborn J Schulze 2009 The non-pathogenic Escherichia coli strain Nissle 1917-features of a versatile probiotic Microb Ecol Health Dis 21 122 158 1:CAS:528:DC%2BD1MXhs1aqtLzE 10.3109/08910600903444267
53. F Sundén L Håkansson E Ljunggren B Wullt 2006 Bacterial interference-is deliberate colonization with Escherichia coli 83972 an alternative treatment for patients with recurrent urinary tract infection? Int J Antimicrob Agents 28S S26 S29 10.1016/j.ijantimicag.2006.05.007 (Pubitemid 44163158)
54. RM Vejborg C Friis V Hancock MA Schembri P Klemm 2010 A virulent parent with probiotic progeny: comparative genomics of Escherichia coli strains CFT073, Nissle 1917 and ABU 83972 Mol Genet Genomics 283 469 484 1:CAS:528: DC%2BC3cXks1SntLY%3D 10.1007/s00438-010-0532-9 20354866
55. JW Warren 2001 Catheter-associated urinary tract infections Int J Antimicrob Agents 17 299 303 1:CAS:528:DC%2BD3MXisVals7Y%3D 10.1016/S0924- 8579(00)00359-9 11295412 (Pubitemid 32288748)
56. Weber MM, French CL, Barnes MB, Siegele DA, McLean RJ (2010) A previously uncharacterized gene, yjfO (bsmA) influences Escherichia coli biofilm formation and stress response. Microbiology 156:139-147
57. RA Welch V Burland G Plunkett 3rd P Redford P Roesch D Rasko EL Buckles SR Liou A Boutin J Hackett D Stroud GF Mayhew DJ Rose S Zhou DC Schwartz NT Perna HL Mobley MS Donnenberg FR Blattner 2002 Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli Proc Natl Acad Sci USA 99 17020 17024 1:CAS:528:DC%2BD3sXhvV2ltA%3D%3D 10.1073/pnas.252529799 12471157 (Pubitemid 36034091)
58. TK Wood 2009 Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling Environ Microbiol 11 1 15 1:CAS:528:DC%2BD1MXjt1eqt7c%3D 10.1111/j.1462-2920.2008.01768.x 19125816
59. TK Wood AF Gonzalez Barrios M Herzberg J Lee 2006 Motility influences biofilm architecture in Escherichia coli Appl Microbiol Biotechnol 72 361 367 1:CAS:528:DC%2BD28XotlCiurw%3D 10.1007/s00253-005-0263-8 16397770 (Pubitemid 44273060)
60. J Zdziarski C Svanborg B Wullt J Hacker U Dobrindt 2007 Molecular basis of commensalism in the urinary tract: low virulence or virulence attenuation? Infect Immun 76 695 703 10.1128/IAI.01215-07 18039831
61. XS Zhang R Garcia-Contreras TK Wood 2007 YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity J Bacteriol 189 3051 3062 1:CAS:528:DC%2BD2sXkslGqtrw%3D 10.1128/JB.01832-06 17293424 (Pubitemid 46697394)