Characterization and global gene expression of F- phenocopies during Escherichia coli biofilm formation

Molecular Genetics and Genomics

Volumn 284, Issue 5, 2010, Pages 333-342

  May, Thithiwat ^a   Ito, Akinobu ^a   Okabe, Satoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Conjugation; F plasmid; Microarray; mRNA expression; Pili; Stationary phase

Indexed keywords

BACTERIAL PROTEIN; MESSENGER RNA;

ARTICLE; BACTERIAL CELL; BACTERIAL CHROMOSOME; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BACTERIUM CONJUGATION; BIOFILM; CELL INTERACTION; CONTROLLED STUDY; DNA MICROARRAY; DNA TRANSFER; DOWN REGULATION; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC HETEROGENEITY; GENETIC LINKAGE; GENOTYPE; MEMBRANE FORMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN STABILITY; RNA SEQUENCE; SESSILE SPECIES; TRANSCRIPTOMICS; UPREGULATION; CYTOLOGY; FIMBRIA; GENETICS; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY;

BIOFILMS; CHROMOSOMES, BACTERIAL; ESCHERICHIA COLI; FIMBRIAE, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; RNA, MESSENGER;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 78049345596     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-010-0571-2     Document Type: Article

References (55)

1. M Achtman N Willetts AJ Clark 1971 Beginning a genetic analysis of conjugational transfer determined by the F factor in Escherichia coli by isolation and characterization of transfer-deficient mutants J Bacteriol 106 2 529 538 1:STN:280:DyaE3M7otl2isg%3D%3D 4929865
2. KG Anthony WA Klimke J Manchak LS Frost 1999 Comparison of proteins involved in pilus synthesis and mating pair stabilization from the related plasmids F and R100-1: insights into the mechanism of conjugation J Bacteriol 181 17 5149 5159 1:CAS:528:DyaK1MXlvVSlsrc%3D 10464182
3. C Beloin J Valle P Latour-Lambert P Faure M Kzreminski D Balestrino JAJ 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 3 659 674 1:CAS:528:DC%2BD2cXhtlWitLo%3D 10.1046/j.1365-2958.2003.03865.x 14731270 (Pubitemid 38233935)
4. TV Biesen LS Frost 1994 The FinO protein of IncF plasmids binds FinP antisense RNA and its target, traJ mRNA, and promotes duplex formation Mol Microbiol 14 3 427 436 10.1111/j.1365-2958.1994.tb02177.x 7533880 (Pubitemid 24337323)
5. BM Bolstad RA Irizarry M Astrand TP Speed 2003 A comparison of normalization methods for high density oligonucleotide array data based on variance and bias Bioinformatics 19 2 185 193 1:CAS:528:DC%2BD3sXitlCnsL4%3D 10.1093/bioinformatics/19.2.185 12538238 (Pubitemid 36181903)
6. L Diederich LJ Rasmussen W Messer 1992 New cloning vectors for integration into the λ attachment site attB of the Escherichia coli chromosome Plasmid 28 1 14 24 1:CAS:528:DyaK38XltVGgtro%3D 10.1016/0147-619X(92) 90032-6 1387714
7. -phenocopies: characterization of expression of the F transfer region in stationary phase Microbiology 144 9 2579 2587 1:CAS:528:DyaK1cXmt1ykurs%3D 10.1099/00221287-144-9-2579 9782507
8. LS Frost K Ippen-Ihler RA Skurray 1994 Analysis of the sequence and gene products of the transfer region of the F sex factor Microbiol Mol Biol Rev 58 2 162 210 1:CAS:528:DyaK2MXitVyruw%3D%3D
9. MP Garcillán-Barcia F de la Cruz 2008 Why is entry exclusion an essential feature of conjugative plasmids? Plasmid 60 1 1 18 10.1016/j.plasmid.2008.03.002 18440635
