Abstract
Probiotic-containing foods are among the most appreciated functional foods; however, probiotic-based dairy products cannot be consumed by people who are lactose intolerant, allergic to milk, or vegetarian or vegan individuals. Thus, new non-dairy matrices have been tested for probiotics delivery. This study evaluated the growth and viability of Limosilactobacillus fermentum ATCC 23271 and Lacticaseibacillus rhamnosus ATCC 9595 in Pitanga juice (Eugenia uniflora L.). The effects of the fermentation on the antioxidant and anti-infective properties of the juice were also analyzed. The E. uniflora juice allowed lactobacilli growth without supplementation, reaching rates around 8.4 Log CFU/mL and producing organic acids (pH values < 4) after 72 h of fermentation. The strain remained viable after 35 days of refrigerated storage. Fermentation by these bacteria increases the antioxidant capacity of the juice. The central composite rotational design was employed to evaluate the effects of bacterial inoculum and pulp concentration on growth and organic acids production by L. fermentum ATCC 23271. The strain was viable and produced organic acids in all tested combinations. L. fermentum-fermented juice and its cell-free supernatant significantly increased the survival of Tenebrio molitor larvae infected by enteroaggregative Escherichia coli 042. The results obtained in this study provide more insights into the potential of Pitanga juice to develop a functional non-dairy probiotic beverage with antioxidant and anti-infective properties.
Data availability
Data are available upon request.
References
Ballini A, Charitos IA, Cantore S, Topi S, Bottalico L, Santacroce L (2023) About Functional Foods: The Probiotics and Prebiotics State of Art. Antibiotics 12:. https://doi.org/10.3390/ANTIBIOTICS12040635
Liu Y, Wang J, Wu C (2022) Modulation of Gut Microbiota and Immune System by Probiotics, Pre-biotics, and post-biotics. Front Nutr 8. https://doi.org/10.3389/FNUT.2021.634897
Gao J, Li X, Zhang G, Sadiq FA, Simal-Gandara J, Xiao J, Sang Y (2021) Probiotics in the dairy industry-advances and opportunities. Compr Rev Food Sci Food Saf 20:3937–3982. https://doi.org/10.1111/1541-4337.12755
Khan FF, Sohail A, Ghazanfar S, Ahmad A, Riaz A, Abbasi KS, Ibrahim MS, Uzair M, Arshad M (2023) Recent innovations in non-dairy prebiotics and probiotics: physiological potential, applications, and characterization. Probiotics Antimicrob Proteins 15. https://doi.org/10.1007/S12602-022-09983-9
Mojikon FD, Kasimin ME, Molujin AM, Gansau JA, Jawan R (2022) Probiotication of Nutritious Fruit and Vegetable juices: an alternative to dairy-based Probiotic Functional products. Nutrients 14. https://doi.org/10.3390/NU14173457
Josino Soares D, Walker J, Pignitter M, Walker JM, Imboeck JM, Ehrnhoefer-Ressler MM, Montenegro Brasil I, Somoza V (2014) Pitanga (Eugenia uniflora L.) fruit juice and two major constituents thereof exhibit anti-inflammatory properties in human gingival and oral gum epithelial cells. Food Funct 5:2981–2988. https://doi.org/10.1039/C4FO00509K
Tambara AL, de Los Santos Moraes L, Dal Forno AH, Boldori JR, Gonçalves Soares AT, de Freitas Rodrigues C, Mariutti LRB, Mercadante AZ, de Ávila DS, Denardin CC (2018) Purple pitanga fruit (Eugenia uniflora L.) protects against oxidative stress and increase the lifespan in Caenorhabditis elegans via the DAF-16/FOXO pathway. Food Chem Toxicol 120:639–650. https://doi.org/10.1016/j.fct.2018.07.057
Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9
