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Probiotics and Antimicrobial Proteins

, Volume 11, Issue 1, pp 65–73 | Cite as

Characterisation of Lactic Acid Bacteria Isolated from the Gut of Cyprinus carpio That May Be Effective Against Lead Toxicity

  • Sib Sankar Giri
  • Jin Woo Jun
  • Saekil Yun
  • Hyoun Joong Kim
  • Sang Guen Kim
  • Jeong Woo Kang
  • Sang Wha Kim
  • Se Jin Han
  • Se Chang ParkEmail author
  • V. SukumaranEmail author
Article

Abstract

The present study was conducted to isolate and characterise Pb-resistant lactic acid bacteria (LAB), and thus determine their potential for use as probiotics against Pb toxicity. A total of 107 Pb-resistant LAB strains were isolated from the gut content of Cyprinus carpio, of which 41 were established to be gram-positive and catalase-negative. Investigation of the Pb-binding ability of these isolated LAB identified seven strains (P2, P6, P7, P9, P16, P19 and P22) with comparatively high Pb-binding activities. These were selected for further screening to establish their Pb tolerance, anti-oxidative capacity and in vitro probiotic characteristics. Strain P16 exhibited both the highest Pb-binding and a relatively good antioxidant capacity. Furthermore, P16 displayed a high survival rate during 4 h of exposure to both low-pH (2.5–3.5) conditions and 10.0% fish bile, and a strong capacity to adhere to fish intestinal mucus (62.4%). Furthermore, P16 showed strong antibacterial activities against all tested fish pathogens. Strains P6, P9, P16, P19 and P22 were susceptible to a range of tested antibiotics, but not to vancomycin. Thus, of the isolated lactobacilli, strain P16 exhibited the best Pb-binding ability, a high level of antioxidant activity and satisfactory in vitro probiotic properties. Biochemical and 16S-rRNA gene analyses identified P16 as Lactobacillus reuteri. Thus, the results of the conducted in vitro tests suggest that the fish-associated P16 Lact. reuteri strain is a promising candidate probiotic, which should undergo further investigation to assess its suitability for use in protecting against lead-exposure-induced toxicities in aquaculture.

Keywords

Lead toxicity Lactic acid bacteria Lead-binding Antioxidant Probiotic characterisation 

