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Abundance of Lactobacillus plantarum Strains with Beneficial Attributes in Blackberries (Rubus sp.), Fresh Figs (Ficus carica), and Prickly Pears (Opuntia ficus-indica) Grown and Harvested in Algeria

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Abstract

This first study performed on traditional fruits consumed in North Africa reveals their richness in microorganisms with beneficial attributes like cholesterol lowering capabilities. Blackberries (Rubus sp.), fresh figs (Ficus carica), and prickly pears (Opuntia ficus-indica) are fruits largely and traditionally consumed in Kabylia, a beautiful northern Algerian region. Here, 85 lactic acid bacteria (LAB)-isolates were isolated and identified by MALDI-TOF mass spectrometry. The identified species belong to Lactobacillus and Leuconostoc genera. These 85 LAB-isolates were then assessed for their capabilities to grow under conditions mimicking the gastrointestinal tract, and the resulting data were statistically treated with principal component analysis (PCA). After which, only 26 LAB-isolates were selected and characterized for their genetic relatedness using random amplified polymorphic DNA (RAPD) method. Following the genetic relatedness assessment, only 10 LAB-strains, among which nine Lactobacillus plantarum and one Lactobacillus paracasei were studied for their pathoproperties and some probiotic features. Interestingly, all of these 10 LAB-strains were devoid of adverse effects, but capable to adhere to human epithelial colorectal adenocarcinoma Caco-2 cells. Of note, these 10 LAB-strains exhibited an important in vitro hypocholesteromia effect, in strain-dependent manner. Moreover, the Lactobacillus strains exhibited a high bile salt hydrolase (BSH) activity which was correlated with expression of bsh2, bsh3 and bsh4 genes.

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References

  1. Fessard A, Kapoor A, Patche J, et al (2017) Lactic fermentation as an efficient tool to enhance the antioxidant activity of tropical fruit juices and teas. Microorganisms 5: pii: E23. doi: https://doi.org/10.3390/microorganisms5020023

  2. Slavin JL, Lloyd B (2012) Health benefits of fruits and vegetables. Adv Nutr 3:506–516. https://doi.org/10.3945/an.112.002154

    Article  CAS  Google Scholar 

  3. Yahia EM, García-Solís P, Celis MEM (2019) Chapter 2 - contribution of fruits and vegetables to human nutrition and health. In: Yahia EM (ed) Postharvest physiology and biochemistry of fruits and vegetables. Woodhead Publishing, pp 19–45

  4. Naeem M, Ilyas M, Haider S et al (2012) Isolation characterization and identification of lactic acid bacteria from fruit juices and their efficacy against antibiotics. Pak J Bot 44: 323–328, Special Issue (March 2012)

  5. Xu X, Luo D, Bao Y, Liao X, Wu J (2018) Characterization of diversity and probiotic efficiency of the autochthonous lactic acid bacteria in the fermentation of selected raw fruit and vegetable juices. Front Microbiol 9:2539. https://doi.org/10.3389/fmicb.2018.02539

    Article  Google Scholar 

  6. Sánchez J, Vegas C, Zavaleta AI, Esteve-Zarzoso B (2019) Predominance of Lactobacillus plantarum strains in Peruvian Amazonian fruits. Pol J Microbiol 68:127–137. https://doi.org/10.21307/pjm-2019-015

    Article  Google Scholar 

  7. FAO/WHO (2002) Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. Guidelines for the Evaluation of Probiotics in Food https://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf Accessed 11 December 2012

  8. Buggio L, Somigliana E, Borghi A, Vercellini P (2019) Probiotics and vaginal microecology: fact or fancy? BMC Womens Health 19:25. https://doi.org/10.1186/s12905-019-0723-4

    Article  Google Scholar 

  9. Oak SJ, Jha R (2019) The effects of probiotics in lactose intolerance: a systematic review. Crit Rev Food Sci Nutr 59:1675–1683. https://doi.org/10.1080/10408398.2018.1425977

