TY - JOUR
AU1 - Raulio, Mari
AU2 - Pore, Viljami
AU3 - Areva, Sami
AU4 - Ritala, Mikko
AU5 - Leskelä, Markku
AU6 - Lindén, Mika
AU7 - Rosenholm, Jarl B
AU8 - Lounatmaa, Kari
AU9 - Salkinoja-Salonen, Mirja
AB - Abstract The aim of the present work was to explore possibilities of photocatalytic TiO2 coating for reducing biofilms on non-living surfaces. The model organism, Deinococcus geothermalis, known to initiate growth of durable, colored biofilms on machine surfaces in the paper industry, was allowed to form biofilms on stainless steel, glass and TiO2 film coated glass or titanium. Field emission electron microscopy revealed that the cells in the biofilm formed at 45°C under vigorous shaking were connected to the surface by means of numerous adhesion threads of 0.1--0.3 μm in length. Adjacent cells were connected to one another by threads of 0.5--1 μm in length. An ultrastructural analysis gave no indication for the involvement of amorphous extracellular materials (e.g., slime) in the biofilm. When biofilms on photocatalytic TiO2 surfaces, submerged in water, were exposed to 20 W h m−2 of 360 nm light, both kinds of adhesion threads were completely destroyed and the D. geothermalis cells were extensively removed (from >107 down to below 106 cells cm−2). TiO2 films prepared by the sol-gel technique were slightly more effective than those prepared by the ALD technique. Doping of the TiO2 with sulfur did not enhance its biofilm-destroying capacity. The results show that photocatalytic TiO2 surfaces have potential as a self-cleaning technology for warm water using industries. Introduction Biofilms are a source of product contamination and defects in water using industries, causing energy transfer loss in heat exchangers, inducing failure of medical devices placed in humans, and causing equipment damage and end product contamination and defects [9]. In many cases the use of chemical cleaning agents or biocides have proven ineffective or their use is restricted by regulations, e.g., in the food industry and in products to be used in food contact [7, 31, 41]. Engineering surfaces to repel microbial adhesion, or using physical methods rather than chemical for antifouling is therefore of great interest. Semiconductors like TiO2 and SnO2 are known to generate microbicidal, reactive oxygen species upon illumination with UVA [3, 8, 17]. The aim of the present work was to explore possibilities of photocatalytic TiO2 film coating for reducing biofilms in warm water using industrial processes like papermaking. We used as the model organism Deinococcus geothermalis, which is a primary biofilm former, capable of forming durable biofilms on abiotic surfaces in the paper industry [18, 19, 39]. We present results obtained by field emission scanning electron microscopy (FESEM) on the details of D. geothermalis adhesion onto the surface, and on the impact of illumination at 360 nm on biofilms grown on various coated and noncoated surfaces. Data on biofilm density and its changes were obtained by scanning fluorometry. The results demonstrate a high potential of photocatalytic TiO2 surfaces for controlling biofilms on metal surfaces. Materials and methods The surfaces and substrata used are listed in Table 1. The model bacterium was D. geothermalis E50051 (HAMBI 2411) [39]. All coupons (Table 1, ~1 cm2) were cleaned with detergent (Nelli soap, Farmos, Turku, Finland), sonicated for 5 min in acetone and in 96% ethanol, disinfected (70% ethanol) and mounted in the wells of a polystyrene plate. The wells were filled with 3 ml of culture medium (oligotrophic medium R2 [2]) and inoculated with 5 vol-% of D. geothermalis -strain E50051 grown for 1 day with shaking in R2 broth at + 45°C. The plate was covered with a lid and incubated with shaking (160 rpm) for 2 day at + 45°C in the dark. The plates holding coupons with pre-grown biofilms, submerged in the R2 medium (3 mm liquid above the biofilm), were illuminated (Sylvania 18 W Blacklight Blue) or not illuminated (control) with 360 nm, 1 W/m2, for 20 h, with shaking at + 45°C. The studied surfaces . Surface code . ALD_1 . ALD_2 . Sol-gel_1 . Sol-gel_2 . Noncoated . Preparing method ALD ALD Sol-gel Sol-gel – As delivered Active substance TiO2, Anatase TiO2:S, Rutile TiO2, Anatase macropores