In Vitro evaluation of probiotic properties of lactic acid bacteria strains isolated from juçara fruit native to the Atlantic Forest

Authors

DOI:

https://doi.org/10.5433/1679-0359.2024v45n5p1443

Keywords:

Lactococcus lactis, Leuconostoc pseudomesenteroides, Euterpe edulis Martius, Aggregation activity, Simulated gastrointestinal.

Abstract

Lactic acid bacteria (LAB) are the microorganisms most commonly used as probiotics. Since probiotic benefits are strain-dependent, there is a continuous need for research into new cultures with probiotic properties. Fruits such as juçara (Euterpe edulis Martius), a palm species from the Atlantic Forest threatened with extinction, are rich niches for microorganisms, including LAB. This study investigated the probiotic properties of Lactococcus lactis J7 and Leuconostoc pseudomesenteroides JF17 strains isolated from juçara fruits native to the Atlantic Forest. Probiotic characteristics, such as tolerance to simulated gastrointestinal fluids or juices, hydrophobicity, autoaggregation, coaggregation properties, inhibition of pathogenic microorganisms, and technological properties were evaluated. The survival rate of L. lactis J7 and L. pseudomesenteroides JF17 decreased after exposure to simulated gastrointestinal conditions; however, L. lactis J7 was more resistant, maintaining viability at the end of the enteric phase of 6.07 ± 0.16 log CFU mL-1. The J7 strain also exhibited the highest values in hydrophobicity (12.55 ± 0.52%), autoaggregation (25.63 ± 0.75%), and coaggregation capacity with E. coli ATCC 25922 (21.52 ± 0.98%) and S. Enteritidis ATCC 13076 (22.68 ± 1.01%). Both J7 and JF17 strains demonstrated antimicrobial activity, confirmed by the multilayer agar plate system. Additionally, the growth of the strains was temperature-dependent, and they were able to thrive in high concentrations of sodium chloride (6%). Thus, L. lactis J7 is a promising probiotic candidate for the development of functional products. Nevertheless, further studies using animal models are necessary to explore the properties of these probiotic bacteria. Novel strains isolated from fruits should be studied to broaden the application of probiotic microorganisms in the development of foods and medicines.

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Author Biographies

Fernanda Silva Farinazzo , Universidade Federal da Fronteira Sul

Profa. Dra. of the Undergraduate Course in Food Engineering, Universidade Federal da Fronteira Sul, UFFS, Laranjeiras do Sul, PR, Brazil.

Maria Thereza Carlos Fernandes, Universidade do Norte do Paraná

Profa. Dra. of the Undergraduate Course in Pharmacy, Universidade do Norte do Paraná, UNOPAR, Arapongas, PR, Brazil.

Carolina Saori Ishii Mauro, Universidade Positivo

Profa. Dra. of the Undergraduate Course in Pharmacy and Biomedicine, Universidade Positivo, UP, Londrina, PR, Brazil.

Marsilvio Lima de Moraes Filho, Universidade Estadual de Maringá

Prof. Dr. of the Undergraduate Course in Food Technology, Universidade Estadual de Maringá, UEM, Umuarama, PR, Brazil.

Fabiane Bach, Universidade Estadual de Mato Grosso do Sul

Profa. Dra. of the Undergraduate Course in Food Engineering, Universidade Estadual do Mato Grosso do Sul, UEMS, Naviraí, MS, Brazil.

Sandra Garcia, Universidade Estadual de Londrina

Profa. Dra., of the Postgraduate Program in Food Science, Universidade Estadual de Londrina, UEL, Londrina, PR, Brazil.

References

Almada, C. N. de, Almada, C. N., Martinez, R. C. R., & Sant’Ana, A. S. (2016). Paraprobiotics: evidences on their ability to modify biological responses, inactivation methods and perspectives on their application in foods. Trends in Food Science & Technology, 58, 96-114. doi: 10.1016/j.tifs.2016.09.011 DOI: https://doi.org/10.1016/j.tifs.2016.09.011

Ammor, S., Tauveron, G., Dufour, E., & Chevallier, I. (2006). Antibacterial activity of lactic acid bacteria against spoilage and pathogenic bacteria isolated from the same meat small-scale facility: 1-Screening and characterization of the antibacterial compounds. Food Control, 17(6), 454-461. doi: 10.1016/j.foodcont.2005.02.006 DOI: https://doi.org/10.1016/j.foodcont.2005.02.006

