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Effects of p-coumaric acid on probiotic properties of Lactobacillus acidophilus LA-5 and lacticaseibacillus rhamnosus GG

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Abstract

Probiotics are defined as “live microorganisms that provide health benefits to the host when administered in adequate amounts.” Probiotics have beneficial effects on human health, including antibacterial activity against intestinal pathogens, regulation of blood cholesterol levels, reduction of colitis and inflammation incidence, regulation of the immune system, and prevention of colon cancer. In addition to probiotic bacteria, some phenolic compounds found in foods we consume (both food and beverages) have positive effects on human health. p-coumaric acid (p-CA) is one of the most abundant phenolic compounds in nature and human diet. The interactions between these two different food components (phenolics and probiotics), resulting in more beneficial combinations called synbiotics, are not well understood in terms of how they will affect the gut microbiota by promoting the probiotic properties and growth of probiotic bacteria. Thus, this study aimed to investigate synbiotic relationship between p-CA and Lactobacillus acidophilus LA-5 (LA-5), Lacticaseibacillus rhamnosus GG (LGG). Probiotic bacteria were grown in the presence of p-CA at different concentrations, and the effects of p-CA on probiotic properties, as well as its in vitro effects on AChE and BChE activities, were investigated. Additionally, Surface analysis was conducted using FTIR. The results showed that treatment with p-CA at different concentrations did not exhibit any inhibitory effect on the growth kinetics of LA-5 and LGG probiotic bacteria. Additionally, both probiotic bacteria demonstrated high levels of antibacterial properties. It showed that it increased the auto-aggregation of both probiotics. While p-CA increased co-aggregation of LA-5 and LGG against Escherichia coli, it decreased co-aggregation against Staphylococcus aureus. Probiotics grown with p-CA were more resistant to pepsin. While p-CA increased the resistance of LA-5 to bile salt, it decreased the resistance of LGG. The combinations of bacteria and p-CA efficiently suppressed AChE and BChE with inhibition (%) 11.04–68.43 and 13.20-65.72, respectively. Furthermore, surface analysis was conducted using FTIR to investigate the interaction of p-coumaric acid with LA-5 and LGG, and changes in cell components on the bacterial surface were analyzed. The results, recorded in range of 4000 –600 cm-1 with resolution of 4 cm-1, demonstrated that p-CA significantly affected only the phosphate/CH ratio for both bacteria. These results indicate the addition of p-CA to the probiotic growth may enhance the probiotic properties of bacteria.

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References

  • Alara OR, Abdurahman NH, Ukaegbu CI (2021) Extraction of phenolic compounds: a review. Curr Res Food Sci 4:200–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Albuquerque BR, Heleno SA, Oliveira MBPP, Barros L, Ferreira ICFR (2021) Phenolic compounds: current industrial applications, limitations and future challenges. Food Funct 12(1):14–29

    Article  CAS  PubMed  Google Scholar 

  • Alcántara C, Blasco A, Zúñiga M, Monedero V (2014) Accumulation of polyphosphate in Lactobacillus spp. and its involvement in stress resistance. Appl Environ Microbiol 80(5):1650–1659

    Article  PubMed  PubMed Central  Google Scholar 

  • Alcántara C, Perez M, Huedo P, Altadill T, Espadaler-Mazo J, Arqués JL, Zúñiga M, Monedero V (2023) Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042. Sci Rep 13(1):11076

    Article  PubMed  PubMed Central  Google Scholar 

  • Alp D, Kuleaşan H, Korkut A, Altıntaş (2020) The importance of the S-layer on the adhesion and aggregation ability of lactic acid bacteria. Mol Biol Rep 47(5):3449–3457

    Article  CAS  PubMed  Google Scholar 

  • Bayrak C, Taslimi P, Kilinc N, Gulcin I, Menzek A (2023) Synthesis and Biological Activity of some bromophenols and their derivatives including Natural products. Chem Biodivers 20(8):e202300469

    Article  CAS  PubMed  Google Scholar 

  • Boo YC (2019) p-Coumaric acid as an active ingredient in cosmetics: a review focusing on its antimelanogenic effects. Antioxidants 8(8):275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandt AL, Castillo A, Harris KB, Keeton JT, Hardin MD, Taylor TM (2010) Inhibition of Listeria monocytogenes by food antimicrobials applied singly and in combination. J Food Sci 75(9):M557–M563

