Journal of Applied Microbiology ISSN 1364-5072

ORIGINAL ARTICLE

Inhibition of green algae growth by corrole-based photosensitizers € der1 J. Pohl1, I. Saltsman2, A. Mahammed2, Z. Gross2 and B. Ro 1 Department of Physics, Humboldt – Universita€t zu Berlin, Berlin, Germany 2 Schulich Faculty of Chemistry, Technion-Israel Institute of Technology, Haifa, Israel

Keywords biofilms, corroles, photodynamic inactivation, phototoxicity, ROS, singlet oxygen. Correspondence €der, Department of Physics, HumBeate Ro boldt, Universit€ at zu Berlin, Newtonstraße 15, 12489 Berlin, Germany. E-mail: [email protected] 2014/1038: received 20 May 2014, revised 1 October 2014 and accepted 5 November 2014 doi:10.1111/jam.12690

Abstract Aims: This study was performed to examine the potential of photodynamic inactivation for growth inhibition of green algae through generation of singlet oxygen. Methods and Results: Two cationic and two anionic corroles were investigated according to their photoinhibitive effect on two strains of green algae using visible light for photoexcitation. The development of biomass over the experimental period of 18 days was followed using absorptive properties of the algae samples. The anionic photosensitizers showed no significant phototoxicity, whereas the cationic photosensitizers caused a drastic reduction of biomass on a short time scale and also displayed long-term inhibition of algae growth. Conclusions: In general, it was proven that photodynamic inactivation of green algae is possible. Concluding from the results of this study, cationic photosensitizers are favourable for this task, while anionic photosensitizers are not suited. Significance and Impact of the Study: Phototrophic biofilms are an important factor in biofouling and biodeterioration of building materials, causing great damage to historic and contemporary constructions. Growth inhibition of phototrophic organisms using photodynamic inactivation could pose an alternative to the use of biocides. To this end, successful application of this approach on green algae is a vital step in the development of suitable photosensitizers.

Introduction Phototrophic organisms are a vital part of most aeroterrestrial biofilms growing on outdoor surfaces. While – superficially speaking – all these biofilms comprise of the same organisms, depending on climate, light, humidity and availability of nutrients as well as characteristics of the populated surfaces, their detailed composition varies largely. Some of the main contributors to aeroterrestrial biofilms are – next to cyanobacteria and fungi – different species of green algae (Crispim et al. 2003; Uher 2008; Hallmann et al. 2011). It was shown (Warscheid and Braams 2000) that biofilms play a dominant role in biofouling and biodeterioration of construction materials, exceeding even that of acid rain. This observation is the

motivation for the numerous ongoing efforts devoted to the removal of biofilms and to the reduction or – ideally – prevention of their formation. Biocides as means for removal of algal growth are well established, but they are posing an environmental risk as their target organisms are quite ubiquitous in various ecosystems. New methodologies for prevention or elimination of biofilm growth that are not based on biocides are hence highly desirable. As phototrophic organisms need light to exist, the usage of photocatalytic or other light-induced mechanisms seem to be promising approaches for avoiding their growth. Photoactive surfaces comprised of semiconductors like TiO2, which generate hydrogen peroxide upon light exposition, are already commercially available as coating on roof tiles (Hashimoto et al. 2005; Fujishima

