Skip to main content

Advertisement

SpringerLink
Log in

Bioluminescence and its application in the monitoring of antimicrobial photodynamic therapy

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Light output from bioluminescent microorganisms is a highly sensitive reporter of their metabolic activity and therefore can be used to monitor in real time the effects of antimicrobials. Antimicrobial photodynamic therapy (aPDT) is receiving considerable attention for its potentialities as a new antimicrobial treatment modality. This therapy combines oxygen, a nontoxic photoactive photosensitizer, and visible light to generate reactive oxygen species (singlet oxygen and free radicals) that efficiently destroy microorganisms. To monitor this photoinactivation process, faster methods are required instead of laborious conventional plating and overnight incubation procedures. The bioluminescence method is a very interesting approach to achieve this goal. This review covers recent developments on the use of microbial bioluminescence in aPDT in the clinical and environmental areas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Airth RL, Foerster GE (1960) Some aspects of fungal bioluminescence. J Cell Comp Physiol 56(3):173–182. doi:10.1002/jcp.1030560307

    Article  CAS  Google Scholar 

  • Allen CM, Weber JM, van Lier JE (1995) Sulfophthalocyanines for photodynamic inactivation of viruses in blood products: effect of structural modifications. Photochem Photobiol 62(1):184–189

    Article  CAS  Google Scholar 

  • Almeida A, Cunha Â, Faustino M, Tomé A, Neves M (2011) Porphyrins as antimicrobial photosensitizing agents. In: Hamblin M, Jori G (eds) Photodynamic inactivation of microbial pathogens: medical and environmental applications. Royal Society of Chemistry, Cambridge, pp 83–160

    Chapter  Google Scholar 

  • Alves E, Carvalho CMB, Tome JPC, Faustino MAF, Neves M, Tome AC, Cavaleiro JAS, Cunha A, Mendo S, Adelaide A (2008) Photodynamic inactivation of recombinant bioluminescent Escherichia coli by cationic porphyrins under artificial and solar irradiation. J Ind Microbiol Biotechnol 35(11):1447–1454

    Article  CAS  Google Scholar 

  • Alves E, Costa L, Carvalho C, Tome J, Faustino M, Neves M, Tome A, Cavaleiro J, Cunha A, Almeida A (2009) Charge effect on the photoinactivation of Gram-negative and Gram-positive bacteria by cationic meso-substituted porphyrins. BMC Microbiol 9(1):70

    Article  Google Scholar 

  • Alves E, Faustino MAF, Tomé JPC, Neves MGPMS, Tomé AC, Cavaleiro JAS, Cunha Â, Gomes NCM, Almeida A (2011) Photodynamic antimicrobial chemotherapy in aquaculture: photoinactivation studies of Vibrio fischeri. PLoS One 6(6):e20970

    Article  CAS  Google Scholar 

  • Arrojado C, Pereira C, Tomé J, Faustino M, Neves M, Tomé A, Cavaleiro J, Calado R, Cunha Â, Gomes N, Almeida A (2011) Applicability of photodynamic antimicrobial chemotherapy as an alternative to inactivate fish pathogenic bacteria in aquaculture systems. Photochem Photobiol Sci. doi:10.1039/C1PP05129F

  • Babu BG, Kannan M (2002) Lightning bugs. Resonance 7(9):49–55

    Article  Google Scholar 

  • Bagchi B, Basu S (1979) Role of dye molecules remaining outside the cell during photodynamic inactivation of Escherichia coli in the presence of acriflavine. Photochem Photobiol 29(2):403–405. doi:10.1111/j.1751-1097.1979.tb07067.x

    Article  CAS  Google Scholar 

  • Baldwin T, Berends T, Bunch T, Holzman T, Rausch S, Shamansky L, Treat M, Ziegler M (1984) Cloning of the luciferase structural genes from Vibrio harveyi and expression of bioluminescence in Escherichia coli. Biochemistry 16(23):3663–3667

    Article  Google Scholar 

  • Bassler B, Silverman M (1995) Intercellular communication in marine Vibrio species: density-dependent regulation of the expression of bioluminescence. In: Silhavy JAHTJ (ed) Two-component signal transduction. American Society for Microbiology, Washington, pp 431–445

    Google Scholar 

  • Baumann P, Baumann L, Woolkalis M, Bang S (1983) Evolutionary relationships in Vibrio and Photobacterium. A basis for a natural classification. Annu Rev Microbiol 37:369–398

    Article  CAS  Google Scholar 

  • Beard S, Salisbury V, Lewis R, Sharpe J, MacGowan A (2002) Expression of lux genes in a clinical isolate of Streptococcus pneumoniae: using bioluminescence to monitor gemifloxacin activity. Antimicrob Agents Chemother 46(2):538–542. doi:10.1128/aac.46.2.538-542.2002

    Article  CAS  Google Scholar 

  • Belas R, Mileham A, Cohn D, Hilman M, Simon M, Silverman M (1982) Bacterial bioluminescence: isolation and expression of the luciferase genes from Vibrio harveyi. Science 218(4574):791–793. doi:10.1126/science.10636771

    Article  CAS  Google Scholar 

  • Bermudes D, Boraas M, Nealson K (1991) In vitro antagonism of bioluminescent fungi by Trichoderma harzianum. Mycopathologia 115(1):19–29