10. JM Ghigo 2001 Natural conjugative plasmids induce bacterial biofilm development Nature 412 6845 442 445 1:CAS:528:DC%2BD3MXlslCqtbc%3D 10.1038/35086581 11473319 (Pubitemid 32702708)
11. V Hancock P Klemm 2007 Global gene expression profiling of asymptomatic bacteria Escherichia coli during biofilm growth in human urine Infect Immun 75 2 966 976 1:CAS:528:DC%2BD2sXhs1ahsbw%3D 10.1128/IAI.01748-06 17145952 (Pubitemid 46203462)
12. B Harr C Schlötterer 2006 Gene expression analysis indicates extensive genotype-specific crosstalk between the conjugative F-plasmid and the E. coli chromosome BMC microbiol 6 1 80 10.1186/1471-2180-6-80 16981998 (Pubitemid 44521573)
13. R Helmuth M Achtman 1978 Cell-cell interactions in conjugating Escherichia coli: purification of F pili with biological activity Proc Natl Acad Sci USA 75 3 1237 1241 1:CAS:528:DyaE1cXktVaru70%3D 10.1073/pnas.75.3.1237 349561 (Pubitemid 8301610)
14. A Heydorn AT Nielsen M Hentzer C Sternberg M Givskov BK Ersboll S Molin 2000 Quantification of biofilm structures by the novel computer program COMSTAT Microbiology 146 10 2395 2407 1:CAS:528:DC%2BD3cXnslWrsbg%3D 11021916
15. KA Ippen-Ihler EG Minkley 1986 The conjugation system of F, the fertility factor of Escherichia Coli Annu Rev Genet 20 1 593 624 1:CAS:528: DyaL2sXmtFyksQ%3D%3D 10.1146/annurev.ge.20.120186.003113 2880557
16. A Ito T May K Kawata S Okabe 2008 Significance of rpoS during maturation of Escherichia coli biofilms Biotechnol Bioeng 99 6 1462 1471 1:CAS:528:DC%2BD1cXktVyntbw%3D 10.1002/bit.21695 17979199 (Pubitemid 351548686)
17. A Ito T May A Taniuchi K Kawata S Okabe 2009 Localized expression profiles of rpoS in Escherichia coli biofilms Biotechnol Bioeng 103 5 975 983 1:CAS:528:DC%2BD1MXosl2nt7Y%3D 10.1002/bit.22305 19288441
18. BC Kline 1985 A review of mini-F plasmid maintenance Plasmid 14 1 1 16 1:CAS:528:DyaL2MXltFOitr4%3D 10.1016/0147-619X(85)90027-7 3898165 (Pubitemid 15023699)
19. EV Koonin KS Makarova L Aravind 2001 Horizontal gene transfer in prokaryotes: quantification and classification Annu Rev Microbiol 55 1 709 742 1:CAS:528:DC%2BD3MXnslKjtbw%3D 10.1146/annurev.micro.55.1.709 11544372 (Pubitemid 32978121)
20. IC Lau-Wong T Locke MJ Ellison TL Raivio LS Frost 2008 Activation of the Cpx regulon destabilizes the F plasmid transfer activator, TraJ, via the HslVU protease in Escherichia coli Mol Microbiol 67 3 516 527 1:CAS:528: DC%2BD1cXktVymsL8%3D 10.1111/j.1365-2958.2007.06055.x 18069965
21. C Li 2008 Automating dChip: toward reproducible sharing of microarray data analysis BMC Bioinformatics 9 1 231 10.1186/1471-2105-9-231 18466620 (Pubitemid 351722535)
22. C Li WH Wong 2001 Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection Proc Natl Acad Sci USA 98 1 31 36 1:CAS:528:DC%2BD3MXkslKnuw%3D%3D 10.1073/pnas.011404098 11134512 (Pubitemid 32095858)
23. G Liu AE Loraine R Shigeta M Cline J Cheng V Valmeekam S Sun D Kulp MA Siani-Rose 2003 NetAffx: affymetrix probesets and annotations Nucleic Acids Res 31 1 82 86 1:CAS:528:DC%2BD3sXhvFSnsrs%3D 10.1093/nar/gkg121 12519953 (Pubitemid 36150339)
24. J Lu LS Frost 2005 Mutations in the C-terminal region of TraM provide evidence for in vivo TraM-TraD interactions during F-plasmid conjugation J Bacteriol 187 14 4767 4773 1:CAS:528:DC%2BD2MXmtVyit7o%3D 10.1128/JB.187.14. 4767-4773.2005 15995191 (Pubitemid 40962194)
