Advertisement

Applied Microbiology and Biotechnology

, Volume 98, Issue 11, pp 5205–5215 | Cite as

Poly-ß-hydroxybutyrate content and dose of the bacterial carrier for Artemia enrichment determine the performance of giant freshwater prawn larvae

  • Truong Quoc Thai
  • Mathieu Wille
  • Linsey Garcia-Gonzalez
  • Patrick Sorgeloos
  • Peter Bossier
  • Peter De SchryverEmail author
Environmental biotechnology

Abstract

The beneficial effects of poly-β-hydroxybutyrate (PHB) for aquaculture animals have been shown in several studies. The strategy of applying PHB contained in a bacterial carrier has, however, hardly been considered. The effect of administering PHB-accumulated Alcaligenes eutrophus H16 containing 10 or 80 % PHB on dry weight, named A10 and A80, respectively, through the live feed Artemia was investigated on the culture performance of larvae of the giant freshwater prawn (Macrobrachium rosenbergii). Feeding larvae with Artemia nauplii enriched in a medium containing 100 and 1,000 mg L−1 A80 significantly increased the survival with about 15 % and the development of the larvae with a larval stage index of about 1 as compared to feeding non-enriched Artemia. The survival of the larvae also significantly increased with about 35 % in case of a challenge with Vibrio harveyi. The efficiency of these treatments was equal to a control treatment of Artemia enriched in an 800 mg L−1 PHB powder suspension, while Artemia enriched in 10 mg L−1 A80, 100 mg L−1 A10, and 1,000 mg L−1 A10 did not bring similar effects. From our results, it can be concluded that PHB supplemented in a bacterial carrier (i.e., amorphous PHB) can increase the larviculture efficiency of giant freshwater prawn similar to supplementation of PHB in powdered form (i.e., crystalline PHB). When the level of PHB in the bacterial carrier is high, similar beneficial effects can be achieved as crystalline PHB, but at a lower live food enrichment concentration expressed on PHB basis.

Keywords

Amorphous Poly-ß-hydroxybutyrate Macrobrachium rosenbergii Survival Growth Disease resistance 

Notes

Acknowledgments

The financial support by the Vietnamese government project “Main program on development and application of Biological technology in agriculture and development of rural country to the year 2020” and the Ghent University project “Host-microbial interactions in aquatic production (BOF12/GOA/022)” is highly appreciated. Peter DS is supported as a post-doctoral researcher by the Research Foundation - Flanders (FWO) (Belgium).

