Let There Be Light! Bioluminescent Imaging to Study Bacterial Pathogenesis in Live Animals and Plants

  • Chapter
  • First Online:
Bioluminescence: Fundamentals and Applications in Biotechnology - Volume 3

Part of the book series: Advances in Biochemical Engineering/Biotechnology ((ABE,volume 154))

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

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** 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. Alexander B, Schnurrenberger PR, Brown RR (1981) Numbers of Brucella abortus in the placenta, umbilicus and fetal fluid of two naturally infected cows. Vet Rec 108:500

    Article  CAS  Google Scholar 

  2. Allen MS, Wilgus JR, Chewning CS, Sayler GS, Simpson ML (2007) A destabilized bacterial luciferase for dynamic gene expression studies. Syst Synth Biol 1:3–9

    Article  Google Scholar 

  3. Andreu N, Zelmer A, Wiles S (2011) Noninvasive biophotonic imaging for studies of infectious disease. FEMS Microbiol Rev 35:360–394

    Article  CAS  Google Scholar 

  4. Carlton WM, Gleason ML, Braun EJ (1998) Ingress of Clavibacter michiganensis subsp. michiganensis into tomato leaves through hydathodes. Phytopathology 88:525–529

    Article  CAS  Google Scholar 

  5. Chabot R, Kloepper JW, Antoun H, Beauchamp CJ (1996) Root colonization of maize and lettuce by bioluminescent Rhizobium leguminosarum biovar phaseoli. Appl Environ Microbiol 62:2767–2772

    CAS  Google Scholar 

  6. Chalupowicz L, Zellermann E-M, Fluegel M, Dror O, Eichenlaub R, Gartemann K-H, Savidor A, Sessa G, Iraki N, Barash I, Manulis-Sasson S (2012) Colonization and movement of GFP labeled Clavibactermichiganensis subsp. michiganensis during tomato infection. Phytopathology 102:23–31

    Article  CAS  Google Scholar 

  7. Chang RJ, Ries SM, Pataky JK (1991) Dissemination of Clavibacter michiganensis subsp. michiganensis by practices used to produce tomato transplants. Phytopathology 81:1276–1281

    Article  Google Scholar 

  8. Cirvilleri G, Lindow SE (1994) Differential expression of genes of Pseudomonas syringae on leaves and in culture evaluated with random genomic lux fusions. Mol Ecol 3:249–257

    Article  CAS  Google Scholar 

  9. Cirvilleri G, BellaP CataraV (2000) Luciferase genes as a marker for Pseudomonas corrugata. J Plant Pathol 82:237–241

    Google Scholar 

  10. 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

    Article  CAS  Google Scholar 

  11. Contag PR (2008) Bioluminescence imaging to evaluate infections and host response in vivo. Methods Mol Biol 415:101–118

    CAS  Google Scholar 

  12. Corbel M (1997) Brucellosis: an overview. Emerg Infect Dis 3:213–221

    Article  CAS  Google Scholar 

  13. Corish P, Tyler-Smith C (1999) Attenuation of green fluorescent protein half-life in mammalian cells. Protein Eng 12:1035–1040

    Article  CAS  Google Scholar 

  14. Delrue RMM-LM, Lestrate P, Danese I, Bielarz V, Mertens P, De Bolle X, Tibor A, Gorvel JP, Letesson JJ (2001) Identification of Brucella spp. genes involved in intracellular trafficking. Cell Microbiol 3:487–497

    Article  CAS  Google Scholar 

  15. De Weger LA, DunbarP MahafeeWF, LugtenbergJJ SaylerGS (1991) Use of bioluminescent markers to detect Pseudomonas spp. in the rhizosphere. Appl Environ Microbiol 57:3641–3644

    Google Scholar 

  16. Engebrecht J, Silverman M (1984) Identification of genes and gene products necessary for bacterial bioluminescence. Proc Natl Acad Sci USA 81:4154–4158