    Article  CAS  PubMed  Google Scholar 

  • Celebioglu HU (2021) Effects of potential synbiotic interaction between Lactobacillus rhamnosus GG and salicylic acid on human colon and prostate cancer cells. Arch Microbiol 203(3):1221–1229

    Article  CAS  PubMed  Google Scholar 

  • Celebioglu HU, Ejby M, Majumder A, Købler C, Goh YJ, Thorsen K, Schmidt B, O’Flaherty S, Abou Hachem M, Lahtinen SJ (2016) Differential proteome and cellular adhesion analyses of the probiotic bacterium Lactobacillus acidophilus NCFM grown on raffinose–an emerging prebiotic. Proteomics 16(9):1361–1375

    Article  CAS  PubMed  Google Scholar 

  • Celebioglu HU, Delsoglio M, Brix S, Pessione E, Svensson B (2018) Plant polyphenols stimulate adhesion to intestinal mucosa and induce proteome changes in the probiotic Lactobacillus acidophilus NCFM. Mol Nutr Food Res 62(4):1700638

    Article  Google Scholar 

  • Celebioglu HU, Erden Y, Ozel HB (2021) In vitro cytotoxic effects of lactobacilli grown with lime honey on human breast and colon cancer cells. Food Bioscience 41:101020

    Article  CAS  Google Scholar 

  • Chou L-S, Weimer B (1999) Isolation and characterization of acid-and bile-tolerant isolates from strains of Lactobacillus acidophilus. J Dairy Sci 82(1):23–31

    Article  CAS  PubMed  Google Scholar 

  • Correa Deza MA, Grillo-Puertas M, Salva S, Rapisarda VA, Gerez CL, de Font G (2017) Inorganic salts and intracellular polyphosphate inclusions play a role in the thermotolerance of the immunobiotic Lactobacillus rhamnosus CRL 1505. PLoS ONE 12(6):e0179242

    Article  PubMed  PubMed Central  Google Scholar 

  • Darveau RP, McFall-Ngai M, Ruby E, Miller S, Mangan DF (2003) Host Tissues may actively respond to beneficial microbes some bacteria are viewed as having a dynamic and positive, rather than passive and harmful, relationship with their hosts. ASM News-American Soc Microbiol 69(4):186–191

    Google Scholar 

  • Deepika G, Green RJ, Frazier RA, Charalampopoulos D (2009) Effect of growth time on the surface and adhesion properties of Lactobacillus rhamnosus GG. J Appl Microbiol 107(4):1230–1240

    Article  CAS  PubMed  Google Scholar 

  • Dehghani S, Edalatian Dovom MR, Yavarmanesh M, Sankian M (2022) In vitro evaluation of potential probiotic characteristics and survival of human and foodborne lactic acid Bacteria (lacticaseibacillus rhamnosus and lactiplantibacillus plantarum) in mice gastrointestinal tract. Appl Biochem Microbiol 58(Suppl 1):S91–S101

    Article  CAS  Google Scholar 

  • Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human–microbe mutualism and disease. Nature 449(7164):811–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deza MAC, de Olmos AR, Suárez NE, de Valdez GF, Salva S, Gerez CL (2021) Inorganic polyphosphate from the immunobiotic Lactobacillus rhamnosus CRL1505 prevents inflammatory response in the respiratory tract. Saudi J Biol Sci 28(10):5684–5692

    Article  Google Scholar 

  • Dlamini ZC, Langa RL, Aiyegoro OA, Okoh AI (2019) Safety evaluation and colonisation abilities of four lactic acid bacteria as future probiotics. Probiotics Antimicrob Proteins 11(2):397–402

    Article  CAS  PubMed  Google Scholar 

  • Dziuba B, Babuchowski A, Nałęcz D, Niklewicz M (2007) Identification of lactic acid bacteria using FTIR spectroscopy and cluster analysis. Int Dairy J 17(3):183–189

    Article  CAS  Google Scholar 

  • Ferreira PS, Victorelli FD, Fonseca-Santos B, Chorilli M (2019) A review of analytical methods for p-coumaric acid in plant-based products, beverages, and biological matrices. Crit Rev Anal Chem 49(1):21–31