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et al. 2007). However, studies of Gladis and Schumann (2011a,b) disclosed significant shortcomings of these coatings under long-term weathering. Furthermore, several studies (Dalton et al. 2002; Kebede et al. 2013; Donaldson et al. 2014) provided evidence for the generation of NOX species upon degeneration of micro-organisms on these photoactive surfaces, which may act as fertilizers for successive airborne biofilms. Another light-induced mechanism that could be utilized for prevention of biofilm growth is the use of the photodynamic effect that may directly or indirectly induce phototoxic effects via the generation of reduced oxygen species and other radicals (type I) or via type II photosensitization in which highly reactive singlet oxygen (1O2) is generated. In this process, nontoxic photosensitizer (PS) molecules are excited by light and subsequently interact with other molecules in their direct vicinity. Upon interaction with molecular oxygen, an energy transfer takes places, resulting in the generation of singlet oxygen which is known to induce cytostatic or even cytotoxic reactions directly or indirectly. The generation of singlet oxygen is a reversible process with the PSs acting as a catalyst for the photosensitization. This photodynamic effect has been investigated in photodynamic therapy (PDT) since the beginning of the twentieth century and is currently used in various fields of medicine like oncology, ophthalmology and dermatology (Moan and Peng 2003; Calzavara-Pinton et al. 2005; R€ oder 2006). Likewise, investigations to utilize photosensitization for photoinduced inactivation of bacteria (PIB) as well as of yeast and fungi arose during the last two decades (Friedberg 2001; Gomes et al. 2011; Andreazza et al. 2013; Preuß et al. 2013). Nevertheless, only few efforts have been made to adopt photodynamic inactivation for inhibition of phototrophic organisms. Drabkova et al. (2007) showed that both green algae and cyanobacteria are sensitive to photosensitization by anionic phthalocyanines, with the latter being even more affected applying H2O2. Later attempts concentrated solely on the application of methylene blue and nuclear fast red (both in combination with hydrogen peroxide) on either suspension cultures of green algae or for the removal of phototrophic biofilms (McCullagh and Robertson 2006; Young et al. 2008; Gladis and Schumann 2011a). Both these photosensitizers are known to possess limited photostability, and indeed, the focus of the aforementioned studies lay on the rapid disposal of the chemical agents applied to surfaces. The lack of photostability of photosensitizers investigated up to date renders their long-time use in photodynamic inhibition of phototrophic organisms for prevention of biofilm formation impossible. We have recently reported four new exceptionally photostable corroles, which proofed to be photodynamically highly efficient against 306

mould fungi (Preuß et al. 2014). This successful application to fungi as one of the constituents in aeroterrestrial biofilms suggested these corroles as promising photosensitizers for use against biofilm growth and motivated the investigations described in this study regarding long-term photodynamic inhibition of green algae. Methods Organisms and culture conditions Two strains of green algae were chosen as model organisms for long-term tests: Stichococcus bacillaris (SAG 379-2) and Chlorella fusca var. vacuolata (SAG 211-8b). Suspension cultures of the algae were inoculated 3 days prior to experiments. Cultures were grown in Bold’s Basal Medium (according to Bischoff and Bold (1963)) at room temperature and shaken on a rotary shaker at 250 rev min1. Illumination of the algal cultures was realized with a daylight bulb (Photographic Lamp, 5400 K, Realm Industrial GmbH) in a rhythm of 12 h:12 h/day:night. All suspension cultures were provided with fresh medium directly before the start of any of the experiments. Photosensitizers Four PSs were tested for their phototoxicity on green algae, as listed in Table 1. As can be seen, the four metallocorroles differ in their charge and the identity of the chelated element. Two dianionic (SbCor, PCor) and two triscationic (SbCor+, PCor+) complexes were synthesized with each either antimony or phosphorus as central atoms, according to (Preuß et al. 2014). Determination of Dark and Phototoxicity Phototoxicity and dark toxicity experiments were conducted on 96-well plates (uncoated) over a period of 18 days. Per well, 200 ll of algae suspension were prepared with an initial cell density of 7106 ml1 and 45106 ml1 for Chlorella and Stichococcus, respectively. Duration of the experiment as well as initial cell density was determined according to the termination of growth curves in precursor experiments on biofilm formation of these strains to ensure reproducible formation of homogeneous biofilms inside the wells of untreated controls during the experiment. The biomass of all samples was calculated from their optical density at 535 nm (OD535). This wavelength was selected as to minimize the effect of PS absorption on the results, as the PS possesses considerable absorption bands

Journal of Applied Microbiology 118, 305--312 © 2014 The Society for Applied Microbiology

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Photodynamic inactivation of green algae

Table 1 Photosensitizers and their singlet oxygen quantum yields (ΦD) according to Preuß et al. (2014) Abbreviation

Chemical structure

SbCor

C6F5

IUPAC name

ΦD [%  7]

2,17-bis-sulfonato-5,10,15-tris(pentafluorophenyl)corrolato(oxo)antimony(V)

