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Isolation of Lactic Acid Bacteria from Intestine of Freshwater Fishes and Elucidation of Probiotic Potential for Aquaculture Application

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Abstract

Probiotics play significant roles in enhancing systemic immunity, improving intestinal balance and feed value, enhancing enzymatic digestion, and inhibiting pathogenic microorganisms of freshwater fish. Probiotics from an identical organism’s gastrointestinal system promote effective colonization and provide greater benefits than other sources. This study aimed to evaluate the usefulness of probiotic bacteria isolated from the intestines of freshwater fishes for a dietary supplement of freshwater aquaculture. A total of 120 isolates were collected from freshwater fishes of Channa striata, Puntius filamentosus, Oreochromis mossambicus, Cirrhinus mrigala, and Rasbora daniconius. Seven of these isolates exhibited antagonistic activity against fish pathogens: Aeromonas hydrophila, Staphylococcus epidermidis, Staphylococcus aureus, Bacillus cereus, Escherichia coli, and Pseudomonas aeruginosa. Using 16S rRNA gene sequencing analysis, the isolates were identified as Enterococcus sp., Lactococcus lactis, Weissella cibaria, and Limosilactobacillus fermentum. Of these tolerates, L. fermentum URLP18 isolated from C. mrigala exhibited high tolerance to low acidic (pH 2.0) and high bile salt (2%) concentrations, exhibiting a significant hydrophobicity and extracellular enzyme secretions like amylase, protease, and lipase. In vitro evaluations on intestinal mucus indicate that L. fermentum URLP18 have strong adherence capacity, and its survival rate increased after being administered to Artemia nauplii. The results suggest that L. fermentum URLP18 has high probiotic potential and is an effective dietary supplement for freshwater aquaculture.

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References

  1. Wanka KM, Damerau T, Costas B, Krueger A, Schulz C, Wuertz S (2018) Isolation and characterization of native probiotics for fish farming. BMC Microbiol 18(1):1–13. https://doi.org/10.1186/s12866-018-1260-2

    Article  CAS  Google Scholar 

  2. FAO (2018) Food and Agriculture Organization of the United Nations. State of the World Fisheries and Aquaculture: meeting the sustainable development goals, Rome, p 227. http://www.fao.org/3/i9540en/i9540en.pdf. Accessed on 4 April 2019.

  3. Ashraf SA, Adnan M, Patel M, Siddiqui AJ, Sachidanandan M, Snoussi M, Hadi S (2020) Fish-based bioactives as potent nutraceuticals: exploring the therapeutic perspective of sustainable food from the Sea. Mar Drugs 18:265–285. https://doi.org/10.3390/md18050265

  4. Patel M, Ashraf MS, Siddiqui AJ, Ashraf SA, Sachidanandan M, Snoussi M, Adnan M, Hadi S (2020) Profiling and role of bioactive molecules from Puntius sophore (freshwater/brackish fish) skin mucus with its potent antibacterial, antiadhesion, and antibiofilm activities. Biomolecules 10:920–946. https://doi.org/10.3390/biom10060920

    Article  CAS  PubMed Central  Google Scholar 

  5. Jennings S, Stentiford GD, Leocadio AM, Jeffery KR, Metcalfe JD, Katsiadaki I, Auchterlonie NA, Mangi SC, Pinnegar JK, Ellis T, Peeler EJ, Luisetti T, Baker-Austin C, Brown M, Catchpole TL, Clyne FJ, Dye SR, Edmonds NJ, Hyder K, Lee J, Lees DN, Morgan OC, O’Brien CM, Oidtmann B, Posen PE, Santos AR, Taylor NGH, Turner AD, Townhill BL, Verner-Jeffreys DW (2016) Aquatic food security: insights into challenges and solutions from an analysis of interactions between fisheries, aquaculture, food safety, human health, fish and human welfare, economy and environment. Fish Fish 17(4):893–938. https://doi.org/10.1111/faf.12152

