Skip to main content
Log in

Effects of Dietary Clostridium butyricum on the Growth, Digestive Enzyme Activity, Antioxidant Capacity, and Resistance to Nitrite Stress of Penaeus monodon

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

The present study investigated the effects of the dietary probiotic Clostridium butyricum (CB) on the growth, intestine digestive enzyme activity, antioxidant capacity and resistance to nitrite stress, and body composition of Penaeus monodon. For 56 days, shrimps were fed diets containing different levels of C. butyricum (1 × 109 CFU g−1), 0% (control), 0.5% (CB1), 1.0% (CB2), and 2.0% (CB3), as treatment groups, followed by an acute nitrite stress test for 48 h. The results indicated that dietary supplementation of C. butyricum increased the growth of shrimp in the CB2 and CB3 groups. The survival rate of shrimp increased after nitrite stress for 24 and 48 h. The intestine amylase and trypsin activities increased in all three C. butyricum groups, while the lipase activity was only affected in the CB3 group. The superoxide dismutase (SOD) activity as well as heat shock protein 70 (hsp70) and ferritin gene expression levels were increased in the intestines of shrimps cultured under normal conditions for 56 days, while the catalase (CAT) activity was not changed and glutathione peroxidase (GPx) activity was only increased in the CB2 and CB3 groups. After exposure to nitrite stress for 24 and 48 h, the intestine antioxidant enzyme (SOD, CAT, and GPx) activity and gene (hsp70 and ferritin) expression levels in the three C. butyricum groups were higher than those of the control. C. butyricum had no effects on the whole body composition of the shrimp. These results revealed that C. butyricum improved the growth as well as enhanced the intestine digestive enzyme and antioxidant activities of P. monodon against nitrite stress, and C. butyricum may be a good probiotic for shrimp aquaculture.

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

Similar content being viewed by others

References

  1. Shi JX, Fu MJ, Zhao C, Zhou FL, Yang QB, Qiu LH (2016) Characterization and function analysis of Hsp60 and Hsp10 under different acute stresses in black tiger shrimp, Penaeus monodon. Cell Stress Chaperones 21:295–312

    Article  CAS  PubMed  Google Scholar 

  2. Dai WT, Fu MJ, Zhao C, Ma ZH, Zhou FL, Yang QB, Qiu LH (2016) Characterization, expression analysis and RNAi of p53 gene in Penaeus monodon. Mol Biol Rep 43(6):549–561

    Article  CAS  PubMed  Google Scholar 

  3. Tourtip S, Wongtripop S, Stentiford GD, Bateman KS, Sriurairatana S, Chavadej J, Sritunyalucksana K, Withyachumnarnkul B (2009) Enterocytozoon hepatopenaei sp nov (Microsporida: Enterocytozoonidae), a parasite of the black tiger shrimp Penaeus monodon (Decapoda: Penaeidae): fine structure and phylogenetic relationships. J Invertebr Pathol 102:21–29

    Article  CAS  PubMed  Google Scholar 

  4. Joshi J, Srisala J, Truong VH, Chen IT, Nuangsaeng B, Suthienkul O, Lo CF, Flegel TW, Sritunyalucksana K, Thitamadee S (2014) Variation in Vibrio parahaemolyticus isolates from a single Thai shrimp farm experiencing an outbreak of acute hepatopancreatic necrosis disease (AHPND). Aquaculture 428:297–302

    Article  Google Scholar 

  5. Chen JC, Kou YZ (1992) Effects of ammonia on growth and molting of Penaeus japonicus juveniles. Aquaculture 104:249–260

    Article  CAS  Google Scholar 

  6. Chen JC, Lin CY (1992) Oxygen consumption and ammonia-N excretion of Penaeus chinensis juveniles exposed to ambient ammonia at different salinity levels. Comp Biochem Physiol C 102:287–291