Santos CI, Campos CDL, Nunes-Neto WR, Do Carmo MS, Nogueira FAB, Ferreira RM, Costa EPS, Gonzaga LF, Araújo JMM, Monteiro JM, Monteiro CRAV, Platner FS, Figueiredo IFS, Holanda RA, Monteiro SG, Fernandes ES, Monteiro AS, Monteiro-Neto V (2021) Genomic Analysis of Limosilactobacillus fermentum ATCC 23271, a potential probiotic strain with Anti- Candida Activity. J fungi 7. https://doi.org/10.3390/JOF7100794
Ribeiro FC, de Barros PP, Rossoni RD, Junqueira JC, Jorge AOC (2017) Lactobacillus rhamnosus inhibits Candida albicans virulence factors in vitro and modulates immune system in Galleria mellonella. J Appl Microbiol 122:201–211. https://doi.org/10.1111/JAM.13324
Mendes YC, Mesquita GP, Costa GDE, Barbosa da Silva AC, Gouveia E, Silva MRC, Monteiro-Neto V, de Miranda R, de CM LC, Zagmignan A (2021) Evaluation of growth, viability, lactic acid production and anti-infective effects of lacticaseibacillus rhamnosus atcc 9595 in bacuri juice (Platonia insignis). Foods 10:. https://doi.org/10.3390/foods10030603
Zagmignan A, Mendes YC, Mesquita GP, Santos GDC, dos, Silva L, dos Souza Sales S, Castelo Branco AC, Junior SJ, Bazán ARC, Alves JMN, Almeida ER, de Santos BL (2023) AKM, Firmo W da CA, Silva MRC, Cantanhede Filho AJ, Miranda R de CM de, Silva LCN da Short-Term Intake of Theobroma grandiflorum Juice Fermented with Lacticaseibacillus rhamnosus ATCC 9595 Amended the Outcome of Endotoxemia Induced by Lipopolysaccharide. Nutrients 15:. https://doi.org/10.3390/NU15041059
Sengun IY, Kirmizigul A, Atlama K, Yilmaz B (2020) The viability of Lactobacillus rhamnosus in orange juice fortified with nettle (Urtica dioica L.) and bioactive properties of the juice during storage. LWT 118:108707. https://doi.org/10.1016/J.LWT.2019.108707
Güney D, Güngörmüşler M (2021) Development and comparative evaluation of a Novel Fermented Juice mixture with probiotic strains of lactic acid Bacteria and Bifidobacteria. Probiotics Antimicrob Proteins 13:495–505. https://doi.org/10.1007/S12602-020-09710-2/TABLES/4
Silva TF, Filho JRNC, Fonsêca MMLB, Dos Santos NM, da Silva ACB, Zagmignan A, Abreu AG, da Silva APS, Lima VL, de Silva M, Dutra NH, da Silva LM, Correia MV, da Silva MTDS (2020) LCN Products derived from Buchenavia tetraphylla leaves have in vitro antioxidant activity and protect Tenebrio molitor larvae against Escherichia coli-induced injury. Pharmaceuticals 13:. https://doi.org/10.3390/ph13030046
Bezerra Filho CM, da Silva LCN, da Silva MV, Løbner-Olesen A, Struve C, Krogfelt KA, Correia MT dos, Vilela Oliva S (2020) ML Antimicrobial and Antivirulence Action of Eugenia brejoensis Essential Oil in vitro and in vivo Invertebrate Models. Front Microbiol 11:506073. https://doi.org/10.3389/FMICB.2020.00424/BIBTEX
Nzeagwu O, Onimawo I (2010) Nutrient composition and sensory properties of juice made from pitanga cherry (Eugenia uniflora L.) fruits. Afr J Food Agric Nutr Dev 10. https://doi.org/10.4314/AJFAND.V10I4.55331
Amoo I, Adebayo O, Oyeleye A (2006) Chemical evaluation of winged beans (Psophocarpus Tetragonolobus), Pitanga cherries (Eugenia uniflora) and orchid fruit (Orchid fruit myristica). Afr J Food Agric Nutr Dev 6. https://doi.org/10.4314/AJFAND.V6I2.71734
Carmo MS, Noronha FMF, Arruda MO, da Silva Costa ÊP, Bomfim MRQ, Monteiro AS, Ferro TAF, Fernandes ES, Girón JA, Monteiro-Neto V (2016) Lactobacillus fermentum ATCC 23271 displays in vitro inhibitory activities against Candida Spp. Front Microbiol 7. https://doi.org/10.3389/FMICB.2016.01722
Fonteles TV, Costa MGM, de Jesus ALT, Rodrigues S (2012) Optimization of the fermentation of Cantaloupe Juice by Lactobacillus casei NRRL B-442. Food Bioproc Tech 5:2819–2826. https://doi.org/10.1007/s11947-011-0600-0