    Article  CAS  Google Scholar 

  10. 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 

  11. Zhang Y, Li L, Guo C, Mu D, Feng B, Zuo X, Li Y (2016) Effects of probiotic type, dose and treatment duration on irritable bowel syndrome diagnosed by Rome III criteria: a meta-analysis. BMC Gastroenterol 16:62. https://doi.org/10.1186/s12876-016-0470-z

    Article  CAS  Google Scholar 

  12. Upadrasta A, Madempudi RS (2016) Probiotics and blood pressure: current insights. Integr Blood Press Control 9:33–42. https://doi.org/10.2147/IBPC.S73246

    Article  Google Scholar 

  13. Belguesmia Y, Domenger D, Caron J et al (2016) Novel probiotic evidence of lactobacilli on immunomodulation and regulation of satiety hormones release in intestinal cells. J Funct Foods 24:276–286. https://doi.org/10.1016/j.jff.2016.04.014

    Article  CAS  Google Scholar 

  14. Ishimwe N, Daliri EB, Lee BH, Fang F, du G (2015) The perspective on cholesterol-lowering mechanisms of probiotics. Mol Nutr Food Res 59:94–105. https://doi.org/10.1002/mnfr.201400548

    Article  CAS  Google Scholar 

  15. Ouarabi L, Chait YA, Seddik HA, Drider D, Bendali F (2019) Newly isolated Lactobacilli strains from Algerian human vaginal microbiota: Lactobacillus fermentum strains relevant probiotic’s candidates. Probiotics Antimicrob Proteins 11:43–54. https://doi.org/10.1007/s12602-017-9360-0

    Article  CAS  Google Scholar 

  16. Zielińska D, Kolożyn-Krajewska D (2018) Food-origin lactic acid bacteria may exhibit probiotic properties: review. Biomed Res Int 2018:5063185. https://doi.org/10.1155/2018/5063185

    Article  CAS  Google Scholar 

  17. García-Ruiz A, González de Llano D, Esteban-Fernández A, Requena T, Bartolomé B, Moreno-Arribas MV (2014) Assessment of probiotic properties in lactic acid bacteria isolated from wine. Food Microbiol 44:220–225. https://doi.org/10.1016/j.fm.2014.06.015

    Article  CAS  Google Scholar 

  18. Soccol CR, Vandenberghe LP de S, Spier MR, et al (2010) The potential of probiotics: a review. Food Technol Biotechnol 48 (4) 413–434

  19. Swain MR, Anandharaj M, Ray RC, Parveen Rani R (2014) Fermented fruits and vegetables of Asia: a potential source of probiotics. Biotechnology Research International, In https://www.hindawi.com/journals/btri/2014/250424/

    Google Scholar 

  20. Di Cagno R, Coda R, De Angelis M, Gobbetti M (2013) Exploitation of vegetables and fruits through lactic acid fermentation. Food Microbiol 33:1–10. https://doi.org/10.1016/j.fm.2012.09.003

    Article  CAS  Google Scholar 

  21. Vitali B, Minervini G, Rizzello CG et al (2012) Novel probiotic candidates for humans isolated from raw fruits and vegetables. Food Microbiol 31:116–125. https://doi.org/10.1016/j.fm.2011.12.027

    Article  CAS  Google Scholar 

  22. Thanina AC, Mourad B, Karim A (2015) Antibacterial activity of two extracts from Rubus fruticosus L. against resistant pathogens and their antioxidant potential. AJMR 9:1255–1262. https://doi.org/10.5897/AJMR2015.7437

    Article  Google Scholar 

  23. Boudchicha RH, Hormaza JI, Benbouza H (2018) Diversity analysis and genetic relationships among local Algerian fig cultivars (Ficus carica l.) using SSR markers. South African journal of botany 116:

  24. Zeghad N, Ahmed E, Belkhiri A et al (2019) Antioxidant activity of Vitis vinifera, Punica granatum, Citrus aurantium and Opuntia ficus indica fruits cultivated in Algeria. Heliyon 5:e01575. https://doi.org/10.1016/j.heliyon.2019.e01575

    Article  Google Scholar 

  25. Nacef M, Chevalier M, Chollet S, Drider D, Flahaut C (2017) MALDI-TOF mass spectrometry for the identification of lactic acid bacteria isolated from a French cheese: the Maroilles. Int J Food Microbiol 247:2–8. https://doi.org/10.1016/j.ijfoodmicro.2016.07.005

    Article  CAS  Google Scholar 

  26. Ait Seddik H, Bendali F, Cudennec B, Drider D (2017) Anti-pathogenic and probiotic attributes of Lactobacillus salivarius and Lactobacillus plantarum strains isolated from feces of Algerian infants and adults. Res Microbiol 168:244–254. https://doi.org/10.1016/j.resmic.2016.12.003

    Article  CAS  Google Scholar 

  27. Stenlid J, Karlsson J-O, Högberg N (1994) Intraspecific genetic variation in Heterobasidion annosum revealed by amplification of minisatellite DNA. Myc Res 98:57–63. https://doi.org/10.1016/S0953-7562(09)80337-7

    Article  CAS  Google Scholar 

  28. Pavel AB, Vasile CI (2012) PyElph - a software tool for gel images analysis and phylogenetics. BMC Bioinformatics 13:9. https://doi.org/10.1186/1471-2105-13-9

    Article  Google Scholar 

  29. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

  30. Argyri AA, Zoumpopoulou G, Karatzas K-AG et al (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33:282–291. https://doi.org/10.1016/j.fm.2012.10.005

    Article  CAS  Google Scholar 

  31. Pan F, Han L, Zhang Y, Yu Y, Liu J (2015) Optimization of Caco-2 and HT29 co-culture in vitro cell models for permeability studies. Int J Food Sci Nutr 66:680–685. https://doi.org/10.3109/09637486.2015.1077792

    Article  CAS  Google Scholar 

  32. Kos B, Susković J, Vuković S, Simpraga M, Frece J, Matosić 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  Google Scholar 

  33. Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Letters 9:29–33

    Article  CAS  Google Scholar 

  34. Pinto M, Robineleon S, Appay MD et al (1983) Enterocyte-like differentiation and polarization of the human-colon carcinoma cell-line Caco-2 in culture. Cell Growth Differ 5:967–973

    Google Scholar 

  35. Bendali F, Durand A, Hébraud M, Sadoun D (2011) Lactobacillus paracasei subsp. paracasei, an Algerian isolate with antibacterial activity against enteric pathogens and probiotic fitness. Journal of Food and Nutrition Research 50:139–149

    Google Scholar 

  36. Bendali F, Kerdouche K, Hamma-Faradji S, Drider D (2017) In vitro and in vivo cholesterol lowering ability of Lactobacillus pentosus KF923750. Benef Microbes 8:271–280. https://doi.org/10.3920/BM2016.0121

    Article  CAS  Google Scholar 

  37. Pisano MB, Viale S, Conti S, Fadda ME, Deplano M, Melis MP, Deiana M, Cosentino S (2014) Preliminary evaluation of probiotic properties of Lactobacillus strains isolated from Sardinian dairy products. Biomed Res Int 2014:286390. https://doi.org/10.1155/2014/286390

    Article  CAS  Google Scholar 

  38. Choi EA, Chang HC (2015) Cholesterol-lowering effects of a putative probiotic strain Lactobacillus plantarum EM isolated from kimchi. LWT Food Sci Technol 62:210–217. https://doi.org/10.1016/j.lwt.2015.01.019