    Article  CAS  Google Scholar 

  • Bertoloni G, Zambotto F, Conventi L, Reddi E, Jori G (1987) Role of specific cellular in the hematoporphyrin-sensitized photoinactivation of microbial cells. Photochem Photobiol 46(5):695–698. doi:10.1111/j.1751-1097.1987.tb04834.x

    Article  CAS  Google Scholar 

  • Bhatti M, MacRobert A, Meghji S, Henderson B, Wilson M (1998) A study of the uptake of toluidine blue O by Porphyromonas gingivalis and the mechanism of lethal photosensitization. Photochem Photobiol 68(3):370–376. doi:10.1111/j.1751-1097.1998.tb09694.x

    Article  CAS  Google Scholar 

  • Boemare N, Akhurst R, Mourant R (1993) DNA relatedness between Xenorhabdus spp. (Enterobacteriaceae), symbiotic bacteria of entomopathogenic nematodes, and a proposal to transfer Xenorhabdus luminescens to a new genus, Photorhabdus gen. nov. Int J Bacteriol 43:249–255

    Article  CAS  Google Scholar 

  • Bombelli C, Bordi F, Ferro S, Giansanti L, Jori G, Mancini G, Mazzuca C, Monti D, Ricchelli F, Sennato S, Venanzi M (2008) New cationic liposomes as vehicles of m-tetrahydroxyphenylchlorin in photodynamic therapy of infectious diseases. Mol Pharm 5(4):672–679

    Article  CAS  Google Scholar 

  • Bonnett R, Krysteva MA, Lalov IG, Artarsky SV (2006) Water disinfection using photosensitizers immobilized on chitosan. Water Res 40(6):1269–1275

    Article  CAS  Google Scholar 

  • Brock M, Jouvion G, Droin-Bergere S, Dussurget O, Nicola M, Ibrahim-Granet O (2008) Bioluminescent Aspergillus fumigatus, a new tool for drug efficiency testing and in vivo monitoring of invasive aspergillosis. Appl Environ Microbiol 74(22):7023

    Article  CAS  Google Scholar 

  • Calin M, Parasca S (2009) Light sources for photodynamic inactivation of bacteria. Lasers Med Sci 24(3):453–460. doi:10.1007/s10103-008-0588-5

    Article  Google Scholar 

  • Campbell A (1989) Living light: biochemistry, function and biomedical applications. Essays Biochem 24:41–76

    CAS  Google Scholar 

  • Carre V, Gaud O, Sylvain I, Bourdon O, Spiro M, Biais J, Granet R, Krausz P, Guilloton M (1999) Fungicidal properties of meso-arylglycosylporphyrins: influence of sugar substituents on photoinduced damage in the yeast Saccharomyces cerevisiae. J Photochem Photobiol B Biol 48(1):57–62

    Article  CAS  Google Scholar 

  • Carvalho CMB, Gomes ATPC, Fernandes SCD, Prata ACB, Almeida MA, Cunha MA, Tome JPC, Faustino MAF, Neves MGPMS, Tome AC, Cavaleiro JAS, Lin Z, Rainho JP, Rocha J (2007) Photoinactivation of bacteria in wastewater by porphyrins: bacterial ß-galactosidase activity and leucine-uptake as methods to monitor the process. J Photochem Photobiol B Biol 88:88–112

    Article  CAS  Google Scholar 

  • Carvalho C, Tomé J, Faustino M, Neves M, Tomé A, Cavaleiro J, Costa L, Alves E, Oliveira A, Cunha Â, Almeida A (2009) Antimicrobial photodynamic activity of porphyrin derivatives: potential application on medical and water disinfection. J Porphyr Phthalocyanines 13:574–577

    Article  CAS  Google Scholar 

  • Cassell GH, Mekalanos J (2001) Development of antimicrobial agents in the era of new and reemerging infectious diseases and increasing antibiotic resistance. JAMA 285(5):601–605. doi:10.1001/jama.285.5.601

    Article  CAS  Google Scholar 

  • Cassidy CM, Tunney MM, McCarron PA, Donnelly RF (2009) Drug delivery strategies for photodynamic antimicrobial chemotherapy: from benchtop to clinical practice. J Photochem Photobiol B Biol 95(2):71–80

    Article  CAS  Google Scholar 

  • Chatterjee J, Meighen E (1995) Biotechnological applications of bacterial bioluminescence genes. Photochem Photobiol 62:641–650

    Article  CAS  Google Scholar 

  • Clark D (1989) The fermentation pathways of Escherichia coli. FEMS Microbiol Rev 5:223–234

    Article  CAS  Google Scholar 

  • Cohn D, Ogden R, Abelson J, Baldwin T, Nealson K, Simon M, Mileham A (1983) Cloning of the Vibrio harveyi luciferase genes: use of a synthetic oligonucleotide probe. Proc Natl Acad Sci U S A 1(80):120–123

    Article  Google Scholar 

  • Colepicolo P, Cho K-W, Poinar G, Hastings J (1989) Growth and luminescence of the bacterium Xenorhabdus luminescens from a human wound. Appl Environ Microbiol 55:2601–2606

    CAS  Google Scholar 

  • Contag C, Contag P, Mullins J, Spilman S, Stevenson D, Benaron D (1995) Photonic detection of bacterial pathogens in living hosts. Mol Microbiol 4(18):593–603