    Article  CAS  Google Scholar 

  17. Eichenlaub R, Gartemann KH (2011) The Clavibacter michiganensis subspecies, molecular investigation of Gram-positive bacterial plant pathogens. Annu Rev Phytopathol 49:445–464

    Article  CAS  Google Scholar 

  18. Essenberg R, Seshadri R, Nelson K, Paulsen I (2002) Sugar metabolism by Brucellae. Vet Microbiol 90:249–261

    Article  CAS  Google Scholar 

  19. European and Mediterranean Plant Protection Organization (2005) Clavibacter michiganensis subsp. michiganensis. EPPO Bull 35:275–283

    Article  Google Scholar 

  20. Fan J, Lamb C, Crooks C (2008) High-throughput quantitative luminescence assay of the growth in planta of Pseudomonas syringae chromosomally tagged with Photorhabdus luminescens luxCDABE. The Plant J 53:393–399

    Article  CAS  Google Scholar 

  21. Fatmi M, Bolkan HA, Schaad NW (1991) Seed treatments for eradicating Clavibacter michiganensis subsp. michiganensis from naturally infected tomato seeds. Plant Dis 75:383–385

    Article  CAS  Google Scholar 

  22. Foulongne VBG, Cazevieille C, Michaux-Charachon S, O’Callaghan D (2000) Identification of Brucella suis genes affecting intracellular survival in an in vitro human macrophage infection model by signature-tagged transposon mutagenesis. Infect Immun 68:1297–1303

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Franz DR (1999) Foreign animal disease agents as weapons in biological warfare. Ann NY Acad Sci 894:100–104

    Article  CAS  Google Scholar 

  26. Fukui R, McElhaney R, Fukui H, Alvarez AM, Nelson SC (1996) Relationship between symptom development and actual sites of infection in leaves of anthurium inoculated with a bioluminescent strain of Xanthomonas campestris pv. dieffenbachiae. Appl Environ Microbiol 62:1021–1028

    CAS  Google Scholar 

  27. Gartemann KH, Kirchner O, Engemann J, Gräfen I, Eichenlaub R, Burger A (2003) Clavibacter michiganensis subsp. michiganensis: first steps in the understanding of virulence of a Gram-positive phytopathogenic bacterium. J Biotechnol 106:179–191

    Article  CAS  Google Scholar 

  28. Gitaitis RD, Beaver RW, Voloudakis AE (1991) Detection of Clavibacter michiganensis subsp. michiganensis in symptomless tomato transplants. Plant Dis 75:834–838

    Article  Google Scholar 

  29. Gleason ML, Ricker MD, Gitaitis RD (1993) Recent progress in understanding and controlling bacterial canker of tomato in Eastern North America. Plant Dis 77:1069–1076

    Article  Google Scholar 

  30. Glomski IJ, Piris-Gimenez A, Huerre M, Mock M, Goossens PL (2007) Primaryinvolvement of pharynx and peyer’s patch in inhalational and intestinal anthrax. PLoS Pathog 3:e76

    Article  CAS  Google Scholar 

  31. Glynn M, Lynn TV (2008) Brucellosis. J Amer Vet Med Assoc 233:900–908

    Article  Google Scholar 

  32. Greer LF III, Szalay AA (2002) Imaging of light emission from the expression ofluciferases in living cells and organisms: a review. Luminescence 17:43–74

    Article  CAS  Google Scholar 

  33. Griffiths MW (2000) How novel methods can help discover more information about foodborne pathogens. Can J Infect Dis 11:142–153

    CAS  Google Scholar 

  34. Hardy J, Francis KP, DeBoer M, Chu P, Gibbs K, Contag CH (2004) Extracellularreplication of Listeria monocytogenes in the murine gall bladder. Science 303:851–853

    Article  CAS  Google Scholar 

  35. Hong PCTR, Ficht TA (2000) Identification of genes required for chronic persistence of Brucella abortus in mice. Infect Immun 68:4102–4107