    Article  CAS  Google Scholar 

  39. Ladjouzi R, Bizzini A, van Schaik W, Zhang X, Rincé A, Benachour A, Hartke A (2015) Loss of antibiotic tolerance in sod-deficient mutants is dependent on the energy source and arginine catabolism in enterococci. J Bacteriol 197:3283–3293. https://doi.org/10.1128/JB.00389-15

    Article  CAS  Google Scholar 

  40. Begley M, Hill C, Gahan CGM (2006) Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72:1729–1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006

    Article  CAS  Google Scholar 

  41. Meijerink J, Mandigers C, van de Locht L, Tönnissen E, Goodsaid F, Raemaekers J (2001) A novel method to compensate for different amplification efficiencies between patient DNA samples in quantitative real-time PCR. J Mol Diagn 3:55–61. https://doi.org/10.1016/S1525-1578(10)60652-6

    Article  CAS  Google Scholar 

  42. Muñoz-Quezada S, Chenoll E, Vieites JM et al (2013) Isolation, identification and characterisation of three novel probiotic strains (Lactobacillus paracasei CNCM I-4034, Bifidobacterium breve CNCM I-4035 and Lactobacillus rhamnosus CNCM I-4036) from the faeces of exclusively breast-fed infants. Br J Nutr 109(Suppl 2):S51–S62. https://doi.org/10.1017/S0007114512005211

    Article  CAS  Google Scholar 

  43. Mallappa RH, Singh DK, Rokana N et al (2019) Screening and selection of probiotic Lactobacillus strains of Indian gut origin based on assessment of desired probiotic attributes combined with principal component and heatmap analysis. LWT 105:272–281. https://doi.org/10.1016/j.lwt.2019.02.002

    Article  CAS  Google Scholar 

  44. Cho SK, Lee SJ, Shin S-Y et al (2015) Development of bile salt-resistant Leuconostoc citreum by expression of bile salt hydrolase gene. J Microbiol Biotechnol 25:2100–2105. https://doi.org/10.4014/jmb.1505.05072

    Article  CAS  Google Scholar 

  45. Nanda DK, Chaudhary R, Kumar D (2018) Molecular approaches for identification of lactobacilli from traditional dairy products. In: Gahlawat SK, Duhan JS, Salar RK et al (eds) Advances in animal biotechnology and its applications. Springer, Singapore, pp 181–196

    Chapter  Google Scholar 

  46. Xu H, Jeong HS, Lee HY, Ahn J (2009) Assessment of cell surface properties and adhesion potential of selected probiotic strains. Lett Appl Microbiol 49:434–442. https://doi.org/10.1111/j.1472-765X.2009.02684.x

    Article  CAS  Google Scholar 

  47. de Albuquerque TMR, Garcia EF, de Oliveira AA et al (2018) In vitro characterization of Lactobacillus strains isolated from fruit processing by-products as potential probiotics. Probiotics Antimicrob Proteins 10:704–716. https://doi.org/10.1007/s12602-017-9318-2

    Article  CAS  Google Scholar 

  48. García-Cayuela T, Korany AM, Bustos I et al (2014) Adhesion abilities of dairy Lactobacillus plantarum strains showing an aggregation phenotype. Food Res Int 57:44–50. https://doi.org/10.1016/j.foodres.2014.01.010

    Article  CAS  Google Scholar 

  49. Greene JD, Klaenhammer TR (1994) Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl Environ Microbiol 60:4487–4494

    Article  CAS  Google Scholar 

  50. Kumar R, Grover S, Batish VK (2012) Bile salt hydrolase (Bsh) activity screening of Lactobacilli: in vitro selection of indigenous Lactobacillus strains with potential bile salt hydrolysing and cholesterol-lowering ability. Probiotics Antimicrob Proteins 4:162–172. https://doi.org/10.1007/s12602-012-9101-3