TiO2, Anatase – – Substratum Borosilicate glass Borosilicate glass Titanium Titanium Borosilicate glass Stainless steel AISI316 . Surface code . ALD_1 . ALD_2 . Sol-gel_1 . Sol-gel_2 . Noncoated . Preparing method ALD ALD Sol-gel Sol-gel – As delivered Active substance TiO2, Anatase TiO2:S, Rutile TiO2, Anatase macropores TiO2, Anatase – – Substratum Borosilicate glass Borosilicate glass Titanium Titanium Borosilicate glass Stainless steel AISI316 Open in new tab The studied surfaces . Surface code . ALD_1 . ALD_2 . Sol-gel_1 . Sol-gel_2 . Noncoated . Preparing method ALD ALD Sol-gel Sol-gel – As delivered Active substance TiO2, Anatase TiO2:S, Rutile TiO2, Anatase macropores TiO2, Anatase – – Substratum Borosilicate glass Borosilicate glass Titanium Titanium Borosilicate glass Stainless steel AISI316 . Surface code . ALD_1 . ALD_2 . Sol-gel_1 . Sol-gel_2 . Noncoated . Preparing method ALD ALD Sol-gel Sol-gel – As delivered Active substance TiO2, Anatase TiO2:S, Rutile TiO2, Anatase macropores TiO2, Anatase – – Substratum Borosilicate glass Borosilicate glass Titanium Titanium Borosilicate glass Stainless steel AISI316 Open in new tab Quantifying density of the biofilms The method for quantifying the density of biofilms was modified from that described by Mattila et al. [28] by replacing ATP content for calibration by microscopic counting. Briefly, the coupons were rinsed with municipal tap water and stained with SYTO9 (Molecular Probes, Leiden, The Netherlands) nucleic acid stain (3.34 μmol l−1) for 5 min. The coupons were rinsed with water and the emitted fluorescence from an area of 245–315 mm2 was measured using a scanning fluorometer (Fluoroskan Ascent, Labsystems, Helsinki, Finland) at excitation wavelength of 478–492 (±2) nm and emission wavelength of 525–551 (±2) nm). Fluorescence intensity was translated into cell number using a calibration curve prepared by microscopic counting. The fluorescence intensity was proportional to cell number up to a biofilm density of 5×108 cm−2. Stained biofilms were viewed with an epifluorescent microscope (Nikon Eclipse E800, Tokyo, Japan) Preparation of samples for FESEM Coupons with biofilms were rinsed with water, fixed in phosphate (0.1 M, pH 7.2) buffered 2.5% glutaraldehyde for 3 h, and rinsed with phosphate buffer three times. Dehydration was carried out with an ethanol series from 50% to 75% to 96% and absolute, followed by hexamethyldisilazane (Fluka, Buchs, Switzerland). Biofilms were coated with chromium (5 nm, 208 HR High Resolution Sputter Coater, Cressington Scientific Instruments Inc, Cranberry, PA, USA) and microscoped with FESEM of JEOL JSM-6330F (Tokyo, Japan), operated at 15 kV (Fig. 3) or Hitachi S-4800 (Tokyo, Japan) operated at 1 kV (Figs 1, 2, 4, 5). Preparation of TiO2 coated surfaces Films ALD_1 and ALD_2 were grown by atomic layer deposition (ALD) on a borosilicate glass substrate. ALD is a gas phase deposition method, which produces uniform and high quality thin films [21, 35]. Film ALD_1 was prepared at 350°C using Ti(OCH3)4 and water as precursors. This process has been shown to produce anatase thin films with good photocatalytic activities [32]. Film ALD_2 was prepared at 500°C using TiCl4, water and H2S as precursors. The role of H2S was to enhance the formation of a rutile phase and to introduce sulfur doping. Both films were approximately 100 nm in thickness. The titanium dioxide coating on titanium substrates was prepared by the sol-gel technique according to [14, 15]. Commercially available tetraisopropyl orthotitanate, Ti((CH3)2CHO)4 (Merck, Whitehouse Station, NJ, USA) was dissolved in half of the prescribed amount of absolute ethanol (solution I). Deionised water, and nitric acid (HNO3, 65%) were mixed with the other half of the prescribed amount of absolute ethanol (solution II). Solution II was then slowly added to solution I under constant stirring at 0°C. Poly(ethylene glycol) (PEG; average molecular weight of 2,000) was used as the macropore forming agent. The temperature of the sols was then raised in order to dissolve the added organic templates. The sols were aged for at least 2 weeks before dip-coating. The coatings were prepared on titanium substrates by dip-coating at a withdrawal speed of 0.48 mm/s. The coated Sol-gel_1 was heat-treated at a heating ramp of 1°C/min until temperature reached 500°C, maintained at 500°C for 1 h and allowed to cool in the oven. The coated Sol-gel_2 was heat-treated at 500°C for 1 h and cooled at room temperature. The prepared films approx. 