Photorhabdus Luminescens: Virulent Properties and Agricultural Applications

Elizabeth Gerdes; Devang Upadhyay; Sivanadane Mandjiny; Rebecca Bullard-Dillard; Meredith Storms; Michael Menefee; Leonard D. Holmes

doi:doi:10.11648/j.ajaf.20150305.12

Photorhabdus Luminescens: Virulent Properties and Agricultural Applications

Elizabeth Gerdes, Devang Upadhyay, Sivanadane Mandjiny, Rebecca Bullard-Dillard, Meredith Storms, Michael Menefee, Leonard D. Holmes

Published in American Journal of Agriculture and Forestry (Volume 3, Issue 5)

Received: 21 July 2015 Accepted: 1 August 2015 Published: 10 August 2015

Views: Downloads:

Download PDF

Share This Article

Twitter
Linked In
Facebook

Abstract

Photorhabdus luminescens is a gram-negative, bioluminescent bacterium from the family Enterobacteriaceae which has been found in countries across the globe. It is part of a symbiotic relationship with, and resides in the gut of the entomopathogenic nematode, Heterorhabditis bacteriophora. Photorhabdus luminescens produces many virulence factors, toxin complexes and antimicrobial compounds which allow it to kill insect hosts while simultaneously protecting itself and its symbiotic partner from other bacteria. Due to its virulent properties and the ability to infect a wide range of insect hosts, the Photorhabdus luminescens-Heterorhabditis bacteriophora relationship is a promising candidate for agricultural use as a mass produced biological control agent. The use of Photorhabdus luminescens has been deemed safe towards humans, animals, non-target insects, plants, as well as the environment. The entomopathogenic nematode is also exempt from registration regulations in most countries. The significance of Photorhabdus luminescens is the potential for an insecticide that allows different species of insect pests to be effectively controlled by a single natural product rather than multiple chemical products. The purpose of this review is to provide readers with an overview of the safety of Photorhabdus luminescens to the community and environment, to inform readers of the virulence factors associated with the bacteria, and to outline the potential the product possesses as a mass produced biological control agent.

Published in	American Journal of Agriculture and Forestry (Volume 3, Issue 5)
DOI	10.11648/j.ajaf.20150305.12
Page(s)	171-177
Creative Commons	This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.
Copyright	Copyright © The Author(s), 2015. Published by Science Publishing Group

Keywords

Photorhabdus Luminescens, Heterorhabditis Bacteriophora, Symbiosis, Bioluminescence, Biocontrol Agent

