Skip to main content

Bioluminescent Models to Evaluate the Efficiency of Light-Based Antibacterial Approaches

  • Protocol
  • First Online:
Photodynamic Therapy

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2451))

  • 1009 Accesses

Abstract

The emergence of microbial resistance to antimicrobials among several common pathogenic microbial strains is an increasing problem worldwide. Thus, it is urgent to develop not only new antimicrobial therapeutics to fight microbial infections, but also new effective, rapid, and inexpensive methods to monitor the efficacy of these new therapeutics. Antimicrobial photodynamic therapy (aPDT) and antimicrobial blue light (aBL) therapy are receiving considerable attention for their antimicrobial potential and represent realistic alternatives to antibiotics. To monitor the photoinactivation process provided by aPDT and aBL, faster and more effective methods are required instead of laborious conventional plating and overnight incubation procedures. Bioluminescent microbial models are very interesting in this context. Light emission from bioluminescent microorganisms is a highly sensitive indication of their metabolic activity and can be used to monitor, in real time, the effects of antimicrobial agents and therapeutics. This chapter reviews the efforts of the scientific community concerning the development of in vitro, ex vivo, and in vivo bioluminescent bacterial models and their potential to evaluate the efficiency of aPDT and aBL in the inactivation of bacteria.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Alves E, Faustino MAF, Neves MGPMS, Cunha Â, Nadais H, Almeida A (2015) Potential applications of porphyrins in photodynamic inactivation beyond the medical scope. J Photochem Photobiol C Photochem Rev 22:34–57. https://doi.org/10.1016/j.jphotochemrev.2014.09.003

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  3. Hu XQ, Huang YY, Wang YG, Wang XY, Hamblin MR (2018) Antimicrobial photodynamic therapy to control clinically relevant biofilm infections. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.01299

  4. Mesquita MQ, Dias CJ, Neves MGPMS, Almeida A, Faustino MAF (2018) Revisiting current photoactive materials for antimicrobial photodynamic therapy. Molecules 23:2424

    Article  Google Scholar 

  5. Hamblin MR (2016) Antimicrobial photodynamic inactivation: a bright new technique to kill resistant microbes. Curr Opin Microbiol 33:67–73. https://doi.org/10.1016/j.mib.2016.06.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Huang Y-Y, Wintner A, Seed PC, Brauns T, Gelfand JA, Hamblin MR (2018) Antimicrobial photodynamic therapy mediated by methylene blue and potassium iodide to treat urinary tract infection in a female rat model. Sci Rep 8:7257. https://doi.org/10.1038/s41598-018-25365-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Cabral J, Rodrigues A (2019) Blue light disinfection in hospital infection control: advantages, drawbacks, and pitfalls. Antibiotics 8:58

    Article  CAS  PubMed Central  Google Scholar 

  8. Wang Y, Harrington OD, Wang Y, Murray CK, Hamblin MR, Dai T (2017) In vivo investigation of antimicrobial blue light therapy for multidrug-resistant Acinetobacter baumannii Burn infections using bioluminescence imaging. J Vis Exp:54997. https://doi.org/10.3791/54997

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

    Article  CAS  Google Scholar 

  10. Beard SJ, Salisbury V, Lewis RJ, Sharpe JA, MacGowan AP (2002) Expression of <em>lux</em> genes in a clinical isolate of <em>Streptococcus pneumoniae</em>: using bioluminescence to monitor gemifloxacin activity. Antimicrob Agents Chemother 46:538–542. https://doi.org/10.1128/aac.46.2.538-542.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sharifian S, Homaei A, Hemmati R, Luwor R, Khajeh K (2018) The emerging use of bioluminescence in medical research. Biomed Pharmacother 101:74–86. https://doi.org/10.1016/j.biopha.2018.02.065

    Article  CAS  PubMed  Google Scholar 

  12. Alves E, Carvalho CMB, Tomé JPC, Faustino MAF, Neves MGPMS, Tomé AC, Cavaleiro JAS, Cunha Â, Mendo S, Almeida A (2008) Photodynamic inactivation of recombinant bioluminescent Escherichia coli by cationic porphyrins under artificial and solar irradiation. J Ind Microb Biotechnol 35:1447. https://doi.org/10.1007/s10295-008-0446-2