250 nm in thickness (as observed by cross-sectional high-resolution scanning electron microscope) were of anatase crystal structure (as observed by Thin-Film X-ray Diffraction). Results Field emission scanning electron microscope was used to establish whether adhesion of D. geothermalis to non-living surfaces is mediated by slime, by specific adhesion organelles like fimbria or by the sticky surface of the cell body, and how the adhesion organelles respond to alkaline washing used in industrial cleaning. D. geothermalis strain E50051 was allowed to form biofilm on glass coupons. The biofilms persisting after subsequent washing were then investigated by FESEM (Fig. 1). Fig. 1 Open in new tabDownload slide Resistance of Deinococcus geothermalis biofilm towards washing with alkali. D. geothermalis E50051 was grown on glass surface in R2 medium at 45°C for 2 day under shaking at 160 rpm. The field emission scanning electron micrographs were taken after the biofilms were washed for 1 h at 45°C with drinking water (a) or with 0.1% (w/v) aqueous sodium hydroxide (b). Biofilm subjected to no washing (not included in the Figure) appeared identical to panel a Figure 1 reveals the dense network of thread-like organelles of D. geothermalis E50051, connecting the cells to the glass surface as well as the adjacent cells to one another. Each cell was connected to the glass by 20–50 threads of 0.3--0.6 μm in length. Adjacent cells were linked to one another by two to ten threads of up to 1 μm in length. The morphology of the cells and their adhesion organelles seemed unaffected by washing with strong alkali under agitation (pH>12, 45°C, Fig. 1b). The amount of adhered cells remained 107 cm−2 (within one log unit), irrespective of the washing. The impact of photocatalysis on the adhesion apparatus of D. geothermalis was investigated using glass coupons coated with TiO2 by the ALD method. D. geothermalis biofilm was grown on the surface and then illuminated or not illuminated at 360 nm (Fig. 2). Fig. 2 Open in new tabDownload slide Photocatalytically induced change in morphology of Deinococcus geothermalis growing on TiO2 coated glass substratum prepared by the ALD method (surface ALD_1 in Table 1). Field emission scanning electron micrographs show 2 day old biofilms of the strain E50051 not illuminated (a, b) or illuminated (c, d) for 20 h at 360 nm The cells adhering to TiO2 possessed threads of 0.5--1 μm in length and ~50 nm in diameter connecting adjacent cells. The short appendices, 0.1--0.3 μm in length connecting the bacterial cell body to the TiO2 surface, were fewer in number (5–20 cell−1) than those connecting the same strain onto plain glass (Fig. 1). Illumination at 360 nm of the biofilm on the TiO2 (ALD) coated glass surface resulted in massive detachment (89±5%) of cells. The cells remaining on the surface appeared collapsed and the adhesion threads destroyed (Fig. 2c, d). Parallel coupons of TiO2 coated surface incubated for the same period (20 h) in the dark, showed no deterioration of the D. geothermalis biofilm. To answer the question of whether the massive collapse of the biofilm on TiO2 (ALD) surface in response to 360 nm irradiation was linked to the photochemistry of the TiO2 film or to other properties of the substratum, TiO2 coatings were prepared on titanium substrate using a different technology; sol-gel was used. D. geothermalis biofilm was grown and the illumination executed as for Fig. 2. It was found (Fig. 3) that the D. geothermalis biofilm was removed by photocatalysis from the sol-gel TiO2 coated titanium surface at least as effectively (>95%) as from the ALD TiO2 surface on glass. Figure 3 shows that the cells remaining on the surface had lost all adhesion threads, even if some of the cells looked otherwise intact. Many of the cells looked lysed (Fig. 3c, d). Fig. 3 Open in new tabDownload slide Photocatalytically induced morphological change in Deinococcus geothermalis growing on titanium substrate coated with TiO2 by the sol-gel method (surface Sol-gel_1 