Probiotics and Antimicrobial Proteins

, Volume 11, Issue 1, pp 113–123 | Cite as

Evaluating the Probiotic Potential of Lactobacillus plantarum Strains from Algerian Infant Feces: Towards the Design of Probiotic Starter Cultures Tailored for Developing Countries

  • Chahira Gheziel
  • Pasquale Russo
  • Mattia Pia Arena
  • Giuseppe Spano
  • Hadda-Imene Ouzari
  • Omar Kheroua
  • Djamel Saidi
  • Daniela FioccoEmail author
  • Hanane Kaddouri
  • Vittorio Capozzi


Lactobacilli naturally present in the neonatal gut are believed to be beneficial for the human hosts and are investigated as potential probiotics. In this study, we aimed to characterize six Lactobacillus plantarum strains derived from the feces of a breast-fed infant, for the development of new probiotic cultures. Our attention was focused on L. plantarum in reason of the presence, within such species, of both pro-technological and probiotic strains, i.e., a combination of particular interest to design tailored probiotic starter cultures for developing countries. The bacterial isolates exhibiting lactobacilli-like phenotypic characteristics were identified as members of the L. plantarum group by 16S rRNA gene sequencing, and their diversity was evaluated by randomly amplified polymorphic DNA (RAPD) PCR patterns. The selected strains were screened for probiotic potential through in vitro tests. Firstly, bacterial survival was evaluated in an in vitro system simulating the human oro-gastrointestinal tract, using also milk as a carrier matrix. Besides, physiological traits such as antibiotic susceptibility, antimicrobial activity against selected enteric pathogens, and adhesion to abiotic surfaces and to gastric mucin were studied. Considering the resistance to simulated gastrointestinal digestion and the results from the biofilm and mucin adhesion tests, a strain-denominated L. plantarum LSC3 was selected for further evaluation of in vitro adhesion ability to intestinal mucosa and immunomodulatory activities. L. plantarum LSC3 was able to adhere efficiently to human enterocyte-like cells (Caco-2 cells), and decreased IL-8 transcription while increasing IL-10 mRNA level, as revealed by transcriptional analysis on LPS-stimulated human (THP-1) macrophages. Our results highlight that L. plantarum LSC3 fulfills major in vitro probiotic criteria as well as interesting immunostimulatory properties, and thus may be a promising candidate for further in vivo studies aiming at the development of novel probiotic starter cultures.


Lactobacillus plantarum Probiotic Infant feces isolates Developing country 



Vittorio Capozzi was supported by Fondo di Sviluppo e Coesione 2007-2013—APQ Ricerca Regione Puglia “Programma regionale a sostegno della specializzazione intelligente e della sostenibilità sociale ed ambientale—FutureInResearch”. Pasquale Russo was supported by a grant of the Apulian Region in the framework of “Perform Tech (Puglia Emerging Food Technology)” project (practice code LPIJ9P2).

This paper is dedicated to the memory of our friend and colleague Prof. Chekroun Abdallah.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Statement

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

Supplementary material

12602_2018_9396_MOESM1_ESM.pdf (110 kb)
ESM 1 (PDF 109 kb)


