Skip to main content
Log in

Evaluation of potential probiotics isolated from saline tilapia in shrimp aquaculture

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Integration of tilapia to shrimp culture is currently being practiced to minimize the growth of pathogenic luminous bacteria. The microorganisms that are associated in tilapia may contribute to the inhibition of the growth of Vibrio harveyi through the production of secondary metabolites. In this study, two Bacillus strains (MJA1.1, MJA2.1) isolated from mucus of tilapia were evaluated for their possible application in shrimp culture. The inhibitory property of these isolates against V. harveyi was determined in vitro using co-culture assay in a liquid medium. Also qualitative extracellular enzyme assay was conducted to assess whether the bacterial isolates produce extracellular enzymes. Furthermore, the potential use of these isolates as shrimp feed additive was tested. Thereafter, shrimps were exposed to lethal dose of ammonia (140 mg l−1) to test the effects of the isolates in vivo. The results showed that in vitro co-culture assay after 72 h caused a significant decline in the population of V. harveyi in treatments with potential probiotic isolates. Both isolates showed protease, amylase, and cellulase activities. Although no significant difference was observed in growth, survival was significantly higher in shrimp fed with diets added with either of the isolates. The shrimp exposed to lethal dose of ammonia demonstrated better survival when supplemented with the probionts compared to the control group. Thus, the efficiency of the isolates in inhibiting V. harveyi population and the improvement of survival and resistance of cultured shrimp to ammonia stress indicate their potential as probionts for shrimp culture.

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

Abbreviations

g:

Gram

kg:

Kilogram

min:

Minutes

mg:

Milligram

MYP:

Mannitol egg yolk polymyxin

μl:

Microliter

NSS:

Natural saline solution

References

  • Akhter N, Wu B, Memon AM, Mohsin M (2015) Probiotics and prebiotics associated with aquaculture: a review. Fish Shellfish Immunol 45:733–741

    Article  PubMed  CAS  Google Scholar 

  • Allemeh SK, Yusoff FM, Ring E, Daud HM, Saad CR, Ideris A (2015) Effects of dietary mono-and multiprobiotic strains on growth performance, gut bacteria and body composition of Javanese car (Puntius gonionotus, Bleeker 1850). Aquac Nutr. https://doi.org/10.1111/anu.12265

  • Askarian F, Zhou Z, Olsen RE, Sperstad S, Ringo E (2012) Culturable autochthounous gut bacteria in Atlantic salmon (Salmo salar L.) fed diets with or without chitin. Characterization by 16S rRNA gene sequencing, ability to produce enzymes and in vitro growth inhibition of four fish pathogens. Aquaculture 326-329:1–8. https://doi.org/10.1016/j.aquaculture.2011.10.016

    Article  CAS  Google Scholar 

  • Balaji N, Rajasekaran KM, Kanipandian N, Vignesh V, Thirumurugan R (2012) Isolation and screening of proteolytic bacteria from freshwater fish Cyprinus carpio. Int Multidiscip Res J 2(6):56–59

    Google Scholar 

  • Balcazar JL, de Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Murquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114:173–186

    Article  PubMed  Google Scholar 

  • Brogden G, von Korkritz-Blickwede M, Adamek M, Reuner FM, Jung-Schoers V, Naim HY, Steinhagen D (2012) β-Glucan protects neutrophil extracellular traps against degradation by Aeromonas hydrophila in carp (Cyprinus carpio). Fish Shellfish Immunol 33:1060–1064

    Article  PubMed  CAS  Google Scholar 

  • Bruno MEC, Montville TJ (1993) Common mechanistic action of bacteriocins fromlactic-acid bacteria. Appl Environ Microbiol 59:3003–3010

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chakrabarti I, Gani MA, Chaki KK, Sur R, Misra KK (1995) Digestive enzymes in 11 freshwater teleost fish species in relation to food habit and niche segregation. Comp Biochem Physiol A 122:167–177