in Table 1). Field emission scanning electron micrographs show 2 day old biofilms of the strain E50051 not illuminated (a, b) or illuminated (c, d) for 20 h at 360 nm We conclude that D. geothermalis E50051 biofilms grown on TiO2 coated surfaces were destroyed and removed by photocatalytic activity independent of the method of preparation (ALD or sol-gel) or the substratum (glass or titanium). To distinguish between the roles of 360 nm illumination as such and of TiO2 mediated photocatalytic activity, the effects of light exposure were inspected with non-photocatalytic stainless steel. To do this, D. geothermalis was allowed to grow on coupons of unpolished stainless steel and then illuminated or not illuminated. It is seen from Fig. 4a, b that D. geothermalis growing on stainless steel possessed attachment structures similar in morphology and number to those connecting D. geothermalis onto TiO2 coated surface on glass or on titanium (Figs 2 b, 3 b). The attachment structures differed from those on uncoated glass surface (Fig. 1a) by their lower density. Fig. 4 Open in new tabDownload slide Effect of 360 nm illumination on Deinococcus geothermalis growing on stainless steel, investigated with field emission scanning electron microscope. The micrographs show D. geothermalis E50051 grown for 2 day on stainless steel not illuminated (a, b), or illuminated (c, d) for 20 h at 360 nm When D. geothermalis E50051 grown on stainless steel was illuminated at 360 nm, no (<< 1 log) reduction was observed in cell density, and the adhesion threads looked similar in density and dimensions independent of the exposure to illumination (Fig. 4a--d). Therefore, the effects displayed in Figs. 2c, d and 3c, d must have been due to TiO2 induced photocatalysis. Ultrastructural details of the cell surface and adhesion organelles of D. geothermalis are shown in high magnification (×100,000) FESEM micrographs in Fig. 5. It shows that the cell surface (Fig. 5a) of D. geothermalis is not smooth but is composed of many differently shaped structures. The adhesion threads are non-uniform in shape, thickness and length (Fig. 5b). Several threads expand to a foot-like form at the site where the thread touches the steel surface (arrows in Fig. 5b). Fig. 5 Open in new tabDownload slide Ultrastructural details of Deinococcus geothermalis cells attached on stainless steel coupons. The images were taken with field emission scanning electron microscope applying ×100,000 magnification. D. geothermalis was grown and illuminated as in Fig. 4. Not illuminated (a), or illuminated (b) for 20 h at 360 nm To collect quantitative data on the effects of the substratum and the treatments on biofilm density, a method is needed for counting of cells independent of the possible presence of extracellular materials like slime. We developed a method based on optical fluorescence reading to quantitate biofilms. The fluorescence emitted by bacterial biomass stained with a nucleic acid specific dye, SYTO9, is quantified using a scanning fluorometer. Figure 6 shows examples of microscopic views of steel coupons prepared for fluorescent readout. It shows surface attached deinococcal cells of diameter of 1 μm occuring singly, in pairs, in small microcolonies where individual cells (3–10) can be distinguished and as larger intensively fluorescing microcolonies where the individual cells can no longer be distinguished. All cell aggregate sizes were approximately equally distributed on the un-coated steel surface whether illuminated (Fig. 6b) or not illuminated (Fig. 6a). Fig. 6 Open in new tabDownload slide Epifluorescence micrographs of SYTO9 stained 2 day grown Deinococcus geothermalis E50051 biofilm on steel before (a) and after (b) illumination at 360 nm (Nikon Eclipse E800; Excitation-λ 478–492 (±2) nm, emission-λ 525–551 (±2) nm). Fluorescent readout (Fig. 7) makes it possible to estimate cell numbers in larger, multi-layered, microcolonies, where microscopic counting is not possible (arrows) Figure 7 shows data obtained by the fluorescent reading technique of D. geothermalis biofilms on different substrates and their responses to photocatalytic activity. It shows that D. geothermalis E50051 adhered approximately 1 log more effectively to steel and to TiO2 coated surfaces