Cell Stress and Chaperones

, 14:603 | Cite as

Ingestion of bacteria overproducing DnaK attenuates Vibrio infection of Artemia franciscana larvae

  • Yeong Yik Sung
  • Till Dhaene
  • Tom Defoirdt
  • Nico Boon
  • Thomas H. MacRae
  • Patrick Sorgeloos
  • Peter Bossier
Original Paper
First Online:
Received:
Accepted:

Abstract

Feeding of bacterially encapsulated heat shock proteins (Hsps) to invertebrates is a novel way to limit Vibrio infection. As an example, ingestion of Escherichia coli overproducing prokaryotic Hsps significantly improves survival of gnotobiotically cultured Artemia larvae upon challenge with pathogenic Vibrio campbellii. The relationship between Hsp accumulation and enhanced resistance to infection may involve DnaK, the prokaryotic equivalent to Hsp70, a major molecular chaperone in eukaryotic cells. In support of this proposal, heat-stressed bacterial strains LVS 2 (Bacillus sp.), LVS 3 (Aeromonas hydrophila), LVS 8 (Vibrio sp.), GR 8 (Cytophaga sp.), and GR 10 (Roseobacter sp.) were shown in this work to be more effective than nonheated bacteria in protecting gnotobiotic Artemia larvae against V. campbellii challenge. Immunoprobing of Western blots and quantification by enzyme-linked immunosorbent assay revealed that the amount of DnaK in bacteria and their ability to enhance larval resistance to infection by V. campbellii are correlated. Although the function of DnaK is uncertain, it may improve tolerance to V. campbellii via immune stimulation, a possibility of significance from a fundamental perspective and also because it could be applied in aquaculture, a major method of food production.

Keywords

Bacteria Heat shock proteins DnaK Vibriosis Artemia 
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Notes

Acknowledgements

This work was supported by the University Malaysia Terengganu (UMT, formerly known as University College of Science and Technology Malaysia, KUSTEM) through a doctoral grant to YYS. Research funding was from the Belgian Foundation for Scientific Research (FWO) through the project “Probiont-induced functional responses in aquatic organisms” (no. G.0491.08) and from the Natural Sciences and Engineering Research Council of Canada to THM. We thank Prof. Dr. Bernd Bukau and Dr. Axel Mogk from the Centrum for Molecular Biology, University Heidelberg, Germany for the generous gift of polyclonal antibody to DnaK.

