A three-step method for analysing bacterial biofilm formation under continuous medium flow

Applied Microbiology and Biotechnology

Volumn 99, Issue 14, 2015, Pages 6035-6047

  Schmutzler, Karolin ^a   Schmid, Andreas ^b   Buehler, Katja ^a,b  

^a TU DORTMUND UNIVERSITY   (Germany)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

Biofilm dry weight; Cyclic diguanylate; Pellicle; Pseudomonas taiwanensis VLB120; Single species biofilm; Tubular biofilm

Indexed keywords

BACTERIA; TUBES (COMPONENTS);

CYCLIC DIGUANYLATE; DRY WEIGHT; PELLICLE; PSEUDOMONAS TAIWANENSIS VLB120; SINGLE SPECIES;

BIOFILMS;

BACTERIAL DNA; CELLULOSE; TAP WATER; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP;

BACTERIUM; BIOASSAY; BIOFILM; CATALYST; ENZYME ACTIVITY; GENOME; GROWTH RATE; HOMOLOGY; MATURATION; MICROBIAL ACTIVITY; MORPHOTYPE; MUTATION; PROTEIN; QUANTITATIVE ANALYSIS;

ANALYTIC METHOD; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM MUTANT; BIOCATALYST; BIOFILM; CELL MOTILITY; CONTROLLED STUDY; DELETION MUTANT; DRY WEIGHT; ESCHERICHIA COLI; GENE DELETION; GROWTH CURVE; INCUBATION TIME; INVERTED REPEAT; MICROBIAL BIOMASS; MORPHOTYPE; NONHUMAN; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; PSEUDOMONAS TAIWANENSIS; QUANTITATIVE ASSAY; SECOND MESSENGER; SILASTIC TUBE; TUBE ASSAY; TUBULAR REACTOR; ANALOGS AND DERIVATIVES; DEVICES; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGICAL EXAMINATION; PHYSIOLOGY; PROCEDURES;

BACTERIA (MICROORGANISMS); PSEUDOMONAS;

BACTERIOLOGICAL TECHNIQUES; BIOFILMS; CYCLIC GMP; PSEUDOMONAS;

EID: 84932199662     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6628-8     Document Type: Article

References (67)