than to glass. Photocatalytic TiO2 ALD surfaces were effective in destroying the adhered biofilms in response to irradiation, reducing the biofilm quantity by 1 log value and those prepared by the sol-gel method, by 2 log values. Doping of ALD-TiO2 with sulfur (ALD_2, Fig. 7) did not enhance its biofilm destroying activity. Fig. 7 Open in new tabDownload slide Densities of Deinococcus geothermalis E50051 biofilms on abiotic surfaces and the effects of illumination at 360 nm. Biofilms were grown and then irradiated as described in the legend for Fig. 1. The coupons were stained with SYTO9 and intensity of the emitted fluorescence quantitated with a scanning fluorometer. Fluorescence values were translated in to cell numbers by using standard curve based on microscopic counting. Error bars indicate standard deviations Discussion This paper describes the biofilm behavior of paper machine pink slime former D. geothermalis on abiotic surfaces and reversal of the adhesion by illuminated photocatalytic films. D. geothermalis adhered onto glass, steel and TiO2 coated materials by an extensive network of adhesion threads. The FESEM images gave no indication of any significant contribution of extracellular materials in the biofilm. The adhesion threads in D. geothermalis were first observed by Kolari et al. [19]. These threads connect the cells to an abiotic substratum, leading to formation of an endurable biofilm that cannot be removed by vigorous shaking in water or by chemically aggressive cleaning formulations such as sodium dodecyl sulphate [19] or sodium hydroxide [this paper; 19] at an elevated temperature. The inertness towards chemical cleaning and shearing forces distinguishes the deinococcal adhesion apparatus from that described for other taxons like Burkholderia cepacia and Staphylococcus epidermidis [19] and Acinetobacter sp. [12]. It has been shown in many studies that bacteria growing as biofilms are more resistant to antimicrobial agents than the same bacteria in planktonic form [4--6, 20, 22, 36]. Kolari et al. [20] reported that in the presence of biocides, many biofilm bacteria, including D. geothermalis, produced even more biofilm than in the absence of biocides. In this study, we show that biofilms of D. geothermalis on TiO2 coated surfaces were effectively removed (1--2 log units) by titanium dioxide generated photocatalytic action in response to irradiation at 360 nm. This wavelength is emitted by daylight sources (fluorescent tubes) commonly used in offices and workspaces. FESEM analysis of D. geothermalis biofilms after exposure to TiO2-generated photocatalysis upon illumination at 360 nm showed that adhesion threads connecting the D. geothermalis cells to each other and to the abiotic surface were completely destroyed. Photocatalytic activity by TiO2 is known to have disinfecting action [1, 11, 13, 24, 26, 37, 40]. Its effectiveness in killing water suspended microorganisms is well documented and also has practical applications. The potential of photocatalytic TiO2 as a tool against a biofilm mode of growth has received little attention so far. Li and Logan [23] studied the response of low density (105 cells cm−2) adhered Escherichia coli (strains JM109, D21 and D21f2), B. cepacia (strains G4 and Env435) and Pseudomonas aeruginosa (strains PA01 and PDO300) on TiO2 coated glass upon illumination at 254 (UVC) and 340 nm (UVA). They achieved up to 50% removal at 340 nm and 30–70% removal at 254 nm using irradiation doses of 28–46 W h m−2. In our study, from 90% to close to 100% removal of D. geothermalis was observed at 360 nm irradiation upon exposure to 20 W h m−2. Li and Logan [23] used a 20 nm thick anatase TiO2 film. Photocatalytic coatings used in our work were prepared by ALD [21] and sol-gel [14, 15] techniques to a thickness of 100 nm, possibly explaining the higher efficacy of biofilm removal achieved. The adhesion threads connecting D. geothermalis to the substratum were shown to be non-uniform in thickness and length, and attachment to an abiotic surface appeared to involve a foot-like structure at the contact site. No similar structure has been reported in any other bacteria until now. D. geothermalis is a non-motile organism, possessing the ability to glide on a surface when exposed to external pressure [19]. Active gliding motility designated as “social gliding motility” or “twitching motility” has been shown in wide range of bacteria, e.g., Pseudomonas aeruginosa, Neisseria gonorrhoeae and Myxococcus xanthus [10. 