    Article  CAS  Google Scholar 

  13. Sharifian S, Homaei A, Hemmati R, Khajeh K (2017) Light emission miracle in the sea and preeminent applications of bioluminescence in recent new biotechnology. J Photochem Photobiol B Biol 172:115–128. https://doi.org/10.1016/j.jphotobiol.2017.05.021

    Article  CAS  Google Scholar 

  14. Farmer JJ, Jorgensen JH, Grimont PAD, Akhurst RJ, Poinar GO, Ageron E, Pierce GV, Smith JA, Carter GP, Wilson KL, Hickmanbrenner FW (1989) Xenorhabdus-luminescens (DNA hybridization group-5) from human clinical specimens. J Clin Microbiol 27:1594–1600

    Article  PubMed  PubMed Central  Google Scholar 

  15. Meighen EA (1991) Molecular-biology of bacterial bioluminescence. Microbiol Rev 55:123–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hastings JW (1996) Chemistries and colors of bioluminescent reactions: a review. Gene 173:5–11. https://doi.org/10.1016/0378-1119(95)00676-1

    Article  CAS  PubMed  Google Scholar 

  17. Nealson KH, Hastings JW (1979) Bacterial bioluminescence—its control and ecological significance. Microbiol Rev 43:496–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Makemson JC, Hastings JW (1982) Iron represses bioluminescence and affects catabolite repression of luminescence in vibrio-harveyi. Curr Microbiol 7:181–186. https://doi.org/10.1007/bf01568972

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  20. 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 47:379–382. https://doi.org/10.1007/s00284-002-4024-y

    Article  CAS  PubMed  Google Scholar 

  21. Avci P, Karimi M, Sadasivam M, Antunes-Melo WC, Carrasco E, Hamblin MR (2018) In-vivo monitoring of infectious diseases in living animals using bioluminescence imaging. Virulence 9:28–63. https://doi.org/10.1080/21505594.2017.1371897

    Article  PubMed  Google Scholar 

  22. Meighen EA, Slessor KN, Grant GG (1982) Development of a bioluminescence assay for aldehyde pheromones of insects. J Chem Ecol 8:911–921. https://doi.org/10.1007/bf00987658

    Article  CAS  PubMed  Google Scholar 

  23. Shimomura O, Johnson FH, 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  PubMed  PubMed Central  Google Scholar 

  24. Rodriguez A, Nabi IR, Meighen E (1985) ATP turnover by the fatty-acid reductase complex of photobacterium-phosphoreum. Can J Biochem Cell Biol 63:1106–1111. https://doi.org/10.1139/o85-138

    Article  CAS  Google Scholar 

  25. Meighen EA, Bartlet I (1980) Complementation of subunits from different bacterial luciferases. Evidence for the role of the beta subunit in the bioluminescent mechanism. J Biol Chem 255:11,181–11,187

    Article  CAS  Google Scholar 

  26. Colepicolo P, Cho KW, Poinar GO, Hastings JW (1989) Growth and luminescence of the bacterium xenorhabdus-luminescens from a human wound. Appl Environ Microbiol 55:2601–2606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Schmidt TM, Kopecky K, Nealson KH (1989) Bioluminescence of the insect pathogen xenorhabdus-luminescens. Appl Environ Microbiol 55:2607–2612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Szittner R, Meighen E (1990) Nucleotide-sequence, expression, and properties of luciferase coded by lux genes from a terrestrial bacterium. J Biol Chem 265:16,581–16,587

    Article  CAS  Google Scholar 

  29. Vesterlund S, Paltta J, Laukova A, Karp M, Ouwehand AC (2004) Rapid screening method for the detection of antimicrobial substances. J Microbiol Methods 57:23–31. https://doi.org/10.1016/j.mimet.2003.11.014

    Article  CAS  PubMed  Google Scholar 

  30. Chatterjee J, Meighen EA (1995) Biotechnological applications of bacterial bioluminescence (lux) genes. Photochem Photobiol 62:641–650. https://doi.org/10.1111/j.1751-1097.1995.tb08711.x

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Hill PJ, Rees CED, Winson MK, Stewart G (1993) The application of lux genes. Biotechnol Appl Biochem 17:3–14

