Skip to main content
Log in

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

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54:450–472

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Madison LL, Huisman GW (1999) Metabolic engineering of poly(3-hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol Rev 63:21–53

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 145–146

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 58:551–556

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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

    Article  Google Scholar 

  • 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 318

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter De Schryver.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thai, T.Q., Wille, M., Garcia-Gonzalez, L. et al. Poly-ß-hydroxybutyrate content and dose of the bacterial carrier for Artemia enrichment determine the performance of giant freshwater prawn larvae. Appl Microbiol Biotechnol 98, 5205–5215 (2014). https://doi.org/10.1007/s00253-014-5536-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-5536-7

Keywords

Navigation