    Article  CAS  Google Scholar 

  51. Lambert JM, Bongers RS, de Vos WM, Kleerebezem M (2008) Functional analysis of four bile salt hydrolase and penicillin acylase family members in Lactobacillus plantarum WCFS1. Appl Environ Microbiol 74:4719–4726. https://doi.org/10.1128/AEM.00137-08

    Article  CAS  Google Scholar 

  52. Gu X-C, Luo X-G, Wang C-X, Ma DY, Wang Y, He YY, Li W, Zhou H, Zhang TC (2014) Cloning and analysis of bile salt hydrolase genes from Lactobacillus plantarum CGMCC no. 8198. Biotechnol Lett 36:975–983. https://doi.org/10.1007/s10529-013-1434-9

    Article  CAS  Google Scholar 

  53. Bustos AY, de Valdez GF, Raya R et al (2015) Proteomic analysis of the probiotic Lactobacillus reuteri CRL1098 reveals novel tolerance biomarkers to bile acid-induced stress. Food Res Int 77:599–607. https://doi.org/10.1016/j.foodres.2015.10.001

    Article  CAS  Google Scholar 

  54. Mathara JM, Schillinger U, Guigas C, Franz C, Kutima PM, Mbugua SK, Shin HK, Holzapfel WH (2008) Functional characteristics of Lactobacillus spp. from traditional Maasai fermented milk products in Kenya. Int J Food Microbiol 126:57–64. https://doi.org/10.1016/j.ijfoodmicro.2008.04.027

    Article  CAS  Google Scholar 

  55. Lye H-S, Rahmat-Ali GR, Liong M-T (2010) Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. Int Dairy J 20:169–175. https://doi.org/10.1016/j.idairyj.2009.10.003

    Article  CAS  Google Scholar 

  56. Le B, Yang S-H (2019) Identification of a novel potential probiotic Lactobacillus plantarum FB003 isolated from salted-fermented shrimp and its effect on cholesterol absorption by regulation of NPC1L1 and PPARα. Probiotics Antimicrob Proteins 11:785–793. https://doi.org/10.1007/s12602-018-9469-9

    Article  CAS  Google Scholar 

  57. Kriaa A, Bourgin M, Potiron A et al (2018) Microbial impact on cholesterol and bile acid metabolism: current status and future prospects. J Lipid Res jlr.R088989. https://doi.org/10.1194/jlr.R088989

  58. Liong MT, Shah NP (2005) Optimization of cholesterol removal, growth and fermentation patterns of Lactobacillus acidophilus ATCC 4962 in the presence of mannitol, fructo-oligosaccharide and inulin: a response surface methodology approach. J Appl Microbiol 98:1115–1126. https://doi.org/10.1111/j.1365-2672.2005.02544.x

    Article  CAS  Google Scholar 

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Acknowledgments

Nacim Barache was supported by a short-term fellowship awarded by the Algerian and French governments through the PROFAS-B+ program. The authors would like to thank Dr. Bruce Seal (USA) for critical reading of the manuscript and English improvement. Research at Lille University was supported by ALIBIOTECH CPER/FEDER program from la Région des Hauts-de-France.

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  1. Laboratoire de Microbiologie Appliquée, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, 06000, Bejaia, Algeria

    Nacim Barache & Farida Bendali

  2. Univ. Lille, INRA, Univ. Artois, Univ. Littoral Côte d’Opale, EA 7394 - ICV - Institut Charles Viollette, F-59000, Lille, France

    Nacim Barache, Rabia Ladjouzi, Yanath Belguesmia & Djamel Drider

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Barache, N., Ladjouzi, R., Belguesmia, Y. et al. Abundance of Lactobacillus plantarum Strains with Beneficial Attributes in Blackberries (Rubus sp.), Fresh Figs (Ficus carica), and Prickly Pears (Opuntia ficus-indica) Grown and Harvested in Algeria. Probiotics & Antimicro. Prot. 12, 1514–1523 (2020). https://doi.org/10.1007/s12602-020-09632-z

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