    Article  Google Scholar 

  6. Boyd CE, D’Abramo LR, Glencross BD, Huyben DC, Juarez LM, Lockwood GS, McNevin AA, Tacon AGJ, Teletchea F, Tomasso JR, Tucker CS, Valenti WC (2020) Achieving sustainable aquaculture: historical and current perspectives and future needs and challenges. J World Aquac Soc 51(3):578–633. https://doi.org/10.1111/jwas.12714

    Article  Google Scholar 

  7. Bondad-Reantaso MG, Subasinghe RP, Arthur JR, Ogawa K, Chinabut S, Adlard R, Tan Z, Shariff M (2005) Disease and health management in Asian aquaculture. Vet Parasitol 132:249–272. https://doi.org/10.1016/j.vetpar.2005.07.005

    Article  PubMed  Google Scholar 

  8. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM, Dawood MA, Kader A, Bulbul M, Fujieda T (2016) Efficacy of nucleotide related products on growth, blood chemistry, oxidative stress and growth factor gene expression of juvenile red sea bream, Pagrus major. Aquaculture 464:8–16. https://doi.org/10.1016/j.aquaculture.2016.06.004

    Article  CAS  Google Scholar 

  9. Fjellheim AJ, Klinkenberg G, Skjermo J, Aasen IM, Vadstein O (2010) Selection of candidate probionts by two different screening strategies from Atlantic cod (Gadus morhua L.) larvae. Vet Microbiol 144(1–2):153–159. https://doi.org/10.1016/j.vetmic.2009.12.032.

  10. Ringø E, Gatesoupe FJ (1998) Lactic acid bacteria in fish: a review. Aquaculture 160:177–203. https://doi.org/10.1016/S0044-8486(97)00299-8

    Article  Google Scholar 

  11. Lazado CC, Caipang CMA (2014) Mucosal immunity and probiotics in fish. Fish Shellfish Immun 39:78–89. https://doi.org/10.1016/j.fsi.2014.04.015

    Article  CAS  Google Scholar 

  12. Balcázar JL, Decamp O, Vendrell D, De Blas I, Ruiz-Zarzuela I (2006) Health and nutritional properties of probiotics in fish and shellfish. Microb Ecol Health Dis 18:65–70. https://doi.org/10.1080/08910600600799497

    Article  CAS  Google Scholar 

  13. Mohapatra S, Chakraborty T, Prusty AK, Das P, Paniprasad K, Mohanta KN (2012) Use of different microbial probiotics in the diet of rohu, Labeo rohita fingerlings: effects on growth, nutrient digestibility and retention, digestive enzyme activities and intestinal microflora. Aquacult Nutr 18:1–11. https://doi.org/10.1111/j.1365-2095.2011.00866.x

    Article  CAS  Google Scholar 

  14. Ridha MT, Azad IS (2016) Effect of autochthonous and commercial probiotic bacteria on growth, persistence, immunity and disease resistance in juvenile and adult Nile tilapia Oreochromis niloticus. Aquac Res 47:2757–2767. https://doi.org/10.1111/are.12726

    Article  CAS  Google Scholar 

  15. Hai NV (2015) The use of probiotics in aquaculture. J Appl Microbiol 119:917–935. https://doi.org/10.1111/jam.12886

  16. Jahangiri L, Esteban MÁ (2018) Administration of probiotics in the water in finfish aquaculture systems: a review. Fishes 3(3):33. https://doi.org/10.3390/fishes3030033

    Article  Google Scholar 

  17. Lamari F, Sadok K, Bakhrouf A, Gatesoupe FJ (2014) Selection of lactic acid bacteria as candidate probiotics and in vivo test on Artemia nauplii. Aquacult Int 22:699–709. https://doi.org/10.1007/s10499-013-9699-5

    Article  CAS  Google Scholar 

  18. Akanmu, OA (2018) Probiotics, an alternative measure to chemotherapy in fish production. In: Probiotics - current knowledge and future prospects. Shymaa Enany, IntechOpen, p151. https://doi.org/10.5772/intechopen.72923. https://www.intechopen.com/books/probiotics-current-knowledge-and-future-prospects/probiotics-an-alternative-measure-to-chemotherapy-in-fish-production

