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Poly-β-hydroxybutyrate (PHB) increases growth performance and intestinal bacterial range-weighted richness in juvenile European sea bass, Dicentrarchus labrax

  • Applied Microbial and Cell Physiology
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Abstract

The bacterial storage polymer poly-β-hydroxybutyrate (PHB) has the potential to be used as an alternative anti-infective strategy for aquaculture rearing. In this research, the effects of (partially) replacing the feed of European sea bass juveniles with PHB were investigated. During a 6-week trial period, the PHB showed the ability to act as an energy source for the fish. This indicated that PHB was degraded and used during gastrointestinal passage. The gut pH decreased from 7.7 to 7.2 suggesting that the presence of PHB in the gut led to the increased production of (short-chain fatty) acids. The diets supplemented with 2% and 5% PHB (w/w) induced a gain of the initial fish weight with a factor 2.4 and 2.7, respectively, relative to a factor 2.2 in the normal feed treatment. Simultaneously, these treatments showed the highest bacterial range-weighted richness in the fish intestine. Based on molecular analysis, higher dietary PHB levels induced larger changes in the bacterial community composition. From our results, it seems that PHB can have a beneficial effect on fish growth performance and that the intestinal bacterial community structure may be closely related to this phenomenon.

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References

  • Acar J, Casewell M, Freeman J, Friis C, Goossens H (2000) Avoparcin and virginiamycin as animal growth promoters: a plea for science in decision-making. Clin Microbial Infect 6:477–482

    Article  CAS  Google Scholar 

  • Azain MJ (2004) Role of fatty acids in adipocyte growth and development. J Anim Sci 82:916–924

    CAS  Google Scholar 

  • Bongers A, van den Heuvel E (2003) Prebiotics and the bioavailability of minerals and trace elements. Food Rev Int 19:397–422

    Article  CAS  Google Scholar 

  • Boon N, De Windt W, Verstraete W, Top EM (2002) Evaluation of nested PCR-DGGE (denaturing gradient gel electrophoresis) with group-specific 16S rRNA primers for the analysis of bacterial communities from different wastewater treatment plants. FEMS Microbiol Ecol 39:101–112

    CAS  Google Scholar 

  • Burr G, Gatlin D, Ricke S (2005) Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture. J World Aquacult Soc 36:425–436

    Article  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

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Defoirdt T, Halet D, Vervaeren H, Boon N, Van de Wiele T, Sorgeloos P, Bossier P, Verstraete W (2007b) The bacterial storage compound poly-beta-hydroxybutyrate protects Artemia franciscana from pathogenic Vibrio campbellii. Environ Microbiol 9:445–452

    Article  CAS  Google Scholar 

  • Dierckens K, Rekecki A, Laureau S, Sorgeloos P, Boon N, Van den Broeck W, Bossier P (2009) Development of a bacterial challenge test for gnotobiotic sea bass (Dicentrarchus labrax) larvae. Environ Microbiol 11:526–533

    Article  CAS  Google Scholar 

  • Gebauer B, Jendrossek D (2006) Assay of poly(3-hydroxybutyrate) depolymerase activity and product determination. Appl Environ Microbiol 72:6094–6100

    Article  CAS  Google Scholar 

  • Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota—introducing the concept of prebiotics. J Nutr 125:1401–1412

    CAS  Google Scholar 

  • Goncalves LMD, Ramos A, Almeida JS, Xavier A, Carrondo MJT (1997) Elucidation of the mechanism of lactic acid growth inhibition and production in batch cultures of Lactobacillus rhamnosus. Appl Microbiol Biotechnol 48:346–350

    Article  CAS  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-beta-hydroxybutyrate-accumulating bacteria protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. FEMS Microbiol Ecol 60:363–369

    Article  CAS  Google Scholar 

  • Hismiogullari SE, Hismiogullari AA, Sahin F, Oner ET, Yenice S, Karasartova D (2008) Investigation of antibacterial and cytotoxic effects of organic acids including ascorbic acid, lactic acid and acetic acids on mammalian cells. J Anim Vet Adv 7:681–684

    CAS  Google Scholar 

  • Jendrossek D, Handrick R (2002) Microbial degradation of polyhydroxyalkanoates. Annu Rev Microbiol 56:403–432

    Article  CAS  Google Scholar 

  • Karunasagar I, Shivu MM, Girisha SK, Krohne G, Karunasagar I (2007) Biocontrol of pathogens in shrimp hatcheries using bacteriophages. Aquaculture 268:288–292

    Article  Google Scholar 

  • Li P, Gatlin DM (2004) Dietary brewers yeast and the prebiotic Grobiotic (TM) AE influence growth performance, immune responses and resistance of hybrid striped bass (Morone chrysops x M-saxatilis) to Streptococcus iniae infection. Aquaculture 231:445–456