Armas, F., Camperio, C., & Marianelli, C. (2017). In vitro assessment of the probiotic potential of Lactococcus lactis LMG 7930 against ruminant mastitis-causing pathogens. Plos One, 12(1), e0169543. doi: 10.1371/journal.pone.0169543 DOI: https://doi.org/10.1371/journal.pone.0169543

Bao, Y., Zhang, Y., Zhang, Y., Liu, Y., Wang, S., Dong, X., Wang, S., Dong, X., Wang, Y., & Zhang, H. (2010). Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control, 21(5), 695-701. doi: 10.1016/j.foodcont.2009.10.010 DOI: https://doi.org/10.1016/j.foodcont.2009.10.010

Bedani, R., Vieira, A. D. S., Rossi, E. A., & Saad, S. M. I. (2014). Tropical fruit pulps decreased probiotic survival to in vitro gastrointestinal stress in synbiotic soy yoghurt with okara during storage. LWT - Food Science and Technology, 55(2), 436-443. doi: 10.1016/j.lwt.2013.10.015 DOI: https://doi.org/10.1016/j.lwt.2013.10.015

Benavides, A. B., Ulcuango, M., Yépez, L., & Tenea, G. N. (2016). Assessment of the in vitro bioactive properties of lactic acid bacteria isolated from native ecological niches of Ecuador. La Revista Argentina de Microbiología, 48(3), 236-244. doi: 10.1016/j.ram.2016.05.003 DOI: https://doi.org/10.1016/j.ram.2016.05.003

Caporaso, J., Lauber, C., Walters, W., Berg-Lyons, D., Lozupone, C., Turnbaugh, P., Fierer, N., & Knight, R. (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences, 108(Suppl 1), 4516-4522. doi: 10.1073/pnas.1000080107 DOI: https://doi.org/10.1073/pnas.1000080107

Cassani, L., Gomez-Zavaglia, A., & Simal-Gandara, J. (2020). Technological strategies ensuring the safe arrival of beneficial microorganisms to the gut: from food processing and storage to their passage through the gastrointestinal tract. Food Research International, 129(11), 108852. doi: 10.1016/j.foodres.2019.108852 DOI: https://doi.org/10.1016/j.foodres.2019.108852

Collado, M., Meriluoto, J., & Salminen, S. (2008). Adhesion and aggregation properties of probiotic and pathogen strains. European Food Research and Technology, 226, 1065-1073. doi: 10.1007/s00217-007-0632-x DOI: https://doi.org/10.1007/s00217-007-0632-x

Costa, G. N., Suguimoto, H. H., Miglioranza, L. H. S., & Gómez, R. J. H. C. (2012). Antimicrobial activity of Lactobacillus and Bifidobacterium strains against pathogenic microorganisms “in vitro”. Semina: Ciências Agrárias, 33(5), 839-1846. doi: 10.5433/1679-0359.2012v33n5p1839 DOI: https://doi.org/10.5433/1679-0359.2012v33n5p1839

Diep, D. B., Håvarstein, L. S., & Nes, I. F. A. (1995). Bacteriocin like peptide induces bacteriocin synthesis in Lactobacillus plantarum C11. Molecular Microbiology, 18(4), 631-639. doi: 10.1111/j.1365-2958.1995.mmi_18040631.x DOI: https://doi.org/10.1111/j.1365-2958.1995.mmi_18040631.x

Food and Agriculture Organization of the United Nations / World Health Organization (2002). Working group report on drafting guidelines for the evaluation of probiotics in food London. FAO/WHO. https://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf

Giaouris, E., Chapot-Chartier, M. P., & Briandet, R. (2009). Surface physicochemical analysis of natural Lactococcus lactis strains reveals the existence of hydrophobic and low charged strains with altered adhesive properties. International Journal of Food Microbiology, 131(1), 2-9. doi: 10.1016/j.ijfoodmicro.2008.09.006 DOI: https://doi.org/10.1016/j.ijfoodmicro.2008.09.006

Gonzalez, E. E., & Aryana, K. (2018). Salt tolerance of cheese culture Lactococcus lactis R-604 as influenced by prior salt exposure and lactose deprivation. Nutrition and Food Science, 9(6), 633-641. doi: 10. 4236/fns.2018.96048. DOI: https://doi.org/10.4236/fns.2018.96048