    Article  CAS  PubMed  Google Scholar 

  • Fujiya M, Ueno N, Kashima S, Tanaka K, Sakatani A, Ando K, Moriichi K, Konishi H, Kamiyama N, Tasaki Y (2020) Long-chain polyphosphate is a potential Agent for Inducing Mucosal Healing of the Colon in Ulcerative Colitis. Clin Pharmacol Ther 107(2):452–461

    Article  CAS  PubMed  Google Scholar 

  • Gök Y, Taslimi P, Şen B, Bal S, Aktaş A, Aygün M, Sadeghi M, Gülçin İ (2023) Design, synthesis, characterization, crystal structure, in silico studies, and inhibitory properties of the PEPPSI type pd (II) NHC complexes bearing chloro/fluorobenzyl group. Bioorg Chem 135:106513

    Article  PubMed  Google Scholar 

  • Gorbach S, Doron S, Magro F (2017) Lactobacillus rhamnosus GG. The microbiota in gastrointestinal pathophysiology. Elsevier, pp 79–88

  • Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S (2014) Activity of cecropin P1 and FA-LL-37 against urogenital microflora. Nat Reviews Gastroenterol Hepatol 11(8):506

    Article  Google Scholar 

  • Holkem AT, Silva MPd, Favaro-Trindade CS (2022) Probiotics and plant extracts: a promising synergy and delivery systems. Crit Rev Food Sci Nutr : 1–19

  • Jang MG, Ko HC, Kim S-J (2020) Effects of p-coumaric acid on microRNA expression profiles in SNU-16 human gastric cancer cells. Genes Genomics 42:817–825

    Article  CAS  PubMed  Google Scholar 

  • Janicke B, Hegardt C, Krogh M, Önning G, Åkesson B, Cirenajwis HM, Oredsson SM (2011) The antiproliferative effect of dietary fiber phenolic compounds ferulic acid and p-coumaric acid on the cell cycle of Caco-2 cells. Nutr Cancer 63(4):611–622

    Article  CAS  PubMed  Google Scholar 

  • Karimov A, Taslimi P, Orujova A, Mammadova K, Kısa D, Farzaliyev V, Sujayev A, Sadeghian N, Taskin-Tok T, Alwasel S (2023) Design, synthesis, characterization and Biological activities of Novel S‐(Acyloxy) butyl‐N, N‐Diethyldithiocarbamate. Compd ChemistrySelect 8(18):e202300286

    Article  CAS  Google Scholar 

  • Kashima S, Fujiya M, Konishi H, Ueno N, Inaba Y, Moriichi K, Tanabe H, Ikuta K, Ohtake T, Kohgo Y (2015) Polyphosphate, an active molecule derived from probiotic Lactobacillus brevis, improves the fibrosis in murine colitis. Translational Res 166(2):163–175

    Article  CAS  Google Scholar 

  • Kiliç I, Yeşiloğlu Y (2013) Spectroscopic studies on the antioxidant activity of p-coumaric acid. Spectrochim Acta Part A Mol Biomol Spectrosc 115:719–724

    Article  Google Scholar 

  • Kısa D, Imamoglu R, Genc N, Taslimi P, Kaya Z, Taskin-Tok T (2023) HPLC analysis, Phytochemical Content, and Biological effects of Centaurea kilae against some metabolic enzymes: in Vitro and in Silico studies. ChemistrySelect 8(6):e202204196

    Article  Google Scholar 

  • Kos B, Šušković J, Vuković S, Šimpraga M, Frece J, Matošić S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94(6):981–987

    Article  CAS  PubMed  Google Scholar 

  • Latha S, Vinothini G, John Dickson Calvin D, Dhanasekaran D (2016) In vitro probiotic profile based selection of indigenous actinobacterial probiont Streptomyces sp. JD9 for enhanced broiler production. J Biosci Bioeng 121(1):124–131

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ, Mun GI, An SM, Boo YC (2009) Evidence for the association of peroxidases with the antioxidant effect of p-coumaric acid in endothelial cells exposed to high Glucose plus arachidonic acid. BMB Rep 42(9):561–567