References

  1. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood SK (2000) HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6:435–442. doi: 10.1038/74697 CrossRefPubMedGoogle Scholar
  2. Athman R, Philpott D (2004) Innate immunity via Toll-like receptors and Nod proteins. Curr Opin Microbiol 7:25–32. doi: 10.1016/j.mib.2003.12.013 CrossRefPubMedGoogle Scholar
  3. Austin B, Zhang XH (2006) Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 43:119–124. doi: 10.1111/j.1472-765X.2006.01989.x CrossRefPubMedGoogle Scholar
  4. Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183. doi: 10.1016/S0378-1119(02)00687-X CrossRefPubMedGoogle Scholar
  5. Bucca G, Brassington AME, Schönfeld HJ, Smith CP (2000) The HspR regulon of Streptomyces coelicolor: a role for the DnaK chaperone as a transcriptional co-repressor. Mol Microbiol 38:1093–1103. doi: 10.1046/j.1365-2958.2000.02194.x CrossRefPubMedGoogle Scholar
  6. Campisi J, Fleshner M (2003) The role of extracellular Hsp72 in acute stress-induced potentiation of innate immunity in physically active rats. J Appl Physiol 94:43–52PubMedGoogle Scholar
  7. Clegg JS, Jackson SA, Hoa NV, Sorgeloos P (2000a) Thermal resistance, developmental rate and heat shock proteins in Artemia franciscana, from San Francisco Bay and Southern Vietnam. J Exp Mar Biol Ecol 252:85–96. doi: 10.1016/S0022-0981(00)00239-2 CrossRefPubMedGoogle Scholar
  8. Clegg JS, Jackson SA, Popov VI (2000b) Long-term anoxia in encysted embryos of the crustacean, Artemia franciscana: viability, ultrastructure and stress proteins. Cell Tissue Res 301:433–446. doi: 10.1007/s004410000249 CrossRefPubMedGoogle Scholar
  9. de la Vega E, Hall MR, Degnan BM, Wilson KJ (2006) Short-term hyperthermic treatment of Penaeus monodon increases expression of heat shock protein 70 (HSP70) and reduces replication of gill associated virus (GAV). Aquaculture 253:82–90. doi: 10.1016/j.aquaculture.2005.07.041 CrossRefGoogle Scholar
  10. Defoirdt T, Crab R, Wood TK, Sorgeloos P, Verstraete W, Bossier P (2006) Quorum sensing-disrupting brominated furanones protect the gnotobiotic brine shrimp Artemia franciscana from pathogenic Vibrio harveyi, Vibrio campbellii, and Vibrio parahaemolyticus isolates. Appl Environ Microbiol 72:6419–6423. doi: 10.1128/AEM.00753-06 CrossRefPubMedGoogle Scholar
  11. Diggles BK, Moss GA, Carson J, Anderson CD (2000) Luminous vibriosis in rock lobster Jasus verreauxi (Decapoda: Palinuridae) phyllosoma larvae associated with infection by Vibrio harveyi. Dis Aquat Org 43:127–137. doi: 10.3354/dao043127 CrossRefPubMedGoogle Scholar
  12. Farzanfar A (2006) The use of probiotics in shrimp aquaculture. FEMS Immunol Med Microbiol 48:149–158. doi: 10.1111/j.1574-695X.2006.00116.x CrossRefPubMedGoogle Scholar
  13. Feder ME, Hofmann GE (1999) Heat shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282. doi: 10.1146/annurev.physiol.61.1.243 CrossRefPubMedGoogle Scholar
  14. Frankenberg MM, Jackson SA, Clegg JS (2000) The heat shock response of adult Artemia franciscana. J Therm Biol 25:481–490. doi: 10.1016/S0306-4565(00)00013-9 CrossRefPubMedGoogle Scholar
  15. Galdiero M, de l'Ero GC, Marcatili A (1997) Cytokine and adhesion molecule expression in human monocytes and endothelial cells stimulated with bacterial heat shock proteins. Infect Immun 65:699–707PubMedGoogle Scholar
  16. Gorospe J, Nakamura K, Abe M, Higashi S (1996) Nutritional contribution of Pseudomonas sp. in Artemia culture. Fish Sci 62:914–918Google Scholar
  17. Hameed A, Balasubramanian G (2000) Antibiotic resistance in bacteria isolated from Artemia nauplii and efficacy of formaldehyde to control bacterial load. Aquaculture 183:195–205. doi: 10.1016/S0044-8486(99)00293-8 CrossRefGoogle Scholar
  18. Hessen D, Andersen T (1990) Bacteria as a source of phosphorous for zooplankton. Hydrobiologia 206:217–223Google Scholar
  19. Jacquier-Sarlin MR, Fuller K, Dinh-Xuan AT, Richard MJ, Polla BS (1994) Protective effects of hsp70 in inflammation. Experientia 50:1031–1038. doi: 10.1007/BF01923458 CrossRefPubMedGoogle Scholar
  20. Johnson JD, Fleshner M (2006) Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J Leukoc Biol 79:425–434. doi: 10.1189/jlb.0905523 CrossRefPubMedGoogle Scholar
  21. Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685. doi: 10.1038/227680a0 CrossRefPubMedGoogle Scholar
  22. MacRae TH (2003) Molecular chaperones, stress resistance and development in Artemia franciscana. Cell Dev Biol 14:251–258. doi: 10.1016/j.semcdb.2003.09.019 CrossRefGoogle Scholar
  23. Marques A, Dhont J, Sorgeloos P, Bossier P (2004a) Evaluation of different yeast cell wall mutants and microalgae strains as feed for gnotobiotically grown brine shrimp Artemia franciscana. J Exp Mar Biol Ecol 321:115–136. doi: 10.1016/j.jembe.2004.06.008 CrossRefGoogle Scholar
  24. Marques A, Francois JM, Dhont J, Bossier P, Sorgeloos P (2004b) Influence of yeast quality on performance of gnotobiotically grown Artemia. J Exp Mar Biol Ecol 310:247–264. doi: 10.1016/j.jembe.2004.04.009 CrossRefGoogle Scholar
  25. Marques A, Dinh T, Ioakeimidis C, Huys G, Swings J, Verstraete W, Dhont J, Sorgeloos P, Bossier P (2005) Effects of bacteria on Artemia franciscana cultured in different gnotobiotic environments. Appl Environ Microbiol 71:4307–4317. doi: 10.1128/AEM.71.8.4307-4317.2005 CrossRefPubMedGoogle Scholar