    Article  CAS  Google Scholar 

  36. Jahr H, Burger A, Bahro R, Eichenlaub R, Ahlemeyer J (1999) Interactions between Clavibacter michiganensis and its host plants. Environ Microbiol 1:113–118

    Article  CAS  Google Scholar 

  37. Kamoun S, Kado CI (1990) A plant-inducible gene of Xanthomonas campestris pv. campestris encodes an exocellular component required for growth in the host and hypersensitivity on nonhosts. J Bacteriol 172:5165–5172

    CAS  Google Scholar 

  38. Kassem II, Sanad Y, Gangaiah D, Lilburn M, Lejeune J, Rajashekara G (2010) Use of bioluminescence imaging to monitor Campylobacter survival in chicken litter. J Appl Microbiol 109:1988–1997

    Article  CAS  Google Scholar 

  39. Kaufmann AF, Meltzer MI, Schmid GP (1997) The economic impact of a bioterrorist attack: are prevention and postattack intervention programs justifiable? Emerg Infect Dis 3:83–94

    Article  CAS  Google Scholar 

  40. Kirchner O, Gartemann KH, Zellermann EM, Eichenlaub R, Burger A (2001) A highlyefficient transposon mutagenesis system for the tomato pathogen Clavibacter michiganensis subsp. michiganensis. Mol Plant Microbe Interact 14:1312–1318

    Article  CAS  Google Scholar 

  41. Ko J, Gendron-Fitzpatrick A, Ficht TA, Splitter GA (2002) Virulence criteria for Brucella abortus strains as determined by interferon regulatory factor 1-deficient mice. Infect Immun 70:7004–7012

    Article  CAS  Google Scholar 

  42. Ko J, Gendron-Fitzpatrick A, Splitter GA (2002) Susceptibility of IFN regulatory factor-1 and IFN consensus sequence binding protein-deficient mice to brucellosis. J Immunol 168:2433–2440

    Article  CAS  Google Scholar 

  43. Koc Z, Turunc T, Boga C (2007) Gonadal brucellar abscess: imaging and clinical findings in 3 cases and review of the literature. J Clin Ultrasound 35:395–400

    Article  Google Scholar 

  44. Kulkarni R, Chunchanur SK, Ajantha GS, Shubhada C, Jain P (2009) Presumptive diagnosis of brucella epididymoorchitis by modified cold ZN staining of testicular pus sample. Indian J Med Res 130:484–486

    CAS  Google Scholar 

  45. Li Z, Szittner R, Meighen EA (1993) Subunit interactions and the role of the luxA polypeptide in controlling thermal stability and catalytic properties in recombinant luciferase hybrids. Biochim Biophys Acta 1158:137–145

    Article  CAS  Google Scholar 

  46. Maudlin I, Weber S (2006) The control of neglected zoonotic diseases: a route to poverty alleviation. WHO, Geneva

    Google Scholar 

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

    CAS  Google Scholar 

  48. Meletzus D, Dreier J, Bermpohl A, Eichenlaub R (1993) Evidence for plasmid-encoded virulence factors in the phytopathogenic bacterium Clavibacter michiganensis subsp. michiganensis NCPPB382. J Bacteriol 175:2131–2136

    CAS  Google Scholar 

  49. Miller SA, Rowe RC, Riedel RM (1996) Bacterial spot, speck, and canker of tomatoes HYG-3120-96. Ohio State Univ Extension

    Google Scholar 

  50. O’Callaghan DCC, Allardet-Servent A, Boschiroli ML, Bourg G, Foulongne V, Frutos P, Kulakov Y, Ramuz M (1999) A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol Microbiol 33:1210–1220

    Article  Google Scholar 

  51. Paynter CD, Arnold DL, Salisbury VC, Jackson RW (2006) The use of bioluminescence for monitoring in planta growth dynamics of a Pseudomonas syringae plant pathogen. Eur J Plant Pathol 115:363–366

