Skip to main content
Log in

Screening of potential probiotic lactic acid bacteria based on gastrointestinal properties and perfluorooctanoate toxicity

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The consumption of lactic acid bacteria capable of binding or degrading food-borne carcinogens may reduce human exposure to these deleterious compounds. In this study, 25 Lactobacillus strains isolated from human, plant, or dairy environments were investigated for their potential probiotic capacity against perfluorooctanoate (PFOA) toxicity. The PFOA binding, tolerance ability, and acid and bile salt tolerance were investigated and assessed by principal component analysis. Additionally, the effect of different pH levels and binding times was assessed. These strains exhibited different degrees of PFOA binding; the strain with the highest PFOA binding capability was Lactobacillus plantarum CCFM738, which bound to 49.40 ± 1.5 % of available PFOA. This strain also exhibited relatively good cellular antioxidative properties, acid and bile salt tolerance, and adhesion to Caco-2 cells. This study suggests that L. plantarum CCFM738 could be used as a potential probiotic in food applications against PFOA toxicity.

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
Fig. 4

Similar content being viewed by others

References

  • Abou-Shanab RA, van Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68(2):360–367. doi:10.1016/j.chemosphere.2006.12.051

    Article  CAS  PubMed  Google Scholar 

  • Alander M, Satokari R, Korpela R, Saxelin M, Vilpponen-Salmela T, Mattila-Sandholm T, von Wright A (1999) Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol 65(1):351–354

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson-Mahoney P, Kotlerman J, Takhar H, Gray D, Dahlgren J (2008) Self-reported health effects among community residents exposed to perfluorooctanoate. New Solutions J Environ Occup Health Pol NS 18(2):129–143. doi:10.2190/NS.18.2.d

    Article  Google Scholar 

  • Bhakta JN, Munekage Y, Ohnishi K, Jana BB (2012) Isolation and identification of cadmium- and lead-resistant lactic acid bacteria for application as metal removing probiotic. Int J Environ Sci Te 9(3):433–440. doi:10.1007/s13762-012-0049-3

    Article  CAS  Google Scholar 

  • Blum S, Reniero R, Schiffrin E, Crittenden R, Mattila-Sandholm T, Ouwehand A, Salminen S, Von Wright A, Saarela M, Saxelin M (1999) Adhesion studies for probiotics: need for validation and refinement. Trends Food Sci Technol 10(12):405–410. doi:10.1016/S0924-2244(00)00028-5

    Article  CAS  Google Scholar 

  • Buck RC, Franklin J, Berger U, Conder JM, Cousins IT, de Voogt P, Jensen AA, Kannan K, Mabury SA, van Leeuwen SP (2011) Perfluoroalkyl and polyfluoroalkyl substances in the environment: terminology, classification, and origins. Integr Environ Assess Manag 7(4):513–541. doi:10.1002/ieam.258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandrasekaran CV, Sundarajan K, David K, Agarwal A (2010) In vitro efficacy and safety of poly-herbal formulations. Toxicol in Vitro 24(3):885–897. doi:10.1016/j.tiv.2009.11.021

  • 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):65–72. doi:10.1016/j.foodcont.2013.06.027

    Article  Google Scholar 

  • Committee on toxicity (COT) (2006) Committee on Toxicity of Chemicals in Food and consumer products and the environment. COT statement on the tolerable daily intake for perfluorooctanoic acid. Available at:http://wwwfoodgovuk/multimedia/pdfs/cotstatementpfoa200610pdf

  • Cui L, Q-f Z, Liao C-y, J-j F, G-b J (2008) Studies on the toxicological effects of PFOA and PFOS on rats using histological observation and chemical analysis. Arch Environ Contam Toxicol 56(2):338–349. doi:10.1007/s00244-008-9194-6

    Article  PubMed  Google Scholar 

  • Domingo JL (2012) Health risks of dietary exposure to perfluorinated compounds. Environ Int 40:187–195. doi:10.1016/j.envint.2011.08.001