  26. Marques A, Dhont J, Sorgeloos P, Bossier P (2006a) Immunostimulatory nature of β-glucans and baker's yeast in the challenge test of Artemia. Fish Shellfish Immunol 20:682–692. doi: 10.1016/j.fsi.2005.08.008 CrossRefPubMedGoogle Scholar
  27. Marques A, Ollevier F, Verstraete W, Sorgeloos P, Bossier P (2006b) Gnotobiotically grown aquatic animals: opportunities to investigate host–microbe interactions. J Appl Microbiol 100:903–918. doi: 10.1111/j.1365-2672.2006.02961.x CrossRefPubMedGoogle Scholar
  28. Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796. doi: 10.1101/gad.12.24.3788 CrossRefPubMedGoogle Scholar
  29. Panjwani NN, Popova L, Srivastava PK (2002) Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J Immunol 168:2997–3003PubMedGoogle Scholar
  30. Parsell DA, Lindquist S (1993) The function of heat shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496. doi: 10.1146/annurev.ge.27.120193.002253 CrossRefPubMedGoogle Scholar
  31. Pockley AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362:469–476. doi: 10.1016/S0140-6736(03)14075-5 CrossRefPubMedGoogle Scholar
  32. Retzlaff C, Yamamoto Y, Hoffman PS, Friedman H, Klein TW (1994) Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect Immun 62:5689–5693PubMedGoogle Scholar
  33. Singh V, Aballay A (2006) Heat-shock transcription factor (HSF)-1 pathway required for Caenorhabditis elegans immunity. Proc Natl Acad Sci U S A 103:13092–13097 10.1073/pnas.0604050103CrossRefPubMedGoogle Scholar
  34. Smith VJ, Brown JH, Hauton C (2003) Immunostimulation in crustaceans: does it really protect against infection? Fish Shellfish Immunol 15:71–90. doi: 10.1016/S1050-4648(02)00140-7 CrossRefPubMedGoogle Scholar
  35. Soltanian S, Dhont J, Sorgeloos P, Bossier P (2007) Influence of different yeast cell-wall mutants on performance and protection against pathogenic bacteria (Vibrio campbellii) in gnotobiotically-grown Artemia. Fish Shellfish Immunol 23:141–153. doi: 10.1016/j.fsi.2006.09.013 CrossRefPubMedGoogle Scholar
  36. Sorgeloos P, Lavens P, Léger P, Tackaert W, Versichele D (1986) Manual for the culture and use of brine shrimp Artemia in aquaculture. Artemia Reference Center, Faculty of Agriculture, State University of Ghent, Belgium, p 318Google Scholar
  37. Soto-Rodriguez SA, Roque A, Lizarraga-Partida ML, Guerra-Flores AL, Gomez-Gil B (2003) Virulence of luminous vibrios to Artemia franciscana nauplii. Dis Aquat Org 53:231–240. doi: 10.3354/dao053231 CrossRefPubMedGoogle Scholar
  38. Sung YY, Van Damme EJM, Sorgeloos P, Bossier P (2007) Non-lethal heat shock protects gnotobiotic Artemia franciscana larvae against virulent Vibrios. Fish Shellfish Immunol 22:318–326. doi: 10.1016/j.fsi.2006.05.008 CrossRefGoogle Scholar
  39. Sung YY, Pineda C, MacRae TH, Sorgeloos P, Bossier P (2008) Exposure of gnotobiotic Artemia franciscana larvae to abiotic stress promotes heat shock protein 70 synthesis and enhances resistance to pathogenic Vibrio campbellii. Cell Stress Chaperones 13:59–66. doi: 10.1007/s12192-008-0011-y CrossRefPubMedGoogle Scholar
  40. Sung YY, Ashame MF, Chen SJ, MacRae TH, Sorgeloos P, Bossier P (2009) Feeding Artemia franciscana (Kellogg) larvae with bacterial heat shock protein, protects from Vibrio campbellii (Baumann) infection. J Fish Dis (in press)Google Scholar
  41. Tinh NTN, Yen VHN, Dierckens K, Sorgeloos P, Bossier P (2008) An acyl homoserine lactone-degrading microbial community improves the survival of first-feeding turbot larvae (Scophthalmus maximus L.). Aquaculture 285:56–62. doi: 10.1016/j.aquaculture.2008.08.018 CrossRefGoogle Scholar
  42. Vadstein O (1997) The use of immunostimulation in marine larviculture: possibilities and challenges. Aquaculture 155:401–17. doi: 10.1016/S0044-8486(97)00114-2 CrossRefGoogle Scholar
  43. Verschuere L, Rombaut G, Huys G, Dhont J, Sorgeloos P, Verstraete W (1999) Microbial control of the culture of Artemia juveniles through pre-emptive colonization by selected bacterial strains. Appl Environ Microbiol 65:2527–2533PubMedGoogle Scholar
  44. Verschuere L, Heang H, Criel G, Sorgeloos P, Verstraete W (2000) Selected bacterial strains protect Artemia sp. from pathogenic effects of Vibrio proteolyticus CW8T2. Appl Environ Microbiol 66:1139–1146. doi: 10.1128/AEM.66.3.1139-1146.2000 CrossRefPubMedGoogle Scholar
  45. Yasuda K, Taga N (1980) A mass culture method for Artemia salina using bacteria as food. Mer 18:53–62Google Scholar

Copyright information

© Cell Stress Society International 2009

Authors and Affiliations

  • Yeong Yik Sung
    • 1
    • 2
  • Till Dhaene
    • 3
  • Tom Defoirdt
    • 3
  • Nico Boon
    • 4
  • Thomas H. MacRae
    • 5
  • Patrick Sorgeloos
    • 3
  • Peter Bossier
    • 3
  1. 1.Department of Fisheries and Aquaculture, Faculty of Agrotechnology and Food ScienceUniversity Malaysia TerengganuKuala TerengganuMalaysia
  2. 2.Institute of Tropical Aquaculture (AQUATROP)University Malaysia TerengganuKuala TerengganuMalaysia
  3. 3.Laboratory of Aquaculture and Artemia Reference CenterGhent UniversityGhentBelgium
  4. 4.Laboratory of Microbial Ecology and Technology (LabMET)Ghent UniversityGhentBelgium
  5. 5.Department of BiologyDalhousie UniversityHalifaxCanada

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