Rapid photokilling of gram-negative Escherichia coli bacteria by platinum dispersed titania...

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Materials Chemistry and Physics xxx (2012) 1e7

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Materials Chemistry and Physics

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Rapid photokilling of gram-negative Escherichia coli bacteria by platinumdispersed titania nanocomposite films

Bonamali Pal a,*, Isha Singh b, Kunal Angrish b, Raghavendra Aminedi b, Niranjan Das b

a School of Chemistry and Biochemistry, Thapar University, Patiala 147004, IndiabDepartment of Biotechnology and Environmental Sciences, Thapar University, Patiala 147004, India

h i g h l i g h t s

* Corresponding author. Tel.: þ91 175 2393443; faxE-mail address: [email protected] (B. Pal).

0254-0584/$ e see front matter � 2012 Elsevier B.V.http://dx.doi.org/10.1016/j.matchemphys.2012.06.001

Please cite this article in press as: B. Pal, enanocomposite films, Materials Chemistry a

g r a p h i c a l a b s t r a c t

< Remarkable antimicrobial activity ofphotorradiated PteTiO2 coated thinfilm.

< Pt impregnation-exhibits superiorphotoactivity than Pt photo-deposition onto TiO2.

< Photokilling of E. coli cells occurwithin 10 min of UV (640 mW cm�2)irradiation.

< Size and nature of Pt depositioncontrol the bactericidal effect ofTiO2 catalyst.

< Photodissolution of bacterial surfaceis occurred on prolong UV lightexposure.

a r t i c l e i n f o

Article history:Received 2 May 2011Received in revised form8 February 2012Accepted 3 June 2012

Keywords:Antimicrobial activityTitania thin filmsPhotocatalytic bacteria killingPt-dispersed TiO2 catalysts

a b s t r a c t

Superior antimicrobial activity of 2 wt.% Pt-dispersed TiO2 thin film was observed in photokilling Gram-negative Escherichia coli bacteria within 5 min irradiation (640 mW cm�2, l > 340 nm) from UV torch thanbare TiO2 film. Severe disruption of cell membrane has occurred over illuminated Pt-TiO2 catalysts filmscoated with 100e300 mg powders per 5 cm2 areas over sterilized glass slides. The Pt dispersion onto TiO2

by impregnationehydrogen reduction always exhibited better photokilling effect than Pt photo-deposition, irrespective of PteTiO2 dose and light exposure time. Similar trend in photoactivity differencebetween two PteTiO2 catalysts is also observed in aqueous slurry because of the unlike surface structureof TiO2 due to different annealing temperatures, size and nature of Pt particles dispersion onto TiO2

photocatalysts.� 2012 Elsevier B.V. All rights reserved.

1. Introduction

The photocatalytic destruction of Escherichia coli bacteria andother species using platinum loaded titania (PteTiO2) suspension isreported byMatsunaga et al [1,2]. Extensive research has been doneabout the destruction of E. coli using TiO2 suspension [3e15]. The

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t al., Rapid photokilling of grnd Physics (2012), http://dx.d

use of TiO2 films has also been investigated in photokilling ofbacterial cells and found to be as effective as the suspended form[8e11]. However, this method does not suit for the practicalapplication due to long contact time for bacterial disinfection.Recent studies have demonstrated that metal (silver, iron, gold etc.)loaded TiO2 particles could be used as efficient bactericidal agentsdue to better charge transfer process between the electrons[12e15]. The electrons accumulate on metal and the holes remainon the photocatalyst surface oxidizing the adsorbed species. It hasalso been reported [16] that undoped films and films doped with

am-negative Escherichia coli bacteria by platinum dispersed titaniaoi.org/10.1016/j.matchemphys.2012.06.001

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B. Pal et al. / Materials Chemistry and Physics xxx (2012) 1e72