27, 29] Such motility has been shown to depend on a type IV pilus. Type IV pili are known to be involved also in adhesion of Shewanella oneidensis onto glass [38], of Ralstonia solanacearum to polyvinylchloride (PVC) plastic [16] and microcolony formation of P. aeruginosa on polyvinylchloride plastic [30]. Interestingly, it was shown recently that the type IV pili occurring in iron reducing Geobacter species are electrically conductive nanowires connecting the bacteria to an inorganic surface [33]. The complete chromosomal sequence of one deinococcal species, D. radiodurans, is known [25]. It contains the full set of genes needed for the type IV pilus production machinery. A preliminary sequence involving type IV pilus genes has also been reported in D. geothermalis DSM11300 (accession number: NZ_AAHE00000000, [34]). However, the structures of D. geothermalis shown in this paper by FESEM and earlier by atomic force microscopy (AFM) [19] neither resemble morphologically the type IV pili such as published by Kang et al. [16] in R. solanacearum nor the anchor-like adhesion organelles of Acinetobacter sp. [12]. In addition to the adhesion threads (Figs. 1, 2, 3, 4, 5 in this paper) D. geothermalis possesses a patchy cell surface responding heterogeneously to adhesion forces measured by AFM [19]. The patchy surface observed by FESEM in this study (Fig. 5) and by AFM by Kolari et al. [19] may thus have local and heterogeneous adhesiveness, possibly explaining why some of the D. geothermalis cells persistently adhered to TiO2 film post irradiation in spite of the complete loss of adhesion threads. The high efficacy of photocatalytic TiO2 films in destroying the adhesion apparatus of the tenacious biofilm former D. geothermalis indicates that this technology could be used as a tool towards a biocide free process in warm water industries such as paper mills. Acknowledgements This work is a part of the technology programme Clean Surfaces 2002–2006 supported by the Finnish National Technology Agency (TEKES) and Academy of Finland Center of Excellence grant Nr. 53305. We thank Dr Marianna Kemell and Dr Pia Niinimäki for expert advice. We also thank Helsinki University Viikki Science Library for excellent information services, the Faculty of Agriculture and Forestry Instrument Centre for technical support and Leena Steininger, Hannele Tukiainen and Tuula Suortti for many kinds of help. References 1. Amézaga-Madrid P , Nevárez-Moorillón GV, Orrantia-Borunda E, Miki-Yoshida M Photoinduced bactericidal activity against Pseudomonas aeruginosa by TiO2 based thin films FEMS Microbiol Lett 2002 211 183 188 10.1016/S0378-1097(02)00686-9 Google Scholar Crossref Search ADS PubMed WorldCat 2. Anonymous (1992) Heterotrophic plate count. In: Clesceri LS, Greenberg AE, Eaton AD (eds) Standard methods for the examination of water and wastewater, American Public Health Association, American Water Works Association and Water Environment Federation, 20th edn. American Public Health Association, Washington DC, pp 9–34 to 9–36 3. Cho M , Chung H, Choi W, Yoon J Linear correlation between inactivation of E. coli and OH radical concentration in TiO2 photocatalytic disinfection Water Res 2004 38 1069 1077 10.1016/j.watres.2003.10.029 Google Scholar Crossref Search ADS PubMed WorldCat 4. Das JR , Bhakoo M, Jones MV, Gilbert P Changes in the biocide susceptibility of Staphylococcus epidermidis and Escherichia coli cells associated with rapid attachment to plastic surfaces J Appl Microbiol 1998 84 852 858 10.1046/j.1365-2672.1998.00422.x Google Scholar Crossref Search ADS PubMed WorldCat 5. Donlan RM , Costerton JW Biofilms: survival mechanisms of clinically relevant microorganisms Clin Microbiol Rev 2002 15 167 193 10.1128/CMR.15.2.167-193.2002 Google Scholar Crossref Search ADS PubMed WorldCat 6. Dunne WM Jr Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 2002 15 155 166 10.1128/CMR.15.2.155-166.2002 Google Scholar Crossref Search ADS PubMed WorldCat 7. Eagon RG Rossmoore HW Paper, pulp and food grade paper Handbook of