Nguyen BT, Bujna E, Fekete N, Tran ATM (2019) Probiotic Beverage from Pineapple Juice Fermented with Lactobacillus and Bifidobacterium strains. 6:1–7. https://doi.org/10.3389/fnut.2019.00054
Mantzourani I, Terpou A, Bekatorou A, Alexopoulos A, Kimbaris A, Koutinas AA, Plessas S (2019) Functional pomegranate beverage production by fermentation with a novel synbiotic L. Paracasei biocatalyst. Food Chem 125658. https://doi.org/10.1016/j.foodchem.2019.125658
Plamada D, Vodnar DC (2021) Polyphenols—gut microbiota interrelationship: a transition to a New Generation of Prebiotics. Nutrients 14:137. https://doi.org/10.3390/NU14010137
de Freitas PL, Barros MVC, Fróes RBL, França LM, de Paes AM A (2023) Prebiotic effects of plant-derived (poly)phenols on host metabolism: is there a role for short-chain fatty acids? Crit Rev Food Sci Nutr 63:12285–12293. https://doi.org/10.1080/10408398.2022.2100315
Migues I, Baenas N, Gironés-Vilaplana A, Cesio MV, Heinzen H, Moreno DA (2018) Phenolic profiling and antioxidant capacity of Eugenia uniflora L. (Pitanga) samples collected in different Uruguayan locations. Foods 7. https://doi.org/10.3390/foods7050067
Bagetti M, Facco EMP, Piccolo J, Hirsch GE, Rodriguez-Amaya D, Kobori CN, Vizzotto M, Emanuelli T (2011) Physicochemical characterization and antioxidant capacity of pitanga fruits (Eugenia uniflora L). Food Sci Technol 31:147–154. https://doi.org/10.1590/S0101-20612011000100021
Melini F, Melini V, Luziatelli F, Ficca AG, Ruzzi M (2019) Health-promoting components in fermented foods: an up-to-date systematic review. Nutrients 11
Mantzourani I, Nouska C, Terpou A, Alexopoulos A, Bezirtzoglou E, Panayiotidis MI, Galanis A, Plessas S (2018) Production of a novel functional fruit beverage consisting of cornelian cherry juice and probiotic bacteria. Antioxidants 7. https://doi.org/10.3390/antiox7110163
Acknowledgements
The authors would like to thank the staff of LACEN-MA.
Funding
This work was funded by Fundação de Amparo à Pesquisa e Desenvolvimento Científico do Maranhão (Processes numbers: POS-GRAD-02460/21, INFRA-02032/21; ACT 05691/21 FAPEMA/CAPES), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grant number: 312349/2020-3).
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Gabrielle Damasceno Costa dos Santos: Conceptualization, Methodology, Investigation, Writing-Original draft preparation; Carlos Drielson da Silva Pereira: Writing-Original draft preparation; Camila Caetano da Silva: Investigation; Marcos Andrade Silva: Investigation; Lucas dos Santos Silva: Investigation; Brenda da Silva Cutrim: Investigation; Simeone Júlio dos Santos Castelo Branco: Investigation; Patrícia Maria Guedes Paiva: Supervision, Funding acquisition; Maria Tereza dos Santos Correia: Supervision, Funding acquisition; Rita de Cássia Mendonça de Miranda: Supervision, Investigation; Adrielle Zagmignan: Conceptualization, Supervision, Methodology, Funding acquisition; Luís Cláudio Nascimento de Silva: Conceptualization, Supervision, Methodology, Funding acquisition, Writing- Reviewing and Editing.
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Costa dos Santos, G.D., da Silva Pereira, C.D., da Silva, C.C. et al. Eugenia uniflora (pitanga) juice as a new alternative vehicle for Limosilactobacillus fermentum ATCC 23271: evaluation of antioxidant and anti-infective effects. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01329-7
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DOI: https://doi.org/10.1007/s42770-024-01329-7