  • Li J, Zhao N, Xu R, Li G, Dong H, Wang B, Li Z, Fan M, Wei X (2022) Deciphering the antibacterial activity and mechanism of p-coumaric acid against Alicyclobacillus acidoterrestris and its application in apple juice. Int J Food Microbiol 378:109822

    Article  CAS  PubMed  Google Scholar 

  • Lou Z, Wang H, Rao S, Sun J, Ma C, Li J (2012) p-Coumaric acid kills bacteria through dual damage mechanisms. Food Control 25(2):550–554

    Article  CAS  Google Scholar 

  • Luceri C, Giannini L, Lodovici M, Antonucci E, Abbate R, Masini E, Dolara P (2007) p-Coumaric acid, a common dietary phenol, inhibits platelet activity in vitro and in vivo. Br J Nutr 97(3):458–463

    Article  CAS  PubMed  Google Scholar 

  • Maquelin K, Kirschner C, Choo-Smith LP, van den Braak N, Endtz HP, Naumann D, Puppels GJ (2002) Identification of medically relevant microorganisms by vibrational spectroscopy. J Microbiol Methods 51(3):255–271

    Article  CAS  PubMed  Google Scholar 

  • Moal VL-L, Servin AL (2014) Anti-infective activities of Lactobacillus strains in the human intestinal microbiota: from Probiotics to gastrointestinal anti-infectious Biotherapeutic agents. Clin Microbiol Rev 27(2):167–199

    Article  Google Scholar 

  • Molska M, Reguła J (2019) Potential Mechanisms of Probiotics Action in the Prevention and Treatment of Colorectal Cancer. Nutrients 11(10):2453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monteagudo-Mera A, Rastall RA, Gibson GR, Charalampopoulos D, Chatzifragkou A (2019) Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl Microbiol Biotechnol 103(16):6463–6472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oak SJ, Jha R (2019) The effects of probiotics in lactose intolerance: a systematic review. Crit Rev Food Sci Nutr 59(11):1675–1683

    Article  CAS  PubMed  Google Scholar 

  • Osmanagaoglu O, Kiran F, Ataoglu H (2010) Evaluation of in vitro probiotic potential of Pediococcus pentosaceus OZF isolated from human breast milk. Probiotics Antimicrob Proteins 2(3):162–174

    Article  PubMed  Google Scholar 

  • Pei K, Ou J, Huang J, & Ou S (2016) p-Coumaric acid and its conjugates: dietary sources, pharmacokinetic properties and biological activities. J Sci Food Agric 96(9):2952–2962

  • Plessas S, Nouska C, Karapetsas A, Kazakos S, Alexopoulos A, Mantzourani I, Chondrou P, Fournomiti M, Galanis A, Bezirtzoglou E (2017) Isolation, characterization and evaluation of the probiotic potential of a novel Lactobacillus strain isolated from feta-type cheese. Food Chem 226:102–108

    Article  CAS  PubMed  Google Scholar 

  • Saiki A, Ishida Y, Segawa S, Hirota R, Nakamura T, Kuroda A, Bioscience (2016) Biotechnol Biochem 80(5): 955–961

    Article  CAS  Google Scholar 

  • Santivarangkna C, Wenning M, Foerst P, Kulozik U (2007) Damage of cell envelope of Lactobacillus helveticus during vacuum drying. J Appl Microbiol 102(3):748–756

    Article  CAS  PubMed  Google Scholar 

  • Shang F, Jiang X, Wang H, Chen S, Wang X, Liu Y, Guo S, Li D, Yu W, Zhao Z, Wang G (2020) The inhibitory effects of probiotics on colon cancer cells: in vitro and in vivo studies. J Gastrointest Oncol 11(6):1224–1232

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma R, Padwad Y (2020) Plant-polyphenols based second-generation synbiotics: emerging concepts, challenges, and opportunities. Nutrition 77:110785

    Article  CAS  PubMed  Google Scholar 

  • Sharma R, Padwad Y (2020b) Probiotic bacteria as modulators of cellular senescence: emerging concepts and opportunities. Gut Microbes 11(3):335–349