    Article  CAS  PubMed  Google Scholar 

  7. Huang WJ, Leu JH, Tsau MT, Chen JC, Chen LL (2011) Differential expression of LvHSP60 in shrimp in response to environmental stress. Fish Shellfish Immunol 30:576–582

    Article  CAS  PubMed  Google Scholar 

  8. Cheng W, Chen SM, Wang FI, Hsu PI, Liu CH, Chen JC (2003) Effects of temperature, pH, salinity and ammonia on the phagocytic activity and clearance efficiency of giant freshwater prawn Macrobrachium rosenbergii to Lactococcus garvieae. Aquaculture 219:111–121

    Article  Google Scholar 

  9. Zheng JB, Mao Y, Su YQ, Wang J (2016) Effects of nitrite stress on mRNA expression of antioxidant enzymes, immune-related genes and apoptosis-related proteins in Marsupenaeus japonicas. Fish Shellfish Immunol 58:239–252

    Article  CAS  PubMed  Google Scholar 

  10. Wang WN, Wang AL, Zhang YJ, Li ZH, Wang JX, Sun RY (2004) Effects of nitrite on lethal and immune response of Macrobrachium nipponense. Aquaculture 232(1):679–686

    Article  CAS  Google Scholar 

  11. Guo H, Xian JA, Li B, Ye CX, Wang AL, Miao YT, Liao SA (2013) Gene expression of apoptosis-related genes, stress protein and antioxidant enzymes in hemocytes of white shrimp Litopenaeus vannamei under nitrite stress. Comp Biochem Physiol C 157(4):366–371

    CAS  Google Scholar 

  12. Chand RK, Sahoo PK (2006) Effect of nitrite on the immune response of freshwater prawn Macrobrachium malcolmsonii and its susceptibility to Aeromonas hydrophila. Aquaculture 258(1):150–156

    Article  CAS  Google Scholar 

  13. Amaretti A, Nunzio MD, Pompei A, Raimondi S, Rossi M, Bordoni A (2013) Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl Microbiol Biotechnol 97:809–817

    Article  CAS  PubMed  Google Scholar 

  14. Giorgio G, Nina C, Yantyati W (2010) Importance of Lactobacilli in food and feed biotechnology. Res Microbiol 161:480–487

    Article  Google Scholar 

  15. De BC, Meena DK, Behera BK, Das P, Das Mohapatra PK, Sharma AP (2014) Probiotics in fish and shellfish culture: immunomodulatory and ecophysiological responses. Fish Physiol Biochem 40(3):921–971

    CAS  Google Scholar 

  16. Cao GT, Xiao YP, Yang CM, Chen AG, Liu TT, Zhou L, Zhang L, Ferket PR (2012) Effects of Clostridium butyricum on growth performance, nitrogen metabolism, intestinal morphology cecal microflora in broiler chickens. J Anim Vet Adv 11:2665–2671

    Article  CAS  Google Scholar 

  17. Douglas F, Hambleton R, Rigby GJ (1973) An investigation of the oxidation-reduction potential and of the effect of oxygen on the germination and outgrowth of Clostridium butyricum spores, using platinum electrodes. J Appl Bacteriol 36:625–633

    Article  CAS  PubMed  Google Scholar 

  18. Junghare M, Subudhi S, Lal B (2012) Improvement of hydrogen production under decreased partial pressure by newly isolated alkaline tolerant anaerobe, Clostridium butyricum TM-9A: optimization of process parameters. Int J Hydrog Energy 37:3160–3168

    Article  CAS  Google Scholar 

  19. Liao XD, Ma G, Cai J, Fu Y, Yan XY, Wei XB, Zhang RJ (2015) Effects of Clostridium butyricum on growth performance, antioxidation, and immune function of broilers. Poult Sci 94:662–667

    Article  CAS  PubMed  Google Scholar 

  20. Liao XD, Wu RJ, Ma G, Zhao LM, Zheng ZJ, Zhang RJ (2015) Effects of Clostridium butyricum on antioxidant properties, meat quality and fatty acid composition of broiler birds. Lipids Health Dis 14:1–9