    Article  Google Scholar 

  • Costa L, Alves E, Carvalho C, Tomé J, Faustino M, Neves M, Tomé A, Cavaleiro J, Cunha Â, Almeida A (2008) Sewage bacteriophage photoinactivation by cationic porphyrins: a study of charge effect. Photochem Photobiol Sci 7:415–422. doi:10.1039/b712749a

    Article  CAS  Google Scholar 

  • Costa L, Tomé JPC, Neves MGPMS, Tomé AC, Cavaleiro JAS, Faustino MAF, Cunha A, Gomes NCM, Almeida A (2011) Evaluation of resistance development and viability recovery by a non-enveloped virus after repeated cycles of aPDT. Antiviral Res 91(3):278–282. doi:10.1016/j.antiviral.2011.06.007

    Article  CAS  Google Scholar 

  • Czyz A, Plata K, Wegrzyn G (2002) Induction of light emission by luminescent bacteria treated with UV light and chemical mutagens. J Appl Gen 43(3):377–389

    Google Scholar 

  • Dai T, Tegos GP, Lu Z, Zhiyentayev T, Franklin MJ, Baer DG, Hamblin MR (2009) Photodynamic therapy for Acinetobacter baumannii burn infections in mice. Antimicrob Agents Chemother 53(9):3929–3934

    Article  CAS  Google Scholar 

  • Delong E, Steinhauer D, Israel A, Nealson K (1987) Isolation of the lux genes from Photobacterium leiognathi and expression in Escherichia coli. Gene 2–3(54):203–210

    Article  Google Scholar 

  • Demidova TN, Gad F, Zahra T, Francis KP, Hamblin MR (2005) Monitoring photodynamic therapy of localized infections by bioluminescence imaging of genetically engineered bacteria. J Photochem Photobiol B Biol 81(1):15–25

    Article  CAS  Google Scholar 

  • DeRosa MC, Crutchley RJ (2002) Photosensitized singlet oxygen and its applications. Coord Chem Rev 233–234:351–371

    Article  Google Scholar 

  • Desjardin DE, Capelari M, Stevani CV (2005) A new bioluminescent agaric from Sao Paulo, Brazil. Fungal Divers 18:9–14

    Google Scholar 

  • Doyle TC, Nawotka KA, Kawahara CB, Francis KP, Contag PR (2006) Visualizing fungal infections in living mice using bioluminescent pathogenic Candida albicans strains transformed with the firefly luciferase gene. Microb Pathog 40(2):82–90

    Article  CAS  Google Scholar 

  • Durantini EN (2006) Photodynamic inactivation of bacteria. Curr Bioact Compd 2:127–142

    Article  CAS  Google Scholar 

  • Egyeki M, Turóczy G, Majer Z, Tóth K, Fekete A, Maillard P, CsIk G (2003) Photosensitized inactivation of T7 phage as surrogate of non-enveloped DNA viruses: efficiency and mechanism of action. Biochim Biophys Acta 1624(1–3):115–124

    Article  CAS  Google Scholar 

  • Ehrenberg B, Malik Z, Nitzan Y, Ladan H, Johnson F, Hemmi G, Sessler J (1993) The binding and photosensitization effects of tetrabenzoporphyrins and texaphyrin in bacterial cells. Lasers Med Sci 8(3):197–203

    Article  Google Scholar 

  • Engebrecht J, Silverman M (1987) Nucleotide sequence of the regulatory locus controlling expression of bacterial genes for bioluminescence. Nucleic Acids Res 15(24):10455–10467. doi:10.1093/nar/15.24.10455

    Article  CAS  Google Scholar 

  • Ergaieg K, Chevanne M, Cillard J, Seux R (2008) Involvement of both type I and type II mechanisms in gram-positive and gram-negative bacteria photosensitization by a meso-substituted cationic porphyrin. Sol Energy 82(12):1107–1117

    Article  CAS  Google Scholar 

  • Evans JF, McCracken S, Miyamoto CM, Meighen EA, Graham AF (1983) In vitro synthesis of subunits of bacterial luciferase in an Escherichia coli system. J Bacteriol 153(1):543–545

    CAS  Google Scholar 

  • Farmer JI, Jorgensen J, Grimont P, Akhurst R, Poinar GJ, Ageron E, Pierce G, Smith J, Carter G, Wilson K, Hickman-Brenner F (1989) Xenorhabdus luminescens (DNA hybridization group 5) from human clinical specimens. J Clin Microbiol 27:1594–1600

    Google Scholar 

  • Frackman S, Anhalt M, Nealson KH (1990) Cloning, organization, and expression of the bioluminescence genes of Xenorhabdus luminescens. J Bacteriol 172(10):5767–5773

    CAS  Google Scholar 

  • Francis KP, Joh D, Bellinger-Kawahara C, Hawkinson MJ, Purchio TF, Contag PR (2000) Monitoring bioluminescent Staphylococcus aureus infections in living mice using a novel luxABCDE construct. Infect Immun 68(6):3594–3600