References

  1. Alavandi SV, Vijayan KK, Santiago TC, Poornima M, Jithendran KP, Ali SA, Rajan JJS (2004) Evaluation of Pseudomonas sp. PM 11 and Vibrio fluvialis PM 17 on immune indices of tiger shrimp, Penaeus monodon. Fish Shellfish Immunol 17:115–120. doi: 10.1016/j.fsi.2003.11.007 PubMedCrossRefGoogle Scholar
  2. Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54:450–472PubMedCentralPubMedGoogle Scholar
  3. Aslim B, Çalişkan F, Beyatli Y, Gündüz U (1998) Poly-ß-hydroxybutyrate production by lactic acid bacteria. FEM Microbiol Lett 159:293–297. doi: 10.1111/j.1574-6968.1998.tb12874.x CrossRefGoogle Scholar
  4. Baruah K, Cam DTV, Dierckens K, Wille M, Defoirdt T, Sorgeloos P, Bossier P (2009) In vivo effects of single or combined N-acyl homoserine lactone quorum sensing signals on the performance of Macrobrachium rosenbergii larvae. Aquaculture 288:233–238. doi: 10.1016/j.aquaculture.2008.11.034 CrossRefGoogle Scholar
  5. Cam DTV, Hao NV, Dierckens K, Defoirdt T, Boon N, Sorgeloos P, Bossier P (2009) Novel approach of using homoserine lactone-degrading and poly-β-hydroxybutyrate-accumulating bacteria to protect Artemia from the pathogenic effects of Vibrio harveyi. Aquaculture 291:23–30. doi: 10.1016/j.aquaculture.2009.03.009 CrossRefGoogle Scholar
  6. Cavalli RO, Lavens P, Sorgeloos P (1999) Performance of Macrobrachium rosenbergii broodstock fed diets with different fatty acid composition. Aquaculture 179:387–402. doi: 10.1016/S0044-8486(99)00173-8 CrossRefGoogle Scholar
  7. Das A, Saha D, Pal J (2009) Antimicrobial resistance and in vitro gene transfer in bacteria isolated from the ulcers of EUS-affected fish in India. Lett Appl Microbiol 49:497–502. doi: 10.1111/j.1472-765X.2009.02700.x PubMedCrossRefGoogle Scholar
  8. De Schryver P, Sinha AK, Kunwar PS, Baruah K, Verstraete W, Boon N, De Boeck G, Bossier P (2010) Poly-ß-hydroxybutyrate (PHB) increases growth performance and intestinal bacterial range-weighted richness in juvenile European sea bass, Dicentrarchus labrax. Appl Microbiol Biotechnol 86:1535–1541. doi: 10.1007/s00253-009-2414-9 PubMedCrossRefGoogle Scholar
  9. Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P (2007a) Alternatives to antibiotics to control bacterial infections: luminescent vibriosis in aquaculture as an example. Trends Biotechnol 25:472–479. doi: 10.1016/j.tibtech.2007.08.001 PubMedCrossRefGoogle Scholar
  10. Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P (2009) Short-chain fatty acids and poly-ß-hydroxyalkanoates: (new) biocontrol agents for a sustainable animal production. Biotechnol Adv 27:680–685. doi: 10.1016/j.biotechadv.2009.04.026 PubMedCrossRefGoogle Scholar
  11. Defoirdt T, Halet D, Sorgeloos P, Bossier P, Verstraete W (2006) Short-chain fatty acids protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. Aquaculture 261:804–808. doi: 10.1016/j.aquaculture.2006.06.038 CrossRefGoogle Scholar
  12. Defoirdt T, Halet D, Vervaeren H, Boon N, De Wiele TV, Sorgeloos P, Bossier P, Verstraete W (2007b) The bacterial storage compound poly-ß-hydroxybutyrate protects Artemia franciscana from pathogenic Vibrio campbellii. Environ Microbiol 9:445–452. doi: 10.1111/j.1462-2920.2006.01161.x PubMedCrossRefGoogle Scholar
  13. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. doi: 10.1021/ac60111a017 CrossRefGoogle Scholar
  14. Elustondo PA, Angelova PR, Kawalec M, Michalak M, Kurcok P, Abramov AY, Pavlov EV (2013) Polyhydroxybutyrate targets mammalian mitochondria and increases permeability of plasmalemmal and mitochondrial membranes. PLoS One 8:e75812. doi: 10.1371/journal.pone.0075812 PubMedCentralPubMedCrossRefGoogle Scholar