biocide and preservative use 1995 Glasgow Blackie Academic & Professional, an imprint of Chapman & Hall 83 132 Google Scholar Crossref Search ADS Google Preview WorldCat COPAC 8. Fujishima A , Honda K Electrochemical photocatalysis of water at a semiconductor electrode Nature 1972 238 37 38 10.1038/238037a0 Google Scholar Crossref Search ADS PubMed WorldCat 9. Geesey GG , Bryers JD Bryers JD Biofouling of engineered materials and systems Biofilms II: process analysis and applications 2000 New York Wiley-Liss, Wiley 237 279 Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC 10. Harshey RM Bacterial motility on a surface: many ways to a common goal Annu Rev Microbiol 2003 57 249 273 10.1146/annurev.micro.57.030502.091014 Google Scholar Crossref Search ADS PubMed WorldCat 11. Huang Z , Maness P-C, Blake DM, Wolfrum EJ, Smolinski SL, Jacoby WA Bactericidal mode of titanium dioxide photocatalysis J Photoch Photobio A 2000 130 163 170 10.1016/S1010-6030(99)00205-1 Google Scholar Crossref Search ADS WorldCat 12. Ishii S , Koki J, Unno H, Hori K Two morphological types of cell appendages on a strongly adhesive bacterium, Acinetobacter sp. Strain Tol 5 Appl Environ Microbiol 2004 70 5026 5029 10.1128/AEM.70.8.5026-5029.2004 Google Scholar Crossref Search ADS PubMed WorldCat 13. Jacoby WA , Maness P-C, Wolfrum EJ, Blake DM, Fennell JA Mineralization of bacterial cell mass on a photocatalytic surface in air Environ Sci Technol 1998 32 2650 2653 10.1021/es980036f Google Scholar Crossref Search ADS WorldCat 14. Kajihara K , Takeshi Y Macroporous morphology of the titania films prepared by a sol-gel dip-coating method from the system containing poly(ethylene glycol). I Effect of humidity J Sol-gel Sci Tech 1998 12 185 192 10.1023/A:1008602419045 Google Scholar Crossref Search ADS WorldCat 15. Kajihara K , Takeshi Y Macroporous morphology of the titania films prepared by a sol-gel dip-coating method from the system containing poly(ethylene glycol). I Effect of solution composition J Sol-gel Sci Tech 1998 12 193 201 10.1023/A:1008606503115 Google Scholar Crossref Search ADS WorldCat 16. Kang Y , Liu H, Genin S, Schell MA, Denny TP Ralstonia solanacearum requires type 4 pili to adhere to multiple surfaces and for natural transformation and virulence Mol Microbiol 2002 2 427 437 10.1046/j.1365-2958.2002.03187.x Google Scholar Crossref Search ADS WorldCat 17. Kikuchi Y , Sunada K, Iyoda T, Hashimoto K, Fujishima A Photocatalytic bactericidal effect of TiO2 thin films: dynamic view of the active oxygen species responsible for the effect J Photoch Photobio A 1997 106 51 56 10.1016/S1010-6030(97)00038-5 Google Scholar Crossref Search ADS WorldCat 18. Kolari M , Nuutinen J, Salkinoja-Salonen MS Mechanisms of biofilm formation in paper machine by Bacillus species: the role of Deinococcus geothermalis J Ind Microbiol Biot 2001 27 343 351 10.1038/sj.jim.7000201 Google Scholar Crossref Search ADS WorldCat 19. Kolari M , Schmidt U, Kuismanen E, Salkinoja-Salonen MS Firm but slippery attachment of Deinococcus geothermalis. J Bacteriol 2002 184 2473 2480 10.1128/JB.184.9.2473-2480.2002 Google Scholar Crossref Search ADS PubMed WorldCat 20. Kolari M , Nuutinen J, Rainey FA, Salkinoja-Salonen MS Colored moderately thermophilic bacteria in paper-machine biofilms J Ind Microbiol Biot 2003 30 225 238 Google Scholar Crossref Search ADS WorldCat 21. Leskelä M , Ritala M Atomic layer deposition (ALD): from precursors to thin film structures Thin Solid Films 2002 204 138 146 10.1016/S0040-6090(02)00117-7 Google Scholar Crossref Search ADS WorldCat 22. Lewis K Riddle of biofilm resistance Antimicrob agents ch 2001 45 999 1007 10.1128/AAC.45.4.999-1007.2001 Google Scholar Crossref Search ADS WorldCat 23. Li B , Logan BE The impact of ultraviolet light on bacterial adhesion to glass and metal oxide-coated surface Colloid Surface B 2005 41 153 161 10.1016/j.colsurfb.2004.12.001 Google Scholar Crossref Search ADS WorldCat 24. Liu H-L , Yang TC-K Photocatalytic inactivation of Escherichia coli and Lactobacillus helveticus by ZnO and TiO2 activated with ultraviolet light Process Biochem 2003 39 475 481 10.1016/S0032-9592(03)00084-0 Google Scholar Crossref Search ADS WorldCat 25. Makarova KS , Aravind L, Wolf YL, Tatusov RL, Minton KW, Koonin EV, Daly