    Article  CAS  PubMed  Google Scholar 

  • El-Nezami HS, Chrevatidis A, Auriola S, Salminen S, Mykkänen H (2002) Removal of common Fusarium toxins in vitro by strains of Lactobacillus and Propionibacterium. Food Addit Contam 19(7):680–686. doi:10.1080/02652030210134236

    Article  CAS  PubMed  Google Scholar 

  • Fang X, Feng Y, Shi Z, Dai J (2009) Alterations of cytokines and MAPK signaling pathways are related to the immunotoxic effect of perfluorononanoic acid. Toxicol Sci 108:367–376. doi:10.1093/toxsci/kfp019

    Article  CAS  PubMed  Google Scholar 

  • Felice DL, Sun J, Liu RH (2009) A modified methylene blue assay for accurate cell counting. J Funct Food 1(1):109–118. doi:10.1016/j.jff.2008.09.014

    Article  Google Scholar 

  • Ferrando V, Quiberoni A, Reinhemer J, Suarez V (2015) Resistance of functional Lactobacillus plantarum strains against food stress conditions. Food Microbiol 48:63–71. doi:10.1016/j.fm.2014.12.005

    Article  CAS  PubMed  Google Scholar 

  • Goyal N, Rishi P, Shukla G (2013) Lactobacillus rhamnosus GG antagonizes Giardia intestinalis induced oxidative stress and intestinal disaccharidases: an experimental study. World J Microbiol Biotechnol 29(6):1049–1057. doi:10.1007/s11274-013-1268-6

    Article  PubMed  Google Scholar 

  • Gratz S, Taubel M, Juvonen RO, Viluksela M, Turner PC, Mykkanen H, El-Nezami H (2006) Lactobacillus rhamnosus strain GG modulates intestinal absorption, fecal excretion, and toxicity of aflatoxin B(1) in rats. Appl Environ Microbiol 72(11):7398–7400. doi:10.1128/AEM.01348-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halttunen T, Collado MC, El-Nezami H, Meriluoto J, Salminen S (2008) Combining strains of lactic acid bacteria may reduce their toxin and heavy metal removal efficiency from aqueous solution. Lett Appl Microbiol 46(2):160–165. doi:10.1111/j.1472-765X.2007.02276.x

    Article  CAS  PubMed  Google Scholar 

  • Haug LS, Salihovic S, Jogsten IE, Thomsen C, van Bavel B, Lindstrom G, Becher G (2010) Levels in food and beverages and daily intake of perfluorinated compounds in Norway. Chemosphere 80(10):1137–1143. doi:10.1016/j.chemosphere.2010.06.023

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Mendoza A, Garcia HS, Steele JL (2009) Screening of Lactobacillus casei strains for their ability to bind aflatoxin B-1. Food Chem Toxicol 47(6):1064–1068. doi:10.1016/j.fct.2009.01.042

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Mendoza A, Rivas-Jimenez L, Garcia HS (2011) Assessment of aflatoxin B1 binding to Lactobacillus reuteri by microscopy and fluorescence techniques. Food Biotechnol 25(2):140–150. doi:10.1080/08905436.2011.576561

    Article  CAS  Google Scholar 

  • Herzke D, Schlabach M, Mariussen E (2007) Literature survey of polyfluorinated organic compounds, phosphor containing flame retardants, 3-nitrobenzanthrone, organic tin compounds, platinum and silver. Universita NILU

  • Hyronimus B, Marrec CL, Sassi AH, Deschamps A (2000) Acid and bile tolerance of spore-forming lactic acid bacteria. Int J Food Microbiol 61:193–197. doi:10.1016/S0168-1605(00)00366-4

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim F, Halttunen T, Tahvonen R, Salminen S (2006) Probiotic bacteria as potential detoxification tools: assessing their heavy metal binding isotherms. Can J Microbiol 52(9):877–885. doi:10.1139/w06-043