66

2,17-bis-sulfonato-5,10,15-tris(pentafluorophenyl)corrolato(trans-dihydroxo)phosphorus(V)

58

5,10,15-tris-(N-methyl-o-pyridylium)corrolato(oxo)antimony(V)

67

5,10,15-tris-(N-methyl-o-pyridylium)corrolato(trans-dihydroxo)phosphorus(V)

81

N O N C6F5

C6F5

Sb

N

N –

+

SO3 Na –

+

SO3 Na

C6F5

PCor

OH N

N C6F5

C6F5

P

N

N –

OH –

+

SO3 Na +

SO3 Na

SbCor+



+I

N

N

O

N

Sb +

N



+

N

N

N– I

I



PCor+

+I

N

OH N

N

P +

N – I

N

N OH

+

N– I

in the regime of 550–630 nm. Data were collected approximately every 3 days. Initial conditions were chosen in a way that the OD535 of the samples did not exceed 10 during the experiment. Growth rates l(ti) of the samples were calculated – under the usual assumption of exponential growth – for each phase between two measurements according to the following formula Bðti Þ ¼ Bðti1 Þ  elðti ÞDt where B(ti) is the cell density in a sample at the time ti of the measurement in days after beginning (t0) of the experiment and Dt is the time interval between ti-1 and ti in days. Aqueous stock solutions of all PS were prepared at 1 mmol l1 (Except SbCor+: 05 mmol l1), from which working solutions of 100 lmol l1 were obtained. PS were added to the algae samples at a final concentration of 5 lmol l1. For each PS, phototoxicity as well as dark toxicity was determined. The PSs were added to the algae suspension at the beginning of the experiment. For determination of dark toxicity, all samples were incubated at room temperature and maintained in dark at all times except for the 01 s of illumination needed to determine the optical density of a sample. Determination of phototoxicity was performed alongside the determination of dark toxicity, with the samples being illuminated using a daylight bulb (Photographic Lamp, 5400 K, Realm Industrial GmbH)

in a light regime of 12 h:12 h/day:night at an intensity of 900 lx. Controls (ref) were included on each multiwell plate accordingly. Results Dark toxicity The PSs chosen in this work were screened regarding their dark toxicity, in addition to their phototoxicity, to ensure that effects observed during phototoxicity tests are due only to photosensitization. Only for samples treated with the anionic corroles SbCor and PCor, some small tendency of reduction in biomass could be ascertained. Over a period of 18 days, reduction did not exceed 5% of the initial biomass of the samples for both algal species. All other samples, including controls, showed no significant reduction in biomass when incubated without illumination (data not shown). Phototoxicity Experiments for evaluation of photodynamic inactivation were designed with a light regime of 12 h:12 h/dark:light (in accordance with a natural day/night rhythm) to factor in possible recovery of cell density in dark phases, which may be expected to occur upon photosensitization under natural conditions.

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The cell density of algal samples with PS exposed to illumination as well as of the according controls is depicted in Figs 1 and 2 for Chlorella fusca var. vacuolata and Stichococcus bacillaris, respectively. Values are normalized to initial cell density in the controls. The progression of cell density of the reference (ref) not incubated with photosensitizer was used to identify possible influences of experimental conditions on consecutive experiments. The reference displayed normal exponential growth behaviour with transition into steady-state phase at the end of the experimental period for both algal species. This behaviour was reproducible in independent experiments (not shown separately). The samples treated with the anionic corroles SbCor and PCor displayed an exponential growth pattern similar to the reference, but some delay of growth was evident for the first 13 days of the experiment. Based on the assumption of exponential growth, the growth rate of each sample was calculated from the cell density on each day of measurement for the immediately preceding growth phase. This data are displayed in Figs 3 and 4 for Chlorella and Stichococcus, respectively. It can be seen that incubation with SbCor and PCor leads to lower growth rates than observed in the untreated control, except for day 18, when the controls enter the steadystate phase. In contrast, no apparent entry into steadystate phase during the 18 days could be observed for the samples incubated with SbCor and PCor. Samples treated with the anionic corroles reached a final cell density of 36–40 times the initial cell density. This equals 79% and 70% of the final biomass in the control samples of Chlorella and Stichococcus, respectively. For both algae strains, no significant difference could be seen between the photodynamic activities of these two corroles, neither regarding cell density nor regarding growth rate.

