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Aquaculture International

, Volume 27, Issue 6, pp 1835–1846 | Cite as

Colonization of enzymatic bacterial flora in biofloc grown shrimp Penaeus vannamei and evaluation of their beneficial effect

  • Akshaya PanigrahiEmail author
  • Palanichamy Esakkiraj
  • Sundaresan Jayashree
  • Chakrapani Saranya
  • Rashmi Ranjan Das
  • Mani Sundaram
Article
  • 39 Downloads

Abstract

Experiments were conducted to explore the colonization of beneficial bacteria in shrimp Penaeus vannamei grown in different sources of biofloc and clear water. Beneficial effect in terms of extracellular enzyme production and antibiofilm activity of the isolated strains was determined. Heterotrophic bacterial population were isolated by using different agar plates and resulted in isolation of 94 isolates in total. Extracellular enzyme production such as amylase, protease, lipase, cellulase, xylanase, and pectinase were screened. Antibiofilm activity of culture supernatants of enzymatic strains against pathogenic Vibrio was also determined. Out of 94 strains screened, 36 strains were found to produce amylase enzyme, 20 strains protease, 27 strains lipase, 6 strains cellulase, and 8 strains xylanase. Totally, 21 isolates selected for further identification and different species of Cobetia, Exiguobacterium, Bacillus, Marinilactibacillus, Staphyllococcus, and Novosphingobium genera from biofloc treatments were identified. In control group animals, strains of Bacillus and Exiguobacterium were isolated and identified. The genus Exiguobacterium was found common in all the different treatments and control. The result showed that shrimp grown on biofloc system allows colonizing more beneficial bacteria in gut than control. Few promising strains under Bacillus genus were found to produce all the extracellular enzymes along with antibiofilm activity.

Keywords

Biofloc Shrimp Enzymatic bacteria Protease Amylase Lipase 

Notes

Acknowledgments

The authors are thankful to the director, CIBA for all his support for conducting this research activity.

Funding

This work received financial assistance extended by the Department of Biotechnology, Ministry of Science and Technology, New Delhi, India (F. No. DBT/PR11721/AAQ/3/683/2014).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

The research undertaken complies with the current animal welfare laws in India. Care and treatment of the experimental animal used in this study were in accordance with the guidelines of the CPCSEA [Committee for the Purpose of Control and Supervision of Experiments on Animals, Ministry of Environment & Forests (Animal Welfare Division), Govt. of India] on care and use of animals in scientific research. The study was undertaken with approval of statutory authorities of the Central Institute of Brackishwater Aquaculture, Chennai, India. The experimental animal Penaeus vannamei is not an endangered shrimp, the provisions of the Govt. of India’s Wildlife Protection Act of 1972 are not applicable for experiments on this fish.

Supplementary material

10499_2019_434_MOESM1_ESM.docx (311 kb)
ESM 1 (DOCX 311 kb)