    Article  CAS  Google Scholar 

  • Francis KP, Yu J, Bellinger-Kawahara C, Joh D, Hawkinson MJ, Xiao G, Purchio TF, Caparon MG, Lipsitch M, Contag PR (2001) Visualizing pneumococcal infections in the lungs of live mice using bioluminescent Streptococcus pneumoniae transformed with a novel Gram-positive lux transposon. Infect Immun 69(5):3350–3358. doi:10.1128/iai.69.5.3350-3358.2001

    Article  CAS  Google Scholar 

  • Gábor F, Szocs K, Maillard P, Csík G (2001) Photobiological activity of exogenous and endogenous porphyrin derivatives in Escherichia coli and Enterococcus hirae cells. Radiat Environ Biophys V40(2):145–151

    Google Scholar 

  • Galluzzi L, Karp M (2007) Intracellular redox equilibrium and growth phase affect the performance of luciferase-based biosensors. J Biotechnol 127(2):188–198

    Article  CAS  Google Scholar 

  • Garcez AS, Ribeiro MS, Tegos GP, Núñez SC, Jorge AOC, Hamblin MR (2007) Antimicrobial photodynamic therapy combined with conventional endodontic treatment to eliminate root canal biofilm infection. Lasers Surg Med 39(1):59–66. doi:10.1002/lsm.20415

    Article  Google Scholar 

  • Grinholc M, Szramka B, Olender K, Graczyk A (2007) Bactericidal effect of photodynamic therapy against methicillin-resistant Staphylococcus aureus strain with the use of various porphyrin photosensitizers. Acta Biochim Pol 54(3):665–670

    CAS  Google Scholar 

  • Hadjur C, Lange N, Rebstein J, Monnier P, Bergh Hvd, Wagnières G (1998) Spectroscopic studies of photobleaching and photoproduct formation of meta(tetrahydroxyphenyl) chlorin (m-THPC) used in photodynamic therapy. The production of singlet oxygen by m-THPC. J Photochem Photobiol B Biol 45:170–178

    Article  CAS  Google Scholar 

  • Hamblin MR, Hasan T (2004) Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem Photobiol Sci 3:436–450. doi:10.1039/b311900a

    Article  CAS  Google Scholar 

  • Hamblin MR, O'Donnell DA, Murthy N, Contag CH, Hasan T (2002) Rapid control of wound infections by targeted photodynamic therapy monitored by in vivo bioluminescence imaging. Photochem Photobiol 75:51–57

    Article  CAS  Google Scholar 

  • Hamblin MR, Zahra T, Contag CH, McManus AT, Hasan T (2003) Optical monitoring and treatment of potentially lethal wound infections in vivo. J Infect Dis 187(11):1717–1726. doi:10.1086/375244

    Article  Google Scholar 

  • Harveyi E (1952) Bioluminescence. Academic, New York

    Google Scholar 

  • Hastings J (1986) Bioluminescence in bacteria and dinoflagellates. In: Govindjee A, Fork D (eds) Light emission by plants and bacteria. Academic, New York, pp 363–398

    Google Scholar 

  • Hastings J (1996) Chemistries and colors of bioluminescent reactions: a review. Gene 173:5–11

    Article  CAS  Google Scholar 

  • Herz J, Gerard RD (1993) Adenovirus-mediated transfer of low density lipoprotein receptor gene acutely accelerates cholesterol clearance in normal mice. Proc Natl Acad Sci U S A 90(7):2812–2816

    Article  CAS  Google Scholar 

  • Hill P, Rees C, Winson M, Stewart G (1993) The application of lux genes. Biotechnol Appl Biochem 17:3–14

    CAS  Google Scholar 

  • Horswell J, Weitz H, Percival H, Speir T (2006) Impact of heavy metal amended sewage sludge on forest soils as assessed by bacterial and fungal biosensors. Biol Fertil Soils 42(6):569–576. doi:10.1007/s00374-005-0070-5

    Article  Google Scholar 

  • Huang L, Dai T, Hamblin M (2010) Antimicrobial photodynamic inactivation and photodynamic therapy for infections. Methods Mol Biol 635:155–173

    Article  CAS  Google Scholar 

  • Imray FP, MacPhee DG (1973) The role of DNA polymerase I and the rec system in survival of bacteria and bacteriophages damaged by the photodynamic action of acridine orange. Mol Gen Genet 123(4):289–298

    Article  CAS  Google Scholar 

  • Ito T, Kobayashi K (1977) In vivo evidence for the photodynamic membrane damage as a determining step of the inactivation of yeast cells sensitized by toluidine blue. Photochem Photobiol 25(4):399–401

    Article  CAS  Google Scholar 

  • Wet J, Wood K, Helinski D, DeLuca M (1985) Cloning of firefly luciferase cDNA and the expression of active luciferase in Escherichia coli. Proc Natl Acad Sci U S A 23(82):7870–7873

    Article  Google Scholar 

  • Jemli M, Alouini Z, Sabbahi S, Gueddari M (2002) Destruction of fecal bacteria in wastewater by three photosensitizers. J Environ Monit 4(4):511–516

    Article  CAS  Google Scholar 

  • Jori G, Fabris C, Soncin M, Ferro S, Coppellotti O, Dei D, Fantetti L, Chiti G, Roncucci G (2006) Photodynamic therapy in the treatment of microbial infections: basic principles and perspective applications. Lasers Surg Med 38(5):468–481