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  22. Gao QX, Wu TX, Wang JB, Zhuang QC (2011) Inhibition of bacterial adhesion to HT-29 cells by lipoteichoic acid extracted from Clostridium butyricum. Afr J Biotechnol 10(39):7633–7639

    CAS  Google Scholar 

  23. Zhang L, Zhang LL, Zhan XA, Zeng XF, Zhou L, Cao GT, Chen AG, Yang CM (2016) Effects of dietary supplementation of probiotic, Clostridium butyricum, on growth performance, immune response, intestinal barrier function, and digestive enzyme activity in broiler chickens challenged with Escherichia coli K88. J Anim Sci Biotechnol 7:1–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gao QX, Xiao YP, Sun P, Peng SM, Yin F, Ma XM, Shi ZH (2013) In Vitro protective efficacy of Clostridium butyricum against fish pathogen infections. Indian J Microbiol 53:453–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rungrassamee W, Klanchui A, Maibunkaew S, Karoonuthaisiri N (2016) Bacterial dynamics in intestines of the black tiger shrimp and the Pacific white shrimp during Vibrio harveyi exposure. J Invertebr Pathol 133:12–19

    Article  CAS  PubMed  Google Scholar 

  26. Rungrassamee W, Klanchui A, Maibunkaew S, Chaiyapechara S, Jiravanichpaisal P, Karoonuthaisiri N (2014) Characterization of intestinal bacteria in wild and domesticated adult black tiger shrimp (Penaeus monodon). PLoS One 9:e91853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Luis-Villaseñor IE, Castellanos-Cervantes T, Gomez-Gil B, Carrillo-García ÁE, Campa-Córdova ÁI, Ascencio F (2013) Probiotics in the intestinal tract of juvenile whiteleg shrimp Litopenaeus vannamei: modulation of the bacterial community. World J Microbiol Biotechnol 29:257–265

    Article  CAS  PubMed  Google Scholar 

  28. Duan YF, Zhang Y, Dong HB, Zheng XT, Wang Y, Li H, Liu QS, Zhang JS (2017) Effect of dietary poly-β-hydroxybutyrate (PHB) on growth performance, intestinal health status and body composition of Pacific white shrimp Litopenaeus vannamei (Boone, 1931). Fish Shellfish Immunol 60:520–528

    Article  CAS  PubMed  Google Scholar 

  29. Orino K, Lehman L, Tsuji Y, Ayski H, Torti SV, Torti FM (2001) Ferritin and the response to oxidative stress. Biochem J 357:241–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Official AOAC (2005) Methods of analysis of AOAC International, 18th edn. AOAC International, Gaithersburg

    Google Scholar 

  31. Li J, Tan B, Mai K (2009) Dietary probiotic Bacillus OJ and isomaltooligosaccharides influence the intestine microbial populations, immune responses and resistance to white spot syndrome virus in shrimp (Litopenaeus vannamei). Aquaculture 291:35–40

    Article  CAS  Google Scholar 

  32. Zheng XT, Duan YF, Dong HB, Zhang JS (2017) Effects of dietary Lactobacillus plantarum in different treatments on growth performance and immune gene expression of white shrimp Litopenaeus vannamei under normal condition and stress of acute low salinity. Fish Shellfish Immunol 62:195–201

    Article  CAS  PubMed  Google Scholar 

  33. Pan XD (2006) Research on adherence and anti-bacteria property of Clostridium butyricum and its effect on Miichthys miiuy intestinal physiology. Zhejiang Univ Dissertation, 48–60

  34. Song ZF, Wu TX, Cai LS, Zhang LJ, Zheng XD (2006) Effects of dietary supplementation with Clostridium butyricum on the growth performance and humoral immune response in Miichthys miiuy. J Zhejiang Univ-Sci B 7:596–602