  1. 1.
    Siezen RJ, Tzeneva VA, Castioni A, Wels M, Phan HTK, Rademaker JLW, Starrenburg MJC, Kleerebezem M, Molenaar D, Vlieg JH (2010) Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ Microbiol 12(3):758–773. Google Scholar
  2. 2.
    Martin R, Langa S, Reviriego C, Jimenez E, Marin ML, Xaus J, Fernandez L, Rodriguez JM (2003) Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr 143(6):754–758. Google Scholar
  3. 3.
    Cho I, Blaser M (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13(4):260–270. Google Scholar
  4. 4.
    Rodrigues da Cunha L, Fortes Ferreira CL, Durmaz E, Goh YJ, Sanozky-Dawes R, Klaenhammer T (2012) Characterization of Lactobacillus gasseri isolates from a breast-fed infant. Gut Microbes 3(1):15–24. Google Scholar
  5. 5.
    Wang CY, Lin PR, Ng CC, Shyu YT (2010) Probiotic properties of Lactobacillus strains isolated from the feces of breast-fed infants and Taiwanese pickled cabbage. Anaerobe 16(6):578–585. Google Scholar
  6. 6.
    Berbegal C, Peña N, Russo P, Grieco F, Pardo I, Ferrer S, Spano G, Capozzi V (2016) Technological properties of Lactobacillus plantarum strains isolated from grape must fermentation. Food Microbiol 57:187–194. Google Scholar
  7. 7.
    Monika S, Kumar V, Kumari A, Angmo K, Bhalla TC (2017) Isolation and characterization of lactic acid bacteria from traditional pickles of Himachal Pradesh, India. J Food Sci Technol 54(7):1945–1952. Google Scholar
  8. 8.
    Russo P, Arena MP, Fiocco D, Capozzi V, Drider D, Spano G (2017) Lactobacillus plantarum with broad antifungal activity: a promising approach to increase safety and shelf-life of cereal-based products. Int J Food Microbiol 247:48–54. Google Scholar
  9. 9.
    Seddik HA, Bendali F, Gancel F, Fliss I, Spano G, Drider D (2017a) Lactobacillus plantarum and its probiotic and food potentialities. Probiotics Antimicrob Proteins 9(2):111–122. Google Scholar
  10. 10.
    Molenaar D, Bringel F, Schuren FH, De vos WM, Siezen RJ, Kleerebezem M (2005) Exploring Lactobacillus plantarum genome diversity by using microarrays. J Bacteriol 187(17):6119–6127. Google Scholar
  11. 11.
    Bove P, Gallone A, Russo P, Capozzi V, Albenzio M, Spano G, Fiocco D (2012) Probiotic features of Lactobacillus plantarum mutant strains. Appl Microbiol Biotechnol 96(2):431–441. Google Scholar
  12. 12.
    FAO-WHO (2002) Joint FAO/WHO Working group report on drafting guidelines for the evaluation of probiotics in food. Food and Agricultural Organization of the United Nations. Available online at: food/wgreport2.pdfGoogle Scholar
  13. 13.
    Bove P, Russo P, Capozzi V, Gallone A, Spano G, Fiocco D (2013) Lactobacillus plantarum passage through an oro-gastro-intestinal tract simulator: carrier matrix effect and transcriptional analysis of genes associated to stress and probiosis. Microbiol Res 168(6):351–359. Google Scholar
  14. 14.
    Donkor ON, Nilmin S, Stolic P, Vasiljevic T, Shah NP (2007) Survival and activity of selected probiotic organisms in set-type yoghurt during cold storage. Int Dairy J 17(6):657–665. Google Scholar
  15. 15.
    Buriti FC, Castro IA, Saad SM (2010) Viability of Lactobacillus acidophilus in synbiotic guava mousses and its survival under in vitro simulated gastrointestinal conditions. Int J Food Microbiol 137(2-3):121–129. Google Scholar
  16. 16.
    Hernandez-Hernandez O, Muthaiyan A, Moreno FJ, Montilla A, Sanz ML, Ricke SC (2012) Effect of prebiotic carbohydrates on the growth and tolerance of Lactobacillus. Food Microbiol 30(2):355–361. Google Scholar