  19. Gómez GD, Balcázar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52(2):145–154. https://doi.org/10.1111/j.1574-695X.2007.00343.x

    Article  CAS  PubMed  Google Scholar 

  20. Banerjee G, Nandi A, Ray AK (2017) Assessment of hemolytic activity, enzyme production and bacteriocin characterization of Bacillus subtilis LR1 isolated from the gastrointestinal tract of fish. Arch Microbiol 199:115–124. https://doi.org/10.1007/s00203-016-1283-8

    Article  CAS  PubMed  Google Scholar 

  21. Zorriehzahra MJ, Delshad ST, Adel M, Tiwari R, Karthik K, Dhama K, Lazado CC (2016) Probiotics as beneficial microbes in aquaculture: an update on their multiple modes of action: a review. Vet Q 36(4):228–241. https://doi.org/10.1080/01652176.2016.1172132

  22. Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64:655–671. https://doi.org/10.1128/MMBR.64.4.655-671.2000

  23. Lazado CC, Caipang CMA, Estante EG (2015) Prospects of host-associated microorganisms in fish and penaeids as probiotics with immunomodulatory functions. Fish Shellfish Immun 45:2–12. https://doi.org/10.1016/j.fsi.2015.02.023

    Article  CAS  Google Scholar 

  24. Van Doan H, Hoseinifar SH, Khanongnuch C, Kanpiengjai A, Unban K, Srichaiyo S (2018) Host-associated probiotics boosted mucosal and serum immunity, disease resistance and growth performance of Nile tilapia (Oreochromis niloticus). Aquaculture 491:94–100. https://doi.org/10.1016/j.aquaculture.2018.03.019

    Article  Google Scholar 

  25. Van Doan H, Hoseinifar SH, Ringø E, Angeles Esteban M, Dadar M, Dawood MA, Faggio C (2020) Host-associated probiotics: a key factor in sustainable aquaculture. Rev Fish Sci Aquac 28(1):16–42. https://doi.org/10.1080/23308249.2019.1643288

    Article  Google Scholar 

  26. Ray AK, Ghosh K, Ringø E (2012) Enzyme-producing bacteria isolated from fish gut: a review. Aquac Nutr 18:465–492. https://doi.org/10.1111/j.1365-2095.2012.00943.x

    Article  CAS  Google Scholar 

  27. Sullam KE, Essinger SD, Lozupone CA, O’Connor MP, Rosen GL, Knight R, Kilham SS, Russel J (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a metaanalysis. Mol Ecol 21:3363–3378. https://doi.org/10.1111/j.1365-294X.2012.05552.x

    Article  PubMed  Google Scholar 

  28. Karl JP, Hatch AM, Arcidiacono SM, Pearce SC, Pantoja-Feliciano IG, Doherty LA, Soares JW (2018) Effects of psychological, environmental and physical stressors on the gut microbiota. Front Microbiol 9:2013. https://doi.org/10.3389/fmicb.2018.02013

    Article  PubMed  PubMed Central  Google Scholar 

  29. Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman W (2009) Bergey’s manual of systematic bacteriology. 3:2 Springer-Verlag New York

  30. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press

    Google Scholar 

  31. Vergin KL, Urbach E, Stein JL, DeLong EF, Lanoil BD, Giovannoni SJ (1998) Screening of a fosmid library of marine environmental genomic DNA fragments reveals four clones related to members of the order Planctomycetales. Appl Environ Microbiol 64:3075–3078. https://doi.org/10.1128/AEM.64.8.3075-3078.1998

  32. Gerhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, Krieg NR, Phillips GB (1981) Manual of methods for general bacteriology, ASM p 415–416. https://www.journals.uchicago.edu/doi/pdf/10.1086/412854

  33. Buxton R (2005) Blood agar plates and hemolysis protocols. ASM p 1–9. https://www.asmscience.org/content/education/protocol/protocol.2885