References

[1]	Daborn, P., Waterfield, N., Blight, M. A. and Ffrench-Constant, R. H. (2001) Measuring Virulence Factor Expression by the Pathogenic Bacterium Photorhabdus luminescens in Culture and during Insect Infection. Journal of Bacteriology, 183(20): 5834-5839.
[2]	Singh, S., Moreau, E., Inman, F. and Holmes, L. D. (2011) Characterization of Photorhabdus luminescens Growth for the Rearing of the Bacterial Nematode Heterorhabditis bacteriophora. Indian Journal of Microbial, 52(3): 325-331.
[3]	Ehlers, R. (2001) Mass production of entomopathogenic nematodes from plant protection. Applied Microbiology and Biotechnology, 56: 623-633.
[4]	Kooliyottil. R, Upadhyay, D., Inman, III F., Mandjiny, S. and Holmes, L.D. (2013) A Comparative Analysis of Entomoparasitic Nematodes Heterorhabditis bacteriophora and Steinernema carpocapsae. Open Journal of Animal Science, 3(4): 326-333.
[5]	Inman, F. L. III, Singh, S. and Holmes, L. D. (2012) Mass Production of the Beneficial Nematode Heterorhabditis bacteriophora and Its Bacterial Symbiont Photorhabdus luminescens. Indian Journal of Microbial, 52(3): 316-324.
[6]	Frost, S. and Clarke, D. (2002) Bacteria-Nematode Symbiosis. In Gaugler R. (Ed.) Entomopathogenic Nematology (pp 57-77).
[7]	Marokhazi, J., Waterfield, N., LeGoff, G., Feil, E., Stabler, R., Hinds, J., Fodor, A. and Ffrench-Constant, R. H. (2003) Using a DNA Microarray To Investigate the Distribution of Insect Virulence Factors in Strains of Photorhabdus Bacteria. Journal of Microbiology, 185(15): 4648-4656.
[8]	Ffrench-Constant, R. H., Waterfield, N., Burland, V., Perna, N. T., Daborn, P. J., Bowen, D. and Blattner, F. R. (2000) A Genomic Sample Sequence of the Entomopathogenic Bacterium Photorhabdus luminescens W14: Potential Implications for Virulence. Applied and Environmental Microbiology, 66(8): 3310–3329.
[9]	Schmidt, T. M., Kopecky, K. and Nealsoni, K. H. (1989) Bioluminescence of the Insect Pathogen Xenorhabdus luminescens. Applied and Environmental Microbiology, 55(10): 2607-2612.
[10]	Daborn, P. J., Waterfield, N., Silva, C. P., Au, C. P. Y., Sharma, S. and Ffrench-Constant, R.H. (2002) A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proceedings of the National Academy of Sciences, 99 (16): 10742-10747.
[11]	Patterson, W., Upadhyay, D., Mandjiny, S., Bullard-Dillard, R., Storms, M., Menefee, M. and Holmes, L. D. (2015) Attractant Role of Bacterial Bioluminescence of Photorhabdus luminescens on a Galleria mellonella Model. American Journal of Life Sciences, 3(4): 290-294.
[12]	Ciche, T. and Ensign, J. C. (2002) For the Insect Pathogen Photorhabdus luminescens, Which End of a Nematode Is Out? Applied and Environmental Microbiology, 69(4): 1890-1897.
[13]	Guo, L., Fatig III, R. O., Orr, G. L., Schafer, B. W., Strickland, J. A., Sukhapinda, K., Woodsworth, A. T. and Petell, J. K. (1999) Photorhabdus luminescens W-14 Insecticidal Activity Consists of at Least Two Similar but Distinct Proteins. The Journal of Biological Chemistry, 274(14): 9836-9842.
[14]	Bowen, D. J. and Ensign, J. C. (1998) Purification and Characterization of a High-Molecular-Weight Insecticidal Protein Complex Produced by the Entomopathogenic Bacterium Photorhabdus luminescens. Applied and Environmental Microbiology, 64(8): 3029–3035.
[15]	Dowds, B. C.A. and Peters, A. (2002) Virulence Mechanisms. In Gaugler R. (Ed.) Entomopathogenic Nematology (pp 79-98).
[16]	Derzelle, S., Turlin, E., Duchaud, E., Pages, S., Kunst, F., Givaudan, A. and Danchin, A. (2003) The PhoP-PhoQ Two-Component Regulatory System of Photorhabdus luminescens Is Essential for Virulence in Insects. Journal of Microbiology, 186(5): 1270-1279.
[17]	Brillard, J., Duchaud, E., Boemare, N., Kunst, F. and Givaudan, A. (2002) The PhIA Hemolysin from the Entomopathogenic Bacterium Photorhabdus luminescens Belongs to the Two-Partner Secretion Family of Hemolysins. Journal of Bacteriology, 184(14): 3871-3878.
[18]	Ffrench-Constant, R. H., Dowling, A. and Waterfield, N. R. (2007) Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture. Toxicon, 49: 436-451.