  17. 17.
    Resta-Lenert S, Barrett KE (2003) Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive Escherichia coli (EIEC). Gut 52(7):988–997. Google Scholar
  18. 18.
    Fogh J, Fogh JM, Orfeo T (1977) One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J Natl Cancer Inst 59(1):221–226. Google Scholar
  19. 19.
    Lomax AR, Calder PC (2009) Probiotics, immune function, infection and inflammation: a review of the evidence from studies conducted in humans. Curr Pharm Des 15(13):1428–1518. Google Scholar
  20. 20.
    Maslowski KM, Mackay CR (2011) Diet, gut microbiota and immune responses. Nat Immunol 12(1):5–9. Google Scholar
  21. 21.
    Arena MP, Russo P, Capozzi V, Rascón A, Felis G, Spano G, Fiocco D (2016a) Combinations of cereal β-glucans and probiotics can enhance the anti-inflammatory activity on host cells by a synergistic effect. J Funct Foods 23:12–23. Google Scholar
  22. 22.
    Reid G, Anand S, Bingham MO, Mbugua G, Wadstrom T, Fuller R, Anukam K, Katsivo M (2005) Probiotics for the developing world. J Clin Gastroenterol 39(6):485–488. Google Scholar
  23. 23.
    Sybesma W, Kort R, Lee YK (2015) Locally sourced probiotics, the next opportunity for developing countries? Trends Biotech 33(4):197–200. Google Scholar
  24. 24.
    Seddik HA, Bendali F, Cudennec B, Drider D (2017b) Anti-pathogenic and probiotic attributes of Lactobacillus salivarius and Lactobacillus plantarum strains isolated from feces of Algerian infants and adults. Res Microbiol 168(3):244–254. Google Scholar
  25. 25.
    Kleerebezem M, Boekhorst J, Van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MW, Stiekema W, Lankhorst RM, Bron PA, Hoffer SM, Groot MN, Kerkhoven R, de Vries M, Ursing B, de Vos WM, Siezen RJ (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100(4):1990–1995. Google Scholar
  26. 26.
    Spano G, Beneduce L, Tarantino D, Zapparoli G, Massa S (2002) Characterization of Lactobacillus plantarum from wine must by PCR species-specific and RAPD-PCR. Lett Appl Microbiol 35(5):370–374. Google Scholar
  27. 27.
    Arena MP, Silvain A, Normanno G, Grieco F, Drider D, Spano G, Fiocco D (2016b) Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front Microbiol 7:464Google Scholar
  28. 28.
    Tulini FL, Winkelströter LK, De Martinis ECP (2013) Identification and evaluation of the probiotic potential of Lactobacillus paraplantarum FT259, a bacteriocinogenic strain isolated from Brazilian semi-hard artisanal cheese. Anaerobe 22:57–63. Google Scholar
  29. 29.
    Vergara-Irigaray M, Valle J, Merino N, Latasa C, García B, De Los R, Mozos I, Solano C, Toledo-Arana A, Penadés JR, Lasa I (2009) Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect Immun 77(9):3978–3991. Google Scholar
  30. 30.
    Leccese Terraf MC, Mendoza LM, Juarez MS, Silva C, Nader-Mac MEF (2014) Phenotypic surface properties (aggregation, adhesion and biofilm formation) and presence of related genes in beneficial vaginal lactobacilli. J Appl Microbiol 117(6):1761–1772. Google Scholar
  31. 31.
    Russo P, López P, Capozzi V, Fernández de Palencia P, Dueñas MT, Spano G, Fiocco D (2012) Beta-glucans improve growth, viability and colonization of probiotic microorganisms. Int J Mol Sci 13(12):6026–6039. Google Scholar
  32. 32.
    Arena MP, Caggianiello G, Russo P, Albenzio M, Massa S, Fiocco D, Capozzi V, Spano G (2015) Functional starters for functional yogurt. Foods 4(4):15–33. Google Scholar