25. J Lu W Zhao LS Frost 2004 Mutational analysis of TraM correlates oligomerization and DNA binding with autoregulation and conjugative DNA transfer J Biol Chem 279 53 55324 55333 1:CAS:528:DC%2BD2cXhtFeis73F 10.1074/jbc.M409352200 15509578 (Pubitemid 40066530)
26. NP Manwaring RA Skurray N Firth 1999 Nucleotide sequence of the F plasmid leading region Plasmid 41 3 219 225 1:CAS:528:DyaK1MXjslSltLc%3D 10.1006/plas.1999.1390 10366527 (Pubitemid 29270257)
27. SW Matson JK Sampson DRN Byrd 2001 F plasmid conjugative DNA transfer: the TraI helicase activity is essential for DNA strand transfer J Biol Chem 276 4 2372 2379 1:CAS:528:DC%2BD3MXhtVGjsr8%3D 10.1074/jbc.M008728200 11054423
28. T May S Okabe 2008 Escherichia coli harboring a natural IncF conjugative F plasmid develops complex mature biofilms by stimulating synthesis of colanic acid and curli J Bacteriol 190 22 7479 7490 1:CAS:528:DC%2BD1cXhtlKiu7%2FF 10.1128/JB.00823-08 18790864
29. T May A Ito S Okabe 2009 Induction of multidrug resistance mechanism in Escherichia coli biofilms by interplay between tetracycline and ampicillin resistance genes Antimicrob Agents Chemother 53 11 4628 4639 1:CAS:528:DC%2BD1MXhtl2itLjJ 10.1128/AAC.00454-09 19721076
30. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor
31. CD Nadell JB Xavier KR Foster 2009 The sociobiology of biofilms FEMS Microbiol Rev 33 1 206 224 1:CAS:528:DC%2BD1MXmtlKjsQ%3D%3D 10.1111/j.1574-6976. 2008.00150.x 19067751
32. FC Neidhardt PL Bloch DF Smith 1974 Culture medium for enterobacteria J Bacteriol 119 3 736 747 1:CAS:528:DyaE2cXlsVygu7k%3D 4604283
33. CP Novotny PF Taylor K Lavin 1972 Effects of growth Inhibitors and ultraviolet irradiation on F pili J Bacteriol 112 3 1083 1089 1:CAS:528:DyaE3sXmslGgug%3D%3D 4565528
34. T Onogi T Miki S Hiraga 2002 Behavior of sister copies of mini-F plasmid after synchronized plasmid replication in Escherichia coli cells J Bacteriol 184 11 3142 3145 1:CAS:528:DC%2BD38XjvVGrt7w%3D 10.1128/JB.184.11.3142-3145.2002 12003959 (Pubitemid 34517841)
35. JT Ou 1973 Inhibition of formation of Escherichia coli mating pairs by f1 and MS2 bacteriophages as determined with a coulter counter J Bacteriol 114 3 1108 1115 1:STN:280:DyaE3s3gt1egsg%3D%3D 4576397
36. A Pereira T Silva A Gomes A Araujo L Giugliano 2010 Diarrhea-associated biofilm formed by enteroaggregative Escherichia coli and aggregative Citrobacter freundii: a consortium mediated by putative F pili BMC microbiol 10 1 57 10.1186/1471-2180-10-57 20175929
37. D Perez-Mendoza F de la Cruz 2009 Escherichia coli genes affecting recipient ability in plasmid conjugation: are there any? BMC Genomics 10 1 71 10.1186/1471-2164-10-71 19203375
38. C Prigent-Combaret O Vidal C Dorel P Lejeune 1999 Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli J Bacteriol 181 19 5993 6002 1:CAS:528:DyaK1MXmsVOrt7k%3D 10498711
39. A Reisner JAJ Haagensen MA Schembri EL Zechner S Molin 2003 Development and maturation of Escherichia coli K-12 biofilms Mol Microbiol 48 4 933 946 1:CAS:528:DC%2BD3sXktV2gs70%3D 10.1046/j.1365-2958.2003.03490.x 12753187 (Pubitemid 36628260)