  34. Harrigan WF, McCance ME (1976) Laboratory methods in food and dairy microbiology. Academic Press Inc. https://doi.org/10.1002/jobm.19780180316

  35. Maijala RL (1993) Formation of histamine and tyramine by some lactic acid bacteria in MRS-broth and modified decarboxylation agar. Lett Appl Microbiol 17:40–43. https://doi.org/10.1080/10942912.2016.1152479

    Article  CAS  Google Scholar 

  36. Conway PL, Gorbach SL, Goldin BR (1987) Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. J Dairy Sci 70:1–12. https://doi.org/10.3168/jds.S0022-0302(87)79974-3

    Article  CAS  PubMed  Google Scholar 

  37. Nikoskelainen S, Ouwehand A, Salminen S, Bylund G (2001) Protection of rainbow trout (Oncorhynchus mykiss) from furunculosis by Lactobacillus rhamnosus. Aquaculture 198:229–236. https://doi.org/10.1016/S0044-8486(01)00593-2

    Article  Google Scholar 

  38. Janković T, Frece J, Abram M, Gobin I (2012) Aggregation ability of potential probiotic Lactobacillus plantarum strains. Int J Sanitary Eng Res 6:19–24. https://journal.institut-isi.si/wp-content/uploads/2016/02/Vol6-no-1_Aggregation-ability.pdf

  39. Handley PS, Harty DW, Wyatt JE, Brown CR, Doran JP, Gibbs AC (1987) A comparison of the adhesion, coaggregation and cell-surface hydrophobicity properties of fibrillar and fimbriate strains of Streptococcus salivarius. Microbiology 133:3207–3217. https://doi.org/10.1099/00221287-133-11-3207

    Article  CAS  Google Scholar 

  40. Qing Li, Liu X, Dong M, Zhou J, Wang Y (2014) Aggregation and adhesion abilities of 18 lactic acid bacteria strains isolated from traditional fermented food. Int J Agric Policy Res 3:84–92. https://doi.org/10.15739/IJAPR.030

  41. Wu SC, Pan CL (2004) Preparation of algal oligosaccharide mixtures by bacterial agaroses and their antioxidative properties. Fish Sci 70:1164–1173. https://doi.org/10.1111/j.1444-2906.2004.00919.x

    Article  CAS  Google Scholar 

  42. Vesterlund S, Paltta J, Karp M, Ouwehand AC (2005) Measurement of bacterial adhesion in vitro evaluation of different methods. J Microbiol Methods 60:225–233. https://doi.org/10.1016/j.mimet.2004.09.013

    Article  CAS  PubMed  Google Scholar 

  43. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3

    Article  CAS  Google Scholar 

  44. Jinendiran S, Boopathi S, Sivakumar N, Selvakumar G (2017) Functional characterization of probiotic potential of novel pigmented bacterial strains for aquaculture applications. Probiotics Antimicrob Proteins 11(1):186–197. https://doi.org/10.1007/s12602-017-9353-z

    Article  CAS  Google Scholar 

  45. Bauer AW, Kirby WMM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496. https://doi.org/10.1093/ajcp/45.4_ts.493

    Article  CAS  PubMed  Google Scholar 

  46. Banerjee G, Ray AK (2017) Bacterial symbiosis in the fish gut and its role in health and metabolism. Symbiosis 72:1–11. https://doi.org/10.1007/s13199-016-0441-8

    Article  CAS  Google Scholar 

  47. Selim KM, Reda RM (2015) Beta-glucans and mannan oligosaccharides enhance growth and immunity in Nile tilapia. N Am J Aquac 77(1):22–30. https://doi.org/10.1080/15222055.2014.951812

    Article  Google Scholar 

  48. Ringø E, Sperstad S, Myklebust R, Refstie S, Krogdahl Å (2006) Characterization of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.): the effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture 261:829–841. https://doi.org/10.1016/j.aquaculture.2006.06.030

    Article  CAS  Google Scholar 

  49. Allameh SK, Daud HM, Yusoff FM, Saad CR, Ideris A (2012) Isolation, identification and characterization of Leuconostoc mesenteroides as a new probiotic from intestine of snakehead fish (Channa striatus). Afr J Biotechnol 11:3810–3816. https://doi.org/10.5897/AJB11.1871