[19]	Waterfield, N., Bowen, D. J., Fetherston, J. D., Perry, R. D. and Ffrench-Constant, R. H. (2001) The tc genes of Photorhabdus: a growing family. Trends in Microbiology, 9(4): 185-191.
[20]	Bowen, D., Rocheleau, T. A., Blackburn, M., Andreev, O., Golubeva, E., Bhartia, R. and Ffrench-Constant, R. H. (1998) Insecticidal Toxins from the Bacterium Photorhabdus luminescens. Science Magazine, 280: Pages 2129-2132.
[21]	Blackburn, M., Golubeva, E., Bowen, D. and Ffrench-Constant, R. (1998) A Novel Insecticidal Toxin from Photorhabdus luminescens, Toxin Complex a (Tca), and Its Histopathological Effects on the Midgut of Manduca sexta. Applied and Environmental Microbiology, 64(8): 3036-3041.
[22]	Ffrench-Constant, R. H. and Bowen, D. J. (2000) Novel insecticidal toxins from nematode-symbiotic bacteria. Cellular and Molecular Life Sciences, 57: 828-833.
[23]	Pinheiro, V. and Ellar, D. J. (2007) Expression and insecticidal activity of Yersinia pseudotuberculosis and Photorhabdus luminescens toxin complex proteins. Cellular Microbiology, 9: 2372-2380.
[24]	Blackburn, M. B., Domek, J. M., Gelman, D. B. and Hu, J. S. (2005) The broadly insecticidal Photorhabdus luminescens toxin complex a (Tca): Activity against the Colorado potato beetle, Leptinotarsa decemlineata, and sweet potato whitefly, Bemisia tabaci. Journal of Insect Science, 5(32): 1-11.
[25]	Rodou, A., Ankrah, D. O. and Stathopoulos, C. (2010) Toxins and Secretion Systems of Photorhabdus luminescens. Toxins, 2: 1250-1264.
[26]	Bondi, M., Messi, P., Sabia, C., Baccarani C. M. and Manicardi, G. (1998) Antimicrobial Properties and Morphological Characteristics Of Two Photorhabdus luminescens strains. Microbiologica, 22: 117-127.
[27]	Derzelle, S., Duchaud, E., Kunst, F., Danchin, A. and Bertin, P. (2002) Identification, Characterization, and Regulation of a Cluster of Genes Involved in Carbapenem Biosynthesis in Photorhabdus luminescens. Applied and Environmental Microbiology, 68(8): 3780–3789.
[28]	Li, J., Chen, G., Wu, H. and Webster, J. M. (1995) Identification of Two Pigments and a Hydroxystilbene Antibiotic from Photorhabdus luminescens. Applied and Environmental Microbiology, 61(12): 4329–4333.
[29]	Peel, M. M., Alfredson, D. A., Gerrard, J. G., Davis, J. M., Robson, J. M., McDougall, R. J., Scullie, B. L. and Akhurst, R. J. (1999) Isolation, Identification, and Molecular Characterization of Strains of Photorhabdus luminescens from Infected Humans in Australia. Journal of Clinical Microbiology, 37(11): 3647–3653.
[30]	Morgan, J.A.W., Kuntzelmann, V., Tavernor, S., Ousley, M.A. and Winstanley, C. (1997) Survival of Xenorhabdus nematophilus and Photorhabdus luminescens in water and soil. Journal of Applied Microbiology, 83: 665-670.
[31]	Ferry, N., Edwards, M. G., Gatehouse, J. A. and Gatehouse, A. M.R. (2004) Plant-insect interactions: molecular approaches to insect resistance. Current Opinion in Biotechnology, 15: 155-161.
[32]	Hazir, S., Kaya, H. K., Stock, S. P. and Keckun, N. (2003) Entomopathogenic Nematodes (Steinernematidae and Heterorhabditidae) for Biological Control of Soil Pests. Turkish Journal of Biology, 27:181-202.
[33]	Ehlers, R., Oestergaard, J., Hollmer, S., Wingen, M. and Strauch, O. (2005) Genetic selection for heat tolerance and low temperature activity of the entomopathogenic nematode-bacterium complex Heterorhabditis bacteriophora-Photorhabdus luminescens. BioControl, 50: 699-716.
[34]	Upadhyay, D., Kooliyottil, R., Mandjiny, S., Inman, III F. and Holmes, L. (2013) Mass production of the beneficial nematode Steinernema carpocapsae utilizing a fed-batch culturing process. EScience Journal of Plant Pathology, 02(01): 52-58.
[35]	Mahajan-Miklos, S., Rahme, L. G. and Ausubel, F. M. (2000) Elucidating the molecular mechanisms of bacterial virulence using non-mammalian hosts. Molecular Microbiology, 37: 981-988.
[36]	Eleftherianos, I., Marokhazi, J., Millichap, P.J., Hodgkinson, A.J., Sriboonlert, A., Ffrench-Constant, R.H. and Reynolds, S.E. (2006) Prior infection of Manduca sexta with non-pathogenic Escherichia coli elicits immunity to pathogenic Photorhabdus luminescens: Roles of immune-related proteins shown by RNA interference. Insect Biochemistry and Molecular Biology, 36: 517-525.