40. A Reisner BM Höller S Molin EL Zechner 2006 Synergistic effects in mixed Escherichia coli biofilms: conjugative plasmid transfer drives biofilm expansion J Bacteriol 188 10 3582 3588 1:CAS:528:DC%2BD28XkslClurg%3D 10.1128/JB.188.10.3582-3588.2006 16672612 (Pubitemid 43726222)
41. A Reisner KA Krogfelt BM Klein EL Zechner S Molin 2006 In vitro biofilm formation of commensal and pathogenic Escherichia coli strains: impact of environmental and genetic factors J Bacteriol 188 10 3572 3581 1:CAS:528:DC%2BD28XkslClurs%3D 10.1128/JB.188.10.3572-3581.2006 16672611 (Pubitemid 43726221)
42. D Ren LA Bedzyk SM Thomas RW Ye TK Wood 2004 Gene expression in Escherichia coli biofilms Appl Microbiol Biotechnol 64 4 515 524 1:CAS:528:DC%2BD2cXjtFyisrk%3D 10.1007/s00253-003-1517-y 14727089 (Pubitemid 38686161)
43. T Saitoh S Hiraga 1975 F deoxyribonucleic acid superinfected into phenocopies of donor strains J Bacteriol 121 3 1007 1013 1:CAS:528: DyaE2MXhsFajtL4%3D 1090583
44. PM Silverman L Tran R Harris HM Gaudin 1993 Accumulation of the F plasmid TraJ protein in cpx mutants of Escherichia coli J Bacteriol 175 4 921 925 1:CAS:528:DyaK3sXhvVGjsL0%3D 8432716
45. RA Skurray P Reeves 1974 F factor-mediated immunity to lethal zygosis in Escherichia coli K-12 J Bacteriol 117 1 100 106 1:STN:280:DyaE2c%2FmtFeisg%3D%3D 4587600
46. SJ Sorensen M Bailey LH Hansen N Kroer S Wuertz 2005 Studying plasmid horizontal transfer in situ: a critical review Nat Rev Microbiol 3 9 700 710 1:CAS:528:DC%2BD2MXps1Kjtbg%3D 10.1038/nrmicro1232 16138098 (Pubitemid 41195086)
47. DR Stallions R Curtiss III 1972 Bacterial conjugation under anaerobic conditions J Bacteriol 111 1 294 295 1:STN:280:DyaE2c%2FpvFagsQ%3D%3D 4591482
48. M Starčič-Erjavec JPM Putten W Gaastra BJAM Jordi M Grabnar D Žgur-Bertok 2003 H-NS and Lrp serve as positive modulators of traJ expression from the Escherichia coli plasmid pRK100 Mol Genet Genomics 270 1 94 102 10.1007/s00438-003-0908-1 12942368 (Pubitemid 37267108)
49. C Sternberg BB Christensen T Johansen A Toftgaard Nielsen JB Andersen M Givskov S Molin 1999 Distribution of bacterial growth activity in flow-chamber biofilms Appl Environ Microbiol 65 9 4108 4117 1:CAS:528:DyaK1MXlvFequ70%3D 10473423
50. PS Stewart MJ Franklin 2008 Physiological heterogeneity in biofilms Nat Rev Microbiol 6 3 199 210 1:CAS:528:DC%2BD1cXhvFCgt7c%3D 10.1038/nrmicro1838 18264116 (Pubitemid 351256315)
51. M Tomoeda M Inuzuka T Date 1976 Bacterial sex pili Prog Biophys Mol Biol 30 23 56 10.1016/0079-6107(76)90004-3
52. R Van Houdt CW Michiels 2005 Role of bacterial cell surface structures in Escherichia coli biofilm formation Res Microbiol 156 5-6 626 633 15950122
53. WR Will LS Frost 2006 Hfq Is a regulator of F-plasmid TraJ and TraM synthesis in Escherichia coli J Bacteriol 188 1 124 131 1:CAS:528: DC%2BD28XksFWrtbg%3D 10.1128/JB.188.1.124-131.2006 16352828
54. WR Will J Lu LS Frost 2004 The role of H-NS in silencing F transfer gene expression during entry into stationary phase Mol Microbiol 54 3 769 782 1:CAS:528:DC%2BD2cXpslKktLY%3D 10.1111/j.1365-2958.2004.04303.x 15491366 (Pubitemid 39457297)
55. X Yang Q Ma TK Wood 2008 The R1 conjugative plasmid increases Escherichia coli biofilm formation through an envelope stress response Appl Environ Microbiol 74 9 2690 2699 1:CAS:528:DC%2BD1cXlslCiuro%3D 10.1128/AEM.02809-07 18344336 (Pubitemid 351632599)