    CAS  PubMed  Google Scholar 

  33. 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 luxABCDEConstruct. Infect Immunity 68:3594–3600. https://doi.org/10.1128/iai.68.6.3594-3600.2000

    Article  CAS  Google Scholar 

  34. Boemare NE, Akhurst RJ, Mourant RG (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 Systematic Bacteriology 43:249–255. https://doi.org/10.1099/00207713-43-2-249

    Article  CAS  Google Scholar 

  35. 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 45:379–381. https://doi.org/10.1099/00207713-45-2-379

    Article  CAS  PubMed  Google Scholar 

  36. Frackman S, Anhalt M, Nealson KH (1990) Cloning, organization, and expression of the bioluminescence genes of xenorhabdus-luminescens. J Bacteriol 172:5767–5773. https://doi.org/10.1128/jb.172.10.5767-5773.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 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 173:1399–1405. https://doi.org/10.1128/jb.173.4.1399-1405.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Roda A, Pasini P, Mirasoli M, Michelini E, Guardigli M (2004) Biotechnological applications of bioluminescence and chemiluminescence. Trends Biotechnol 22:295–303. https://doi.org/10.1016/j.tibtech.2004.03.011

    Article  CAS  PubMed  Google Scholar 

  39. Contag CH, Contag PR, Mullins JI, Spilman SD, Stevenson DK, Benaron DA (1995) Photonic detection of bacterial pathogens in living hosts. Mol Microbiol 18:593–603. https://doi.org/10.1111/j.1365-2958.1995.mmi_18040593.x

    Article  CAS  PubMed  Google Scholar 

  40. Clark DP (1989) The fermentation pathways of Escherichia coli. FEMS Microbiol Lett 63:223–234. https://doi.org/10.1016/0378-1097(89)90132-8

    Article  CAS  Google Scholar 

  41. Galluzzi L, Karp M (2007) Intracellular redox equilibrium and growth phase affect the performance of luciferase-based biosensors. J Biotechnol 127:188–198. https://doi.org/10.1016/j.jbiotec.2006.06.019

    Article  CAS  PubMed  Google Scholar 

  42. 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 1141:297–302. https://doi.org/10.1016/0005-2728(93)90056-L

    Article  CAS  Google Scholar 

  43. 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 Biol Sci 78:3338–3342. https://doi.org/10.1073/pnas.78.6.3338

    Article  CAS  Google Scholar 

  44. 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 170:1505–1510. https://doi.org/10.1128/jb.170.4.1505-1510.1988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Kudryasheva N, Vetrova E, Kuznetsov A, Kratasyuk V, Stom D (2002) Bioluminescence assays: effects of quinones and phenols. Ecotoxicol Environ Saf 53:221–225. https://doi.org/10.1006/eesa.2002.2214

    Article  CAS  PubMed  Google Scholar 

  46. Ismailov AD, Pogosyan SI, Mitrofanova TI, Egorov NS, Netrusov AI (2000) Bacterial bioluminescence inhibition by Chlorophenols. Appl Biochem Microbiol 36:404–408. https://doi.org/10.1007/bf02738051

    Article  Google Scholar 

  47. 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. https://doi.org/10.1562/0031-8655(2002)0750051RCOWIB2.0.CO2

    Article  CAS  PubMed  Google Scholar 

  48. Demidova TN, Hamblin MR (2004) Photodynamic therapy targeted to pathogens. Int J Immunopathol Pharmacol 17:245–254

    Article  CAS  PubMed  Google Scholar 

  49. 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 187:1717–1726. https://doi.org/10.1086/375244

    Article  PubMed  Google Scholar 

  50. Gad F, Zahra T, Francis KP, Hasan T, Hamblin MR (2004) Targeted photodynamic therapy of established soft-tissue infections in mice. Photochem Photobiol Sci 3:451–458. https://doi.org/10.1039/b311901g

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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 81:15–25. https://doi.org/10.1016/j.jphotobiol.2005.05.007

    Article  CAS  Google Scholar 

  52. 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 Immunity 69:3350–3358. https://doi.org/10.1128/iai.69.5.3350-3358.2001