Cu and Al, showed a photoinduced bactericidal effect on Pseudo-monas aeruginosa (108 CFU ml�1) with bacterial inhibition varyingbetween 28 and 96%, depending on the composition of the films.The undoped films resulted in a greater bacterial inhibition,although the Cu-doped films had the greatest quantum yield. Thephotoactivity of AueTiO2 hybrid structures depends on the Audeposition method, while Pt/TiO2 photocatalysts are less sensitiveto the preparation techniques [17]. Pt nanoparticles have beenextensively used to obtain PteTiO2 nanocomposites whose pho-toefficiency depends on various structural and morphologicalfeatures as a function of the preparation techniques. The mecha-nism of nucleation and growth of platinum nanoparticles over thesurface of TiO2 prepared by different route are found to playa dominant role in many photocatalytic reactions. However, veryfew studies are conducted using PteTiO2 thin film coating toinvestigate the bactericidal activity compared with bare TiO2. Here,we report the superior bactericidal effect of PteTiO2 catalystsprepared by impregnationehydrogen reduction (IR), whichexhibited higher photokilling rate of Gram-negative E. coli cells ascompared to Pt photodeposition (PD) method.

2. Experimental details

Pt (2 wt.%)-impregnated TiO2 (Degussa P25) were prepared bymixing aqueous solution of TiO2 and H2PtCl6$6H2O followed bydrying and subsequent H2 reduction in a furnace at 753 K [18e23].Photodeposition of Pt was done with 50% aqueous methanolsuspension of TiO2 and H2PtCl6$6H2O under N2 atmosphere for 1 hlight irradiation (125 W, Hg-arc lamp) and dried to use. Theprepared PteTiO2 catalysts are characterized by HR-TEM (Hitachi7500) size, SEM surface morphology and EDS elemental analysis.

Fig. 1. SEM images and EDS analysis of (a) 2 wt.% PteTiO

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Gram-negative E. coliDH5a strainwas aerobically grown in 25ml ofLuria Bertani Broth (LB) medium at 37 �C, 120 rpm for 14 h and250 ml of this culture was inoculated in a fresh LB medium (25 ml).The sterilized glass slides were coated (2 � 2.5 cm2) with requiredamounts of PteTiO2 inwater (0.5 ml) and heated at 200 �C for 2 h toensure proper immobilization. The Pt-TiO2 coated slide was evenlyspreaded with 200 ml of cell suspension (106 CFU ml�1) andexposed to light irradiation from UV torch (6 W, wavelength,l > 340 nm, 0.64 mW cm�2 at a distance of 5.5 cm) for differenttime periods. Cell viability was determined by counting the numberof colonies after plating 100 ml aliquots onto LB agar plates, incu-bated at 37 �C for 24 h. The culture was subjected to centrifugationat 10,000 rpm for 10 min. The pellet was resuspended in 2% para-formaldehyde and 2.5% glutaraldehyde in 0.1 M phosphate buffer,cut into thin sections using microtome and these were droppedonto copper grids to get the Transmission Electron Microscopic,TEM (Philips CM-10) images.

3. Results and discussion

Fig. 1 shows the SEM surface morphology and EDS elementalanalysis of PteTiO2 catalysts. It can be seen that PteTiO2 (IR)catalysts (Fig. 1a) prepared by impregnationehydrogen reductionexhibit more homogenous dispersion of Pt and TiO2 particles thanPt photodeposition onto TiO2 (Fig. 1b). The PteTiO2 (PD) catalystspowders showed many aggregated particles of relatively large sizedistribution as seen in the SEM images of Fig. 1b. Although, no clearcontrast between Pt deposits and TiO2 particles can bemade in SEMimages, but the EDS elemental analysis (right graph of Fig. 1)confirmed the presence of Pt dispersion in PteTiO2 catalysts. Theelemental compositions are 5.63 wt.% C, 35. 08 wt.% O, 4.55 wt.% Pt

2 (IR) and (b) 2 wt.% PteTiO2 (PD) catalysts powders.

ram-negative Escherichia coli bacteria by platinum dispersed titaniadoi.org/10.1016/j.matchemphys.2012.06.001