    Article  Google Scholar 

  • Kaplan HB, Greenberg EP (1987) Overproduction and purification of the luxR gene product: transcriptional activator of the Vibrio fischeri luminescence system. Proc Natl Acad Sci U S A 84(19):6639–6643

    Article  CAS  Google Scholar 

  • Käsermann F, Kempf C (1997) Photodynamic inactivation of enveloped viruses by buckminsterfullerene. Antiviral Res 34(1):65–70

    Article  Google Scholar 

  • Kassab K, Dei D, Roncucci G, Jori G, Coppellotti O (2003) Phthalocyanine-photosensitized inactivation of a pathogenic protozoan, Acanthamoeba palestinensis. Photochem Photobiol Sci 2(6):668–672

    Article  CAS  Google Scholar 

  • Katsev AM, Węgrzyn G, Szpilewska H (2004) Effects of hydrogen peroxide on light emission by various strains of marine luminescent bacteria. J Basic Microbiol 44(3):178–184. doi:10.1002/jobm.200310330

    Article  CAS  Google Scholar 

  • Kawamura S (1915) Studies on the luminous fungus, Pleurotus japonicus sp. nov. Journal of the College of Science, Tokyo Imperial University 35(Art. 3):1–38

    Google Scholar 

  • Kim SY, Kwon OJ, Park J-W (2001) Inactivation of catalase and superoxide dismutase by singlet oxygen derived from photoactivated dye. Biochimie 83(5):437–444

    Article  CAS  Google Scholar 

  • Koga K, Harada T, Shimizu H, Tanaka K (2005) Bacterial luciferase activity and the intracellular redox pool in Escherichia coli. Mol Genet Genomics 274(2):180–188. doi:10.1007/s00438-005-0008-5

    Article  CAS  Google Scholar 

  • Kosaka S, Akilov OE, O'Riordan K, Hasan T (2007) A mechanistic study of [delta]-aminolevulinic acid-based photodynamic therapy for cutaneous leishmaniasis. J Invest Dermatol 127(6):1546–1549

    Article  CAS  Google Scholar 

  • Kratzer S, Mundigl O, Dicker F, Seeber S (2001) Digital imaging microscopy of firefly luciferase activity to directly monitor differences in cell transduction efficiencies between AdCMVLuc and Ad5LucRGD vectors having different cell binding properties. J Virol Methods 93(1–2):175–179

    Article  CAS  Google Scholar 

  • Kuhn J, Suissa M, Wyse J, Cohen I, Weiser I, Reznick S, Lubinsky-Mink S, Stewart G, Ulitzur S (2002) Detection of bacteria using foreign DNA: the development of a bacteriophage reagent for Salmonella. Int J Food Microbiol 74(3):229–238

    Article  CAS  Google Scholar 

  • Kurose K, Inouye S, Sakaki Y, Tsuji FI (1989) Bioluminescence of the Ca2+-binding photoprotein aequorin after cysteine modification. Proc Natl Acad Sci U S A 86(1):80–84. doi:10.1073/pnas.86.1.80

    Article  CAS  Google Scholar 

  • Lambrechts SAG, Aalders MCG, Van Marle J (2005a) Mechanistic study of the photodynamic inactivation of Candida albicans by a cationic porphyrin. Antimicrob Agents Chemother 49(5):2026–2034. doi:10.1128/aac.49.5.2026-2034.2005

    Article  CAS  Google Scholar 

  • Lambrechts SAG, Demidova TN, Aalders MCG, Hasan T, Hamblin MR (2005b) Photodynamic therapy for Staphylococcus aureus infected burn wounds in mice. Photochem Photobiol Sci 4(7):503–509

    Article  CAS  Google Scholar 

  • Lauro FM, Pretto P, Covolo L, Jori G, Bertoloni G (2002) Photoinactivation of bacterial strains involved in periodontal diseases sensitized by porphycene–polylysine conjugates. Photochem Photobiol Sci 1(7):468–470

    Article  CAS  Google Scholar 

  • Li H, Fedorova OS, Grachev AN, Trumble WR, Bohach GA, Czuchajowski L (1997) A series of meso-tris(N-methyl-pyridiniumyl)-(4-alkylamidophenyl) porphyrins: synthesis, interaction with DNA and antibacterial activity. Biochim Biophys Acta 1354(3):252–260

    CAS  Google Scholar 

  • Loessner M, Rees C, Stewart G, Scherer S (1996) Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells. Appl Environ Microbiol 62(4):1133–1140

    CAS  Google Scholar 

  • Loessner MJ, Rudolf M, Scherer S (1997) Evaluation of luciferase reporter bacteriophage A511::luxAB for detection of Listeria monocytogenes in contaminated foods. Appl Environ Microbiol 63(8):2961–2965

    CAS  Google Scholar 

  • Maclean M, MacGregor SJ, Anderson JG, Woolsey GA (2008) The role of oxygen in the visible-light inactivation of Staphylococcus aureus. J Photochem Photobiol B Biol 92(3):180–184

    Article  CAS  Google Scholar 

  • Magaraggia M, Faccenda F, Gandolfi A, Jori G (2006) Treatment of microbiologically polluted aquaculture waters by a novel photochemical technique of potentially low environmental impact. J Environ Monit 8(9):923–931