Notes

Funding information

This research was supported by the ‘Korea Research Fellowship Program’ of the National Research Foundation of Korea (NRF), Ministry of Science and ICT (2016H1D3A1909005) and by the NRF grants funded by the Korean government (MSIP) (NRF-2014R1A2A1A11050093, NRF-2017R1C1B2004616).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Monachese M, Burton JP, Reid G (2012) Bioremediation and tolerance of humans to heavy metals through microbial processes: a potential role for probiotics. Appl Environ Microbiol 78(18):6397–6404.  https://doi.org/10.1128/AEM.01665-12 CrossRefGoogle Scholar
  2. 2.
    Yi Y-J, Lim J-M, Gu S, Lee W-K, Oh E, Lee S-M, Oh B-T (2017) Potential use of lactic acid bacteria Leuconostoc mesenteroides as a probiotic for the removal of Pb(II) toxicity. J Microbiol 55(4):296–303.  https://doi.org/10.1007/s12275-017-6642-x CrossRefGoogle Scholar
  3. 3.
    Chambial S, Bhardwaj P, Mahdi AA, Sharma P (2017) Lead poisoning due to herbal medications. Indian J Clin Biochem 32(2):246–247.  https://doi.org/10.1007/s12291-016-0617-2 CrossRefGoogle Scholar
  4. 4.
    Ruby SM, Hull R, Anderson P (2000) Sublethal lead affects pituitary function of rainbow trout during exogenous vitellogenesis. Arch Environ Contam Toxicol 38(1):46–51.  https://doi.org/10.1007/s002449910006 CrossRefGoogle Scholar
  5. 5.
    Alsop D, Ng TY, Chowdhury MJ, Wood CM (2016) Interactions of waterborne and dietborne Pb in rainbow trout, Oncorhynchus mykiss: bioaccumulation, physiological responses, and chronic toxicity. Aquat Toxicol 177:343–354.  https://doi.org/10.1016/j.aquatox.2016.06.007 CrossRefGoogle Scholar
  6. 6.
    Kaya H, Akbulut M (2015) Effects of waterborne lead exposure in Mozambique tilapia: oxidative stress, osmoregulatory responses, and tissue accumulation. J Aquat Anim Health 27(2):77–87.  https://doi.org/10.1080/08997659.2014.1001533 CrossRefGoogle Scholar
  7. 7.
    Farombi EO, Adelowo OA, Ajimoko YR (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. Int J Environ Res Public Health 4(2):158–165.  https://doi.org/10.3390/ijerph2007040011 CrossRefGoogle Scholar
  8. 8.
    Gu Y-G, Huang H-H, Lin Q (2016) Concentrations and human health implications of heavy metals in wild aquatic organisms captured from the core area of Daya Bay’s Fishery Resource Reserve, South China Sea. Environ Toxicol Pharmacol 45:90–94CrossRefGoogle Scholar
  9. 9.
    Aryal M, Liakopoulou-Kyriakides M (2015) Bioremoval of heavy metals by bacterial biomass. Environ Monit Assess 187(1):4173–4199.  https://doi.org/10.1007/s10661-014-4173-z CrossRefGoogle Scholar
  10. 10.
    Gόmez GD, Balcẚzar 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 CrossRefGoogle Scholar
  11. 11.
    Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41(11):1553–1573.  https://doi.org/10.1111/j.1365-2109.2010.02546.x CrossRefGoogle Scholar
  12. 12.
    Majlesi M, Shekarforoush SS, Ha RG, Nazifi S, Sajedianfard J, Eskandari MH (2017) Effect of probiotic Bacillus coagulans and Lactobacillus plantarum on alleviation of mercury toxicity in rat. Probiotics Antimicrob Proteins 9(3):300–309.  https://doi.org/10.1007/s12602-016-9250-x CrossRefGoogle Scholar
  13. 13.
    Zhai Q, Yu L, Li T, Zhu J, Zhang C, Zhao J, Zhang H, Chen W (2017a) Effect of dietary probiotic supplementation on intestinal microbiota and physiological conditions of Nile tilapia (Oreochromis niloticus) under waterborne cadmium exposure. Antonie Van Leeuwenhoek 110(4):501–513.  https://doi.org/10.1007/s10482-016-0819-x CrossRefGoogle Scholar
  14. 14.
    Ojekunle O, Banwo K, Sanni AI (2017) In vitro and in vivo evaluation of Weissella cibaria and Lactobacillus plantarum for their protective effect against cadmium and lead toxicities. Lett Appl Microbiol 64(5):379–385.  https://doi.org/10.1111/lam.12731 CrossRefGoogle Scholar
  15. 15.
    Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K, Wei MQ (2012) Characterization of lactic acid bacteria-based probiotics as potential heavy metal sorbents. J Appl Microbiol 112(6):1193–1206.  https://doi.org/10.1111/j.1365-2672.2012.05284.x CrossRefGoogle Scholar
  16. 16.
    Zhai Q, Yin R, Yu L, Wang G, Tian F, Yu R, Zhao J, Liu X, Chen YQ, Zhang H, Chen W (2015) Screening of lactic acid bacteria with potential protective effects against cadmium toxicity. Food Control 54:23–30.  https://doi.org/10.1016/j.foodcont.2015.01.037 CrossRefGoogle Scholar
  17. 17.
    Gatesoupe F (1999) The use of probiotics in aquaculture. Aquaculture 180(1-2):147–165.  https://doi.org/10.1016/S0044-8486(99)00187-8 CrossRefGoogle Scholar
  18. 18.