B. Pal et al. / Materials Chemistry and Physics xxx (2012) 1e7 3

and 54.74 wt.% Ti for PteTiO2 (IR) catalysts and 3.63 wt.% C,35.64 wt.% O, 3.04 wt.% Pt and 57.69 wt.% Ti for PteTiO2 (PD)catalysts as seen in Fig. 1-inset of respective EDS graph. It is foundthat higher amount of Pt (4.55 wt.%) dispersion occurs duringimpregnationereduction of PteTiO2 powder than Pt photo-deposition (3.04 wt.%) onto TiO2 powder. This Pt content seems tobe little higher than the actual amount (2 wt.%) used for PteTiO2catalysts preparation. Fig. 2 shows the HR-TEM images of twodifferent PteTiO2 catalysts which revealed that Pt photodepositiononto TiO2 catalyst exhibited relatively larger size of Pt dispersionthan Pt impregnation into TiO2 powders. One can observe (Fig. 2a)that black colored Pt deposits of size range w8e10 nm are depos-ited onto TiO2 (gray color) TiO2 particles and Pt is not consistentlydeposited to all TiO2 particles and many bare TiO2 particles areclearly noticed in the HR-TEM images. However, in case of Ptimpregnationereduction method, very small Pt deposits aredistinctly seen to be homogenously dispersed over the entiresurface of agglomerated TiO2 particles as shown in HR-TEM imagesof Fig. 2b. An enlarge view at higher resolution in Fig. 2c ensuredthat a large number of black dots of Pt nanoparticles of size rangew2e5 nm are deposited onto almost all TiO2 particles and no bareTiO2 clusters are obtained in all the HR-TEM images of PteTiO2 (IR)catalyst. This is in accordance with the SEM-EDS data of having

Fig. 2. HR-TEM images of (a) 2 wt.% PteTiO2 (PD) and (b and c) 2 w

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higher Pt content in PteTiO2 (IR) catalyst than PteTiO2 (PD) cata-lysts. In fact, some spherical shaped TiO2 particles attached to thedead bacterial cells are seen to be coated with thin layer of Ptdeposition as discussed in Fig. 5 below.

The cell wall of the Gram-negative bacteria is chemically morecomplex and the outer membrane is about 6e18 nm thickin contrast to 20e80 nm of gram-positive bacteria. Thephotocatalytic killing rate follows the order as: E. coli (Gram-negative) > Staphylococcus aureus (Gram-positive) > Candida albi-cans (thick eukaryotic cell) because of the complexity and gradualincrease in cell wall thickness from E. coli to C. albicans [9]. Thus,photocatalytic killing of Gram-negative E. coli cells by TiO2 isa viable perception. Fig. 3a shows that longer wavelength light(>340 nm) irradiation for 15 min killed 40% of the bacterial cellsand the bare TiO2 (5 mg) coated thin film showed 75% killing ascompared with the control culture. However, when irradiated inpresence of 5 mg PteTiO2 (IR & PD) coated films, almost 97e100%cell death was observed. The bacterial colonies formed are gradu-ally decreased from left to right plate (as shown in Fig. 3b), whichare in accordancewith the various experimental sequence of Fig. 3aand its finding. Many bacterial colonies are seen (1st row-3rd plate)after 15 min irradiation of E. coli suspension over bare TiO2 film.However, irradiated cell suspensions over PteTiO2 (PD & IR) films

t.% PteTiO2 (IR) photocatalysts at two different magnifications.


0

20

40

60

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% s

urvi

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UV light

TiO2

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UV irradiation-15 min

a

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0

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4

6

% s

urvi

val

PD5 min

IR5 m in

IR10 m in

PD10 m in

c

b

PD

d

IR

Fig. 3. (a) Bactericidal activity of bare TiO2 and PteTiO2 (PD & IR) films (5 mg catalysts) after 15 min light irradiation compared with control and UV exposure only, (b) gradualdecrease (left to right plate) in bacterial colonies in sequence of Fig. 1a experimental results, (c) % cell survival after 5 and 10 min irradiation on PteTiO2 (PD & IR) films, (d) disparityin colony counts after 5 min irradiation over PteTiO2 (PD & IR) films as found in Fig. 1c experiment.


did not show any growth of bacterial colony (bottom two plates),indicating 100% killing of bacteria due to high photoactivity of bothPD & IR catalysts compared to poor activity of bare TiO2. Fig. 3cconfirms that the bacterial cells were almost completely killed evenafter 5 min irradiation over IR films, whereas PD films till exhibited6.5% and 5% survival after 5 and 10 min irradiation, respectively. Nobacterial colonies are found (as seen in Fig. 3d) even after 5 minirradiation of E. coli suspension over PteTiO2 (IR) catalysts film,

0

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/ m

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PD

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1 mg/ ml Pt-TiO2

suspension

0

20

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urvi

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IR

control

Fig. 4. Effect of the amount of PteTiO2 (PD & IR) catalysts on the biocidal action ofvarious films. Inset: Comparative antimicrobial activity of PteTiO2 (PD & IR) catalystspowders in aqueous (5 ml) suspension after 10 min irradiation.


whereas number of colonies are seen (Fig. 3d) when irradiatedwithPteTiO2 (PD) catalysts film. This can be ascribed to the betterphotoactivity of PteTiO2 (IR) than PteTiO2 (PD) catalysts due to theinfluence of difference in size and nature of Pt dispersion and theirdistribution onto TiO2 prepared by two separate techniques.