    Article  CAS  Google Scholar 

  50. Ringø E, Strøm E, Tabachek JA (1995) Intestinal microflora of salmonids: a review. Aquac Res 26:773–789. https://doi.org/10.1111/j.1365-2109.1995.tb00870.x

    Article  Google Scholar 

  51. Cai Y, Suyanandana P, Saman P, Benno Y (1999) Classification and characterization of lactic acid bacteria isolated from the intestines of common carp and freshwater prawns. J Gen Appl Microbiol 45:177–184. https://doi.org/10.2323/jgam.45.177

    Article  CAS  PubMed  Google Scholar 

  52. Kaktcham PM, Temgoua JB, Zambou FN, Diaz-Ruiz G, Wacher C, de Lourdes P-C (2017) Quantitative analyses of the bacterial microbiota of rearing environment, tilapia and common carp cultured in earthen ponds and inhibitory activity of its lactic acid bacteria on fish spoilage and pathogenic bacteria. World J Microbiol Biotechnol 33(2):32. https://doi.org/10.1007/s11274-016-2197-y

    Article  PubMed  Google Scholar 

  53. Pérez-Sánchez T, Balcázar JL, García Y, Halaihel N, Vendrell D, De Blas I, Merrifield DL, Ruiz-Zarzuela I (2011) Identification and characterization of lactic acid bacteria isolated from rainbow trout, Oncorhynchus mykiss (Walbaum), with inhibitory activity against Lactococcus garvieae. J Fish Dis 34:499–507. https://doi.org/10.1111/j.1365-2761.2011.01260.x

    Article  CAS  PubMed  Google Scholar 

  54. Reda RM, Selim KM, El-Sayed HM, El-Hady MA (2018) In vitro selection and identification of potential probiotics isolated from the gastrointestinal tract of Nile tilapia, Oreochromis niloticus. Probiotics Antimicrob Proteins 10:692–703. https://doi.org/10.1007/s12602-017-9314-6

    Article  CAS  PubMed  Google Scholar 

  55. Gonçalves LMD, Ramos A, Almeida JS, Xavier AMRB, 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. https://doi.org/10.1007/s002530051060

    Article  Google Scholar 

  56. Lin YH, Chen YS, Wu HC, Pan SF, Yu B, Chiang CM, Chiu CM, Yanagida F (2013) Screening and characterization of LAB-produced bacteriocin-like substances from the intestine of grey mullet (Mugil cephalus L.) as potential biocontrol agents in aquaculture. J Appl Microbiol 114:299–307. https://doi.org/10.1111/jam.12041

    Article  CAS  PubMed  Google Scholar 

  57. Martínez Cruz PM, Ibáñez AL, Monroy Hermosillo OA, Ramírez Saad HC (2012) Use of probiotics in aquaculture. Int Sch Res Notices Microbiol 2012:916845. https://doi.org/10.5402/2012/916845

  58. Gupta A, Gupta P, Dhawan A (2016) Paenibacillus polymyxa as a water additive improved immune response of Cyprinus carpio and disease resistance against Aeromonas hydrophila. Aquacult Rep 4:86–92. https://doi.org/10.1016/j.aqrep.2016.07.002

    Article  Google Scholar 

  59. Ruiz L, Margolles A, Sánchez B (2013) Bile resistance mechanisms in Lactobacillus and Bifidobacterium. Front Microbiol 4:396. https://doi.org/10.3389/fmicb.2013.00396

  60. Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41:1553–1573. https://doi.org/10.1111/j.1365-2109.2010.02546.x

  61. Succi M, Tremonte P, Reale A, Sorrentino E, Grazia L, Pacifico S, Coppola R (2005) Bile salt and acid tolerance of Lactobacillus rhamnosus strains isolated from Parmigiano Reggiano cheese. FEMS Microbiol Lett 244:129–137. https://doi.org/10.1016/j.femsle.2005.01.037