    Article  CAS  Google Scholar 

  53. Lambrechts SAG, Demidova TN, Aalders MCG, Hasan T, Hamblin MR (2005) Photodynamic therapy for Staphylococcus aureus infected burn wounds in mice. Photochem Photobiol Sci 4:503–509. https://doi.org/10.1039/b502125a

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Dai TH, Tegos GP, Lu ZS, Huang LY, Zhiyentayev T, Franklin MJ, Baer DG, Hamblin MR (2009) Photodynamic therapy for Acinetobacter baumannii burn infections in mice. Antimicrob Agents Chemother 53:3929–3934. https://doi.org/10.1128/aac.00027-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Dai T, Tegos GP, Zhiyentayev T, Mylonakis E, Hamblin MR (2010) Photodynamic therapy for methicillin-resistant Staphylococcus aureus infection in a mouse skin abrasion model. Lasers Surg Med 42:38. https://doi.org/10.1002/lsm.20887

    Article  PubMed  PubMed Central  Google Scholar 

  56. Vecchio D, Dai T, Huang L, Fantetti L, Roncucci G, Hamblin MR (2013) Antimicrobial photodynamic therapy with RLP068 kills methicillin-resistant Staphylococcus aureus and improves wound healing in a mouse model of infected skin abrasion. J Biophoton 6:733–742. https://doi.org/10.1002/jbio.201200121

    Article  CAS  Google Scholar 

  57. Sánchez-García D, Sessler JL (2008) Porphycenes: synthesis and derivatives. Chem Soc Rev 37:215–232. https://doi.org/10.1039/B704945E

    Article  PubMed  Google Scholar 

  58. Masiera N, Bojarska A, Gawryszewska I, Sadowy E, Hryniewicz W, Waluk J (2017) Antimicrobial photodynamic therapy by means of porphycene photosensitizers. J Photochem Photobiol B Biol 174:84–89. https://doi.org/10.1016/j.jphotobiol.2017.07.016

    Article  CAS  Google Scholar 

  59. Ragàs X, Sánchez-García D, Ruiz-González R, Dai T, Agut M, Hamblin MR, Nonell S (2010) Cationic porphycenes as potential photosensitizers for antimicrobial photodynamic therapy. J Med Chem 53:7796–7803. https://doi.org/10.1021/jm1009555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  61. 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 68:5737–5740. https://doi.org/10.1128/aem.68.11.5737-5740.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Fila G, Kasimova K, Arenas Y, Nakonieczna J, Grinholc M, Bielawski KP, Lilge L (2016) Murine model imitating chronic wound infections for evaluation of antimicrobial photodynamic therapy efficacy. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.01258

  63. Ramphal R, Balloy V, Jyot J, Verma A, Si-Tahar M, Chignard M (2008) Control of Pseudomonas aeruginosa in the lung requires the recognition of either lipopolysaccharide or flagellin. J Immunol (Baltimore, MD: 1950) 181:586–592

    Article  CAS  Google Scholar 

  64. Lu Z, Dai T, Huang L, Kurup DB, Tegos GP, Jahnke A, Wharton T, Hamblin MR (2010) Photodynamic therapy with a cationic functionalized fullerene rescues mice from fatal wound infections. Nanomedicine 5:1525–1533. https://doi.org/10.2217/nnm.10.98

    Article  CAS  PubMed  Google Scholar 

  65. Yin R, Hamblin MR (2015) Antimicrobial photosensitizers: drug discovery under the spotlight. Curr Med Chem 22:2159–2185. https://doi.org/10.2174/0929867322666150319120134

    Article  CAS  PubMed  Google Scholar 

  66. Tegos GP, Hamblin MR (2006) Phenothiazinium antimicrobial photosensitizers are substrates of bacterial multidrug resistance pumps. Antimicrob Agents Chemother 50:196–203. https://doi.org/10.1128/aac.50.1.196-203.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Ragàs X, Dai T, Tegos GP, Agut M, Nonell S, Hamblin MR (2010) Photodynamic inactivation of Acinetobacter baumannii using phenothiazinium dyes: in vitro and in vivo studies. Lasers Surg Med 42:384–390. https://doi.org/10.1002/lsm.20922

    Article  PubMed  PubMed Central  Google Scholar 

  68. Garcez AS, Hamblin MR (2017) Methylene blue and hydrogen peroxide for photodynamic inactivation in root canal—a new protocol for use in endodontics. Eur Endodontic J 2:29. https://doi.org/10.5152/eej.2017.17023