To get the optimum dose of PteTiO2 catalysts, bacteria killingwas studied with various amounts (ca. 0.1, 0.3, 0.4, 1 and 3 mg) ofPteTiO2 (PD and IR) films under 10 min UV irradiation. Fig. 4indicated the large discrepancy in the bactericidal activitybetween PD & IR catalysts in the range of 0.1e0.3 mg of PteTiO2coating. The cell survival is almost zero upto 0.3 mg coating of IRcatalysts after 10 min irradiation, while PD film till exhibits littlesurvival that gradually reduced to zero upto 3 mg PteTiO2 coatingper film. This can be attributed to the fact that only illuminatedsurface layer is effective for photoinduced charge carriers forma-tion which are responsible for killing the surface bound bacteria.The PteTiO2 particles located on the inner layer of the films do nottake part in photoreaction due to the limitation of light penetrationand other interference. Therefore, biocidal activity becomes inde-pendent of catalyst concentration beyond the monolayer coverage,irrespective of Pt loading techniques. Hence, the film thickness is animportant parameter [8e11] to be considered for the optimalactivity although not measured here. This fact implies that it is theunlike nature, size and distribution of Pt nanodeposits and surfacestructural change of TiO2 probably altering the catalytic activityinspite of the same amount of Pt (2 wt.%) loading in both thepreparative conditions [18e24]. Moreover, thermal treatment ofPteTiO2 (IR) catalysts at 753 K during H2 reduction may alsoinfluence the electronic properties that could be accountable forthe observed difference in photoactivity between these twocatalysts.

A similar trend is also observed (Fig. 4. inset) during 10 min lightexposure of 5 ml cell (106 CFU ml�1) suspension of 1 mg ml�1 bare


Fig. 5. TEM images of three dead E. coli cells obtained after 40 min UV irradiation over PteTiO2 (IR, 5 mg) films containing 500 ml cell (106 CFU ml�1) suspension. Spherical black-gray composites of PteTiO2 and severely damaged (marked area) cell wall of bacteria are seen.


TiO2 and Pt loaded TiO2. It has been observed that irradiated bareTiO2 showed the growth of TNT (too numerous to count) colonies,whereas Pt loaded TiO2 (PD and IR) catalysts displayed a greatreduction in cell survival (ca.w88% andw99.5%), respectively. Thisphenomenon again clearly illustrates the dissimilar activity of PDand IR catalysts (Fig. 4. inset) in aqueous suspension too. Theimproved photokilling effect of PteTiO2 comparedwith that of bareTiO2 could be confirmed by the work of Huang et al. They reportedthat when E. coli cells underwent illumination for 15 min in thepresence of 1 mg ml�1 bare TiO2 suspension, almost all of the cellswere still viable and increasing the illumination time resulted incomplete killing after 60 min [24] irradiation. Increasing lightintensity from 320 to 640 mW cm�2 during 10 min UV exposure of100 � 104 CFU ml�1 cells over 1 mg PteTiO2 (IR) films, the survivalof E. coliwas also found to be decreased from 7.08� 104 CFUml�1 to1.16 � 104 CFU ml�1, respectively. This dependence of UV intensityon E. coli death is certainly caused due to photosensitive catalyticprocess.