References

  1. Aguilera-Rivera D, Prieto-Davó A, Escalante K, Chávez C, Cuzon G, Gaxiola G (2014) Probiotic effect of FLOC on Vibrios in the pacific white shrimp Litopenaeus vannamei. Aquaculture 424:215–219CrossRefGoogle Scholar
  2. Avnimelech Y (1999) Carbon / nitrogen ratio as a control element in aquaculture systems. Aquaculture 176:227–235CrossRefGoogle Scholar
  3. Balcázar JL, Vendrell D, de Blas I, Ruiz-Zarzuela I, Muzquiz JL, Girones O (2008) Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture 278(1–4):188–191CrossRefGoogle Scholar
  4. Banerjee S, Ghosh K (2014) Enumeration of gut associated extracellular enzyme-producing yeasts in some freshwater fishes. J Appl Ichthyol 30(5):986–993CrossRefGoogle Scholar
  5. Banerjee G, Dan SK, Ankita N, Pinki G, Ray AK (2015) Autochthonous gut bacteria in two Indian air-breathing fish, climbing perch (Anabas testudineus) and walking catfish (Clarias batrachus): mode of association, identification, and enzyme producing ability. Pol J Microbiol 64(4):361–368CrossRefGoogle Scholar
  6. Cardona E, Gueguen Y, Magré K, Lorgeoux B, Piquemal D, Pierrat F, Noguier F, Saulnier D (2016) Bacterial community characterization of water and intestine of the shrimp Litopenaeus stylirostris in a biofloc system. BMC Microbiol 16(1):157CrossRefGoogle Scholar
  7. Crab R, Kochva M, Verstraete W, Avnimelech Y (2009) Bio-flocs technology application in over-wintering of tilapia. Aquac Eng 40:105–112CrossRefGoogle Scholar
  8. Crab R, Lambert A, Defoirdt T, Bossier P, Verstraete W (2010) The application of bioflocs technology to protect brine shrimp (Artemia franciscana) from pathogenic Vibrio harveyi. J Appl Microbiol 109(5):1643–1649PubMedGoogle Scholar
  9. Ebeling JM, Timmons MB, Bisogni JJ (2006) Engineering analysis of the stoichiometry of photoautotrophic, autotrophic, and heterotrophic removal of ammonia–nitrogen in aquaculture systems. Aquaculture 257:346–358CrossRefGoogle Scholar
  10. Ekasari J, Azhar MH, Surawidjaja EH, Nuryati S, De Schryver P, Bossier P (2014) Immune response and disease resistance of shrimp fed biofloc grown on different carbon sources. Fish Shellfish Immunol 41(2):332–339CrossRefGoogle Scholar
  11. Emerenciano M, Ballester EL, Cavalli RO, Wasielesky W (2012) Biofloc technology application as a food source in a limited water exchange nursery system for pink shrimp Farfantepenaeus brasiliensis (Latreille, 1817). Aquac Res 43(3):447–457CrossRefGoogle Scholar
  12. Esakkiraj P, Immanuel G, Sowmya SM, Iyapparaj P, Palavesam A (2009) Evaluation of protease-producing ability of fish gut isolate Bacillus cereus for aqua feed. Food Bioprocess Technol 2(4):383–390CrossRefGoogle Scholar
  13. Esakkiraj P, Rajkumarbharathi M, Palavesam A, Immanuel G (2010) Lipase production by Staphylococcus epidermidis CMST-Pi 1 isolated from the gut of shrimp Penaeus indicus. Ann Microbiol 60(1):37–42CrossRefGoogle Scholar
  14. Esakkiraj P, Meleppat B, Lakra AK, Ayyanna R, Arul V (2016) Cloning, expression, characterization and application of protease produced by Bacillus cereus PMW8. RSC Adv 6(45):38611–38616CrossRefGoogle Scholar
  15. Hargreaves JA (2006) Photosynthetic suspended-growth systems in aquaculture. Aquacult Eng 34:344–363CrossRefGoogle Scholar
  16. Kalpana BJ, Aarthy S, Pandian SK (2012) Antibiofilm activity of α-amylase from Bacillus subtilis S8-18 against biofilm forming human bacterial pathogens. Appl Biochem Biotechnol 167(6):1778–1794CrossRefGoogle Scholar
  17. Kumar PA, Suresh PV (2014) Biodegradation of shrimp biowaste by marine Exiguobacterium sp. CFR26M and concomitant production of extracellular protease and antioxidant materials: production and process optimization by response surface methodology. Mar Biotechnol 16(2):202–218CrossRefGoogle Scholar
  18. Lei F, Cui C, Zhao Q, Sun-Waterhouse D, Zhao M (2014) Evaluation of the hydrolysis specificity of protease from marine Exiguobacterium sp. SWJS2 via free amino acid analysis. Appl Biochem Biotechnol 174(4):1260–1271CrossRefGoogle Scholar
  19. Liu H, Guo X, Gooneratne R, Lai R, Zeng C, Zhan F, Wang W (2016) The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Sci Rep 6:24340CrossRefGoogle Scholar
  20. Lyu Y, Zheng W, Zheng T, Tian Y (2014) Biodegradation of polycyclic aromatic hydrocarbons by Novosphingobium pentaromativorans US6-1. PLoS One 9(7):e101438CrossRefGoogle Scholar
  21. Mawlankar R, Thorat MN, Krishnamurthi S, Dastager SG (2016) Bacillus cellulasensis sp. nov., isolated from marine sediment. Arch Microbiol 198(1):83–89CrossRefGoogle Scholar
  22. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267CrossRefGoogle Scholar
  23. Nikoskelainen S, Ouwehand AC, Bylund G, Salminen S, Lilius E (2003) Immune enhancement in rainbow trout (Oncorhynchus mykiss) by potential probiotic bacteria (Lactobacillus rhamnosus). Fish Shellfish Immunol 15(5):443–452CrossRefGoogle Scholar