    Article  Google Scholar 

  69. Grinholc M, Nakonieczna J, Fila G, Taraszkiewicz A, Kawiak A, Szewczyk G, Sarna T, Lilge L, Bielawski KP (2015) Antimicrobial photodynamic therapy with fulleropyrrolidine: photoinactivation mechanism of Staphylococcus aureus, in vitro and in vivo studies. Appl Microbiol Biotechnol 99:4031–4043. https://doi.org/10.1007/s00253-015-6539-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Park SJ, Mehrad B (2009) Innate immunity to <em>Aspergillus</em> species. Clin Microbiol Rev 22:535–551. https://doi.org/10.1128/cmr.00014-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Tim M. A New strategy to destroy antibiotic resistant microorganisms: antimicrobial photodynamic treatment. Mini-Rev Med Chem. 2009; 9: 974-983. doi: https://doi.org/10.2174/138955709788681582.

  72. Slock J, Vanriet D, Kolibachuk D, Greenberg EP (1990) Critical regions of the vibrio-fischeri luxr protein defined by mutational analysis. J Bacteriol 172:3974–3979. https://doi.org/10.1128/jb.172.7.3974-3979.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 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:e20970. https://doi.org/10.1371/journal.pone.0020970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Bartolomeu M, Reis S, Fontes M, Neves M, Faustino M, Almeida A (2017) Photodynamic action against wastewater microorganisms and chemical pollutants: an effective approach with low environmental impact. Water 9:630

    Article  Google Scholar 

  75. Bartolomeu M, Neves MGPMS, Faustino MAF, Almeida A (2018) Wastewater chemical contaminants: remediation by advanced oxidation processes. Photochem Photobiol Sci 17:1573–1598. https://doi.org/10.1039/C8PP00249E

    Article  CAS  PubMed  Google Scholar 

  76. Carvalho CMB, Alves E, Costa L, Tomé JPC, Faustino MAF, Neves MGPMS, Tomé AC, Cavaleiro JAS, Almeida A, Cunha Â, Lin Z, Rocha J (2010) Functional cationic nanomagnet−porphyrin hybrids for the photoinactivation of microorganisms. ACS Nano 4:7133–7140. https://doi.org/10.1021/nn1026092

    Article  CAS  PubMed  Google Scholar 

  77. Alves E, Rodrigues JMM, Faustino MAF, Neves MGPMS, Cavaleiro JAS, Lin Z, Cunha Â, Nadais MH, Tomé JPC, Almeida A (2014) A new insight on nanomagnet–porphyrin hybrids for photodynamic inactivation of microorganisms. Dyes Pigments 110:80–88. https://doi.org/10.1016/j.dyepig.2014.05.016

    Article  CAS  Google Scholar 

  78. Spagnul C, Greenman J, Wainwright M, Kamil Z, Boyle RW (2016) Synthesis, characterization and biological evaluation of a new photoactive hydrogel against Gram-positive and Gram-negative bacteria. J Mater Chem B 4:1499–1509. https://doi.org/10.1039/C5TB02569A

    Article  CAS  PubMed  Google Scholar 

  79. Parveen A, Smith G, Salisbury V, Nelson SM (2001) Biofilm culture of Pseudomonas aeruginosa expressing lux genes as a model to study susceptibility to antimicrobials. FEMS Microbiol Lett 199:115–118. https://doi.org/10.1111/j.1574-6968.2001.tb10660.x

    Article  CAS  PubMed  Google Scholar 

  80. Tenhami M, Hakkila K, Karp M (2001) Measurement of Effects of Antibiotics in Bioluminescent <em>Staphylococcus aureus</em> RN4220. Antimicrob Agents Chemother 45:3456–3461. https://doi.org/10.1128/aac.45.12.3456-3461.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Spagnul C, Turner LC, Giuntini F, Greenman J, Boyle RW (2017) Synthesis and bactericidal properties of porphyrins immobilized in a polyacrylamide support: influence of metal complexation on photoactivity. J Mater Chem B 5:1834–1845. https://doi.org/10.1039/C6TB03198F