MJ Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics Microbiol Mol Biol R 2001 65 44 79 10.1128/MMBR.65.1.44-79.2001 Google Scholar Crossref Search ADS WorldCat 26. Maness P-C , Smolinski S, Blake DM, Huang Z, Wolfrum EJ, Jacoby WA Bactericidal activity of photocatalytic TiO2 reaction: toward an understanding of its killing mechanism Appl Environ Microbiol 1999 65 4094 4098 Google Scholar Crossref Search ADS PubMed WorldCat 27. Mattick JS Type IV pili and twitching motility Annu Rev Microbiol 2002 56 289 314 10.1146/annurev.micro.56.012302.160938 Google Scholar Crossref Search ADS PubMed WorldCat 28. Mattila K , Weber A, Salkinoja-Salonen MS Structure and on-site formation of biofilms in paper machine water flow J Ind Microbiol Biot 2002 28 268 279 10.1038/sj.jim.7000242 Google Scholar Crossref Search ADS WorldCat 29. McBride MJ Bacterial glidingmotility: multiple mechanisms for cell movement over surfaces Annu Rev Microbiol 2001 55 49 75 10.1146/annurev.micro.55.1.49 Google Scholar Crossref Search ADS PubMed WorldCat 30. O’Toole GA , Kolter R Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development Mol Microbiol 1998 30 295 304 10.1046/j.1365-2958.1998.01062.x Google Scholar Crossref Search ADS PubMed WorldCat 31. Ottenio D , Escabasse J-Y, Podd B Packaging materials 6. Paper and board for food packaging applications 2004 Brussels ILSI Report Series 6, International Life Sciences Institute, ILSI Press Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC 32. Pore V , Rahtu A, Leskelä M, Ritala M, Sajavaara T, Keinonen J Atomic layer deposition of photocatalytic TiO2 thin films from titanium tetramethoxide and water Chem Vapor Depos 2004 10 143 148 10.1002/cvde.200306289 Google Scholar Crossref Search ADS WorldCat 33. Reguera G , McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR Extracellular electron transfer via microbial nanowires Nature 2005 435 1098 1101 10.1038/nature03661 Google Scholar Crossref Search ADS PubMed WorldCat 34. Richardson P (2005) Annotation of the draft genome assembly of Deinococcus geothermalis DSM 11300. http://genome.ornl.gov/microbial/dgeo/15apr04/dgeo_N_cogs.html 35. Ritala M, Leskelä M (2002) Atomic layer deposition, chapter 2. In: Nalwa HS (ed) Handbook of thin film materials vol 1. Academic, New York, pp 103–159 36. Stewart PS , Costerton JW Antibiotic resistance of bacteria in biofilms Lancet 2001 358 135 138 10.1016/S0140-6736(01)05321-1 Google Scholar Crossref Search ADS PubMed WorldCat 37. Sunada K , Watanabe T, Hashimoto K Studies on photokilling of bacteria on TiO2 thin film J Photoch Photobio A 2003 156 227 233 10.1016/S1010-6030(02)00434-3 Google Scholar Crossref Search ADS WorldCat 38. Thormann KM , Saville RM, Shukla S, Pelletier DA, Spormann AM Initial phases of biofilm formation in Shewanella oneidensis MR-1 J Bacteriol 2004 186 8096 8104 10.1128/JB.186.23.8096-8104.2004 Google Scholar Crossref Search ADS PubMed WorldCat 39. Väisänen OM , Weber A, Bennasar A, Rainey FA, Busse H-J, Salkinoja-Salonen MS Microbial communities of printing paper machines J Appl Microbiol 1998 84 1069 1084 10.1046/j.1365-2672.1998.00447.x Google Scholar Crossref Search ADS PubMed WorldCat 40. Wolfrum EJ , Huang J, Blake DM, Maness P-C, Huang Z, Fiest J, Jacoby WA Photocatalytic oxidation of bacterial, bacterial and fungal spores, and model biofilm components to carbon dioxide on titanium dioxide-coated surfaces Environ Sci Technol 2002 36 3412 3419 10.1021/es011423j Google Scholar Crossref Search ADS PubMed WorldCat 41. Yeager CC Rossmoore HW Legislative aspects Handbook of biocide and preservative use 1995 Glasgow Blackie Academic & Professional, an imprint of Chapman & Hall 19 49 Google Scholar Crossref Search ADS Google Preview WorldCat COPAC © Society for Industrial Microbiology 2006 This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model) © Society for Industrial Microbiology 2006
TI - Destruction of Deinococcus geothermalis biofilm by photocatalytic ALD and sol-gel TiO2 surfaces
JF - Journal of Industrial Microbiology and Biotechnology
DO - 10.1007/s10295-005-0063-2
DA - 2006-04-01
UR - https://www.deepdyve.com/lp/oxford-university-press/destruction-of-deinococcus-geothermalis-biofilm-by-photocatalytic-ald-ctLM39nw6W
SP - 261
EP - 268
VL - 33
IS - 4
DP - DeepDyve
ER -