  24. Ohta Y, Nishi S, Hasegawa R, Hatada Y (2015) Combination of six enzymes of a marine Novosphingobium converts the stereoisomers of β-O-4 lignin model dimers into the respective monomers. Sci Rep 5:15105CrossRefGoogle Scholar
  25. Otta SK, Praveena PE, Raj RA, Saravanan P, Priya MS, Amarnath CB, Bhuvaneswari T, Panigrahi A, Ravichandran P (2018) Pythium insidiosum as a new opportunistic fungal pathogen for Pacific white shrimp, Litopenaeus vannamei. Indian J Geomarine Sci 47:1036–1041Google Scholar
  26. Panigrahi A, Kiron V, Puangkaew J, Kobayashi T, Satoh S, Sugita H (2005) The viability of probiotic bacteria as a factor influencing the immune response in rainbow trout Oncorhynchus mykiss. Aquaculture. 243(1–4):241–254CrossRefGoogle Scholar
  27. Panigrahi A, Saranya C, Sundaram M, Vinoth Kannan SR, Das Rasmi R, Satish Kumar R, Rajesh P, Otta SK (2018) Carbon: nitrogen (C:N) ratio level variation influences microbial community of the system and growth as well as immunity of shrimp (Litopenaeus vannamei) in biofloc based culture system. Fish Shellfish Immunol 81:329–337CrossRefGoogle Scholar
  28. Panigrahi A, Sundaram M, Sarany C, Rajasekar S, Syama Dayal J, Gopal C (2019a) Effect of carbon and nitrogen ratio (C: N) manipulation on the production performance and immunity of Pacific white shrimp Litopenaeus vannamei (Boone, 1931) in a biofloc-based rearing system. Aquac Res 50(1):29–41CrossRefGoogle Scholar
  29. Panigrahi A, Sundaram M, Saranya C, Kumar RS, Dayal JS, Saraswathy R, Otta SK, Anand PS, Rekha PN, Gopal C (2019b) Influence of differential protein levels of feed on production performance and immune response of pacific white leg shrimp in a biofloc–based system. Aquacult 503:118–127CrossRefGoogle Scholar
  30. Panigrahi A, Sundaram M, Saranya C, Swain S, Das RR, Dayal JS (2019c) Carbohydrate sources deferentially influence growth performances, microbial dynamics and immunomodulation in Pacific white shrimp (Litopenaeus vannamei) under biofloc system. Fish Shellfish Immunol 86:1207–1216CrossRefGoogle Scholar
  31. Ray AJ, Dillon KS, Lotz JM (2011) Water quality dynamics and shrimp (Litopenaeus vannamei) production in intensive, mesohaline culture systems with two levels of biofloc management. Aquac Eng 45(3):127–136CrossRefGoogle Scholar
  32. Saha S, Roy RN, Sen SK, Ray AK (2006) Characterization of cellulase producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (Peters) and grass carp, Ctenopharyngodon idella (Valenciennes). Aquac Res 37(4):380–388CrossRefGoogle Scholar
  33. Suryakumar B, Avnimelech Y (2017) Adapting biofloc technology for use in small-scale ponds with vertical substrate. World Aquacult 55Google Scholar
  34. Tzuc JT, Escalante DR, Herrera RR, Cortés GG, Ortiz MLA (2014) Microbiota from Litopenaeus vannamei: digestive tract microbial community of Pacific white shrimp (Litopenaeus vannamei). SpringerPlus 3(1):280CrossRefGoogle Scholar
  35. Ugbenyen AM, Okoh AI (2014) Characteristics of a bioflocculant produced by a consortium of Cobetia and Bacillus species and its application in the treatment of wastewaters. Water SA 40(1):140–144CrossRefGoogle Scholar
  36. Ugbenyen A, Cosa S, Mabinya L, Babalola OO, Aghdasi F, Okoh A (2012) Thermostable bacterial bioflocculant produced by Cobetia spp. isolated from Algoa Bay (South Africa). Int J Environl Res Public Health 9(6):2108–2120CrossRefGoogle Scholar
  37. Waite R, Beveridge M, Brummett R, Castine S, Chaiyawannakarn N, Kaushik S, Mungkung R, Nawapakpilai S, Phillips M (2014) Improving productivity and environmental performance of aquaculture. WorldFish:1–60Google Scholar
  38. Xie TT, Zeng H, Ren XP, Wang N, Chen ZJ, Zhang Y, Chen W (2019) Antibiofilm activity of three Actinomycete strains against Staphylococcus epidermidis. Lett Appl Microbiol 68(1):73–80CrossRefGoogle Scholar
  39. Xu WJ, Pan LQ, Sun XH, Huang J (2013) Effects of bioflocs on water quality, and survival, growth and digestive enzyme activities of Litopenaeus vannamei (Boone) in zero-water exchange culture tanks. Aquac Res 44(7):1093–1102CrossRefGoogle Scholar
  40. Yuan J, Lai Q, Zheng T, Shao Z (2009) Novosphingobium indicum sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from a deep-sea environment. Int J Syst Evol Microbiol 59(8):2084–2088CrossRefGoogle Scholar
  41. Yuvaraj N, Arul V (2014) Preliminary screening of anti-biofilm, anti-larval settlement and cytotoxic potential of seaweeds and seagrasses collected from Pondicherry and Rameshwaram coastal line, India. World J Fish Mar Sci 6(2):169–175Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Akshaya Panigrahi
    • 1
    Email author
  • Palanichamy Esakkiraj
    • 1
  • Sundaresan Jayashree
    • 1
  • Chakrapani Saranya
    • 1
  • Rashmi Ranjan Das
    • 1
  • Mani Sundaram
    • 1
  1. 1.Crustacean Culture DivisionICAR-Central Institute of Brackishwater AquacultureChennaiIndia

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