    Article  CAS  PubMed  Google Scholar 

  82. Mesquita MQ, Menezes JCJMDS, Neves MGPMS, Tomé AC, Cavaleiro JAS, Cunha Â, Almeida A, Hackbarth S, Röder B, Faustino MAF (2014) Photodynamic inactivation of bioluminescent Escherichia coli by neutral and cationic pyrrolidine-fused chlorins and isobacteriochlorins. Bioorg Med Chem Lett 24:808–812. https://doi.org/10.1016/j.bmcl.2013.12.097

    Article  CAS  PubMed  Google Scholar 

  83. Alves E, Costa L, Carvalho CMB, Tome JPC, Faustino MA, Neves M, Tome AC, Cavaleiro JAS, Cunha A, Almeida A (2009) Charge effect on the photoinactivation of Gram-negative and Gram-positive bacteria by cationic meso-substituted porphyrins. BMC Microbiol 9:13. https://doi.org/10.1186/1471-2180-9-70

    Article  Google Scholar 

  84. Mesquita MQ, Menezes JCJMDS, Pires SMG, Neves MGPMS, Simões MMQ, Tomé AC, Cavaleiro JAS, Cunha Â, Daniel-da-Silva AL, Almeida A, Faustino MAF (2014) Pyrrolidine-fused chlorin photosensitizer immobilized on solid supports for the photoinactivation of Gram-negative bacteria. Dyes Pigments 110:123–133. https://doi.org/10.1016/j.dyepig.2014.04.025

    Article  CAS  Google Scholar 

  85. Kuznetsova NA, Yuzhakova OA, Strakhovskaya MG, Shumarina AO, Kozlov AS, Krasnovsky AA, Kaliya OL (2011) New heterogeneous photosensitizers with phthalocyanine molecules covalently linked to aminopropyl silica gel. J Porphyrins Phthalocyanines 15:718–726. https://doi.org/10.1142/s1088424611003690

    Article  CAS  Google Scholar 

  86. George L, Müller A, Röder B, Santala V, Efimov A (2017) Photodynamic self–disinfecting surface using pyridinium phthalocyanine. Dyes Pigments 147:334–342. https://doi.org/10.1016/j.dyepig.2017.08.021

    Article  CAS  Google Scholar 

  87. Moura NMM, Ramos CIV, Linhares I, Santos SM, Faustino MAF, Almeida A, Cavaleiro JAS, Amado FML, Lodeiro C, Neves MGPMS (2016) Synthesis, characterization and biological evaluation of cationic porphyrin–terpyridine derivatives. RSC Adv 6:110,674–110,685. https://doi.org/10.1039/C6RA25373C

    Article  CAS  Google Scholar 

  88. Moura NMM, Esteves M, Vieira C, Rocha GMSRO, Faustino MAF, Almeida A, Cavaleiro JAS, Lodeiro C, Neves MGPMS (2019) Novel β-functionalized mono-charged porphyrinic derivatives: Synthesis and photoinactivation of Escherichia coli. Dyes Pigments 160:361–371. https://doi.org/10.1016/j.dyepig.2018.06.048

    Article  CAS  Google Scholar 

  89. da Silva RN, Cunha Â, Tomé AC (2018) Phthalocyanine–sulfonamide conjugates: Synthesis and photodynamic inactivation of Gram-negative and Gram-positive bacteria. Eur J Med Chem 154:60–67. https://doi.org/10.1016/j.ejmech.2018.05.009

    Article  CAS  PubMed  Google Scholar 

  90. Pereira JB, Carvalho EFA, Faustino MAF, Fernandes R, Neves MGPMS, Cavaleiro JAS, Gomes NCM, Cunha Â, Almeida A, Tomé JPC (2012) Phthalocyanine Thio-pyridinium derivatives as antibacterial photosensitizers. Photochem Photobiol 88:537–547. https://doi.org/10.1111/j.1751-1097.2012.01113.x

    Article  CAS  PubMed  Google Scholar 

  91. Lourenço LMO, Sousa A, Gomes MC, Faustino MAF, Almeida A, Silva AMS, Neves MGPMS, Cavaleiro JAS, Cunha Â, Tomé JPC (2015) Inverted methoxypyridinium phthalocyanines for PDI of pathogenic bacteria. Photochem Photobiol Sci 14:1853–1863. https://doi.org/10.1039/C5PP00145E