    Article  CAS  PubMed  Google Scholar 

  62. Amin M, Adams M, Bolch CJ, Burke CM (2017) In vitro screening of lactic acid bacteria isolated from gastrointestinal tract of Atlantic Salmon (Salmo salar) as probiont candidates. Aquacult Int 25:485–498. https://doi.org/10.1007/s10499-016-0045-6

    Article  CAS  Google Scholar 

  63. Allameh SK, Yusoff FM, Daud HM, Ringø E, Ideris A, Saad CR (2013) Characterization of a probiotic Lactobacillus fermentum isolated from snakehead, Channa striatus stomach. J World Aquac Soc 44(6):835–844. https://doi.org/10.1111/jwas.12075

    Article  Google Scholar 

  64. 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 278:188–191. https://doi.org/10.1016/j.aquaculture.2008.03.014

    Article  CAS  Google Scholar 

  65. Tuan TN, Duc PM, Hatai K (2013) Overview of the use of probiotics in aquaculture. Int J Res Fish Aquac 3:89–97

    Google Scholar 

  66. Adel M, El-Sayed AFM, Yeganeh S, Dadar M, Giri SS (2017) Effect of potential probiotic Lactococcus lactis subsp. lactis on growth performance, intestinal microbiota, digestive enzyme activities, and disease resistance of Litopenaeus vannamei. Probiotics Antimicro Prot 9:150–156. https://doi.org/10.1007/s12602-016-9235-9

    Article  CAS  Google Scholar 

  67. Huddy RJ, Coyne VE (2015) Characterisation of the role of an alkaline protease from Vibrio midae SY9 in enhancing the growth rate of cultured abalone fed a probiotic-supplemented feed. Aquaculture 448:128–134. https://doi.org/10.1016/j.aquaculture.2015.05.048

    Article  CAS  Google Scholar 

  68. Boris S, Suárez JE, Vázquez F, Barbés C (1998) Adherence of human vaginal lactobacilli to vaginal epithelial cells and interaction with uropathogens. Infect Immun 66:1985–1989. https://doi.org/10.1128/IAI.66.5.1985-1989.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Collado MC, Meriluoto J, Salminen S (2008) Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol 226:1065–1073. https://doi.org/10.1007/s00217-007-0632-x

    Article  CAS  Google Scholar 

  70. Kos BVZE, Šušković J, Vuković S, Šimpraga M, Frece J, Matošić S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94:981–987. https://doi.org/10.1046/j.1365-2672.2003.01915.x

    Article  CAS  PubMed  Google Scholar 

  71. Sánchez-Ortiz AC, Luna-González A, Campa-Córdova ÁI, Escamilla-Montes R, del Carmen F-M, Mazón-Suástegu JM (2015) Isolation and characterization of potential probiotic bacteria from pustulose ark (Anadara tuberculosa) suitable for shrimp farming. Lat AM J Aquat Res 43:123–136. https://doi.org/10.3856/vol43-issue1-fulltext-11

    Article  Google Scholar 

  72. Yadav VK, Oury F, Suda N, Liu ZW, Gao XB, Confavreux C, Klemenhagen CK, Tanaka KF, Gingrich JA, Guo XE, Tecott LH, Mann JJ, Hen R, Horvath TL, Karsenty G (2009) A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell 138:976–989. https://doi.org/10.1016/j.cell.2009.06.051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Ismail M, Ibrar M, Iqbal Z, Hussain J, Hussain H, Ahmed M, Ejaz A, Choudhary MI (2009) Chemical constituents and antioxidant activity of Geranium wallichianum. Rec Nat Prod 3(4):193–197. https://www.acgpubs.org/doc/2018080514503728-RNP-0907-122.pdf

  74. Adnan M, Patel M, Hadi S (2017) Functional and health promoting inherent attributes of Enterococcus hirae F2 as a novel probiotic isolated from the digestive tract of the freshwater fish Catla catla. Peer J 5:e3085. https://doi.org/10.7717/peerj.3085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Ouwehand A, Vankerckhoven V, Goossens H, Huys G, Swings J, Vancanneyt M, Lähteenmäki A (2005) The safety of probiotics in foods in Europe and its legislation. Probiotics in food safety and human health. CRC Press, Boca Raton, pp 405–429