    Article  PubMed  Google Scholar 

  • Soni R, Jain NK, Shah V, Soni J, Suthar D, Gohel P (2020) Development of probiotic yogurt: effect of strain combination on nutritional, rheological, organoleptic and probiotic properties. J Food Sci Technol 57(6):2038–2050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Succi M, Tremonte P, Reale A, Sorrentino E, Grazia L, Pacifico S, Coppola R (2005) Bile salt and acid tolerance of Lactobacillus rhamnosus strains isolated from Parmigiano Reggiano cheese. FEMS Microbiol Lett 244(1):129–137

    Article  CAS  PubMed  Google Scholar 

  • Takauji S, Konishi H, Fujiya M, Ueno N, Tanaka H, Sato H, Isozaki S, Kashima S, Moriichi K, Mizukami Y, Okumura T (2021) Polyphosphate, derived from Lactobacillus brevis, modulates the intestinal microbiome and attenuates Acute Pancreatitis. Dig Dis Sci 66(11):3872–3884

    Article  CAS  PubMed  Google Scholar 

  • Tariq Riaz M, Taslimi P, Yaqub M, al-Rashida M, Alharthy RD, El-Gokha A, Shafiq Z (2023) Functionalized Diazabenzo[a]anthracenediones: Regioselective Multicomponent Synthesis and Biological and Computational studies as. Potential Cholinesterase Inhibitors ChemistrySelect 8(22):e202300648

    CAS  Google Scholar 

  • Tas A, Tüzün B, Khalilov AN, Taslimi P, Ağbektas T, Cakmak NK (2023) In vitro cytotoxic effects, in silico studies, some metabolic enzymes inhibition, and vibrational spectral analysis of novel β-amino alcohol compounds. J Mol Struct 1273:134282

    Article  CAS  Google Scholar 

  • Tokalı FS, Taslimi P, Tüzün B, Karakuş A, Sadeghian N, Gulçin İ (2023b) Synthesis of new carboxylates and sulfonates containing thiazolidin-4-one ring and evaluation of inhibitory properties against some metabolic enzymes. J Iran Chem Soc 20(10):2631–2642

    Article  Google Scholar 

  • Xu J, Gordon JI (2003) Honor thy symbionts. Proceedings of the National Academy of Sciences 100(18):10452–10459

  • Yakan H, Azam M, Kansız S, Muğlu H, Ergül M, Taslimi P, Koçyiğit ÜM, Karaman M, Al-Resayes SI, Min K (Jul 3, 2023) Isatin/thiosemicarbohydrazone hybrids: facile synthesis, and their evaluation as anti-proliferatıve agents and metabolıc enzyme inhibitors. Bull Chem Soc Ethiop 5(37):1221–1236

  • Yu C, Irudayaraj J (2005) Spectroscopic characterization of microorganisms by Fourier transform infrared microspectroscopy. Biopolymers 77(6):368–377

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge Chr. Hansen, Turkey for the probiotic strains. This study was supported by The Scientific and Technological Research Council of Türkiye, TUBITAK (2209-A, 1919B012001002).

Funding

This study was supported by The Scientific and Technological Research Council of Türkiye, TUBITAK (2209-A, 1919B012001002).

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Authors and Affiliations

  1. Department of Biotechnology, Faculty of Science, Bartin University, Bartin, Turkey

    Buse Nur Derebasi, Sena Davran Bulut, Nastaran Sadeghian, Parham Taslimi & Hasan Ufuk Celebioglu

  2. Central Research Laboratory Application and Research Center, Bartin University, Bartin, Turkey

    Busra Aksoy Erden

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  1. Buse Nur Derebasi
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  2. Sena Davran Bulut
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  4. Nastaran Sadeghian
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  6. Hasan Ufuk Celebioglu
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Contributions

Conceptualisation, H.U.C.,B.N.D.; Methodology, H.U.C., B.N.D., S.D.B., B.A.E., N.S.; Writing-Original draft preparation, H.U.C.,S.D.B., B.A.E., P.T.; Writing-review and editing, H.U.C., S.D.B. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Hasan Ufuk Celebioglu.

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Communicated by Christopher Franco.

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Derebasi, B.N., Davran Bulut, S., Aksoy Erden, B. et al. Effects of p-coumaric acid on probiotic properties of Lactobacillus acidophilus LA-5 and lacticaseibacillus rhamnosus GG. Arch Microbiol 206, 223 (2024). https://doi.org/10.1007/s00203-024-03957-x

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