    Article  CAS  Google Scholar 

  • Maisch T, Szeimies RM, Jori G, Abels C (2004) Antibacterial photodynamic therapy in dermatology. Photochem Photobiol Sci 3(10):907–917

    Article  CAS  Google Scholar 

  • Maisch T, Bosl C, Szeimies RM, Lehn N, Abels C (2005) Photodynamic effects of novel XF porphyrin derivatives on prokaryotic and eukaryotic cells. Antimicrob Agents Chemother 49(4):1542–1552. doi:10.1128/aac.49.4.1542-1552.2005

    Article  CAS  Google Scholar 

  • Maisch T, Baier J, Franz B, Maier M, Landthaler M, Szeimies R-M, Baumler W (2007) The role of singlet oxygen and oxygen concentration in photodynamic inactivation of bacteria. Proc Natl Acad Sci U S A 104(17):7223–7228. doi:10.1073/pnas.0611328104

    Article  CAS  Google Scholar 

  • Makemson J (1986) Luciferase-dependent oxygen consumption by bioluminescent Vibrio. J Bacteriol 165:461–466

    CAS  Google Scholar 

  • Makemson JC, Hastings JW (1982) Iron represses bioluminescence and affects catabolite repression of luminescence in Vibrio harveyi. Curr Microbiol 7(3):181–186

    Article  CAS  Google Scholar 

  • Mancini JA, Boylan M, Soly RR, Graham AF, Meighen EA (1988) Cloning and expression of the Photobacterium phosphoreum luminescence system demonstrates a unique lux gene organization. J Biol Chem 263(28):14308–14314

    CAS  Google Scholar 

  • Maoz A, Mayr R, Bresolin G, Neuhaus K, Francis KP, Scherer S (2002) Sensitive in situ monitoring of a recombinant bioluminescent Yersinia enterocolitica reporter mutant in real time on camembert cheese. Appl Environ Microbiol 68(11):5737–5740. doi:10.1128/aem.68.11.5737-5740.2002

    Article  CAS  Google Scholar 

  • Meighen EA (1991) Molecular biology of bacterial bioluminescence. Microbiol Mol Biol Rev 55(1):123–142

    CAS  Google Scholar 

  • Meighen EA (1993) Bacterial bioluminescence: organization, regulation, and application of the lux genes. FASEB J 7(11):1016–1022

    CAS  Google Scholar 

  • Meighen E, Bartlet I (1980) Complementation of subunits from different bacterial luciferases. Evidence for the role of the P subunit in the bioluminescent mechanism. J Biol Chem 255:11181–11187

    CAS  Google Scholar 

  • Meighen E, Grant G (1985) Bioluminescence analysis of long chain aldehydes: detection of insect pheromones. In: Dyke KV (ed) Bioluminescence and chemiluminescence: instruments and applications, vol II. CRC Press, Boca Raton, pp 253–268

    Google Scholar 

  • Meighen E, Slessor K, Grant G (1982) Development of a bioluminescence assays for aldehyde pheromones of insects. I. Sensitivity and specificity. J Chem Ecol 8:911–921

    Article  CAS  Google Scholar 

  • Merchat M, Bertolini G, Giacomini P, Villanueva A, Jori G (1996a) Meso-substituted cationic porphyrins as efficient photosensitizers of gram-positive and gram-negative bacteria. J Photochem Photobiol B Biol 32(3):153–157

    Article  CAS  Google Scholar 

  • Merchat M, Spikes J, Bertoloni G, Jori G (1996b) Studies on the mechanism of bacteria photosensitization by meso-substituted cationic porphyrins. J Photochem Photobiol B Biol 35(3):149–157

    Article  CAS  Google Scholar 

  • Mettath S, Munson BR, Pandey RK (1998) DNA interaction and photocleavage properties of porphyrins containing cationic substituents at the peripheral position. Bioconjugate Chem 10(1):94–102. doi:10.1021/bc9800872

    Article  Google Scholar 

  • Minnock A, Vernon DI, Schofield J, Griffiths J, Parish JH, Brown SB (1996) Photoinactivation of bacteria. Use of a cationic water-soluble zinc phthalocyanine to photoinactivate both gram-negative and gram-positive bacteria. J Photochem Photobiol B Biol 32(3):159–164

    Article  CAS  Google Scholar 

  • Moncalvo J-M, Vilgalys R, Redhead SA, Johnson JE, James TY, Catherine Aime M, Hofstetter V, Verduin SJW, Larsson E, Baroni TJ, Greg Thorn R, Jacobsson S, Clémençon H, Miller OK (2002) One hundred and seventeen clades of euagarics. Mol Phylogenet Evol 23(3):357–400

    Article  CAS  Google Scholar 

  • Müller-Breitkreutz K, Mohr H, Briviba K, Sies H (1995) Inactivation of viruses by chemically and photochemically generated singlet molecular oxygen. J Photochem Photobiol B Biol 30(1):63–70

    Article  Google Scholar 

  • Nealson K, Hastings J (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43:496–518

    CAS  Google Scholar 

  • Nitzan Y, Shainberg B, Malik Z (1989) The mechanism of photodynamic inactivation of Staphylococcus aureus by deuteroporphyrin. Curr Microbiol 19(4):265–269