  15. Halet D, Defoirdt T, Van Damme P, Vervaeren H, Forrez I, Van De Wiele T, Boon N, Sorgeloos P, Bossier P, Verstraete W (2007) Poly-ß-hydroxybutyrate-accumulating bacteria protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. FEMS Microbiol Ecol 60:363–369. doi: 10.1111/j.1574-6941.2007.00305.x PubMedCrossRefGoogle Scholar
  16. Huys L, Dhert P, Robles R, Ollevier F, Sorgeloos P, Swings J (2001) Search for beneficial bacterial strains for turbot (Scophthalmus maximus L.) larviculture. Aquaculture 193:25–37. doi: 10.1016/S0044-8486(00)00474-9 CrossRefGoogle Scholar
  17. Jayaprakash NS, Kumar VJR, Philip R, Singh ISB (2006) Vibrios associated with Macrobrachium rosenbergii (De Man, 1879) larvae from three hatcheries on the Indian southwest coast. Aquac Res 37:351–358. doi: 10.1111/j.1365-2109.2005.01432.x CrossRefGoogle Scholar
  18. Kato N, Konishi H, Shimao M, Sakazawa C (1992) Production of 3-hydroxybutyric acid trimer by Bacillus megaterium B-124. J Ferment Bioeng 73:246–247. doi: 10.1016/0922-338X(92)90173-R CrossRefGoogle Scholar
  19. Kaynar P, Beyatli Y (2009) Determination of poly-ß-hydroxybutyrate production by Bacillus spp. isolated from the intestines of various fishes. Fish Sci 75:439–443. doi: 10.1007/s12562-008-0047-z CrossRefGoogle Scholar
  20. Kennedy B, Venugopal MN, Karunasagar I, Karunasagar I (2006) Bacterial flora associated with the giant freshwater prawn Macrobrachium rosenbergii, in the hatchery system. Aquaculture 261:1156–1167. doi: 10.1016/j.aquaculture.2006.09.015 CrossRefGoogle Scholar
  21. Liu Y, De Schryver P, Van Delsen B, Maignien L, Boon N, Sorgeloos P, Verstraete W, Bossier P, Defoirdt T (2010) PHB-degrading bacteria isolated from the gastrointestinal tract of aquatic animals as protective actors against luminescent vibriosis. FEMS Microbiol Ecol 74:196–204. doi: 10.1111/j.1574-6941.2010.00926.x PubMedCrossRefGoogle Scholar
  22. López-Torres MA, Lizárraga-Partida ML (2001) Bacteria isolated on TCBS medium associated with hatched Artemia cysts of commercial brands. Aquaculture 194:11–20. doi: 10.1016/S0044-8486(00)00505-6 CrossRefGoogle Scholar
  23. Madison LL, Huisman GW (1999) Metabolic engineering of poly(3-hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol Rev 63:21–53PubMedCentralPubMedGoogle Scholar
  24. Mallasen M, Valenti WC (2006) Effect of nitrite on larval development of giant river prawn Macrobrachium rosenbergii. Aquaculture 261:1292–1298. doi: 10.1016/j.aquaculture.2006.07.048 CrossRefGoogle Scholar
  25. Marques A, Dhont J, Sorgeloos P, Bossier P (2004) Evaluation of different yeast cell wall mutants and microalgae strains as feed for gnotobiotically grown brine shrimp Artemia franciscana. J Exp Mar Bio Ecol 312:115–136. doi: 10.1016/j.jembe.2004.06.008 CrossRefGoogle Scholar
  26. Najdegerami EH, Tran TN, Defoirdt T, Marzorati M, Sorgeloos P, Boon N, Bossier P (2012) Effects of poly-β-hydroxybutyrate (PHB) on Siberian sturgeon (Acipenser baerii) fingerlings performance and its gastrointestinal tract microbial community. FEMS Microbiol Ecol 79:25–33. doi: 10.1111/j.1574-6941.2011.01194.x PubMedCrossRefGoogle Scholar
  27. New MB (2002) Farming freshwater prawns: a manual for the culture of the giant river prawn (Macrobrachium rosenbergii). FAO fisheries technical paper No. 428, Rome, pp 145–146Google Scholar
  28. Nhan DT, Wille M, De Schryver P, Defoirdt T, Bossier P, Sorgeloos P (2010a) The effect of poly-β-hydroxybutyrate on larviculture of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 302:76–81. doi: 10.1016/j.aquaculture.2010.02.011 CrossRefGoogle Scholar