    Zhai Q, Wang H, Tian F, Zhao J, Zhang H, Chen W (2017b) Dietary Lactobacillus plantarum supplementation decreases tissue lead accumulation and alleviates lead toxicity in Nile tilapia (Oreochromis niloticus). Aquac Res 48(9):5094–5103.  https://doi.org/10.1111/are.13326 CrossRefGoogle Scholar
  19. 19.
    Sinha V, Mishra R, Kumar A, Kannan A, Upreti RK (2011) Amplification of arsH gene in Lactobacillus acidophilus resistant to arsenite. Biotechnology 10:101–107CrossRefGoogle Scholar
  20. 20.
    Chen P, Zhang Q, Dang H, Liu X, Tian F, Zhao J, Chen Y, Zhang H, Chen W (2014) Screening for potential new probiotic based on probiotic properties and α-glucosidase inhibitory activity. Food Control 35(1):65–72CrossRefGoogle Scholar
  21. 21.
    Giri SS, Sukumaran V, Dangi NK (2012) Characteristics of bacterial isolates from the gut of freshwater fish, Labeo rohita that may be useful as potential probiotic bacteria. Probiotics Antimicrob Proteins 4(4):238–242.  https://doi.org/10.1007/s12602-012-9119-6 CrossRefGoogle Scholar
  22. 22.
    Balcázar JL, Vendrell D, de Blas I, Ruiz-Zarzuela I, Muzquiz JL, Gironés O (2008) Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture 278(1-4):188–191.  https://doi.org/10.1016/j.aquaculture.2008.03.014 CrossRefGoogle Scholar
  23. 23.
    European Food Safety Authority (EFSA) (2012) Scientific opinion. Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J 10:2740.  https://doi.org/10.2903/j.efsa.2012.2740 Google Scholar
  24. 24.
    Garcia EF, Luciano WA, Xavier DE, da Costa WCA, de Sousa OK et al (2016) Identification of lactic acid bacteria in fruit pulp processing byproducts and potential probiotic properties of selected Lactobacillus strains. Front Microbiol 7:1371Google Scholar
  25. 25.
    Halttunen T, Salminen S, Tahvonen R (2007) Rapid removal of lead and cadmium from water by specific lactic acid bacteria. Int J Food Microbiol 114(1):30–35.  https://doi.org/10.1016/j.ijfoodmicro.2006.10.040 CrossRefGoogle Scholar
  26. 26.
    Landersjö C, Yang Z, Huttunen E, Widmalm G (2002) Structural studies of the exopolysaccharide produced by Lactobacillus rhamnosus strain GG (ATCC 53103). Biomacromolecules 3(4):880–884.  https://doi.org/10.1021/bm020040q CrossRefGoogle Scholar
  27. 27.
    Thijssen S, Cuypers A, Maringwa J, Smeets K, Horemans N, Lambrichts I, van Kerkhove E (2007) Low cadmium exposure triggers a biphasic oxidative stress response in mice kidneys. Toxicology 236(1):29–41.  https://doi.org/10.1016/j.tox.2007.03.022 CrossRefGoogle Scholar
  28. 28.
    Jain S, Yadav H, Sinha PR (2009) Antioxidant and cholesterol assimilation activities of selected lactobacilli and lactococci cultures. J Dairy Res 76(04):385–391.  https://doi.org/10.1017/S0022029909990094 CrossRefGoogle Scholar
  29. 29.
    Tong Y, Wang G, Zhang Q, Tian F, Liu X, Zhao J, Zhangac H, Chen W (2016) Systematic understanding of the potential manganese-adsorption components of a screened Lactobacillus plantarum CCFM436. RSC Adv 6(104):102804–102813.  https://doi.org/10.1039/C6RA23877G CrossRefGoogle Scholar
  30. 30.
    Jena PK, Trivedi D, Thakore K, Chaudhary H, Giri SS, Seshadri S (2013) Isolation and characterization of probiotic properties of lactobacilli isolated from rat fecal microbiota. Microbiol Immunol 5:1–14Google Scholar
  31. 31.
    Oh YG, Jung DS (2015) Evaluation of probiotic properties of Lactobacillus and Pediococcus strains isolated from Omegisool, a traditionally fermented millet alcoholic beverage in Korea. LWT - Food Sci Technol 63:437–444CrossRefGoogle Scholar
  32. 32.
    Hamon E, Horvatovich P, Izquierdo E, Bringel F, Marchioni E, Aoude-Werner D et al (2011) Comparative proteomic analysis of Lactobacillus plantarum for the identification of key proteins in bile tolerance. BMC Microbiol 11(1):63.  https://doi.org/10.1186/1471-2180-11-63 CrossRefGoogle Scholar
  33. 33.
    Manini F, Casiraghi MC, Poutanen K, Brasca M, Erba D, Plumed-Ferrer C (2016) Characterization of lactic acid bacteria isolated from wheat bran sourdough. LWT - Food Sci Technol 66:275–283CrossRefGoogle Scholar
  34. 34.
    Servin A, Coconnier MH (2003) Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol 17(5):741–754.  https://doi.org/10.1016/S1521-6918(03)00052-0 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Laboratory of Aquatic Biomedicine, College of Veterinary Medicine and Research Institute for Veterinary ScienceSeoul National UniversitySeoulSouth Korea
  2. 2.Department of BiotechnologyPeriyar Maniammai UniversityThanjavurIndia
  3. 3.Department of ZoologyKundavai Nachiyar Government Arts College for Women (Autonomous)ThanjavurIndia

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