    Article  CAS  Google Scholar 

  • North J, Coombs R, Levy J (1994) Photodynamic inactivation of free and cell-associated HIV-1 using the photosensitizer, benzoporphyrin derivative. JAIDS 7(9):891–898

    CAS  Google Scholar 

  • O'Kane DJ, Lingle WL, Porter D, Wampler JE (1990) Localization of bioluminescent tissues during basidiocarp development in Panellus stypticus. Mycologia 82(5):595–606

    Article  Google Scholar 

  • Oliveira AG, Stevani CV (2009) The enzymatic nature of fungal bioluminescence. Photochem Photobiol Sci 8(10):1416–1421

    Article  CAS  Google Scholar 

  • Perry BA (2007) MycoDigest: bioluminescent fungi. Mycena News 58(03):1–2

    Google Scholar 

  • Prasher D, McCann C, Longlaru M, Cormier M (1987) Sequence comparisons of complementary DNAs encoding aequorin isotypes. Biochemistry 26:1326–1332

    Article  CAS  Google Scholar 

  • Rainey FA, Ehlers RU, Stackebrandt E (1995) Inability of the polyphasic approach to systematics to determine the relatedness of the genera Xenorhabdus and Photorhabdus. Int J Syst Bacteriol 45(2):379–381

    Article  CAS  Google Scholar 

  • Rocchetta HL, Boylan CJ, Foley JW, Iversen PW, LeTourneau DL, McMillian CL, Contag PR, Jenkins DE, Parr TR Jr (2001) Validation of a noninvasive, real-time imaging technology using bioluminescent Escherichia coli in the neutropenic mouse thigh model of infection. Antimicrob Agents Chemother 45(1):129–137. doi:10.1128/aac.45.1.129-137.2001

    Article  CAS  Google Scholar 

  • Rodriguez A, Nabi I, Meighen E (1985) ATP turnover by the fatty acid reductase complex of Photobacterium phosphoreum. Can J Biochem Cell Biol 63:1106–1111

    Article  CAS  Google Scholar 

  • Schagen F, Moor A, Cheong S, Cramer S, van Ormondt H, van der Eb A, Dubbelman T, Hoeben R (1999) Photodynamic treatment of adenoviral vectors with visible light: an easy and convenient method for viral inactivation. Gene Ther 6(5):873–881

    Article  CAS  Google Scholar 

  • Schmidt T, Kopecky K, Nealson K (1989) Bioluminescence of the insect pathogen Xenorhabdus luminescens. Appl Environ Microbiol 55:2607–2612

    CAS  Google Scholar 

  • Schofield DA, Westwater C (2009) Phage-mediated bioluminescent detection of Bacillus anthracis. J Appl Microbiol 107(5):1468–1478. doi:10.1111/j.1365-2672.2009.04332.x

    Article  CAS  Google Scholar 

  • Scholar EM, Pratt WB (2000) The antimicrobial drugs, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Shimomura O (1992) The role of superoxide dismutase in regulating the light emission of luminescent fungi. J Exp Bot 43(11):1519–1525. doi:10.1093/jxb/43.11.1519

    Article  CAS  Google Scholar 

  • Shimomura O, Johnson F, Morise H (1974) The aldehyde content of luminous bacteria and of an “aldehydeless” dark mutant. Proc Natl Acad Sci U S A 71:4666–4669

    Article  CAS  Google Scholar 

  • Sivinski J (1981) Arthropods attracted to luminous fungi. Psyche 88(3–4):383–390

    Article  Google Scholar 

  • Slock J (2000) Molecular biology experiments utilizing the lux genes of Vibrio fischeri and gfp gene of Aequoria victoria. Biology Department, King’s College. http://departments.kings.edu/biology/lux/bacterial.html. Accessed 7 Aug 2007

  • Slock J, VanRiet D, Kolibachuk D, Greenberg EP (1990) Critical regions of the Vibrio fischeri luxR protein defined by mutational analysis. J Bacteriol 172(7):3974–3979

    CAS  Google Scholar 

  • Szittner R, Meighen E (1990) Nucleotide sequence, expression and properties of luciferase coded by lux genes from a terrestrial bacterium. J Biol Chem 265:16581–16587

    CAS  Google Scholar 

  • Szpilewska H, Czyz A, Wegrzyn G (2003) Experimental evidence for the physiological role of bacterial luciferase in the protection of cells against oxidative stress. Curr Microbiol 47(5):379–382

    Article  CAS  Google Scholar 

  • Tavares A, Carvalho CMB, Faustino MA, Neves MGPMS, Tomé JPC, Tomé AC, Cavaleiro JAS, Cunha Â, Gomes NCM, Alves E, Almeida A (2010) Antimicrobial photodynamic therapy: study of bacterial recovery viability and potential development of resistance after treatment. Mar Drugs 8(1):91–105. doi:10.3390/md8010091

    Article  CAS  Google Scholar 

  • Thompson EM, Nagata S, Tsuji FI (1989) Cloning and expression of cDNA for the luciferase from the marine ostracod Vargula hilgendorfii. Proc Natl Acad Sci U S A 86(17):6567–6571. doi:10.1073/pnas.86.17.6567