    Article  Google Scholar 

  • Chiu YN, Benitez LV (1981) Studies on the carbohydrases in the digestive tract of the milkfish Chanos chanos. Mar Biol 61:247–254

    Article  Google Scholar 

  • Chong A, Hashim R, Ali A, Latiff A, Foo J, Lam TJ (2002) Investigation on some nutritionally important properties from mucus of discus fish (Symphysodon spp.). Paper presented at the World Aquaculture 2002, Beijing, PR China, 23–27 April 2002

  • Corre VL Jr, Janeo R, Caipang CM, Calpe AT (2000) Use of probiotics and reservoir with “green water” and other tips of a successful culture. Aquacult Asia 5:14–18

    Google Scholar 

  • Cruz PM, Ana LI, Oscar AM, Hugo CR (2012) Use of probiotics in aquaculture. Int Sch Res Netw ISRN Microbiol 916845:1–14

    Google Scholar 

  • de la Pena LD, Lavilla-Pitogo CR, Paner MG (2001) Luminescent vibrios associated with morality in pond-cultured shrimp Penaeus monodon in the Philippines: species composition. Fish Pathol 36:133–138

    Article  Google Scholar 

  • De BC, Meena DK, Behera BK, Das P, Mahapatra PKD, Sharma AP (2014) Probiotics in fish and shellfish culture: immunomodulatory and ecophysiological responses. Fish Physiol Biochem 40:921–971. https://doi.org/10.1007/s10695-013-9897-0

    Article  CAS  Google Scholar 

  • Devaraja T, Banerjee S, Sariff YM, Khatoon H (2013) A holistic approach for selection of Bacillus sp. as a bioremediator for shrimp post larvae culture. Turk J Biol 37:92–100

    Google Scholar 

  • Ebran N, Julien S, Organge N, Saglio P, Lemaitre C, Molle G (1999) Pore-forming properties and antibacterial activity of proteins extracted from epidermal fish mucus of fish. Comp Biochem Physiol Mol Integr Physiol 122:181–189

    Article  CAS  Google Scholar 

  • Gildberg A, Mikkelsen H, Sandaker H, Ringo E (1997) Probiotic effect of lactic acid bacteria in the feed on growth and survival of fry of Atlantic cod (Gadus Morhua). Hydrobiologia 352:279–285

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Jacob MB, Gerstein MJ (1960) Handbook of microbiology. D. Van Nostrand Co. Inc., Princeton 61 pp

    Google Scholar 

  • Kaplan M, Koprowski H (1973) Laboratory techniques in rabies. World Health Organization, Geneva

    Google Scholar 

  • Kasana RC, Salwan R, Dhar H, Dutt S, Gulati A (2008) A rapid and easy method for the detection of microbial cellulases on agar plates using Gram’s iodine. Curr Microbiol 57:503–507

    Article  PubMed  CAS  Google Scholar 

  • Kesarcodi-Watson A, Kaspar H, M Lategan J, Gibson L (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274:1–14

  • Keysami MA, Saad CR, Sijam K, Daud HM, Alimon AR (2007) Effect of Bacillus subtilis on growth development and survival of postlarvae Macrobrachium rosenbergii (de Man). Aquac Nutr 13:131e6

    Article  Google Scholar 

  • Kolndadacha OD, Adikwu IA, Okaeme AN, Atiribom RY, Mohammed A, Musa YM (2011) The role of probiotics in aquaculture in Nigeria (a review). Cont J Fish Aquatic Sci 5(1):8–15

    Google Scholar 

  • Krogdahl Å, Hemre GI, Mommsen TP (2005) Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquac Nutr 11:103–122

    Article  CAS  Google Scholar 

  • Lara-Flores M (2011) The use of probiotic in aquaculture: an overview. Int Res J 12:471–478

    Google Scholar 

  • Laranja JL, Ludevese-Pascual G, Amar E, Sorgeloos P, Bossier P, De Schryver P (2014) Poly-β-hydroxybutyrate (PHB) accumulating Bacillus spp. improve the survival growth, growth and robustness of Penaeus monodon postlarvae. Vet Microbiol 173:310–317