    Article  CAS  PubMed  Google Scholar 

  • Jacquet N, Maire MA, Rast C, Bonnard M, Vasseur P (2011) Perfluorooctanoic acid (PFOA) acts as a tumor promoter on Syrian hamster embryo (SHE) cells. Environ Sci Pollut Res Int 19(7):2537–2549. doi:10.1007/s11356-012-0968-z

    Article  CAS  PubMed  Google Scholar 

  • Kannan K, Hansen S, Franson C, Bowerman W, Hansen K, Jones P, Giesy J (2001) Perfluorochemical surfactants in the environment. Environ Sci Technol 35:3065–3070

    Article  CAS  PubMed  Google Scholar 

  • Kennedy GL, Butenhoff JL, Olsen GW, O’Connor JC, Seacat AM, Perkins RG, Biegel LB, Murphy SR, Farrar DG (2004) The toxicology of perfluorooctanoate. Crit Rev Toxicol 34(4):351–384. doi:10.1080/10408440490464705

    Article  CAS  PubMed  Google Scholar 

  • Kissa E (2001) Fluorinated surfactants and repellents, vol 97. CRC Press

  • Kudo N, Kawashima Y (2003) Toxicity and toxicokinetics of perfluorooctanoic acid in humans and animals. J Toxicol Sci 28(2):49–57. doi:10.2131/jts.28.49

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, El-Nezami H, Haskard C, Gratz S, Puong K, Salminen S, Mykkänen H (2003) Kinetics of adsorption and desorption of aflatoxin B1 by viable and nonviable bacteria. J Food Protect 66(3):426–430

    CAS  Google Scholar 

  • Liu C, Yu K, Shi X, Wang J, Lam PKS, Wu RSS, Zhou B (2007) Induction of oxidative stress and apoptosis by PFOS and PFOA in primary cultured hepatocytes of freshwater tilapia (Oreochromis niloticus). Aquatic Toxicol (Amsterdam, Netherlands) 82(2):135–143. doi:10.1016/j.aquatox.2007.02.006

    Article  CAS  Google Scholar 

  • Luo C (2014) Pollution levels of perfluorinated alkylated substances in rice from Fujian Province. JIMEI University, Master

    Google Scholar 

  • Noorlander CW, van Leeuwen SPJ, Biesebeek JDT, Mengelers MJB, Zeilmaker MJ (2011) Levels of perfluorinated compounds in food and dietary intake of PFOS and PFOA in the Netherlands. J Agr Food Chem 59(13):7496–7505. doi:10.1021/jf104943p

    Article  CAS  Google Scholar 

  • OECD (2006) Results of the 2006 survey on production and use of PFOS, PFAS, PFOA, PFCA, their related substances and products/mixtures containing these substances. Environment Directorate Joint Meeting of the Chemicals Committee and the Working Party on Chemicals, PaB (Ed)

  • Olsen GW, Zobel LR (2007) Assessment of lipid, hepatic, and thyroid parameters with serum perfluorooctanoate (PFOA) concentrations in fluorochemical production workers. Int Arch Occup Environ Health 81(2):231–246. doi:10.1007/s00420-007-0213-0

    Article  CAS  PubMed  Google Scholar 

  • Orrhage K, Sillerström E, Gustafsson JA, Nord CE, Rafter J (1994) Binding of mutagenic heterocyclic amines by intestinal and lactic acid bacteria. Mutat Res 311:239–248. doi:10.1016/0027-5107(94)90182-1

    Article  CAS  PubMed  Google Scholar 

  • Paul D, Hoskins LC (1972) Effect of oral lactobacillus feedings on fecal lactobacillus counts. Am J Clin Nutr 25(8):763–765

    CAS  PubMed  Google Scholar 

  • Qazi MR, Nelson BD, DePierre JW, Abedi-Valugerdi M (2012) High-dose dietary exposure of mice to perfluorooctanoate or perfluorooctane sulfonate exerts toxic effects on myeloid and B-lymphoid cells in the bone marrow and these effects are partially dependent on reduced food consumption. Food Chem Toxicol 50(9):2955–2963. doi:10.1016/j.fct.2012.06.023