    Article  CAS  Google Scholar 

  • Trannoy LL, Terpstra FG, De Korte D, Lagerberg JWM, Verhoeven AJ, Brand A, Van Engelenburg FAC (2006) Differential sensitivities of pathogens in red cell concentrates to Tri-P(4)-photoinactivation. Vox Sang 91(2):111–118. doi:10.1111/j.1423-0410.2006.00791.x

    Article  CAS  Google Scholar 

  • Ulitzur S, Hastings J (1979) Evidence for tetradecanal as the natural aldehyde in bacterial bioluminescence. Proc Natl Acad Sci U S A 76:265–267

    Article  CAS  Google Scholar 

  • Ulitzur S, Weiser I (1981) Acridine dyes and other DNA-intercalating agents induce the luminescence system of luminous bacteria and their dark variants. Proc Natl Acad Sci U S A 78(6):3338–3342

    Article  CAS  Google Scholar 

  • Valduga G, Breda B, Giacometti GM, Jori G, Reddi E (1999) Photosensitization of wild and mutant strains of Escherichia coli by meso-tetra(N-methyl-4-pyridyl)porphine. Biochem Biophys Res Commun 256(1):84–88

    Article  CAS  Google Scholar 

  • Vesterlund S, Paltta J, Laukova A, Karp M, Ouwehand AC (2004) Rapid screening method for the detection of antimicrobial substances. J Microbiol Meth 57(1):23–31

    Article  CAS  Google Scholar 

  • Vzorov AN, Dixon DW, Trommel JS, Marzilli LG, Compans RW (2002) Inactivation of human immunodeficiency virus type 1 by porphyrins. Antimicrob Agents Chemother 46(12):3917–3925. doi:10.1128/aac.46.12.3917-3925.2002

    Article  CAS  Google Scholar 

  • Wainwright M (1998) Photodynamic antimicrobial chemotherapy (PACT). J Antimicrob Chemother 42(1):13–28. doi:10.1093/jac/42.1.13

    Article  CAS  Google Scholar 

  • Wainwright M, Crossley KB (2004) Photosensitising agents—circumventing resistance and breaking down biofilms: a review. Int Biodeterior Biodegrad 53(2):119–126

    Article  CAS  Google Scholar 

  • Watanabe H, Hastings J (1990) Expression of bacterial bioluminescence is stimulated by naldixic acid in a naldixic acid resistent mutant. Arch Microbiol 154:239–243

    Article  CAS  Google Scholar 

  • Watanabe H, Nagoshi T, Inaba H (1993) Luminescence of a bacterial luciferase intermediate by reaction with H2O2: the evolutionary origin of luciferase and source of endogenous light emission. Biochim Biophys Acta Bioenerg 1141(2–3):297–302

    Article  CAS  Google Scholar 

  • Weiner JH, MacIsaac DP, Bishop RE, Bilous PT (1988) Purification and properties of Escherichia coli dimethyl sulfoxide reductase, an iron–sulfur molybdoenzyme with broad substrate specificity. J Bacteriol 170(4):1505–1510

    CAS  Google Scholar 

  • Weitz WHJ (2004) Naturally bioluminescent fungi. Mycologist 18(01):4–5. doi:10.1017/S0269915X04001016

    Article  Google Scholar 

  • Wilson M, Yianni C (1995) Killing of methicillin-resistant Staphylococcus aureus by low-power laser light. J Med Microbiol 42:62–66

    Article  CAS  Google Scholar 

  • Winckler KD (2007) Special section: focus on anti-microbial photodynamic therapy (PDT). J Photochem Photobiol B Biol 86(1):43–44

    Article  CAS  Google Scholar 

  • Wood KV, Lam YA, Seliger HH, McElroy WD (1989) Complementary DNA coding click beetle luciferases can elicit bioluminescence of different colors. Science 244(4905):700–702. doi:10.1126/science.2655091

    Article  CAS  Google Scholar 

  • Xi L, Cho KW, Tu SC (1991) Cloning and nucleotide sequences of lux genes and characterization of luciferase of Xenorhabdus luminescens from a human wound. J Bacteriol 173(4):1399–1405

    CAS  Google Scholar 

  • Ziegler M, Baldwin T (1981) Biochemistry of bacterial bioluminescence. Curr Top Bioenerg 12:65–113

    CAS  Google Scholar 

  • Zupán K, Egyeki M, Tóth K, Fekete A, Herényi L, Módos K, Csík G (2008) Comparison of the efficiency and the specificity of DNA-bound and free cationic porphyrin in photodynamic virus inactivation. J Photochem Photobiol B Biol 90(2):105–112

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology and CESAM, University of Aveiro, 3810-193, Aveiro, Portugal

    Eliana Alves, Liliana Costa, Ângela Cunha & Adelaide Almeida

  2. Department of Chemistry and QOPNA, University of Aveiro, 3810-193, Aveiro, Portugal

    Maria Amparo F. Faustino & Maria Graça P. M. S. Neves

Authors
  1. Eliana Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liliana Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ângela Cunha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Amparo F. Faustino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Graça P. M. S. Neves
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Adelaide Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adelaide Almeida.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alves, E., Costa, L., Cunha, Â. et al. Bioluminescence and its application in the monitoring of antimicrobial photodynamic therapy. Appl Microbiol Biotechnol 92, 1115–1128 (2011). https://doi.org/10.1007/s00253-011-3639-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3639-y

Keywords

Search

Navigation