    Google Scholar 

  76. Mete A, Coşansu S, Demirkol O, Ayhan K (2017) Amino acid decarboxylase activities and biogenic amine formation abilities of lactic acid bacteria isolated from shalgam. Int J Food Prop 20(1):171–178. https://doi.org/10.1080/10942912.2016.1152479

    Article  CAS  Google Scholar 

  77. Panigrahi A, Azad I (2007) Microbial intervention for better fish health in aquaculture: the Indian scenario. Fish Physiol Biochem 33:429–440. https://doi.org/10.1007/s10695-007-9160-7

    Article  CAS  Google Scholar 

  78. Conway PL (1996) Selection criteria for probiotic microorganisms. Asia Pac J Clin Nutr 5:10–14. http://apjcn.nhri.org.tw/server/APJCN/5/1/10.pdf

  79. Collado MC, Meriluoto J, Salminen S (2007) In vitro analysis of probiotic strain combinations to inhibit pathogen adhesion to human intestinal mucus. Food Res Int 40:629–636. https://doi.org/10.1016/j.foodres.2006.11.007

    Article  CAS  Google Scholar 

  80. Sugimura Y, Hagi T, Hoshino T (2011) Correlation between in vitro mucus adhesion and the in vivo colonization ability of lactic acid bacteria: screening of new candidate carp probiotics. Biosci Biotechnol Biochem 75:511–515. https://doi.org/10.1271/bbb.100732

    Article  CAS  PubMed  Google Scholar 

  81. Senthong R, Chanthachum S, Sumpavapol P (2012) Screening and identification of probiotic lactic acid bacteria isolated from Poo-Khem, A traditional salted crab. International Conference on Nutrition and Food Sciences 39:111–115

    Google Scholar 

  82. Sha Y, Wang L, Liu M, Jiang K, Xin F, Wang B (2016) Effects of lactic acid bacteria and the corresponding supernatant on the survival, growth performance, immune response and disease resistance of Litopenaeus vannamei. Aquaculture 452:28–36. https://doi.org/10.1016/j.aquaculture.2015.10.014

    Article  CAS  Google Scholar 

  83. 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 Biol Ecol 312:115–136. https://doi.org/10.1016/j.jembe.2004.06.008

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to acknowledge UGC-NRCBS and UGC-CEGS for the instrumentation facility.

Funding

GK was supported by a UGC-BSR fellowship (F.25–1/2013–14(BSR)/5–67/2007(BSR).

Author information

Authors and Affiliations

  1. Department of Molecular Biology, School of Biological Sciences, Madurai Kamaraj University, Tamil Nadu, Madurai, 625 021, India

    Krishnaveni Govindaraj, Vignesh Samayanpaulraj, Vidhyalakshmi Narayanadoss & Ramesh Uthandakalaipandian

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  1. Krishnaveni Govindaraj
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  2. Vignesh Samayanpaulraj
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  3. Vidhyalakshmi Narayanadoss
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  4. Ramesh Uthandakalaipandian
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Corresponding author

Correspondence to Ramesh Uthandakalaipandian.

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Ethical Statement

Collected fishes in this experiment were commonly used for human consumption and are naturally available in rivers, lakes, and ponds. The protocols for the handling of animals and experimental methods were carried out by the approval of the Institutional Internal Research and Review Board, Biosafety and Animal Welfare Committee of Madurai Kamaraj University, dated on June 22, 2015.

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The authors declare no competing interests

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Govindaraj, K., Samayanpaulraj, V., Narayanadoss, V. et al. Isolation of Lactic Acid Bacteria from Intestine of Freshwater Fishes and Elucidation of Probiotic Potential for Aquaculture Application. Probiotics & Antimicro. Prot. 13, 1598–1610 (2021). https://doi.org/10.1007/s12602-021-09811-6

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