Cite This Article

Plain Text BibTeX RIS

APA Style

Elizabeth Gerdes, Devang Upadhyay, Sivanadane Mandjiny, Rebecca Bullard-Dillard, Meredith Storms, et al. (2015). Photorhabdus Luminescens: Virulent Properties and Agricultural Applications. American Journal of Agriculture and Forestry, 3(5), 171-177. https://doi.org/10.11648/j.ajaf.20150305.12

Copy | Download

ACS Style

Elizabeth Gerdes; Devang Upadhyay; Sivanadane Mandjiny; Rebecca Bullard-Dillard; Meredith Storms, et al. Photorhabdus Luminescens: Virulent Properties and Agricultural Applications. Am. J. Agric. For. 2015, 3(5), 171-177. doi: 10.11648/j.ajaf.20150305.12

Copy | Download

AMA Style

Elizabeth Gerdes, Devang Upadhyay, Sivanadane Mandjiny, Rebecca Bullard-Dillard, Meredith Storms, et al. Photorhabdus Luminescens: Virulent Properties and Agricultural Applications. Am J Agric For. 2015;3(5):171-177. doi: 10.11648/j.ajaf.20150305.12

Copy | Download

@article{10.11648/j.ajaf.20150305.12,
  author = {Elizabeth Gerdes and Devang Upadhyay and Sivanadane Mandjiny and Rebecca Bullard-Dillard and Meredith Storms and Michael Menefee and Leonard D. Holmes},
  title = {Photorhabdus Luminescens: Virulent Properties and Agricultural Applications},
  journal = {American Journal of Agriculture and Forestry},
  volume = {3},
  number = {5},
  pages = {171-177},
  doi = {10.11648/j.ajaf.20150305.12},
  url = {https://doi.org/10.11648/j.ajaf.20150305.12},
  eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.ajaf.20150305.12},
  abstract = {Photorhabdus luminescens is a gram-negative, bioluminescent bacterium from the family Enterobacteriaceae which has been found in countries across the globe. It is part of a symbiotic relationship with, and resides in the gut of the entomopathogenic nematode, Heterorhabditis bacteriophora. Photorhabdus luminescens produces many virulence factors, toxin complexes and antimicrobial compounds which allow it to kill insect hosts while simultaneously protecting itself and its symbiotic partner from other bacteria. Due to its virulent properties and the ability to infect a wide range of insect hosts, the Photorhabdus luminescens-Heterorhabditis bacteriophora relationship is a promising candidate for agricultural use as a mass produced biological control agent. The use of Photorhabdus luminescens has been deemed safe towards humans, animals, non-target insects, plants, as well as the environment. The entomopathogenic nematode is also exempt from registration regulations in most countries. The significance of Photorhabdus luminescens is the potential for an insecticide that allows different species of insect pests to be effectively controlled by a single natural product rather than multiple chemical products. The purpose of this review is to provide readers with an overview of the safety of Photorhabdus luminescens to the community and environment, to inform readers of the virulence factors associated with the bacteria, and to outline the potential the product possesses as a mass produced biological control agent.},
 year = {2015}
}