In contrast to the negatively charged molecules, the two cationic corroles SbCor+ and PCor+ displayed ongoing inhibiting effects on samples of green algae. Reduction of biomass was clearly evident throughout the experiment for both PSs, as can be deduced both from cell density in the samples and exclusively negative growth rates throughout the experiment. The PSs differed in their effect on the algae, with PCor+ having a more severe impact than SbCor+. Incubation with SbCor+ resulted in cell densities of 50% and 52% relative to the initial biomass in the samples for Chlorella and Stichococcus, respectively. Samples treated with PCor+ demonstrated an even higher reduction of biomass down to 37% of the initial values. For SbCor+, this final biomass equals 10% of the final biomass in the control for both algal species, and for PCor+, it equals 75 and 67% for Chlorella and Stichococcus, respectively. All phototoxicity tests were monitored photographically on a microscopic, as well as a macroscopic scale. The results after day 18 of the experiments are depicted in Fig. 5. On a macroscopic scale, samples incubated with both cationic corroles show evident destruction of algae cultures, with PCor+ leading to almost transparent wells and SbCor+ leaving only marginal residues of biofilm (see Fig. 5a: left edge of the wells). From the microscopic pictures, it can be clearly seen that samples incubated with the two cationic corroles not only show much lower cell density than the other samples but also appear to be bleached. A minor difference between the effects of SbCor+ and PCor+ can only be noticed from the distribution of the cells: they are more separated and singularized in the case of PCor+, while they form clusters in the case of SbCor+. For incubation with the two anionic corroles, no difference to the reference can be made out on the macroscopic scale. Only on the microscopic scale, it becomes

6

Normalized cell density

5 4 3 2 1 0

308

day 1

day 4

day 7

day 8

day 11

day 13

day 18

Figure 1 Phototoxicity of corroles on Chlorella fusca var. vacuolata monitored over 18 days via optical density at 535 nm with illumination in a light regime of 12 h:12 h/ dark:light. Cell density is normalized to the initial cell density in the control. (Error bars: SD of n = 9) SbCor+ PCor+ SbCor PCor reference.

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6·0

Figure 2 Phototoxicity of corroles on Stichococcus bacillaris monitored over 18 days via optical density at 535 nm with illumination in a light regime of 12 h:12 h/ dark:light. Cell density is normalized to the initial cell density in the control. (Error bars: SD of n = 9) SbCor+ PCor+ SbCor PCor reference.

Normalized cell density

5·0 4·0 3·0 2·0 1·0 0·0

day 1

day 4

day 7

day 8

day 11

day 13

day 18

0·208 0·156

Figure 3 Growth rates of Chlorella fusca var. vacuolata over 18 days with illumination in a light regime of 12 h:12 h/day:night in photosensitized samples and controls. Growth rates were calculated for each day based on change in biomass during the preceding growth phase. (error bars: SD of n = 9) SbCor+ PCor+ SbCor PCor reference.

Growth rate [d–1]

0·104 0·052 0·000 –0·052 –0·104 –0·156

day 4

apparent that the photosensitized samples formed less dense biofilms, more distinctly for Stichococcus than for Chlorella. Discussion In this work, the photodynamic action of different positively and negatively charged corroles on green algae was investigated for the first time. The four corroles were chosen because of their favourable photophysical properties and the promising results in photodynamic inactivation of mould fungi that were recently reported (Preuß et al. 2014). In this study, no dark toxicity of the corroles on green algae could be found. As we reported recently, all of the four corroles feature high singlet oxygen quantum yields of over 50% and high photostability. Nevertheless, the anionic corroles showed weak growth inhibition of green algae when illuminated with visible light. In contrast, both photoactivated cationic corroles