1. An S, Wu J, Zhang LH (2010) Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclic-Di-GMP phosphodiesterase with a putative hypoxia-sensing domain. Appl Environ Microbiol 76:8160–8173
2. Ausmees N, Mayer R, Weinhouse H, Volman G, Amikam D, Benziman M, Lindberg M (2001) Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity. FEMS Microbiol Lett 204:163–167
3. Bertani G (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62:293–300
4. Bordeleau E, Fortier LC, Malouin F, Burrus V (2011) C-di-GMP turn-over in Clostridium difficile is controlled by a plethora of diguanylate cyclases and phosphodiesterases. PLoS Genet 7:e1002039
5. Borucki MK, Peppin JD, White D, Loge F, Call DR (2003) Variation in biofilm formation among strains of Listeria monocytogenes. Appl Environ Microbiol 69:7336–7342
6. Choi KH, Schweizer HP (2006) Mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc 1:153–161
7. Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, Schweizer HP (2005) A Tn7-based broad-range bacterial cloning and expression system. Nat Methods 2:443–448
8. Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867
9. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193
10. Duque E, de la Torre J, Bernal P, Molina-Henares MA, Alaminos M, Espinosa-Urgel M, Roca A, Fernandez M, de Bentzmann S, Ramos JL (2013) Identification of reciprocal adhesion genes in pathogenic and non-pathogenic Pseudomonas. Environ Microbiol 15:36–48
11. Eighmy TT, Maratea D, Bishop PL (1983) Electron microscopic examination of wastewater biofilm formation and structural components. Appl Environ Microbiol 45:1921–1931
12. Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J Bacteriol 189:7945–7947
13. Franklin FC, Bagdasarian M, Bagdasarian MM, Timmis KN (1981) Molecular and functional analysis of the TOL plasmid pWWO from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta cleavage pathway. Proc Natl Acad Sci U S A 78:7458–7462
14. Friedman L, Kolter R (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675–690
15. Gjermansen M, Ragas P, Tolker-Nielsen T (2006) Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol Lett 265:215–224
16. Gross R, Hauer B, Otto K, Schmid A (2007) Microbial biofilms: new catalysts for maximizing productivity of long-term biotransformations. Biotechnol Bioeng 98:1123–1134
17. Gross R, Lang K, Buehler K, Schmid A (2010) Characterization of a biofilm membrane reactor and its prospects for fine chemical synthesis. Biotechnol Bioeng 105:705–717
18. Halan B, Schmid A, Buehler K (2010) Maximizing the productivity of catalytic biofilms on solid supports in membrane reactors. Biotechnol Bioeng 106:516–527
19. Halan B, Schmid A, Buehler K (2011) Real-time solvent tolerance analysis of Pseudomonas sp. strain VLB120ΔC catalytic biofilms. Appl Environ Microbiol 77:1563–1571
20. Halan B, Buehler K, Schmid A (2012) Biofilms as living catalysts in continuous chemical syntheses. Trends Biotechnol 30:453–465
21. Hammar M, Bian Z, Normark S (1996) Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc Natl Acad Sci U S A 93:6562–6566
22. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580
23. Hay ID, Remminghorst U, Rehm BHA (2009) MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl Environ Microbiol 75:1110–1120
24. Hollander M, Wolfe DA, Chicken E (2014) Nonparametric statistical methods, 3rd edn. Wiley, Hoboken
25. Inglis TJ, Millar MR, Jones JG, Robinson DA (1989) Tracheal tube biofilm as a source of bacterial colonization of the lung. J Clin Microbiol 27:2014–2018
26. Karande R, Halan B, Schmid A, Buehler K (2014) Segmented flow is controlling growth of catalytic biofilms in continuous multiphase microreactors. Biotechnol Bioeng 111:1831–1840
27. Kim H, Ryu JH, Beuchat LR (2006) Attachment of and biofilm formation by Enterobacter sakazakii on stainless steel and enteral feeding tubes. Appl Environ Microbiol 72:5846–5856
28. Kirisits MJ, Prost L, Starkey M, Parsek MR (2005) Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71:4809–4821
29. Koehler KA, Rueckert C, Schatschneider S, Vorhoelter FJ, Szczepanowski R, Blank LM, Niehaus K, Goesmann A, Puehler A, Kalinowski J, Schmid A (2013) Complete genome sequence of Pseudomonas sp. strain VLB120 a solvent tolerant, styrene degrading bacterium, isolated from forest soil. J Biotechnol 168:729–730
30. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103:2839–2844
31. Lambert JM, Bongers RS, Kleerebezem M (2007) Cre-lox-based system for multiple gene deletions and selectable-marker removal in Lactobacillus plantarum. Appl Environ Microbiol 73:1126–1135
32. Lappin-Scott HM, Bass C (2001) Biofilm formation: attachment, growth, and detachment of microbes from surfaces. Am J Infect Control 29:250–251
33. Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE (1991) Optical sectioning of microbial biofilms. J Bacteriol 173:6558–6567
34. Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y, Lory S (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65:1474–1484
35. Li YH, Tian X (2012) Quorum sensing and bacterial social interactions in biofilms. Sensors (Basel) 12:2519–2538
36. Lynch AS, Robertson GT (2008) Bacterial and fungal biofilm infections. Annu Rev Med 59:415–428
37. Mann EE, Wozniak DJ (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36:893–916
38. Martinez-Garcia E, de Lorenzo V (2011) Engineering multiple genomic deletions in Gram-negative bacteria: analysis of the multi-resistant antibiotic profile of Pseudomonas putida KT2440. Environ Microbiol 13:2702–2716
39. McDonald MJ, Gehrig SM, Meintjes PL, Zhang XX, Rainey PB (2009) Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 183:1041–1053
40. Misiak K, Casey E, Murphy CD (2011) Factors influencing 4-fluorobenzoate degradation in biofilm cultures of Pseudomonas knackmussii B13. Water Res 45:3512–3520
41. Newell PD, Yoshioka S, Hvorecny KL, Monds RD, O’Toole GA (2011) Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens p f0–1. J Bacteriol 193:4685–4698
42. Nicolella C, van Loosdrecht MC, Heijnen JJ (2000) Wastewater treatment with particulate biofilm reactors. J Biotechnol 80:1–33
43. O’Shea TM, Klein AH, Geszvain K, Wolfe AJ, Visick KL (2006) Diguanylate cyclases control magnesium-dependent motility of Vibrio fischeri. J Bacteriol 188:8196–8205
44. O’Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304
45. Panke S, Witholt B, Schmid A, Wubbolts MG (1998) Towards a biocatalyst for (S)-styrene oxide production: characterization of the styrene degradation pathway of Pseudomonas sp. strain VLB120. Appl Environ Microbiol 64:2032–2043
46. Park JB, Buehler B, Panke S, Witholt B, Schmid A (2007) Carbon metabolism and product inhibition determine the epoxidation efficiency of solvent-tolerant Pseudomonas sp. strain VLB120ΔC. Biotechnol Bioeng 98:1219–1229
47. Rashid MH, Kornberg A (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 97:4885–4890
48. Römling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57:629–639
49. Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52
50. Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, Mayer R, Braun S, de Vroom E, van der Marel GA, van Boom JH, Benziman M (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281
51. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
52. Sanchez-Torres V, Hu H, Wood T (2011) GGDEF proteins YeaI, YedQ, and YfiN reduce early biofilm formation and swimming motility in Escherichia coli. Appl Microbiol Biotechnol 90:651–658
53. Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14:389–397
54. Spiers AJ, Kahn SG, Bohannon J, Travisano M, Rainey PB (2002) Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161:33–46
55. Spiers AJ, Bohannon J, Gehrig SM, Rainey PB (2003) Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50:15–27
56. Spurbeck RR, Tarrien RJ, Mobley HL (2012) Enzymatically active and inactive phosphodiesterases and diguanylate cyclases are involved in regulation of motility or sessility in Escherichia coli CFT073. MBio 3:e00307–e00312
57. Stanier RY, Palleroni NJ, Doudoroff M (1966) The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43:159–271
58. Starkey M, Hickman JH, Ma L, Zhang N, De Long S, Hinz A, Palacios S, Manoil C, Kirisits MJ, Starner TD, Wozniak DJ, Harwood CS, Parsek MR (2009) Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191:3492–3503
59. Tal R, Wong HC, Calhoon R, Gelfand D, Fear AL, Volman G, Mayer R, Ross P, Amikam D, Weinhouse H, Cohen A, Sapir S, Ohana P, Benziman M (1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180:4416–4425
60. Troeschel SC, Thies S, Link O, Real CI, Knops K, Wilhelm S, Rosenau F, Jaeger K-E (2012) Novel broad host range shuttle vectors for expression in Escherichia coli, Bacillus subtilis and Pseudomonas putida. J Biotechnol 161:71–79
61. Ude S, Arnold DL, Moon CD, Timms-Wilson T, Spiers AJ (2006) Biofilm formation and cellulose expression among diverse environmental Pseudomonas isolates. Environ Microbiol 8:1997–2011
62. Ueda A, Wood TK (2009) Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5:e1000483
63. Weiner R, Seagren E, Arnosti C, Quintero E (1999) Bacterial survival in biofilms: probes for exopolysaccharide and its hydrolysis, and measurements of intra- and interphase mass fluxes. Methods Enzymol 310:403–426
64. Williams P, Winzer K, Chan WC, Camara M (2007) Look who’s talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 362:1119–1134
65. Winn M, Casey E, Habimana O, Murphy CD (2014) Characteristics of Streptomyces griseus biofilms in continuous flow tubular reactors. FEMS Microbiol Lett 352:157–164
66. Wood TK, Gonzalez Barrios AF, Herzberg M, Lee J (2006) Motility influences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol 72:361–367
67. Wood TK, Hong SH, Ma Q (2011) Engineering biofilm formation and dispersal. Trends Biotechnol 29:87–94