Copy | Download

TY  - JOUR
T1  - Photorhabdus Luminescens: Virulent Properties and Agricultural Applications
AU  - Elizabeth Gerdes
AU  - Devang Upadhyay
AU  - Sivanadane Mandjiny
AU  - Rebecca Bullard-Dillard
AU  - Meredith Storms
AU  - Michael Menefee
AU  - Leonard D. Holmes
Y1  - 2015/08/10
PY  - 2015
N1  - https://doi.org/10.11648/j.ajaf.20150305.12
DO  - 10.11648/j.ajaf.20150305.12
T2  - American Journal of Agriculture and Forestry
JF  - American Journal of Agriculture and Forestry
JO  - American Journal of Agriculture and Forestry
SP  - 171
EP  - 177
PB  - Science Publishing Group
SN  - 2330-8591
UR  - https://doi.org/10.11648/j.ajaf.20150305.12
AB  - Photorhabdus luminescens is a gram-negative, bioluminescent bacterium from the family Enterobacteriaceae which has been found in countries across the globe. It is part of a symbiotic relationship with, and resides in the gut of the entomopathogenic nematode, Heterorhabditis bacteriophora. Photorhabdus luminescens produces many virulence factors, toxin complexes and antimicrobial compounds which allow it to kill insect hosts while simultaneously protecting itself and its symbiotic partner from other bacteria. Due to its virulent properties and the ability to infect a wide range of insect hosts, the Photorhabdus luminescens-Heterorhabditis bacteriophora relationship is a promising candidate for agricultural use as a mass produced biological control agent. The use of Photorhabdus luminescens has been deemed safe towards humans, animals, non-target insects, plants, as well as the environment. The entomopathogenic nematode is also exempt from registration regulations in most countries. The significance of Photorhabdus luminescens is the potential for an insecticide that allows different species of insect pests to be effectively controlled by a single natural product rather than multiple chemical products. The purpose of this review is to provide readers with an overview of the safety of Photorhabdus luminescens to the community and environment, to inform readers of the virulence factors associated with the bacteria, and to outline the potential the product possesses as a mass produced biological control agent.
VL  - 3
IS  - 5
ER  -

Copy | Download

Author Information

Elizabeth Gerdes

Sartorius Stedim Biotechnology Laboratory, Biotechnology Research and Training Center, The University of North Carolina at Pembroke, Pembroke, USA
Devang Upadhyay

Sartorius Stedim Biotechnology Laboratory, Biotechnology Research and Training Center, The University of North Carolina at Pembroke, Pembroke, USA
Sivanadane Mandjiny

Department of Chemistry and Physics, The University of North Carolina at Pembroke, Pembroke, USA
Rebecca Bullard-Dillard

School of Graduate Studies and Research, The University of North Carolina at Pembroke, Pembroke, USA
Meredith Storms

College of Arts & Sciences, The University of North Carolina at Pembroke, Pembroke, USA
Michael Menefee

Thomas Family Center for Entrepreneurship, The University of North Carolina at Pembroke, Pembroke, USA
Leonard D. Holmes

Sartorius Stedim Biotechnology Laboratory, Biotechnology Research and Training Center, The University of North Carolina at Pembroke, Pembroke, USA

Download PDF

Sections

Plain Text BibTeX RIS

APA Style

Elizabeth Gerdes, Devang Upadhyay, Sivanadane Mandjiny, Rebecca Bullard-Dillard, Meredith Storms, et al. (2015). Photorhabdus Luminescens: Virulent Properties and Agricultural Applications. American Journal of Agriculture and Forestry, 3(5), 171-177. https://doi.org/10.11648/j.ajaf.20150305.12

Copy | Download

ACS Style

Elizabeth Gerdes; Devang Upadhyay; Sivanadane Mandjiny; Rebecca Bullard-Dillard; Meredith Storms, et al. Photorhabdus Luminescens: Virulent Properties and Agricultural Applications. Am. J. Agric. For. 2015, 3(5), 171-177. doi: 10.11648/j.ajaf.20150305.12

Copy | Download

AMA Style

Elizabeth Gerdes, Devang Upadhyay, Sivanadane Mandjiny, Rebecca Bullard-Dillard, Meredith Storms, et al. Photorhabdus Luminescens: Virulent Properties and Agricultural Applications. Am J Agric For. 2015;3(5):171-177. doi: 10.11648/j.ajaf.20150305.12