day 7

day 8

day 11

day 13

day 18

prevented algae growth and even caused effective reduction of biomass in all treated samples. As the singlet oxygen quantum yields of both SbCor and PCor are in the same range as that of SbCor+, it is unlikely for insufficient generation of singlet oxygen to be accountable for these results. Instead, it may be concluded that the interaction of anionic corroles with green algae is unfavourable for photodynamic inactivation. Indeed, the negatively charged sulphonated phthalocyanines used by Drabkova et al. (2007) for photodynamic inactivation of similar strains of green algae and cyanobacteria showed unsatisfactory results. The inhibitory effects of the phthalocyanines after 3 days of continuous illumination with fluorescent tubes at 5000 lx bore no correlation to their relative ΦD. The obtained EC50 values of growth inhibition equal concentrations of the PSs between 1–8 lmol l1. Using a concentration of 5 lmol l1 and a light intensity only 20% of the one used by Drabkova et al. (2007), the anionic corroles

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0·250

day 4

day 7

day 8

day 11

day 13

day 18

0·200

Growth rate [d–1]

0·150 0·100 0·050 Figure 4 Growth rate of Stichococcus bacillaris over 18 days with illumination in a light regime of 12 h:12 h/day:night in photosensitized samples and controles. Growth rates were calculated for each day based on change in biomass during the preceding growth phase. SbCor+ PCor+ SbCor PCor reference.

0·000 –0·050 –0·100 –0·150 –0·200

(a)

ref

SbCor–

PCor–

SbCor+

PCor+

SbCor–

PCor–

SbCor+

PCor+

Chlorella fusca var. vacuolatus

Stichococcus bacillaris 5 mm (b)

ref

Chlorella fusca var. vacuolatus 100 µm

Stichococcus bacillaris

Figure 5 Macroscopic (a) and microscopic (b) photographic documentation of phototoxicity tests on green algae after 18 days of incubation.

investigated in this work also led to reduction in growth rate to 45–50% of the control growth rates during the first 7 days of the experiment. Under the same 310

conditions, the cationic corroles resulted in truly negative growth rates. Thus, our results for the negatively charged corroles are comparable to the findings of Drabkova et al.

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(2007) on anionic phthalocyanines. The inhibitory effect of the cationic corroles on the other hand exceeds far beyond previously reported results, further confirming the hypothesis of preference for positively charged PSs for photodynamic inactivation of green algae. The cationic corroles SbCor+ and PCor+ revealed high phototoxicity on Chlorella fusca var. vacuolata and Stichococcus bacillaris and an ongoing reduction of algal biomass not only during the first 7 days, but over the entire time of the experiment. Dark phases without illumination in accordance with a natural day/night rhythm could allow for algae growth due to interruption of photoinduced generation of singlet oxygen and stimulating effect on biomass production regulated by the circadian rhythm of the algae (Wu et al. 1986). Here, we were able to show for the first time that even interrupted illumination with white light – as may be expected under weathering conditions of building materials – provoked no recovery of the algae cultures as obtained for photoactive surfaces. The difference in photodynamic efficiency of the two cationic corroles can be mainly attributed to the difference in ΦD, which for PCor+ with 81% is significantly higher than that of SbCor+ with 67%. It is known that photosynthesis under high-intensity light conditions can lead to generation of singlet oxygen as well as a decline in photosynthetic activity (Powles 1984). This decline was reported to be reversible on a short-term scale, followed by photooxidation and pigment bleaching on a long-term scale. As reported by Triantaphylides et al. (2008), this photoactive damage is mainly caused by 1O2. It is widely presumed that carotenoids as well as fatty acids inside algae and green plants act as quenchers for 1O2, preventing structural damage resulting from intracellular generation of ROS during photosynthesis. Because of this natural protective mechanism, we initially assumed that it is more likely for PSs to evoke photosensitized destruction of outer cell membranes than inhibition of the photosynthetic systems. Yet, the microscopic imaging of green algae incubated with the two cationic corroles revealed not only reduction of cell density but also bleaching, that is photooxidation of chromophores inside the cells similar to the observations following massive photoinactivation of the photosynthetic centres. An effect of the PSs on the photosynthetic organelles might be the cause of the bleaching, but further studies have to be conducted, concerning uptake of the PSs and their intracellular distribution, to gain insight into the detailed mechanisms of photosensitization in green algae. The seemingly charge-related difference in phototoxicity between the corroles investigated in this work matches similar effects reported for the photoinactivation of bacteria (Demidova and Hamblin 2004; Hamblin and Hasan 2004; Jori et al. 2006). The results also correspond well