    Article  CAS  PubMed  Google Scholar 

  • Ricciardi A, Blaiotta G, Di Cerbo A, Succi M, Aponte M (2014) Behaviour of lactic acid bacteria populations in Pecorino di Carmasciano cheese samples submitted to environmental conditions prevailing in the gastrointestinal tract: evaluation by means of a polyphasic approach. Int J Food Microbiol 179:64–71. doi:10.1016/j.ijfoodmicro.2014.03.014

    Article  CAS  PubMed  Google Scholar 

  • Rodea-Palomares I, Makowski M, Gonzalo S, Gonzalez-Pleiter M, Leganes F, Fernandez-Pinas F (2015) Effect of PFOA/PFOS pre-exposure on the toxicity of the herbicides 2,4-D, atrazine, diuron and paraquat to a model aquatic photosynthetic microorganism. Chemosphere 139:65–72. doi:10.1016/j.chemosphere.2015.05.078

    Article  CAS  PubMed  Google Scholar 

  • Salminen S, Von Wright A (2004) Lactic acid bacteria: microbiological and functional aspects, vol 139. CRC Press

  • Shabalina IG, Panaretakis T, Bergstrand A, Depierre JW (1999) Effects of the rodent peroxisome proliferator and hepatocarcinogen, perfluorooctanoic acid, on apoptosis in human hepatoma HepG2 cells. Carcinogenesis 20(12):2237–2246. doi:10.1093/carcin/20.12.2237

    Article  CAS  PubMed  Google Scholar 

  • Shahin A (2007) Removal of aflatoxin B1 from contaminated liquid media by dairy lactic acid bacteria. Int J Agric Biol 9:71–75

    CAS  Google Scholar 

  • Sim I, Koh JH, Kim DJ, Gu SH, Park A, Lim YH (2015) In vitro assessment of the gastrointestinal tolerance and immunomodulatory function of Bacillus methylotrophicus isolated from a traditional Korean fermented soybean food. J Appl Microbiol 118(3):718–726. doi:10.1111/jam.12719

    Article  CAS  PubMed  Google Scholar 

  • So MK, Taniyasu S, Yamashita N, Giesy JP, Zheng J, Fang Z, Im SH, Lam PKS (2004) Perfluorinated compounds in coastal waters of Hong Kong, South China, and Korea. Environ Sci Technol 38(15):4056–4063. doi:10.1021/es049441z

    Article  CAS  PubMed  Google Scholar 

  • Son H-Y, Kim S-H, Shin H-I, Bae HI, Yang J-H (2008) Perfluorooctanoic acid-induced hepatic toxicity following 21-day oral exposure in mice. Arch Toxicol 82(4):239–246. doi:10.1007/s00204-007-0246-x

    Article  CAS  PubMed  Google Scholar 

  • Tsakalidou E, Papadimitriou K (2011) Stress responses of lactic acid bacteria. Springer Science & Business Media

  • Vosough PR, Sani AM, Mehraban M, Karazhyan R (2014) In vitro effect of Lactobacillus rhamnosus GG on reduction of aflatoxin B1. Nutr Food Sci 44(1):32–40. doi:10.1108/NFS-11-2012-0122

    Article  Google Scholar 

  • Wang L, Chen J, Xie H, Ju X, Liu RH (2013) Phytochemical profiles and antioxidant activity of Adlay varieties. J Agr Food Chem 61(21):5103–5113. doi:10.1021/jf400556s

    Article  CAS  Google Scholar 

  • Wolfe KL, Liu RH (2007) Cellular antioxidant activity (CAA) assay for assessing antioxidants, foods, and dietary supplements. J Agr Food Chem 55(22):8896–8907. doi:10.1021/jf0715166

    Article  CAS  Google Scholar 

  • Xing J, Wang G, Gu Z, Liu X, Zhang Q, Zhao J, Zhang H, Chen YQ, Chen W (2015a) Cellular model to assess the antioxidant activity of lactobacilli. RSC Adv 5(47):37626–37634. doi:10.1039/c5ra02215k