Copy | Download

@article{10.11648/j.ajaf.20150305.12,
  author = {Elizabeth Gerdes and Devang Upadhyay and Sivanadane Mandjiny and Rebecca Bullard-Dillard and Meredith Storms and Michael Menefee and Leonard D. Holmes},
  title = {Photorhabdus Luminescens: Virulent Properties and Agricultural Applications},
  journal = {American Journal of Agriculture and Forestry},
  volume = {3},
  number = {5},
  pages = {171-177},
  doi = {10.11648/j.ajaf.20150305.12},
  url = {https://doi.org/10.11648/j.ajaf.20150305.12},
  eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.ajaf.20150305.12},
  abstract = {Photorhabdus luminescens is a gram-negative, bioluminescent bacterium from the family Enterobacteriaceae which has been found in countries across the globe. It is part of a symbiotic relationship with, and resides in the gut of the entomopathogenic nematode, Heterorhabditis bacteriophora. Photorhabdus luminescens produces many virulence factors, toxin complexes and antimicrobial compounds which allow it to kill insect hosts while simultaneously protecting itself and its symbiotic partner from other bacteria. Due to its virulent properties and the ability to infect a wide range of insect hosts, the Photorhabdus luminescens-Heterorhabditis bacteriophora relationship is a promising candidate for agricultural use as a mass produced biological control agent. The use of Photorhabdus luminescens has been deemed safe towards humans, animals, non-target insects, plants, as well as the environment. The entomopathogenic nematode is also exempt from registration regulations in most countries. The significance of Photorhabdus luminescens is the potential for an insecticide that allows different species of insect pests to be effectively controlled by a single natural product rather than multiple chemical products. The purpose of this review is to provide readers with an overview of the safety of Photorhabdus luminescens to the community and environment, to inform readers of the virulence factors associated with the bacteria, and to outline the potential the product possesses as a mass produced biological control agent.},
 year = {2015}
}

Copy | Download

TY  - JOUR
T1  - Photorhabdus Luminescens: Virulent Properties and Agricultural Applications
AU  - Elizabeth Gerdes
AU  - Devang Upadhyay
AU  - Sivanadane Mandjiny
AU  - Rebecca Bullard-Dillard
AU  - Meredith Storms
AU  - Michael Menefee
AU  - Leonard D. Holmes
Y1  - 2015/08/10
PY  - 2015
N1  - https://doi.org/10.11648/j.ajaf.20150305.12
DO  - 10.11648/j.ajaf.20150305.12
T2  - American Journal of Agriculture and Forestry
JF  - American Journal of Agriculture and Forestry
JO  - American Journal of Agriculture and Forestry
SP  - 171
EP  - 177
PB  - Science Publishing Group
SN  - 2330-8591
UR  - https://doi.org/10.11648/j.ajaf.20150305.12
AB  - Photorhabdus luminescens is a gram-negative, bioluminescent bacterium from the family Enterobacteriaceae which has been found in countries across the globe. It is part of a symbiotic relationship with, and resides in the gut of the entomopathogenic nematode, Heterorhabditis bacteriophora. Photorhabdus luminescens produces many virulence factors, toxin complexes and antimicrobial compounds which allow it to kill insect hosts while simultaneously protecting itself and its symbiotic partner from other bacteria. Due to its virulent properties and the ability to infect a wide range of insect hosts, the Photorhabdus luminescens-Heterorhabditis bacteriophora relationship is a promising candidate for agricultural use as a mass produced biological control agent. The use of Photorhabdus luminescens has been deemed safe towards humans, animals, non-target insects, plants, as well as the environment. The entomopathogenic nematode is also exempt from registration regulations in most countries. The significance of Photorhabdus luminescens is the potential for an insecticide that allows different species of insect pests to be effectively controlled by a single natural product rather than multiple chemical products. The purpose of this review is to provide readers with an overview of the safety of Photorhabdus luminescens to the community and environment, to inform readers of the virulence factors associated with the bacteria, and to outline the potential the product possesses as a mass produced biological control agent.
VL  - 3
IS  - 5
ER  -

Copy | Download