Grujović, M. Ž., Mladenović, K. G., Semedo-Lemsaddek, T., Laranjo, M., Stefanović, O. D., & Kocić-Tanacko, S. D. (2022). Advantages and disadvantages of non-starter lactic acid bacteria from traditional fermented foods: potential use as starters or probiotics. Comprehensive Reviews in Food Science and Food Safety, 21(2), 1537-1567. doi: 10.1111/1541-4337.12897 DOI: https://doi.org/10.1111/1541-4337.12897

Huang, S., Vignolles, M. L., Chen, X. D., Le Loir, Y., Jan, G., Schuck, P., & Jeantet, R. (2017). Spray drying of probiotics and other food-grade bacteria: a review. Trends in Food Science & Technology, 63(2), 1-17. doi: 10.1016/j.tifs.2017.02.007 DOI: https://doi.org/10.1016/j.tifs.2017.02.007

Hwanhlem, N., Ivanova, T., Haertle, T., Jaffres, E., & Dousset, X. (2017). Inhibition of food-spoilage and foodborne pathogenic bacteria by a nisin Z-producing Lactococcus lactis subsp. lactis KT2W2L. LWT - Food Science and Technology, 82(1), 170-175. doi: 10.1016/j.lwt.2017.04.052 DOI: https://doi.org/10.1016/j.lwt.2017.04.052

Kimoto-Nira, H., Chise Suzuki, C., Sasaki, K., Kobayashi, M., & Mizumachi, K. (2010). Survival of a Lactococcus lactis strain varies with its carbohydrate preference under in vitro conditions simulated gastrointestinal tract. International Journal of Food Microbiology, 143(3), 226-229. doi: 10.1016/j.ijfoodmicro.2010.07.033 DOI: https://doi.org/10.1016/j.ijfoodmicro.2010.07.033

Lee, N. K., Han, K. J., Son, S. H., Eom, S. J., Lee, S. K., & Paik, H. B. (2015). Multifunctional effect of probiotic Lactococcus lactis KC24 isolated from kimchi. LWT - Food Science and Technology, 64(2), 1036-1041. doi: 10.1016/j.lwt.2015.07.019 DOI: https://doi.org/10.1016/j.lwt.2015.07.019

Linares, D. M., Gómez, C., Renes, E., Fresno, J. M., Tornadijo, M. E., Ross, R. P., & Stanton, C. (2017). Lactic acid bacteria and bifidobacteria with potential to design natural biofunctional health-promoting dairy foods. Frontiers in Microbiology, 8, 846. doi: 10.3389/fmicb.2017.00846 DOI: https://doi.org/10.3389/fmicb.2017.00846

Marteau, P., & Rambaud, J. C. (1993). Potential of using lactic acid bacteria for therapy and immunomodulation in man. FEMS Microbiology Reviews, 12(1-3), 207-220. doi: 10.1111/j.1574-6976.1993.tb00019.x DOI: https://doi.org/10.1111/j.1574-6976.1993.tb00019.x

Makinen, K., Berger, B., Bel-Rhlid, R., & Ananta, E. (2012). Science and technology for the mastership of probiotic applications in food products. Journal of Biotechnology, 162(4), 356-365. doi: 10.1016/j.jbiotec.2012.07.006 DOI: https://doi.org/10.1016/j.jbiotec.2012.07.006

Mendonça, A. A., Pinto, W. P., Neto, Paixão, G. A. da, Santos, D. S., Morais, M. A. de, Jr., & Souza, R. B. (2023). Journey of the probiotic bacteria: survival of the fittest. Microorganisms, 11(1), 95. doi: 10.3390/microorganisms11010095 DOI: https://doi.org/10.3390/microorganisms11010095

Meidistria, T. R., Sembiring, L., Rahayu, E. S., Haedar, N., & Dwyana, Z. (2020). Survival of Lactobacillus plantarum dad 13 in probiotic cheese making. IOP Conference Series: Earth and Environmental Science, 575(1), 012020. doi: 10.1088/1755-1315/575/1/012020 DOI: https://doi.org/10.1088/1755-1315/575/1/012020

Miranda, J. S., Costa, B. V., Oliveira, I. V. de, Lima, D. C. N. de, Martins, E. M. F., Leite, B. R. C, Jr., Benevenuto, W. C. A. N., Queiroz, I. C. de, Silva, R. R. da, & Martins, M. L. (2020). Probiotic jelly candies enriched with native Atlantic Forest fruits and Bacillus coagulans GBI-30 6086. LWT - Food Science and Technology, 126, 109275. doi: 10.1016/j.lwt.2020.109275 DOI: https://doi.org/10.1016/j.lwt.2020.109275