    Article  Google Scholar 

  • Li P, Burr GS, Gatlin DM, Hume ME, Patnaik S, Castille FL, Lawrence AL (2007) Dietary supplementation of short-chain fructooligosaccharides influences gastrointestinal microbiota composition and immunity characteristics of pacific white shrimp, Litopenaeus vannamei, cultured in a recirculating system. J Nutr 137:2763–2768

    CAS  Google Scholar 

  • Listewnik HF, Wendlandt KD, Jechorek M, Mirschel G (2007) Process design for the microbial synthesis of poly-beta-hydroxybutyrate (PHB) from natural gas. Eng Life Sci 7:278–282

    Article  CAS  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  Google Scholar 

  • Mahious AS, Gatesoupe FJ, Hervi M, Metailler R, Ollevier F (2006) Effect of dietary inulin and oligosaccharides as prebiotics for weaning turbot, Psetta maxima (Linnaeus, C. 1758). Aquac Int 14:219–229

    Article  CAS  Google Scholar 

  • Marzorati M, Wittebolle L, Boon N, Daffonchio D, Verstraete W (2008) How to get more out of molecular fingerprints: practical tools for microbial ecology. Environ Microbiol 10:1571–1581

    CAS  Google Scholar 

  • Nicolas JL, Gatesoupe FJ, Froueli S, Bachere E, Gueguen Y (2007) What alternatives to antibiotics are conceivable for aquaculture? Prod Anim 20:253–258

    CAS  Google Scholar 

  • Panigrahi A, Azad IS (2007) Microbial intervention for better fish health in aquaculture: the Indian scenario. Fish Physiol Biochem 33:429–440

    Article  CAS  Google Scholar 

  • Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci U S A 101:4596–4601

    Article  CAS  Google Scholar 

  • Ricke SC (2003) Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult Sci 82:632–639

    CAS  Google Scholar 

  • Sammouth S, d'Orbcastel ER, Gasset E, LemariÈ G, Breuil G, Marino G, Coeurdacier J-L, Fivelstad S, Blancheton J-P (2009) The effect of density on sea bass (Dicentrarchus labrax) performance in a tank-based recirculating system. Aquac Eng 40:72–78

    Article  Google Scholar 

  • Sapkota A, Sapkota AR, Kucharski M, Burke J, McKenzie S, Walker P, Lawrence R (2008) Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int 34:1215–1226

    Article  Google Scholar 

  • Scholz-Ahrens KE, Ade P, Marten B, Weber P, Timm W, Asil Y, Gluer CC, Schrezenmeir J (2007) Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr 137:838S–846S

    CAS  Google Scholar 

  • Thompson JL, Hinton M (1996) Effect of short-chain fatty acids on the size of enteric bacteria. Lett Appl Microbiol 22:408–412

    Article  CAS  Google Scholar 

  • Tokiwa Y, Calabia BP (2004) Degradation of microbial polyesters. Biotechnol Lett 26:1181–1189

    Article  CAS  Google Scholar 

  • Tokiwa Y, Calabia BP (2007) Biodegradability and biodegradation of polyesters. J Polym Environ 15:259–267

    Article  CAS  Google Scholar 

  • Vazquez JA, Gonzalez MP, Murado MA (2005) Effects of lactic acid bacteria cultures on pathogenic microbiota from fish. Aquaculture 245:149–161

    Article  Google Scholar 

  • Zhou ZG, Ding ZK, Huiyuan LV (2007) Effects of dietary short-chain fructooligosaccharides on intestinal microflora, survival, and growth performance of juvenile white shrimp, Litopenaeus vannamei. J World Aquacult Soc 38:296–301

    Article  Google Scholar 

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Acknowledgments

This work was performed and funded within the frame of the Research Foundation of Flanders (FWO) project ‘‘Probiont-induced functional responses in aquatic organisms” and the European FP7 project “Promicrobe-Microbes as positive actors for more sustainable aquaculture” (Project Reference: 227197). The authors would also like to thank Dr. ir. Tom Defoirdt, lic. Kristof Dierckens and ir. Charlotte Grootaert for the critical reading of the manuscript and the helpful suggestions.

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Correspondence to Willy Verstraete.

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Peter De Schryver and Amit Kumar Sinha contributed equally to this work.

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De Schryver, P., Sinha, A.K., Kunwar, P.S. et al. Poly-β-hydroxybutyrate (PHB) increases growth performance and intestinal bacterial range-weighted richness in juvenile European sea bass, Dicentrarchus labrax . Appl Microbiol Biotechnol 86, 1535–1541 (2010). https://doi.org/10.1007/s00253-009-2414-9

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