Fig. 5 shows the TEM images of the dead bacterial cells obtainedafter 40 min irradiation of 500 ml cell suspension (106 CFU ml�1)over 5 mg PteTiO2 (IR) coated film. Many spherical particles ofuniform Pt dispersion onto TiO2 particles (30e50 nm) with darkcontrast could be seen as compared to fewer bare TiO2 particles ofgray contrast that are attached to the bacterial surface. A vastchange has taken place on the surface morphology of E. coli cellsafter 40 min of irradiation as compared to untreated bacterial cells.It is noted that only the contact area between bacterial surface andPteTiO2 (marked area in Fig. 5a and b) are badly damaged due tothe oxidative dissolution of the biochemical constituents of cellmembrane by the highly oxidizing photogenerated holes and/orhydroxyl radicals generated during light irradiation. This processresulted in the gradual photodegradation [3e5] of intracellularchemical constituents [12,13] (phospholipids, proteins and DNA,etc) and consequently leading to the decomposition of cell wall. Asboth the PteTiO2 particles and bacteria are stationary, the contactarea (marked area in Fig. 5c) of the cell surface is persistentlyphotoetched and punctured by the attack of photoexcited holes orOH radicals during prolonged irradiation. As a consequence the cell


wall gradually damaged and eventually leads to functional disor-ders of the cytoplasmic membrane that causes the cell death. Adetailed kinetic analysis [24,25] demonstrated that cell walldamage occurred in less than 20 min, followed by progressivedamage of the cytoplasmic membrane and intracellular compo-nents. It is also reported that the decomposition of a toxin, endo-toxin from E. coli cells certainly points out that the TiO2photocatalyst destroys the outer membrane of the E. coli cell. Thisfact of cell damage is further evident from the TEM images ofstrongly decomposed bacterial cells as compared to intact E. coli ofFig. 6. One can clearly noticed the bacterial nucleus (white spots) inall intact E. coli cells (before UV irradiation) in the TEM picture ofFig. 6a. However, after photoreaction with PteTiO2 catalysts slurry,the entire cell membrane is etched uniformly and gradually becamethinner & decayed as compared to intact cells (Fig. 6a), and rottenbacterial mass is found in the TEM picture of Fig. 6b. Similarlya bacterial lump is vigorously disrupted & fractured and the scat-tered remains plus some PteTiO2 particles are observed in thesurroundings as shown in Fig. 6c. Therefore, the antibacterialeffects of TiO2-coated materials involve not only nullification of theviability of the bacteria, but also destruction of the bacterial cell.Another study demonstrated that the antibacterial effect of TiO2-coated materials is not a simple bacteriostatic action, but a bacte-ricidal action that involves the decomposition of the cell wall.

The Pt dispersion onto TiO2 enhances the interfacial chargetransfer rate by attracting conduction band electrons into Pt phasethrough Schottky-barrier electron trapping and retarding theelectron (e�)ehole (hþ) pair recombination. Therefore, accessibilityof hþ for the oxidizing reactions is greatly enhanced as compared tobare TiO2. Also, Pt nanodeposits [12e14] could be beneficial[24e27] by reducing the overpotential of electron transfer toadsorbed oxygen and helps the generation of additional OH radicalsalong with water photooxidation by hþ and initiate the oxidativereactions. An excellent linear correlation [3e5] between E. colideath and OH radicals confirms that the OH radical is the primaryoxidant species responsible for inactivating E. coli cells. When 2-propanol (100 ml) was added to E. coli suspension(10 � 105 CFU ml�1) of PteTiO2 (IR) catalysts and irradiated for


Fig. 6. TEM images of (a) intact original E. coli cells (b) decayed E. coli cells and (c) ruptured bacterial lump obtained after 40 min UV irradiation over aqueous PteTiO2 (IR, 5 mg)powders and 500 ml (106 CFU ml�1) cells suspension.


10 min, the cell count is found to be almost same as that ofcontrol culture, whereas E. coli death is nearly complete(0.02 � 105 CFU ml�1) when PteTiO2 is irradiated in the absence of2-propanol. This is due to the fact that, 2-propanol is reported toscavenge hþ or OH radicals, which mainly act as primary oxidantsfor bacteria killing process.