    Article  Google Scholar 

  52. Petersen E, Rajashekara G, Sanakkayala N, Eskra L, Harms J, Splitter G (2013) Erythritol triggers expression of virulence traits in Brucella melitensis. Microbes Infect 15:440–449

    Article  CAS  Google Scholar 

  53. Radhakrishnan GKYQ, Harms JS, Splitter GA (2009) Brucella TIR domain-containing protein mimics properties of the toll-like receptor adaptor protein TIRAP. J Biol Chem 284:9892–9898

    Article  CAS  Google Scholar 

  54. Rajashekara G, Glover DA, Banai M, O’Callaghan D, Splitter GA (2006) Attenuated bioluminescent Brucella melitensis mutants GR019 (virB4), GR024 (galE), and GR026 (BMEI1090-BMEI1091) confer protection in mice. Infect Immun 74:2925–2936

    Article  CAS  Google Scholar 

  55. Rajashekara G, Glover DA, Krepps M, Splitter GA (2005) Temporal analysis of pathogenic events in virulent and avirulent Brucella melitensis infections. Cell Microbiol 7:1459–1473

    Article  CAS  Google Scholar 

  56. Rajashekara G, Krepps M, Eskra L, Mathison A, Montgomery A, Ishii Y, Splitter G (2005) Unraveling Brucella genomics and pathogenesis in immunocompromised IRF-1-/- mice. Am J Reprod Immunol 54:358–368

    Article  CAS  Google Scholar 

  57. Ricker MD, Riedel RM (1993) Effect of secondary spread of Clavibacter michiganensis subsp. michiganensis on yield of northern processing tomatoes. Plant Dis 77:364–366

    Article  Google Scholar 

  58. Ritchie JM, Campbell GR, Shepherd J, Beaton Y, Jones D, Killham K, Artz RR (2003) A stable bioluminescent construct of Escherichia coli O157:H7 for hazard assessments of long-term survival in the environment. Appl Environ Microbiol 69:3359–3367

    Article  CAS  Google Scholar 

  59. Samartino L, Enright FM (1993) Pathogenesis of abortion of bovine brucellosis. Comp Immunol Microbiol Infect Dis 16:95–101

    Article  CAS  Google Scholar 

  60. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2:905–909

    Article  CAS  Google Scholar 

  61. Sharabani G, Manulis-Sasson S, Borenstein M, Shulhani R, Chalupowicz L, Lofthouse M, Shtienberg D (2013) The significance of guttation inthe secondary spread of Clavibactermichiganensis in tomato greenhouses. Plant Pathol 62:578–586

    Article  Google Scholar 

  62. Sharabani G, Shtienberg D, Borenstein M, Shulhani R, Sofer M, Lofthouse M, Chalupowicz L, Barel V, Manulis-Sasson S (2012) Effects of plant age on disease development and virulence of Clavibacter michiganensis subsp. michiganensis on tomato. Plant Pathology 62:1114–1122

    Article  CAS  Google Scholar 

  63. Shaw JJ, DaneF GeigerD, Kloepper JW (1992) Use of bioluminescence for detection of genetically engineered microorganisms released into the environment. Appl Environ Microbiol 58:267–273

    CAS  Google Scholar 

  64. Shaw JJ, Kado CI, Settles LG (1988) Transposon Tn4431 mutagenesis of Xanthomonas campestris pv. campestris: characterization of a non pathogenic mutant and cloning of a locus for pathogenicity. Mol Plant-Microbe Interact 1:39–45

    Article  Google Scholar 

  65. Shirakawa T, Sasaki T, Ozaki K (1991) Ecology and control of tomato bacterial canker and detection methods of its pathogen. Jpn Agric Res Q 25:27–32

    Google Scholar 

  66. Sieira R, Comerci DJ, Sanchez DO, Ugalde RA (2000) A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular multiplication. J Bacteriol 182:4849–4855