  33. 33.
    Gu CT, Ly CY, Yang LJ, Huo GC (2013) Lactobacillus mudanjiangensis sp. nov., Lactobacillus songhuajiangensis sp. nov. and Lactobacillus nenjiangensis sp. nov., isolated from Chinese traditional pickle and sourdough. Int J Syst Evol Microbiol 63(Pt 12):4698–4706. Google Scholar
  34. 34.
    Arena MP, Caggianiello G, Fiocco D, Russo P, Torelli M, Spano G, Capozzi V (2014) Barley β-glucans-containing food enhances probiotic performances of beneficial bacteria. Int J Mol Sci 15:3026–3039Google Scholar
  35. 35.
    Chen JJ, Cai W, Feng Y (2007) Development of intestinal bifidobacteria and lactobacilli in breast fed neonates. Clin Nutr 26(5):559–566. Google Scholar
  36. 36.
    Sanders ME, Marco ML (2010) Food formats for effective delivery of probiotics. Annu Rev Food Sci Technol 1(1):65–85. Google Scholar
  37. 37.
    Bosch M, Rodriguez M, Garcia F, Fernandez E, Fuentes MC, Cune J (2011) Probiotic properties of Lactobacillus plantarum CECT 7315 and CECT 7316 isolated from faeces of healthy children. Lett Appl Microbiol 54:240–246Google Scholar
  38. 38.
    Fernández de Palencia P, López P, Corbí AL, Peláez C, Requena T (2008) Probiotic strains: survival under simulated gastrointestinal conditions, in vitro adhesion to Caco-2 cells and effect on cytokine secretion. Europ Food Res Technol 227:1475–1484Google Scholar
  39. 39.
    Ziarno M, Zareba D (2015) Effect of milk components and food additives on survival of three bifidobacteria. Microb Ecol Health Dis 26:27812Google Scholar
  40. 40.
    Castellano P, Belfiore C, Fadda S, Vignolo G (2008) A review of bacteriocinogenic lactic acid bacteria used as bioprotective cultures in fresh meat produced in Argentina. Meat Sci 79(3):483–499. Google Scholar
  41. 41.
    Gaudana SB, Dhanani AS, Bagchi T (2010) Probiotic attributes of Lactobacillus strains isolated from food and of human origin. Br J Nutr 103(11):1620–1628. Google Scholar
  42. 42.
    Lavanya B, Sowmiya S, Balaji S, Muthuvelan B (2011) Screening and characterization of lactic acid bacteria from fermented milk. Br. J Dairy Sci 2:5–10Google Scholar
  43. 43.
    Silva BC, Sandes SHC, Alvim LB, Bomfim MRQ, Nicoli JR, Neumann E, Nunes AC (2016) Selection of a candidate probiotic strain of Pediococcus pentosaceus from the faecal microbiota of horses by in vitro testing and health claims in a mouse model of Salmonella infection. J Appl Microbiol 122:225–238Google Scholar
  44. 44.
    Zommiti M, Connil N, Hamida JB, Ferchichi M (2017) Probiotic characteristics of Lactobacillus curvatus DN317, a strain isolated from chicken ceca. Probiotics Antimicrob Proteins 9(4):415–424. Google Scholar
  45. 45.
    Argyri A, Zoumpopoulou G, Karatzas K, Tsakalidou E, Nychas G, Panagou E, Tassou C (2012) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33:282–291Google Scholar
  46. 46.
    Salas-Jara M, Ilabaca A, Vega M, García A (2016) Biofilm forming Lactobacillus: new challenges for the development of probiotics. Microorganisms 4(4):35. Google Scholar
  47. 47.
    Arena MP, Capozzi V, Spano G, Fiocco D (2017) The potential of lactic acid bacteria to colonize biotic and abiotic surfaces and the investigation of their interactions and mechanisms. Appl Microbiol Biotechnol 101(7):2641–2657. Google Scholar
  48. 48.