    Article  PubMed  CAS  Google Scholar 

  • Lavilla-Pitogo CR, Baticados MCL, Cruz-Lazierda ER, de la Pena LD (1990) Occurrence of luminous bacterial disease of Penaeus monodon larvae in the Philippines. Aquaculture 91:1–13

    Article  Google Scholar 

  • Lazado CC, Caipang CMA (2014) Mucosal immunity and probiotics in fish. Fish Shellfish Immunol 39:78–89

    Article  PubMed  CAS  Google Scholar 

  • Lazado CC, Caipang CMA, Estante EG (2015) Prospects of host-associated microorganism in fish and penaeids as probiotics with immunomodulatory functions. Fish Shellfish Immunol 45:2e12

    Article  CAS  Google Scholar 

  • Li J, Mai K, Ai Q, Zhang W, Xu W, Liufu Z, Ma H (2006) Comparative study between probiotic bacterium Arthrobacter XE-7 and chloramphenicol on protection of Penaeus chinensis post-larvae from pathogenic vibrios. Aquaculture 253:140–147

    Article  CAS  Google Scholar 

  • Lindsay GJH, Harris JE (1980) Carbomethylcellulase activity in the digestive tract of fish. J Fish Biol 16:219–233

    Article  CAS  Google Scholar 

  • Lio-Po GD, Sombito CT, Usero RC (2001) Bacterial flora associated with the “greenwater” culture of the tiger shrimp, Penaeus monodon. Paper presented at the Asian Regional Workshop on Marine Bacterial Diversity, Ocean University of Qingdao, Qingdao, PR China, 9–12 July 2001

  • Mahdhi A, Hmila Z, Chaieb K, Kamoun F, Bakhrouf A (2011) Probiotic properties of halophilic Bacillus strains enhance protection of Artemia culture against pathogenic Vibrio. Aquat Biol 13:225–231

    Article  Google Scholar 

  • Moriarty DJW (1999) Disease control in shrimp aquaculture with probiotic bacteria. In: Proceedings of the 8th international symposium on microbial ecology. Atlantic Canada society for microbial ecology, Halifax, pp 237e43

  • Nair AV, Vijayan KK, Chakraborty K, Leo Antony M (2012) Diversity and characterization of antagonistic bacteria from tropical estuarine habitats of Cochin, India for fish health management. World J Microbiol Biotechnol 28:2581–2592. https://doi.org/10.1007/s11274-012-1067-5

    Article  PubMed  Google Scholar 

  • Nakayama T, Lu H, Nomura N (2009) Inhibitory effects of Bacillus probionts on growth and toxin production of Vibrio harveyi pathogens of shrimp. Appl Microbiol 49(6):679–684

    Article  CAS  Google Scholar 

  • NavinChandran M, Iyapparaj P, Moovendhan S, Ramasubburayan R, Prakash S, Immanuel G (2014) Influence of probiotic bacterium Bacillus cereus isolated from the gut of wild shrimp Penaeus monodon in turn as a potent growth promoter and immune enhancer in P. monodon. Fish Shellfish Immunol 36:38e45

    Article  CAS  Google Scholar 

  • Nimrat S, Suksawat S, Boonthai T, Vuthiphandchai V (2012) Potential Bacillus probiotics enhance bacterial numbers, water quality and growth during early development of white shrimp (Litopenaeus vannamei). Vet Microbiol 159:443–450

    Article  PubMed  Google Scholar 

  • Oke AO, Olaoye OJ, Nnali KE (2013) Recent advances in fish diseases treatment: probiotics as alternative therapy to antibiotics in aquaculture (a review). Adv Agric Sci Eng Res 3(2):668–676

    Google Scholar 

  • Platon RR (1997) Shrimp diseases: are they what ails the shrimp culture industry? Paper presented at the 9th Council Meeting and Business Conference of the Asean Fisheries Federation (AFF), Davao City, Philippines, 2–3 June 1997. 19 p