Nami, Y., Bakhshayesh, R. V., Jalaly, H. M., Lotfi, H., Eslami, S., & Hejazi, M. A. (2019). Probiotic properties of Enterococcus isolated from artisanal dairy products. Frontiers in Microbiology, 10, 300, 1-13. doi: 10.3389/fmicb.2019.00300 DOI: https://doi.org/10.3389/fmicb.2019.00300

Ng, S. Y., Koon, S. S., Padam, B. S., & Chye, F. Y. (2015). Evaluation of probiotic potential of lactic acid bacteria isolated from traditional Malaysian fermented Bambangan (Mangifera pajang). CyTA - Journal of Food, 13(4), 1-10. doi: 10.1080/19476337.2015.1020342 DOI: https://doi.org/10.1080/19476337.2015.1020342

Nikaido, H. (1996). Outer membrane. In F. C. Neidhardt, & R. Curtiss (Eds.), Escherichia coli and Salmonella: cellular and molecular biology (pp. 29-47). Washington, DC.

Olaimat, A. N., Aolymat, I., Al-Holy, M., Ayyash, M., Abu Ghoush, M., Al-Nabulsi, A. A., Osaili, T., Apostolopoulos, V., Liu, S.-Q., & Shah, N. P. (2020). The potential application of probiotics and prebiotics for the prevention and treatment of COVID-19. NPJ Science of Food, 4, 17. doi: 10.1038/s41538-020-00078-9 DOI: https://doi.org/10.1038/s41538-020-00078-9

Ouwehand, A. C., Tuomola, E. M., Tölkkö, S., & Salminen, S. (2001). Assessment of adhesion properties of novel probiotic strains to human intestinal mucus. International Journal of Food Microbiology, 64(1-2), 119-126. doi: 10.1016/S0168-1605(00)00440-2 DOI: https://doi.org/10.1016/S0168-1605(00)00440-2

Öz, E., Kaban, G., Barış, Ö., & Kaya, M. (2017). Isolation and identification of lactic acid bacteria from pastirma. Food Control, 77, 158-162. doi: 10.1016/j.foodcont.2017.02.017 DOI: https://doi.org/10.1016/j.foodcont.2017.02.017

Palanivelu, J., Thanigaivel, S., Vickram, S., Dey, N., Mihaylova, D., & Desseva I. (2022). Probiotics in functional foods: survival assessment and approaches for improved viability. Applied Sciences, 12(1), 455. doi: 10.3390/app12010455 DOI: https://doi.org/10.3390/app12010455

Rodrigues, L. R. (2011). Inhibition of bacterial adhesion on medical devices. In D. Linke, & A. Goldman (Ed.), Bacterial adhesion. Advances in experimental medicine and biology (pp. 351-367). Dordrecht. DOI: https://doi.org/10.1007/978-94-007-0940-9_22

Sakandar, H. A., Kubow, S., & Sadiq, F. A. (2019). Isolation and in-vitro probiotic characterization of fructophilic lactic acid bacteria from Chinese fruits and flowers. LWT - Food Science and Technology, 104, 70-75. doi: 10.1016/j.lwt.2019.01.038 DOI: https://doi.org/10.1016/j.lwt.2019.01.038

Sánchez, B., Ruiz, L., Gueimonde, M., Ruas-Madiedo, P., & Margolles, A. (2012). Toward improving technological and functional properties of probiotics in foods. Trends in Food Science & Technology, 26(1), 56-63. doi: 10.1016/j.tifs.2012.02.002 DOI: https://doi.org/10.1016/j.tifs.2012.02.002

Sharma, M., Wasan, A., & Sharma, R. K. (2021). Recent developments in probiotics: an emphasis on Bifidobacterium. Food Bioscience, 41, 100993. doi: 10.1016/j.fbio.2021.100993 DOI: https://doi.org/10.1016/j.fbio.2021.100993

Sionek, B., Szydłowska, A., Zielińska, D., Neffe-Skocińska, K., & Kołożyn-Krajewska, D. (2023). Beneficial bacteria isolated from food in relation to the next generation of probiotics. Microorganisms, 11(7), 1714. doi: 10.3390/microorganisms11071714 DOI: https://doi.org/10.3390/microorganisms11071714

Smith, W. M., Dykes, G. A., Soomro, A. H., & Turner, M. S. (2010). Molecular mechanisms of stress resistance in Lactococcus lactis. In Méndez-Vilas, A. (Ed.), Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology (pp.1106-1118) Formatex Research Center.