  29. Nhan DT, Cam DTV, Wille M, Defoirdt T, Bossier P, Sorgeloos P (2010b) Quorum quenching bacteria protect Macrobrachium rosenbergii larvae from Vibrio harveyi infection. J Appl Microbiol 109:1007–1016. doi: 10.1111/j.1365-2672.2010.04728.x PubMedCrossRefGoogle Scholar
  30. Niu Y, Defoirdt T, Rekecki A, De Schryver P, Van de Broeck W, Dong S, Sorgeloos P, Boon N, Bossier P (2012) A method for the specific detection of resident bacteria in brine shrimp larvae. J Microbiol Methods 89:33–37. doi: 10.1016/j.mimet.2012.02.004 PubMedCrossRefGoogle Scholar
  31. Olsson JC, Westerdahl A, Conway PL, Kjelleberg S (1992) Intestinal colonization potential of turbot (Scophthalmus maximus)- and dab (Limanda limanda)-associated bacteria with inhibitory effects against Vibrio anguillarum. Appl Environ Microbiol 58:551–556PubMedCentralPubMedGoogle Scholar
  32. Reusch RN, Bryant EM, Henry DN (2003) Increased poly-(R)-3-hydroxybutyrate concentrations in streptozotocin (STZ) diabetic rats. Acta Diabetol 40:91–94. doi: 10.1007/s005920300011 PubMedCrossRefGoogle Scholar
  33. Seebach D, Fritz MG (1999) Detection, synthesis, structure, and function of oligo(3-hydroxyalkanoates): contributions by synthetic organic chemists. Int J Biol Macromol 25:217–236. doi: 10.1016/S0141-8130(99)00037-9 PubMedCrossRefGoogle Scholar
  34. Shailender M, Krishna PV, Suresh Babu C, Srikanth B (2012) Impact of diseases on the growth and survival of giant freshwater prawn, Macrobrachium rosenbergii (De Man) larvae in the hatchery level. World J Fish Mar Sci 4:620–625. doi: 10.5829/idosi.wjfms.2012.04.06.65154 Google Scholar
  35. Sorgeloos P, Léger P (1992) Improved larviculture outputs of marine fish, shrimp and prawn. J World Aquacult Soc 23:251–264. doi: 10.1111/j.1749-7345.1992.tb00788.x CrossRefGoogle 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, Ghent, p 318Google Scholar
  37. Suguna P, Binuramesh C, Abirami P, Saranya V, Poornima K, Rajeswari V, Shenbagarathai R (2013) Immunostimulation by poly-β hydroxybutyrate-hydroxyvalerate (PHB-HV) from Bacillus thuringiensis in Oreochromis mossambicus. Fish Shellfish Immunol. doi: 10.1016/j.fsi.2013.10.012 PubMedGoogle Scholar
  38. Sui L, Liu Y, Sun H, Wille M, Bossier P, De Schryver P (2012) The effect of poly-β-hydroxybutyrate on the performance of Chinese mitten crab (Eriocheir sinensis Milne-Edwards) zoea larvae. Aquac Res 1–8. doi:  10.1111/are.12077
  39. Sung HH, Hwang SF, Tasi FM (2000) Responses of gaint freshwater prawn (Macrobrachium rosenbergii) to challenge by two strains of Aeromonas spp. J Invertebr Pathol 76:278–284. doi: 10.1006/jipa.2000.4981 PubMedCrossRefGoogle Scholar
  40. Teo JWP, Suwanto A, Poh CL (2000) Novel β-lactamase genes from two environmental isolates of Vibrio harveyi. Antimicrob Agents Chemother 44:1309–1314. doi: 10.1128/AAC.44.5.1309-1314.2000 PubMedCentralPubMedCrossRefGoogle Scholar
  41. Teo JWP, Tan TMC, Poh CL (2002) Genetic determinants of tetracycline resistance in Vibrio harveyi. Antimicrob Agents Chemother 46:1038–1045. doi: 10.1128/aac.46.4.1038-1045.2002 PubMedCentralPubMedCrossRefGoogle Scholar
  42. Weltzien FA, Hemre GI, Evjemo JO, Olsen Y, Fyhn HJ (2000) β-hydroxybutyrate in developing nauplii of brine shrimp (Artemia franciscana K.) under feeding and non-feeding conditions. Comp Biochem Physiol Part B 125:63–69. doi: 10.1016/S0305-0491(99)00159-5 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Truong Quoc Thai
    • 1
    • 2
  • Mathieu Wille
    • 1
  • Linsey Garcia-Gonzalez
    • 3
  • Patrick Sorgeloos
    • 1
  • Peter Bossier
    • 1
  • Peter De Schryver
    • 1
    Email author
  1. 1.Laboratory of Aquaculture and Artemia Reference CenterGhent UniversityGhentBelgium
  2. 2.Research Institute for AquacultureNha Trang CityVietnam
  3. 3.VITOMolBelgium

Personalised recommendations