    Article  CAS  PubMed  Google Scholar 

  92. Rocha DMGC, Venkatramaiah N, Gomes MC, Almeida A, Faustino MAF, Almeida Paz FA, Cunha Â, Tomé JPC (2015) Photodynamic inactivation of Escherichia coli with cationic ammonium Zn(ii) phthalocyanines. Photochem Photobiol Sci 14:1872–1879. https://doi.org/10.1039/C5PP00147A

    Article  CAS  PubMed  Google Scholar 

  93. Castro KADF, Moura NMM, Figueira F, Ferreira RI, Simões MMQ, Cavaleiro JAS, Faustino MAF, Silvestre AJD, Freire CSR, Tomé JPC, Nakagaki S, Almeida A, Neves MGPMS (2019) New materials based on cationic porphyrins conjugated to chitosan or titanium dioxide: synthesis, characterization and antimicrobial efficacy. Int J Mol Sci 20:2522

    Article  CAS  PubMed Central  Google Scholar 

  94. Taylor PW, Stapleton PD, Luzio JP (2002) New ways to treat bacterial infections. Drug Discovery Today 7:1086–1091. https://doi.org/10.1016/s1359-6446(02)02498-4

    Article  PubMed  Google Scholar 

  95. Alves E, Faustino MA, Neves MG, Cunha A, Tome J, Almeida A (2014) An insight on bacterial cellular targets of photodynamic inactivation. Future Med Chem 6:141–164. https://doi.org/10.4155/fmc.13.211

    Article  CAS  PubMed  Google Scholar 

  96. Costa L, Faustino MAF, Neves MGPMS, Cunha Â, Almeida A (2012) Photodynamic inactivation of mammalian viruses and bacteriophages. Viruses 4:1034–1074

    Article  PubMed  PubMed Central  Google Scholar 

  97. Oliveira A, Almeida A, Carvalho CMB, Tomé JPC, Faustino MAF, Neves MGPMS, Tomé AC, Cavaleiro JAS, Cunha  (2009) Porphyrin derivatives as photosensitizers for the inactivation of Bacillus cereus endospores. J Appl Microbiol 106:1986–1995. https://doi.org/10.1111/j.1365-2672.2009.04168.x

    Article  CAS  PubMed  Google Scholar 

  98. 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. Marine Drugs 8:91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Costa L, Alves E, Carvalho CMB, Tome JPC, Faustino MAF, Neves M, Tome AC, Cavaleiro JAS, Cunha A, Almeida A (2008) Sewage bacteriophage photoinactivation by cationic porphyrins: a study of charge effect. Photochem Photobiol Sci 7:415–422. https://doi.org/10.1039/15712749a

    Article  CAS  PubMed  Google Scholar 

  100. Tavares A, Dias SRS, Carvalho CMB, Faustino MAF, Tomé JPC, Neves MGPMS, Tomé AC, Cavaleiro JAS, Cunha Â, Gomes NCM, Alves E, Almeida A (2011) Mechanisms of photodynamic inactivation of a Gram-negative recombinant bioluminescent bacterium by cationic porphyrins. Photochem Photobiol Sci 10:1659–1669. https://doi.org/10.1039/C1PP05097D

    Article  CAS  PubMed  Google Scholar 

  101. Hamblin MR, Abrahamse H (2018) Inorganic salts and antimicrobial photodynamic therapy: mechanistic conundrums? Molecules 23. https://doi.org/10.3390/molecules23123190

  102. Vieira C, Gomes ATPC, Mesquita MQ, Moura NMM, Neves MGPMS, Faustino MAF, Almeida A (2018) An insight into the potentiation effect of potassium iodide on aPDT efficacy. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.02665

  103. Zhang Y, Dai T, Wang M, Vecchio D, Chiang LY, Hamblin MR (2015) Potentiation of antimicrobial photodynamic inactivation mediated by a cationic fullerene by added iodide: in vitro and in vivo studies. Nanomedicine 10:603–614. https://doi.org/10.2217/nnm.14.131