    Article  CAS  Google Scholar 

  67. Smith H, Williams AE, Pearce JH, Keppie J, Harris-Smith PW, Fitz-George RB, Witt K (1962) Foetal erythritol: a cause of the localization of Brucella abortus in bovine contagious abortion. Nature 193:47–49

    Article  CAS  Google Scholar 

  68. Strider DL (1969) Bacterial canker of tomato, a literature review and bibliography. NC Agric Exp Stn Tech Bull 193:1–80

    Google Scholar 

  69. 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 

  70. Tancos MA, Chalupowicz L, Barash I, Manulis-Sasson S, Smart CD (2013) Tomato fruit and seed colonization by Clavibacter michiganensis subsp. michiganensis through external and internal routes. Appl Env Microbiol 79:6948–6957

    Article  CAS  Google Scholar 

  71. Thorn RM, Nelson SM, Greenman J (2007) Use of a bioluminescent Pseudomonas aeruginosa strain within an in vitro microbiological system, as a model of wound infection, to assess the antimicrobial efficacy of wound dressings by monitoring light production. Antimicrob Agents Chemother 51:3217–3224

    Article  CAS  Google Scholar 

  72. Tsiantos J (1987) Transmission of bacterium Corynebacterium michiganense pv. michiganense by seeds. J Phytopathology 119:142–146

    Article  Google Scholar 

  73. Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67:509–544

    Article  CAS  Google Scholar 

  74. Vallejo JG, Stevens AM, Dutton RV, Kaplan SL (1996) Hepatosplenic abscesses due to Brucella melitensis: report of a case involving a child and review of the literature. Clin Infect Dis 22:485–489

    Article  CAS  Google Scholar 

  75. Verkhusha VV, Lukyanov KA (2004) The molecular properties and applications of Anthozoa fluorescent proteins and chromoproteins. Nat Biotechnol 22:289–296

    Article  CAS  Google Scholar 

  76. Waidmann MS, Bleichrodt FS, Laslo T, Riedel CU (2011) Bacterial luciferasereporters: the Swiss army knife of molecular biology. Bioeng Bugs 2:8–16

    Article  Google Scholar 

  77. Widder EA (2010) Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science 328:704–708

    Article  CAS  Google Scholar 

  78. Wiles S, Clare S, Harker J, Huett A, Young D, Dougan G, Frankel G (2004) Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol 6:963–972

    Article  CAS  Google Scholar 

  79. Xu X, Miller SA, Baysal-Gurel F, Gartemann KH, Eichenlaub R, Rajashekara G (2010) Bioluminescence imaging of Clavibacter michiganensis subsp. michiganensis infection of tomato seeds and plants. Appl Environ Microbiol 76:3978–3988

    Article  CAS  Google Scholar 

  80. Xu X, Rajashekara G, Paul PA, Miller SA (2012) Colonization of tomato seedlings by bioluminescent Clavibacter michiganensis subsp. michiganensis under different humidity regimes. Phytopathology. 102:177–184

    Article  Google Scholar 

  81. Young E (1995) An overview of human brucellosis. Clin Infect Dis 21:283–289

    Article  CAS  Google Scholar 

Download references

Acknowledgment

Research in the Rajashekara and Miller laboratories is supported by funds from the Agriculture and Food Research Initiative (AFRI, USDA), the Specialty Crops Research Initiative (SCRI-2010-600-25320, USDA), the Ohio Agricultural Research and Development Center, and the Ohio State University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gireesh Rajashekara .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Kassem, I.I., Splitter, G.A., Miller, S., Rajashekara, G. (2014). Let There Be Light! Bioluminescent Imaging to Study Bacterial Pathogenesis in Live Animals and Plants. In: Thouand, G., Marks, R. (eds) Bioluminescence: Fundamentals and Applications in Biotechnology - Volume 3. Advances in Biochemical Engineering/Biotechnology, vol 154. Springer, Cham. https://doi.org/10.1007/10_2014_280

Download citation

Publish with us

Policies and ethics

Navigation