    Yadav AK, Tyagi A, Kumar A, Panwar S, Grover S, Saklani AC, Hemalatha R, Batish VK (2017) Adhesion of lactobacilli and their anti-infectivity potential. Crit Rev Food Sci Nutr 57(10):2042–2056. Google Scholar
  49. 49.
    Mackenzie DA, Jeffers F, Parker ML, Vibert-Vallet A, Bongaerts RJ, Roos S, Walter J, Juge N (2010) Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiol 156(11):3368–3378. Google Scholar
  50. 50.
    García-Ruiz A, De llano D, Esteban-Fernández A, Requena T, Bartolomé B, Moreno-Arribas V (2014) Assessment of probiotic properties in lactic acid bacteria isolated from wine. Food Microbiol 44:220–225. Google Scholar
  51. 51.
    Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72(4):728–764. Google Scholar
  52. 52.
    Cader MZ, Kaser A (2013) Recent advances in inflammatory bowel disease: mucosal immune cells in intestinal inflammation. Gut 62(11):1653–1664. Google Scholar
  53. 53.
    Ducrotté P, Sawant P, Jayanthi V (2012) Clinical trial: Lactobacillus plantarum 299v (DSM 9843) improves symptoms of irritable bowel syndrome. World J Gastoenterol 18(30):4012–4018. Google Scholar
  54. 54.
    Bauerl C, Llopis M, Antol M (2013) Lactobacillus paracasei and Lactobacillus plantarum strains downregulate proinflammatory genes in an ex vivo system of cultured human colonic mucosa. Genes Nutr 8(2):165–180. Google Scholar
  55. 55.
    Riedel CU, Foata F, Philippe D, Adolfsson O, Eikmanns BJ, Blum S (2006) Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-kappaB activation. World J Gastroenterol 12(23):3729–3735. Google Scholar
  56. 56.
    Duary RJ, Batish VK, Grover S (2014) Immunomodulatory activity of two potential probiotic strains in LPS-stimulated HT-29 cells. Genes Nutr 9(3):398. Google Scholar
  57. 57.
    Helwig U, Lammers KM, Rizzello F, Brigidi P, Rohleder V, Caramelli E, Gionchetti P, Schrezenmeir J, Foelsch UR, Schreiber S, Campieri M (2006) Lactobacilli, bifidobacteria and E. coli nissle induce pro- and anti-inflammatory cytokines in peripheral blood mononuclear cells. World J Gastroenterol 12(37):5978–5986. Google Scholar
  58. 58.
    Messaoudi S, Madi A, Prévost H, Feuilloley M, Manai M, Dousset X, Connil N (2012) In vitro evaluation of the probiotic potential of Lactobacillus salivarius SMXD51. Anaerobe 18(6):584–589. Google Scholar
  59. 59.
    Rong J, Zheng H, Liu M, Hu X, Wang T, Zhang X, Jin F, Wang L (2015) Probiotic and anti-inflammatory attributes of an isolate Lactobacillus helveticus NS8 from Mongolian fermented koumiss. BMC Microbiol 15(1):196. Google Scholar
  60. 60.
    Hill DA, Artis D (2010) Intestinal bacteria and the regulation of immune cell homeostasis. Annu Rev Immunol 28(1):623–667. Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Chahira Gheziel
    • 1
  • Pasquale Russo
    • 2
  • Mattia Pia Arena
    • 2
  • Giuseppe Spano
    • 2
  • Hadda-Imene Ouzari
    • 3
  • Omar Kheroua
    • 1
  • Djamel Saidi
    • 1
  • Daniela Fiocco
    • 4
    Email author
  • Hanane Kaddouri
    • 1
  • Vittorio Capozzi
    • 2
  1. 1.Laboratory of Physiology of the Nutrition and Food Security, Department of Biology, Faculty of Natural and Life SciencesUniversity of OranOranAlgeria
  2. 2.Department of Agriculture, Food and Environment SciencesUniversity of FoggiaFoggiaItaly
  3. 3.Laboratoire de Microorganismes et Biomolécules Actives, Faculté des Sciences de TunisUniversité Tunis El ManarTunisTunisie
  4. 4.Department of Clinical and Experimental MedicineUniversity of FoggiaFoggiaItaly

Personalised recommendations