    Article  PubMed  PubMed Central  Google Scholar 

  35. Duan YF, Zhang Y, Dong HB, Wang Y, Zheng XT, Zhang JS (2017) Effect of dietary Clostridium butyricum on growth, intestine health status and resistance to ammonia stress in Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 65:25–33

    Article  CAS  PubMed  Google Scholar 

  36. Wang JH, Zhao LQ, Liu JF, Wang H, Xiao S (2015) Effect of potential probiotic Rhodotorula benthica D30 on the growth performance, digestive enzyme activity and immunity in juvenile sea cucumber Apostichopus japonicas. Fish Shellfish Immunol 43:330–336

    Article  CAS  PubMed  Google Scholar 

  37. Araki Y, Andoh A, Fujiyama Y, Takizawa J, Takizawa W, Bamba T (2002) Oral administration of a product derive from Clostridium butyricum in rats. Int J Mol Med 9:53–57

    CAS  PubMed  Google Scholar 

  38. Li Y, Wei L, Cao JR, Qiu LG, Jiang X, Li P, Song QQ, Zhou HL, Han Q, Diao XP (2016) Oxidative stress, DNA damage and antioxidant enzyme activities in the pacific white shrimp (Litopenaeus vannamei) when exposed to hypoxia and reoxygenation. Chemosphere 144:234–240

    Article  CAS  PubMed  Google Scholar 

  39. Arockiaraj J, Easwvaran S, Vanaraja P, Singh A, Othman RY, Bhassu S (2012) Molecular cloning, characterization and gene expression of an antioxidant enzyme catalase (MrCat) from Macrobrachium rosenbergii. Fish Shellfish Immunol 32:670–682

    Article  CAS  PubMed  Google Scholar 

  40. Tian JX, Chen J, Jiang D, Liao SA, Wang AL (2011) Transcriptional regulation of extracellular copper zinc superoxide dismutase from white shrimp Litopenaeus vannamei following Vibrio alginolyticus and WSSV infection. Fish Shellfish Immunol 30:234–240

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors were grateful to all the laboratory members for experimental material preparation and technical assistance. This study was supported by the earmarked fund for Guangdong Provincial Special Fund for Marine Fisheries Technology (A201701B09), Fund of Key Laboratory of South China Sea Fishery Resources Exploitation & Utilization, Ministry of Agriculture, People’s Republic of China (FREU2017-01), Guangdong Natural Science Foundation (2017A030313147), Guangdong Provincial Key Laboratory of Fishery Ecology and Environment (LFE-2016-12), Central Public-interest Scientific Institution Basal Research Fund, South China Sea Fisheries Research Institute, CAFS (2016TS07), Shenzhen Science and Technology Planning Project (JCYJ20170412110605075).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jiasong Zhang or Jianhua Huang.

Ethics declarations

Conflict of Interest

The authors declare no competing financial interests.

Ethical Approval

The collection and handling of the animals in this study was approved by the Animal Care and Use Committee at the Chinese Academy of Fishery Sciences, and all experimental animal protocols were carried out in accordance with national and institutional guidelines for the care and use of laboratory animals at the Chinese Academy of Fishery Sciences.

Additional information

Highlights

• Effect of dietary Clostridium butyricum supplementation in Penaeus monodon was studied.

C. butyricum improved the growth performance and feed utilization of P. monodon.

C. butyricum influenced the intestine digestive enzyme of P. monodon.

C. butyricum increased the intestine antioxidant capacity of P. monodon resistance to nitrite stress.

C. butyricum had no effect on the body composition of P. monodon.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Duan, Y., Zhang, J., Huang, J. et al. Effects of Dietary Clostridium butyricum on the Growth, Digestive Enzyme Activity, Antioxidant Capacity, and Resistance to Nitrite Stress of Penaeus monodon. Probiotics & Antimicro. Prot. 11, 938–945 (2019). https://doi.org/10.1007/s12602-018-9421-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-018-9421-z

Keywords

Navigation