  • Rengpipat S, Phianphak W, Piyatiratitivorakul S, Menasveta P (1998) Effects of a probiotic bacterium on black tiger shrimp Penaeus monodon survival and growth. Aquaculture 167:301e13

    Article  Google Scholar 

  • Ridha M, Azad I (2012) Preliminary evaluation of growth performance and immune response of Nile tilapia Oreochromis niloticus supplemented with two putative probiotic bacteria. Aquac Res 43:843–852

    Article  CAS  Google Scholar 

  • Sanchez-Ortiz AC, Luna-Gonzalez A, Campa-Cordova AI, Escamilla-ontes R, Flores-Miranda MDC, Mazon-Suasteguin JM (2015) Isolation and characterization of potential probiotic bacteria from pustulose ark (Anadara tuberculosa) suitable for shrimp farming. Lat Am J Aquat Res 43(1):123–136

    Article  Google Scholar 

  • Simora RM, Traifalgar RF, Legario F (2015) Characterization of extracellular enzymes from culturable autochthonous gut bacteria in rabbitfish (Siganus guttatus). ELBA Bioflux 7(1):67–76

    Google Scholar 

  • Sreedevi S, Sreedharan S, Sailas B (2013) Cellulase producing bacteria from the wood-yards on Kallai River Bank. Adv Microbiol 3:326–332. https://doi.org/10.4236/aim.2013.34046

    Article  CAS  Google Scholar 

  • Sugita H, Shibuya K, Hanada H, Deguchi Y (1997) Anti-bacterial abilities of intestinal microflora of the river fish. FishSci 63:378–383

    CAS  Google Scholar 

  • Sutton S (2011) Measurement of microbial cell using optical density. J Validation Technol 17:46–49

    Google Scholar 

  • Tendencia EA, Lavilla-Pitogo CR (2004) Chapter 2. Bacterial diseases. In: Nagasawa K, Cruz-Lacierda ER (eds) Diseases of cultured groupers. SEAFDEC Aquaculture Department, Tigbauan, pp 19–28

    Google Scholar 

  • Turnbull PCB (1996) Bacillus. In: Baron S et al (eds) Barron’s medical microbiology, 4th edn. University of Texas Medical Branch, Galveston

  • Wang YB (2007) Effect of probiotics on growth performance and digestive enzyme activity of the shrimp Penaeus vannamei. Aquaculture 269:259–264

    Article  CAS  Google Scholar 

  • Welker TL, Lim C (2011) Use of probiotics in diets of tilapia. J Aquac Res Dev S1:014. https://doi.org/10.4172/2155-9546.S1-014

    Article  Google Scholar 

  • Williams ST, Goodfellow M, Vickers JC (1984) New microbes from old habitats? In: Kelly DP, Carr NG (eds) The microbe 1984. Part II. Prokaryotes and eukaryotes. Cambridge University Press, Cambridge, pp 219–256

    Google Scholar 

  • Zhou XX, Wang YB, Li WF (2009) Effect of probiotic on larvae shrimp (Penaeus vannamei) based on water quality, survival rate and digestive enzyme activities. Aquaculture 287:349–353

    Article  CAS  Google Scholar 

  • Zokaeifar H, Babaei N, Saad C, Kamarudin MS, Sijam K, Balcazar JL (2014) Administration of Bacillus subtilis strains in the rearing water enhances the water quality, growth performance, immune response, and resistance against Vibrio harveyi infection in juvenile white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 36:68–74

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Department of Science and Technology – Accelerated Science and Technology Human Resource Development Program (DOST-ASTHRDP) and the University of the Philippines Visayas in-house research grant for the financial support extended to this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mary Jane S. Apines-Amar.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Doroteo, A.M., Pedroso, F.L., Lopez, J.D.M. et al. Evaluation of potential probiotics isolated from saline tilapia in shrimp aquaculture. Aquacult Int 26, 1095–1107 (2018). https://doi.org/10.1007/s10499-018-0270-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-018-0270-2

Keywords

Navigation