Photodynamic inactivation of green algae

to their photodynamic efficiency on mould fungi: the positively charged corroles show higher phototoxicity than the negatively charged, mostly independent of their relative singlet oxygen quantum yields (Preuß et al. 2014). Photosensitization with SbCor+ and PCor+ leads to total destruction of the treated algae cultures even without continuous illumination, just like reported for mould fungi. The anionic corroles only inhibited growth of mould fungi, but no destruction of the conidia was induced. Likewise, these corroles had little to no effect on green algae. Regarding the different target organisms in these two studies, the anionic corroles appear to be less suited for the photodynamic inactivation of microorganisms than the corresponding cationic corroles. In conclusion, cationic PSs as the ones investigated in this study seem to be of higher photodynamic efficiency to green algae than anionic PSs, for which no reduction of biomass was observed in this work. The two new cationic corroles PCor+ and SbCor+ investigated in this work proofed to have an inhibiting effect on algae due to photodynamic inactivation, which is desired for prevention of biofilm formation. Further studies should be carried out, looking into their photodynamic efficiency on biofilms of cyanobacteria, bacteria and lichens. But already their successful application to green algae in addition to the reported destruction of mould fungi conidia makes them promising candidates for inhibition or removal of biofilms on surfaces that are subject to weathering or biodeterioration. Acknowledgement Judith Pohl acknowledges DBU (Deutsche Bundestiftung Umwelt) for funding. Conflict of Interest No conflict of interest declared. References Andreazza, N.L., de Lourenco, C.C., Siqueira, C.A.T., Sawaya, A.C.H.F., Lapinski, T.F., Gasparetto, A., Khouri, S., Zamuner, S.R. et al. (2013) Photodynamic inactivation of yeast and bacteria by extracts of Alternanthera brasiliana. Curr Drug Targets 9, 1015–1022. Bischoff, H.W. and Bold, H.C. (1963) Phycological Studies. IV. Some Soil Algae from Enchanted Rock and Related Algal Species. The University of Texas Publication 6318, 1–95. Calzavara-Pinton, P.G., Venturini, M. and Sala, R. (2005) A comprehensive overview of photodynamic therapy in the treatment of superficial fungal infections of the skin. J Photochem Photobiol, B 78, 1–6.

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Crispim, C.A., Gaylarde, P.M. and Gaylarde, C.C. (2003) Algal and cyanobacterial biofilms on calcareaous historic buildings. Curr Microbiol 46, 79–82. Dalton, J.S., Janes, P.A., Jones, N.G., Nicholson, J.A., Hallam, K.R. and Allen, G.C. (2002) Photocatalytic oxidation of NOx gases using TiO2: a surface spectroscopic approach. Environ Pollut 120, 415–422. Demidova, T.N. and Hamblin, M.R. (2004) Photodynamic therapy targeted to pathogens. Int J Immunopathol Pharmacol 17, 245–254. Donaldson, M.A., Berke, A.E. and Raff, J.D. (2014) Uptake of gas phase nitrous acid onto boundary layer soil surfaces. Environ Sci Technol 48, 375–383. Drabkova, M., Marsalek, B. and Admiraal, W. (2007) Photodynamic therapy against cyanobacteria. Environ Toxicol 22, 112–115. Friedberg, J.S. (2001) In vitro effects of photodynamic therapy on Aspergillus fumigatus. J Antimicrob Chemother 48, 105– 107. Fujishima, A., Zhang, X. and Tryk, D.A. (2007) Heterogeneous photocatalysis: from water photolysis to applications in environmental cleanup. Int J Hydrogen Energy 32, 2664– 2672. Gladis, F. and Schumann, R. (2011a) A suggested standardised method for testing photocatalytic inactivation of aeroterrestrial algal growth on TiO2-coated glass. Int Biodeterior Biodegradation 65, 415–422. Gladis, F. and Schumann, R. (2011b) Influence of material properties and photocatalysis on phototrophic growth in multi-year roof weathering. Int Biodeterior Biodegradation 65, 36–44. Gomes, M.C., Woranovicz-Barreira, S.M., Faustino, M.A.F., Fernandes, R., Neves, M.G.P.M.S., Tome, A.C., Gomes, N.C., Almeida, A. et al. (2011) Photodynamic inactivation of Penicillium chrysogenum conidia by cationic porphyrins. Photochem Photobiol Sci 10, 1735–1743. Hallmann, C., R€ udrich, J., Enseleit, M., Friedl, T. and Hoppert, M. (2011) Microbial diversity on a marble monument: a case study. Environ Earth Sci 63, 1701–1711. Hamblin, M.R. and Hasan, T. (2004) Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem Photobiol Sci 3, 436–450. Hashimoto, K., Irie, H. and Fujishima, A. (2005) TiO2 photocatalysis: a historical overview and future prospects. Jpn J Appl Phys 44(Pt 1), 8269–8285. Jori, G., Fabris, C., Soncin, M., Ferro, S., Coppellotti, O., Dei, D., Fantetti, L., Chiti, G. et al. (2006) Photodynamic