Sunny-Roberts, E. O., & Knorr, D. (2008). Evaluation of the response of Lactobacillus rhamnosus VTT E-97800 to sucrose-induced osmotic stress. Food Microbiology, 25(1), 183-189. doi: 10.1016/j.fm.2007.05.003 DOI: https://doi.org/10.1016/j.fm.2007.05.003

Tallapragada, P., Rayavarapu, B., Rao, P. P., Ranganath, N. N., & Veerabhadrappa, P. P. (2018). Screening of potential probiotic lactic acid bacteria and production of amylase and its partial purification. Journal of Genetic Engineering and Biotechnology, 16(2), 357-362. doi: 10.1016/j.jgeb.2018.03.005 DOI: https://doi.org/10.1016/j.jgeb.2018.03.005

Todorov, S. D., Furtado, D. N., Saad, S. M., Tome, E., & Franco, B. D. (2011). Potential beneficial properties of bacteriocin-producing lactic acid bacteria isolated from smoked salmon. Journal of Applied Microbiology, 110(4), 971-986. doi: 10.1111/j.1365-2672.2011.04950.x DOI: https://doi.org/10.1111/j.1365-2672.2011.04950.x

Topçu, K. C., Kaya, M., & Kaban, G. (2020). Probiotic properties of lactic acid bacteria strains isolated from pastırma. LWT - Food Science and Technology, 134(nº), 110216. doi: 10.1016/j.lwt.2020.110216 DOI: https://doi.org/10.1016/j.lwt.2020.110216

Tuo, Y., Yu, H., Ai, L., Wu, Z., Guo, B., & Chen, W. (2013). Aggregation and adhesion properties of Lactobacillus strains. Journal of Dairy Science, 96(7), 4252-4257. doi: 10.3168/jds.2013-6547 DOI: https://doi.org/10.3168/jds.2013-6547

Wang, C. Y., Lin, P. R., Ng, C. C., & Shyu, Y. T. (2010). Probiotic properties of Lactobacillus strains isolated from the feces of breastfed infants and Taiwanese pickled cabbage. Anaerobe, 16(6), 578-585. doi: 10.1016/j.anaerobe.2010.10.003 DOI: https://doi.org/10.1016/j.anaerobe.2010.10.003

Wang, Y., Li, A., Jiang, X., Zhang, H., Mehmood, K., Zhang, L., Jiang, J., Waqas, M., Iqbal, M., & Li, J. (2018). Probiotic potential of Leuconostoc pseudomesenteroides and Lactobacillus strains isolated from yaks. Frontiers in Microbiology, 9, 2987, 1-10. doi: 10.3389/fmicb.2018.02987 DOI: https://doi.org/10.3389/fmicb.2018.02987

Wang, Y., & Quian, P. Y. (2009. Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PloS One, 4(10), 1-9. doi: 10.1371/journal.pone.0007401 DOI: https://doi.org/10.1371/journal.pone.0007401

Xu, T., Zhou, T., Tang, H., Li, X., Chen, Y., Zhang, L., & Zhang, J. (2020). Probiotic potential and amylolytic properties of lactic acid bacteria isolated from Chinese fermented cereal foods. Food Control, 111(6), 107057. doi: 10.1016/j.foodcont.2019.107057 DOI: https://doi.org/10.1016/j.foodcont.2019.107057

Yong, L., Yong, Z., Yan, B., & Heping, Z. (2010). Study on cell surface properties and inhibitory effects on pathogens of four probiotic strains. Journal of Chinese Institute of Food Science and Technology, 10(5), 28-34.

Zhang, W., Liu, M., & Dai, X. (2013). Biological characteristics and probiotic effect of Leuconostoc lactis strain isolated from the intestine of black porgy fish. Brazilian Journal of Microbiology, 44(3), 685-691. doi: 10.1590/S1517-83822013005000053 DOI: https://doi.org/10.1590/S1517-83822013005000053

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2024-09-04

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Farinazzo , F. S., Fernandes, M. T. C., Mauro, C. S. I., Moraes Filho, M. L. de, Bach, F., & Garcia, S. (2024). In Vitro evaluation of probiotic properties of lactic acid bacteria strains isolated from juçara fruit native to the Atlantic Forest. Semina: Ciências Agrárias, 45(5), 1443–1462. https://doi.org/10.5433/1679-0359.2024v45n5p1443

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