    Article  CAS  Google Scholar 

  • Xing J, Wang G, Zhang Q, Liu X, Gu Z, Zhang H, Chen YQ, Chen W (2015b) Determining antioxidant activities of lactobacilli cell-free supernatants by cellular antioxidant assay: a comparison with traditional methods. PLoS One 10(3). doi:10.1371/journal.pone.0119058

  • Xing J, Wang G, Zhang Q, Liu X, Yin B, Fang D, Zhao J, Zhang H, Chen YQ, Chen W (2015c) Determining antioxidant activities of lactobacilli by cellular antioxidant assay in mammal cells. J Funct Food 19:554–562. doi:10.1016/j.jff.2015.09.017

    Article  CAS  Google Scholar 

  • Yao X, Zhong L (2005) Genotoxic risk and oxidative DNA damage in HepG2 cells exposed to perfluorooctanoic acid. Mutat Res Genet Toxicol Environ Mutagen 587(1–2):38–44. doi:10.1016/j.mrgentox.2005.07.010

    Article  CAS  Google Scholar 

  • Yu Q, Zhang R, Deng S, Huang J, Yu G (2009) Sorption of perfluorooctane sulfonate and perfluorooctanoate on activated carbons and resin: Kinetic and isotherm study. Water Res 43(4):1150–1158. doi:10.1016/j.watres.2008.12.001

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Sun HW, Wu Q, Zhang XZ, Yun SH, Kannan K (2010) Perfluorochemicals in meat, eggs and indoor dust in china: assessment of sources and pathways of human exposure to perfluorochemicals. Environ Sci Technol 44(9):3572–3579. doi:10.1021/es1000159

    Article  CAS  PubMed  Google Scholar 

  • Zhao G, Wang J, Wang X, Chen S, Zhao Y, Gu F, Xu A, Wu L (2011) Mutagenicity of PFOA in mammalian cells: role of mitochondria-dependent reactive oxygen species. Environ Sci Technol 45(4):1638–1644. doi:10.1021/es1026129

    Article  CAS  PubMed  Google Scholar 

  • Zheng XM, Liu HL, Shi W, Wei S, Giesy JP, Yu HX (2011) Effects of perfluorinated compounds on development of zebrafish embryos. Environ Sci Pollut Res Int 19(7):2498–2505. doi:10.1007/s11356-012-0977-y

    Article  PubMed  Google Scholar 

  • Zinedine A, Faid M, Benlemlih M (2005) In vitro reduction of aflatoxin B1 by strains of lactic acid bacteria isolated from Moroccan sourdough bread. Int J Agric Biol 7(1):67–70

    CAS  Google Scholar 

  • Zou W, Liu W, Yang B, Wu L, Yang J, Zou T, Liu F, Xia L, Zhang D (2015) Quercetin protects against perfluorooctanoic acid-induced liver injury by attenuating oxidative stress and inflammatory response in mice. Int Immunopharmacol 28(1):129–135. doi:10.1016/j.intimp.2015.05.043

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31301407), the Key Projects in the National Science and Technology Pillar Program during the 12th Five-Year Plan (Nos. 2013BAD18B01, 2013BAD18B02, and 2012BAD12B08), the Graduate Student Innovation Project of Jiangsu Province (KYLX15_1135), the National Basic Research Program of China (973 Program No. 2012CB720802), the Program of Introducing Talents of Discipline to Universities (B07029), the Fundamental Research Funds for the Central Universities (JUSRP51501), and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions and the Program of Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gang Wang.

Ethics declarations

Conflict of interest statement

The authors have declared no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic Supplementary Material

ESM 1

(PDF 132 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xing, J., Wang, F., Xu, Q. et al. Screening of potential probiotic lactic acid bacteria based on gastrointestinal properties and perfluorooctanoate toxicity. Appl Microbiol Biotechnol 100, 6755–6766 (2016). https://doi.org/10.1007/s00253-016-7535-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7535-3

Keywords

Navigation