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therapy in the treatment of microbial infections: basic principles and perspective applications. Lasers Surg Med 38, 468–481. Kebede, M.A., Scharko, N.K., Appelt, L.E. and Raff, J.D. (2013) Formation of nitrous acid during ammonia photooxidation on TiO2 under atmospherically relevant conditions. J Phys Chem Lett 4, 2618–2623. McCullagh, C. and Robertson, P.K.J. (2006) Photosensitized destruction of Chlorella vulgaris by methylene blue or nuclear fast red combined with hydrogen peroxide under visible light irradiation. Environ Sci Technol 7, 2421–2425. Moan, J. and Peng, Q. (2003) An outline of the history of PDT. In Photodynamic Therapy ed. Patrice, T. pp. 1–17. Great Britain: Royal Society of Chemistry. Powles, S.B. (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Biol 35, 15–44. Preuß, A., Zeugner, L., Hackbarth, S., Faustino, M.A.F., Neves, M.G.P.M.S., Cavaleiro, J.A.S. and Roeder, B. (2013) Photoinactivatin of Escherichia coli (SURE2) without intracellular uptake of the photosensitizer. J Appl Microbiol 114, 36–43. Preuß, A., Saltsman, I., Mahammed, A., Pfitzner, M., Goldberg, I., Gross, Z. and R€ oder, B. (2014) Photodynamic inactivation of mold fungi spores by newly developed charged corroles. J Photochem Photobiol, B 133, 39–46. R€ oder, B. (2006) Photodynamic therapy. In Encyclopedia of Analytical Chemistry ed. Meyers, R.A. pp. 302–320. Chichester and UK: John Wiley & Sons, Ltd. Triantaphylides, C., Krischke, M., Hoeberichts, F.A., Ksas, B., Gresser, G., Havaux, M., Van Breusegem, F. and Mueller, M.J. (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148, 960–968. Uher, B. (2008) Spatial distribution of cyanobacteria and algae from the tombstone in a historic cemetery in Bratislava, Slovakia. Fottea 9, 81–92. Warscheid, T. and Braams, J. (2000) Biodeterioration of stone: a review. Int Biodeterior Biodegradation 46, 343–368. Wu, J.T., Tischner, R. and Lorenzen, H. (1986) A circadian rhythm in the number of daughter cells in synchronous Chlorella fusca var vacuolata. Plant Physiol 80, 20–22. Young, M.E., Alakomi, H.-L., Fortune, I., Gorbushina, A.A., Krumbein, W.E., Maxwell, I., McCullagh, C., Robertson, P. et al. (2008) Development of a biocidal treatment regime to inhibit biological growths on cultural heritage: BIODAM. Envion Geol 56, 631–641.

Journal of Applied Microbiology 118, 305--312 © 2014 The Society for Applied Microbiology

Inhibition of green algae growth by corrole-based photosensitizers.

This study was performed to examine the potential of photodynamic inactivation for growth inhibition of green algae through generation of singlet oxyg...
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