The present findings proved the strong biocidal activity ofPteTiO2 photocatalysts both as suspension (1 mg ml�1) and thinfilms form compared to bare TiO2. The PteTiO2 (IR) catalysts alwaysexpose higher activity than PteTiO2 (PD) catalysts. This depen-dence on the Pt dispersion technique suggests that unlike natureand size of platinum species [18e20] (mainly, Pt & PtO by IRmethod and Pt, Pt(OH)2, & PtO2 by PDmethod) deposition ontoTiO2could have large influence on the photoactivity in which Pt0 showshighest activity. The HR-TEM images (Fig. 2) also confirmed that thesize and nature of Pt dispersion onto TiO2 catalyst obtained by twodifferent techniques is quite different. Photodeposition methoddisplayed relatively larger distribution of Pt nanoparticles size(8e10 nm) than that (2e5 nm) of impregnationereduction tech-nique. The size and number of Pt particles can also influence theelectronic properties of the PteTiO2 composites as investigated bymany researchers [17e27]. Due to uniform Pt deposition of smallerparticles size (ca. 2e5 nm) on each TiO2 and large number of Ptloaded TiO2 particles obtained by Pt impregnationmethod, PteTiO2(IR) catalysts display high photoreactivity. In fact the SEM-EDS andHR-TEM analysis in Figs. 1 and 2 showed that the two PteTiO2catalysts have different surface structure and nature of Pt disper-sion. The higher amount of Pt (4.55 wt.%) dispersion and homog-enous PteTiO2 particles are obtained duringimpregnationereduction method. During Pt photodeposition ontoTiO2 arbitrary dispersal of Pt particles of quite bigger size is found inmany reports [14e20].

Studies [21e27] have revealed that metal-semiconductorcomposites exhibit shifts in the Fermi level to more negativepotentials which is metal size-dependent. This shift enhances thecharge transfer process in a different extent as a function of Pt size,resulting in the dissimilar activity of two (IR & PD) PteTiO2 pho-tocatalysts. While specific reasons for different photoactivity arenot clearly understood, many experimental results [28e31]demonstrated that the photocatalytic activity were remarkablyenhanced by using the H2-treated TiO2 catalysts and an optimumtemperature for the H2 treatment was found to be of 500e600 �C.The results confirmed that the crystallinity, the presence of oxygenvacancies and Ti3þ in the lattice of the H2 treated TiO2 are ascribed[28e31] to the enhancement of photocatalytic activity. The thermalH2 treatment of TiO2 was also found to be capable to prolong the


holes’ lifetime by reducing the number of bulk recombinationcenters. It is also proposed [30e33] that the reduction of the TiO2particles raised their Fermi level and increased the height of thebarrier that repels electrons from the particles surface because ofmore Ti3þ available in the TiO2 particles. Appropriate oxygenvacancies concentration in thermally treated TiO2 could improvethe separation rate of electron and hole pairs, so that it couldimprove its photocatalytic properties. In addition, it was reported[32,33] that oxygen vacancy could change the band gap of TiO2 andextend the photocatalytic activities to visible light. Thus, thesuperior efficiency of PteTiO2 (IR & PD) catalysts as compared tobare TiO2 for photokilling of E. coli bacteria is presented in thisresearch investigation. Both the thin film and powder catalysts maybe useful for instant applications in self-cleaning/rapid disinfectionof hospital/house flooring tiles and portable water purificationtechnology etc.

4. Conclusions

We demonstrated the drastic inactivation (<10 min) of E. colicells by low intensity UV exposure onto PteTiO2 suspension andthin films compared to longer contact time (>30 min) as reportedtill date. We provide strong evidence for the vigorous photoetchingof cell wall due to oxidative degradation of biomolecules present inbacteria. The biocidal activity varied with the nature and size of Ptdispersion onto TiO2 and the IR catalysts always exhibited betterreactivity than PD. The dopant Pt may also introduce impuritystates in various positions in the band gap of TiO2 and lead todifferent degrees of modification in charge transportation, therebyenhance the photochemical activity. Defects change electronicproperties of the materials and reduction of stoichiometric TiO2 byH2 during thermal treatment leads mainly to lattice Ti3þ ions andoxygen vacancies that play a critical role in determining the elec-tronic properties of TiO2. Therefore, the superior antimicrobialactivity of Pt-impregnationereduction on TiO2 at high temperaturein comparison to Pt photodeposition at room temperature couldnot be ruled out. Hence, fine-tuning themetal deposition techniqueand thermal annealing temperature, the best photoactive metal-etitania composite catalyst and its thin film can be made forvarious applications.

Acknowledgment

We thank to the Department of Chemical Engineering, ThaparUniversity and All India Institute of Medical Science, New Delhi, fortimely help in measuring light intensity and TEM image analysis,



respectively. P-25-Degussa Company, Germany is gratefullyacknowledged for gift sample TiO2.

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