    Article  CAS  PubMed  Google Scholar 

  104. Wen X, Zhang X, Szewczyk G, El-Hussein A, Huang Y-Y, Sarna T, Hamblin MR (2017) Potassium iodide potentiates antimicrobial photodynamic inactivation mediated by rose bengal in in vitro and in vivo studies. Antimicrob Agents Chemother 61. https://doi.org/10.1128/aac.00467-17

  105. Marciel L, Mesquita MQ, Ferreira R, Moreira B, Graca M, Neves PMS, Faustino MAF, Almeida A (2018) An efficient formulation based on cationic porphyrins to photoinactivate Staphylococcus aureus and Escherichia coli. Future Med Chem 10:1821–1833. https://doi.org/10.4155/fmc-2018-0010

    Article  CAS  PubMed  Google Scholar 

  106. Martins D, Mesquita MQ, Neves M, Faustino MAF, Reis L, Figueira E, Almeida A (2018) Photoinactivation of Pseudomonas syringae pv. actinidiae in kiwifruit plants by cationic porphyrins. Planta 248:409–421. https://doi.org/10.1007/s00425-018-2913-y

    Article  CAS  PubMed  Google Scholar 

  107. Enwemeka CS (2013) Antimicrobial blue light: an emerging alternative to antibiotics. Photomed Laser Surg 31:509–511. https://doi.org/10.1089/pho.2013.9871

    Article  PubMed  Google Scholar 

  108. Dai T, Garcia B, Murray CK, Vrahas MS, Hamblin MR (2012) UVC light prophylaxis for cutaneous wound infections in mice. Antimicrob Agents Chemother 56:3841–3848. https://doi.org/10.1128/aac.00161-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Maclean M, MacGregor SJ, Anderson JG, Woolsey G (2009) Inactivation of bacterial pathogens following exposure to light from a 405-nanometer light-emitting diode array. Appl Environ Microbiol 75:1932–1937. https://doi.org/10.1128/aem.01892-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Dai T, Gupta A, Huang Y-Y, Sherwood ME, Murray CK, Vrahas MS, Kielian T, Hamblin MR (2013) Blue light eliminates community-acquired methicillin-resistant Staphylococcus aureus in infected mouse skin abrasions. Photomed Laser Surg 31:531–538. https://doi.org/10.1089/pho.2012.3365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Zhang Y, Zhu Y, Gupta A, Huang Y, Murray CK, Vrahas MS, Sherwood ME, Baer DG, Hamblin MR, Dai T (2014) Antimicrobial blue light therapy for multidrug-resistant Acinetobacter baumannii infection in a mouse burn model: implications for prophylaxis and treatment of combat-related wound infections. J Infect Dis 209:1963–1971. https://doi.org/10.1093/infdis/jit842

    Article  CAS  PubMed  Google Scholar 

  112. Amin RM, Bhayana B, Hamblin MR, Dai T (2016) Antimicrobial blue light inactivation of Pseudomonas aeruginosa by photo-excitation of endogenous porphyrins: in vitro and in vivo studies. Lasers Surg Med 48:562–568. https://doi.org/10.1002/lsm.22474

    Article  PubMed  PubMed Central  Google Scholar 

  113. Zhu H, Kochevar IE, Behlau I, Zhao J, Wang F, Wang Y, Sun X, Hamblin MR, Dai T (2017) Antimicrobial blue light therapy for infectious keratitis: ex vivo and in vivo studies. Investig Ophthalmol Vis Sci 58:586–593. https://doi.org/10.1167/iovs.16-20272

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the University of Aveiro and the FCT/MCT for the financial support for the CESAM (UID/50017/2020) and LAQV-REQUIMTE (UIDB/50006/2020), and the FCT project PREVINE (FCT-PTDC/ASP-PES/29576/2017), through national funds and, where applicable, co-financed by the FEDER.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adelaide Almeida .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Gomes, A.T.P.C., Faustino, M.A.F., Neves, M.G.P.M.S., Almeida, A. (2022). Bioluminescent Models to Evaluate the Efficiency of Light-Based Antibacterial Approaches. In: Broekgaarden, M., Zhang, H., Korbelik, M., Hamblin, M.R., Heger, M. (eds) Photodynamic Therapy. Methods in Molecular Biology, vol 2451. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2099-1_34

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-2099-1_34

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-2098-4

  • Online ISBN: 978-1-0716-2099-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics