Effect of By-Product from C-Phycocyanin Extraction as a Prebiotic Properties and Probiotic Microbial Population https://doi.org/10.12982/VIS.2025.003

Main Article Content

Kannikar Hamprakorn
Buaream Maneewan
Wantamas Jantasin
Julakorn Panatuk

Abstract

 This study was designed to investigate the efficacy of alternative prebiotic supplements derived from phycocyanin extraction by-product in enhancing the growth of probiotic. These alternative prebiotic supplements included Spirulina platensis, the by-product of phycocyanin extraction, and inulin. The efficacy of alternative prebiotics was assessed using beneficial bacteria (Lactobacillus johnsonii ck-3 and ck-8), pathogenic bacteria (Staphylococcus aureus and Escherichia coli), and yeast (Saccharomyces cerevisiae). The alternative prebiotics source was used to analyse the chemical composition, prebiotic activity, and bacteria growth. It was demonstrated that the phycocyanin extraction by-product included a high concentration of crude protein (67.74% DM), carbohydrates (31.29% DM). The phycocyanin extraction by-product has a high content of glucose, fructose, and sucrose (63.55, 68.00, and 0.24 µg/ml, respectively). The phycocyanin extraction by-product has presented hydrolysis ability (in vitro) at 2.51% while S. platensis showed at 1.81 %. The composition of the phycocyanin extraction by-product showed similar activation of probiotic bacteria to inulin. Especially, Lactobacillus strain showed the best growth was achieved with the phycocyanin extraction by-product with decrease the final pH and high microbial colony number at 48 hours in 7.5–9.5 log10 colony-forming unit per milliliter (CFU/ml) when compared with the glucose group. The study results revealed that the phycocyanin extraction by-product with the prebiotic potential are effective at increasing numbers of Lactobacillus strain. Consequently, the study reveals that phycocyanin extraction by-product are effective as alternative prebiotic supplement, significantly enhancing beneficial probiotic bacteria. These findings suggest the potential use of phycocyanin extraction by-products in creating new prebiotic formulations for gut microbiota modulation through dietary

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How to Cite
Hamprakorn, K., Maneewan, B., Jantasin, W., & Panatuk, J. (2024). Effect of By-Product from C-Phycocyanin Extraction as a Prebiotic Properties and Probiotic Microbial Population: https://doi.org/10.12982/VIS.2025.003. Veterinary Integrative Sciences, 23(1), 1–16. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/266814
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Research Articles

References

Abd El‐Hack, M., Mahgoub, S., Alagawany, M., Ashour, E., 2017. Improving productive performance and mitigating harmful emissions from laying hen excreta via feeding on graded levels of corn DDGS with or without Bacillus subtilis probiotic. J. Anim. Physiol. Anim. Nutr. 101(5), 904-913.

Abdel-Latif, H.M., El-Ashram, S., Yilmaz, S., Naiel, M.A., Kari, Z.A., Hamid, N.K.A., Dawood, M.A., Nowosad, J., Kucharczyk, D., 2022. The effectiveness of Arthrospira platensis and microalgae in relieving stressful conditions affecting finfish and shellfish species: An overview. Aquac. Rep. 24, 101135.

Ak, B., Avsaroglu, E., Isik, O., Özyurt, G., Kafkas, E., Etyemez, M., 2016. Nutritional and physicochemical characteristics of bread enriched with microalgae Spirulina platensis. Int. J. Eng. Res. Appl. 6(12), 30-38.

Al-Khalaifah, H., 2018. Benefits of probiotics and/or prebiotics for antibioticreduced poultry. Poul. Sci. 97(11), 3807-3815.

Alagawany, M., Abd El-Hack, M.E., Farag, M.R., Sachan, S., Karthik, K., Dhama,K., 2018. The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environ. Sci. Pollut. Res. 25, 10611-10618.

Alwaleed, E.A., El-Sheekh, M., Abdel-Daim, M.M., Saber, H., 2021. Effects of Spirulina platensis and Amphora coffeaeformis as dietary supplements on blood biochemical parameters, intestinal microbial population, and productive performance in broiler chickens. Environ. Sci. Pollut. Res. 28, 1801-1811.

Ashraf, R., Shah, N.P., 2014. Immune system stimulation by probiotic microorganisms. Crit. Rev. Food Sci. Nutr. 54(7), 938-956.

Ashwini, A., Ramya, H., Ramkumar, C., Reddy, K.R., Kulkarni, R.V., Abinaya, V.,Naveen, S., Raghu, A.V., 2019. Reactive mechanism and the applications of bioactive prebiotics for human health. J. Microbiol. Methods. 159, 128-137.

Awad, W., Ghareeb, K., Böhm, J., 2008. Intestinal structure and function of broiler chickens on diets supplemented with a synbiotic containing Enterococcus faecium and oligosaccharides. Int. J. Mol. Sci. 9(11), 2205-2216.

Bai, K., Huang, Q., Zhang, J., He, J., Zhang, L., Wang, T., 2017. Supplemental effects of probiotic Bacillus subtilis fmbJ on growth performance, antioxidant capacity, and meat quality of broiler chickens. Poul. Sci. 96(1), 74-82.

Bamigbade, G.B., Subhash, A.J., Kamal-Eldin, A., Nyström, L., Ayyash, M., 2022. An updated review on prebiotics: insights on potentials of food seeds waste as source of potential prebiotics. Molecules 27(18), 5947.

Bintsis, T., 2018. Lactic acid bacteria as starter cultures: an update in their metabolism and genetics. AIMS Microbiol. 4(4), 665.

Bodke, H., Jogdand, S., Jogdand, S.D., 2022. Role of probiotics in human health. Cureus. 14(11).

Bohn, T., 2014. Dietary factors affecting polyphenol bioavailability. Nutr. Rev. 72(7),429-452.

Bolla, P.A., Carasi, P., de los Angeles Bolla, M., De Antoni, G.L., de los Angeles Serradell, M., 2013. Protective effect of a mixture of kefir-isolated lactic acid bacteria and yeasts in a hamster model of Clostridium difficile infection. Anaerobe. 21, 28-33.

Castellano, P., Pérez Ibarreche, M., Blanco Massani, M., Fontana, C., Vignolo, G.M., 2017. Strategies for pathogen biocontrol using lactic acid bacteria and their metabolites: a focus on meat ecosystems and industrial environments. Microorganisms. 5(3), 38.

Cotas, J., Leandro, A., Pacheco, D., Gonçalves, A.M., Pereira, L., 2020. A comprehensive review of the nutraceutical and therapeutic applications of red seaweeds (Rhodophyta). Life. 10(3), 19.

de Morais, M.G., da Fontoura Prates, D., Moreira, J.B., Duarte, J.H., Costa, J.A.V., 2018. Phycocyanin from microalgae: properties, extraction and purification, with some recent applications. Ind. Biotechnol. 14(1), 30-37.

Dev, A., Mohanbhai, S.J., Kushwaha, A.C., Sood, A., Sardoiwala, M.N., Choudhury, S.R., Karmakar, S., 2020. κ-carrageenan-C-phycocyanin based smart injectable hydrogels for accelerated wound recovery and real-time monitoring. Acta Biomater. 109, 121-131.

Devi, M., Rebecca, L.J., Sumathy, S., 2013. Bactericidal activity of the lactic acid bacteria Lactobacillus delbreukii. J. Chem. Pharm. Res. 5(2), 176-180.

Di Gioia, D., Mazzola, G., Nikodinoska, I., Aloisio, I., Langerholc, T., Rossi, M., Raimondi, S., Melero, B., Rovira, J., 2016. Lactic acid bacteria as protective cultures in fermented pork meat to prevent Clostridium spp. growth. Int. J.Food. Microbiol. 235, 53-59.

Ding, S., Wang, Y., Yan, W., Li, A., Jiang, H., Fang, J., 2019. Effects of Lactobacillus plantarum 15-1 and fructooligosaccharides on the response of broilers to pathogenic Escherichia coli O78 challenge. PLoS One. 14(6), e0212079.

Fitriyah, N.S., Oluodo, L.A., Hnokaew, P., Umsook, S., Thirawong, P., Khamlor, T., Yammuen-Art, S., 2024. Optimum Level of Lactobacillus plantarum Supplementation as Probiotic on In Vitro Digestibility and Rumen Fermentation Products in Thai Native Cattle. Vet. Integr. Sci. 22(2), 489-500.

Giorgino, A., Raspa, F., Valle, E., Bergero, D., Cavallini, D., Gariglio, M., Bongiorno, V., Bussone, G., Bergagna, S., Cimino, F., 2023. Effect of dietary organic acids and botanicals on metabolic status and milk parameters in mid–late lactating goats. Animals. 13(5), 797.

Goering, H.K., Van Soest, P.J., 1970. Forage fiber analyses (apparatus, reagents, procedures, and some applications). US Agricultural Research Service, Washington DC.

Gomez, B., Gullon, B., Remoroza, C., Schols, H.A., Parajo, J.C., Alonso, J.L., 2014. Purification, characterization, and prebiotic properties of pectic oligosaccharides from orange peel wastes. J. Agric. Food. Chem. 62(40),9769-9782.

Guo, W., Zeng, M., Zhu, S., Li, S., Qian, Y., Wu, H., 2022. Phycocyanin ameliorates mouse colitis via phycocyanobilin-dependent antioxidant and antiinflammatory protection of the intestinal epithelial barrier. Food. Funct. 13(6),3294-3307.

Gupta, S., Gupta, C., Garg, A., Prakash, D., 2017. Prebiotic efficiency of blue green algae on probiotics microorganisms. J. Microbiol. Exp. 4(4), 4-7.

Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B., Morelli, L.,Canani, R.B., Flint, H.J., Salminen, S., 2014. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev.Gastroenterol. Hepatol. 11(8), 506-514.

Huebner, J., Wehling, R., Hutkins, R., 2007. Functional activity of commercial prebiotics. Int. Dairy J. 17(7), 770-775.

Khan, S., Mobashar, M., Mahsood, F.K., Javaid, S., Abdel-Wareth, A.,Ammanullah, H., Mahmood, A., 2020. Spirulina inclusion levels in a broiler ration: evaluation of growth performance, gut integrity, and immunity. Trop.Anim. Health. Prod. 52, 3233-3240.

Kumar, S., Sahoo, D., 2017. A comprehensive analysis of alginate content and biochemical composition of leftover pulp from brown seaweed Sargassum wightii. Algal. Res. 23, 233-239.

La Ragione, R., Narbad, A., Gasson, M., Woodward, M.J., 2004. In vivo characterization of Lactobacillus johnsonii FI9785 for use as a defined competitive exclusion agent against bacterial pathogens in poultry. Lett. Appl.Microbiol. 38(3), 197-205.

Lin, X.B., Lohans, C.T., Duar, R., Zheng, J., Vederas, J.C., Walter, J., Gänzle, M.,2015. Genetic determinants of reutericyclin biosynthesis in Lactobacillus reuteri. Appl. Environ. Microbiol. 81(6), 2032-2041.

Liu, R., Qin, S., Li, W., 2022. Phycocyanin: Anti-inflammatory effect and mechanism. Biomed. Pharmacother. 153, 113362.

Lynch, K.M., Steffen, E.J., Arendt, E.K., 2016. Brewers' spent grain: a review with an emphasis on food and health. J. Inst. Brew. 122(4), 553-568.

Manning, T.S., Gibson, G.R., 2004. Prebiotics. Best Pract. Res. Clin. Gastroenterol.18(2), 287-298.

Mappley, L.J., Tchórzewska, M.A., Nunez, A., Woodward, M.J., Bramley, P.M., La Ragione, R.M., 2013. Oral treatment of chickens with Lactobacillus reuteri LM1 reduces Brachyspira pilosicoli-induced pathology. J. Med. Microbiol.62(2), 287-296.

Markowiak, P., Śliżewska, K., 2018. The role of probiotics, prebiotics and synbiotics in animal nutrition. Gut. Pathog. 10(1), 1-20.

McCarty, M.F., DiNicolantonio, J.J., 2020. Nutraceuticals have potential for boosting the type 1 interferon response to RNA viruses including influenza and coronavirus. Prog. Cardiovasc. Dis. 63(3), 383.

Miller, G.L., 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31(3), 426-428.

Mohanty, D., Misra, S., Mohapatra, S., Sahu, P.S., 2018. Prebiotics and synbiotics: recent concepts in nutrition. Food. Biosci. 26, 152-160.

Moniz, P., Ho, A.L., Duarte, L.C., Kolida, S., Rastall, R.A., Pereira, H., Carvalheiro, F., 2016. Assessment of the bifidogenic effect of substituted xylooligosaccharides obtained from corn straw. Carbohydr. Polym. 136, 466-473.

Pagels, F., Guedes, A.C., Amaro, H.M., Kijjoa, A., Vasconcelos, V., 2019. Phycobiliproteins from cyanobacteria: chemistry and biotechnological applications. Biotechnol. Adv. 37(3), 422-443.

Pagels, F., Vasconcelos, V., Guedes, A.C., 2021. Carotenoids from cyanobacteria: Biotechnological potential and optimization strategies. Biomol. 11(5), 735.

Park, J., Lee, S., Kim, I., 2018. Effect of dietary Spirulina (Arthrospira) platensis on the growth performance, antioxidant enzyme activity, nutrient digestibility,cecal microflora, excreta noxious gas emission, and breast meat quality of broiler chickens. Poul. Sci. 97(7), 2451-2459.

Pattananandecha, T., Sirilun, S., Sivamaruthi, B., Suwannalert, P., Peerajan, S.,Chaiyasut, C., 2015. Hydrolyzed inulin with different degree of polymerization as prebiotic for Lactobacillus plantarum. J. Pure. Appl. Microbiol. 9(2), 973-979.

Piyadeatsoontorn, S., Sornplang, P., Chuachan, U., Puyati, B., 2018. Effect of lactobacilli probiotics supplementation on intestinal bacteria and growth performance in weaned pigs. Vet. Integ. Sci. 16(3), 211-221.

Pridmore, R.D., Pittet, A.C., Praplan, F., Cavadini, C., 2008. Hydrogen peroxide production by Lactobacillus johnsonii NCC 533 and its role in anti-Salmonella activity. FEMS Microbiol. Lett. 283(2), 210-215.

Raj, T.K., Ranjithkumar, R., Kanthesh, B., Gopenath, T., 2020. C-Phycocyanin of Spirulina platensis inhibits NSP12 required for replication of SARS-COV-2: a novel finding in silico. Int. J. Pharm. Sci. Res. 11(9), 271-278.

Richmond, A., 2013. Biological principles of mass cultivation of photoautotrophic microalgae. Handbook of microalgal culture: applied phycology and biotechnology, 169-204.

Rubel, I.A., Pérez, E.E., Genovese, D.B., Manrique, G.D., 2014. In vitro prebiotic activity of inulin-rich carbohydrates extracted from Jerusalem artichoke (Helianthus tuberosus L.) tubers at different storage times by Lactobacillus paracasei. Food. Res. Int. 62, 59-65.

Sabo, S.d.S., Mendes, M.A., Araujo, E.d.S., Muradian, L.B.d.A., Makiyama, E.N.,LeBlanc, J.G., Borelli, P., Fock, R.A., Knöbl, T., Oliveira, R.P.d.S., 2020.

Bioprospecting of probiotics with antimicrobial activities against Salmonella Heidelberg and that produce B-complex vitamins as potential supplements in poultry nutrition. Sci. Rep. 10(1), 7235.

Samanta, A., Jayapal, N., Jayaram, C., Roy, S., Kolte, A., Senani, S., Sridhar, M., 2015. Xylooligosaccharides as prebiotics from agricultural by-products: production and applications. Bioact. Carbohydr. Diet. Fibre. 5(1), 62-71.

Sánchez, B., Delgado, S., Blanco‐Míguez, A., Lourenço, A., Gueimonde, M.,Margolles, A., 2017. Probiotics, gut microbiota, and their influence on host health and disease. Mol. Nutr. Food Res. 61(1), 1600240.

Saura-Calixto, F., García-Alonso, A., Goni, I., Bravo, L., 2000. In vitro determination of the indigestible fraction in foods: an alternative to dietary fiber analysis. J.Agric. Food Chem. 48(8), 3342-3347.

Seal, B.S., Lillehoj, H.S., Donovan, D.M., Gay, C.G., 2013. Alternatives to antibiotics: a symposium on the challenges and solutions for animal production. Anim. Health. Res. Rev. 14(1), 78-87.

Seghiri, R., Kharbach, M., Essamri, A., 2019. Functional composition, nutritional properties, and biological activities of Moroccan Spirulina microalga. J. Food.Qual. 2019.

Silveira, S.T., Burkert, J.d.M., Costa, J.A.V., Burkert, C.A.V., Kalil, S.J., 2007.Optimization of phycocyanin extraction from Spirulina platensis using factorial design. Bioresour. Technol. 98(8), 1629-1634.

Stanic-Vucinic, D., Minic, S., Nikolic, M.R., Velickovic, T.C., 2018. Spirulina phycobiliproteins as food components and complements. Microalgal.Biotechnol., 129-149.

Taylor, S.R., Ramsamooj, S., Liang, R.J., Katti, A., Pozovskiy, R., Vasan, N.,Hwang, S.-K., Nahiyaan, N., Francoeur, N.J., Schatoff, E.M., 2021. Dietary fructose improves intestinal cell survival and nutrient absorption. Nature. 597(7875), 263-267.

Travers, M.A., Sow, C., Zirah, S., Deregnaucourt, C., Chaouch, S., Queiroz, R.M., Charneau, S., Allain, T., Florent, I., Grellier, P., 2016. Deconjugated bile salts produced by extracellular bile-salt hydrolase-like activities from the probiotic Lactobacillus johnsonii La1 inhibit Giardia duodenalis in vitro growth. Front.Microbiol. 7, 1453.

Truong, T.T., Tran, H.L., Nguyen, N.K., Nguyen, T.T., 2024. Effects of the fermented soya waste supplementation with various probiotic sources on growth performance of crossbred rabbits. Vet. Integ. Sci. 22(3), 787-803.

Verma, P., Kumar, M., Mishra, G., Sahoo, D., 2017. Multivariate analysis of fatty acid and biochemical constitutes of seaweeds to characterize their potential as bioresource for biofuel and fine chemicals. Bioresour. Technol. 226, 132-144.

Wang, T., Teng, K., Liu, G., Liu, Y., Zhang, J., Zhang, X., Zhang, M., Tao, Y., Zhong, J., 2018a. Lactobacillus reuteri HCM2 protects mice against Enterotoxigenic Escherichia coli through modulation of gut microbiota. Sci. Rep. 8(1), 17485.

Wang, Y., Li, A., Jiang, X., Zhang, H., Mehmood, K., Zhang, L., Jiang, J., Waqas,M., Iqbal, M., Li, J., 2018b. Probiotic potential of Leuconostoc pseudomesenteroides and Lactobacillus strains isolated from yaks. Front. Microbiol. 9, 2987.

Wongputtisin, P., Khanongnuch, C., Kongbuntad, W., Niamsup, P., Lumyong, S., Sarkar, P., 2014. Use of Bacillus subtilis isolates from Tua‐nao towards nutritional improvement of soya bean hull for monogastric feed application.Lett. Appl. Microbiol. 59(3), 328-333.

Yousefi, B., Eslami, M., Ghasemian, A., Kokhaei, P., Salek Farrokhi, A., Darabi, N.,2019. Probiotics importance and their immunomodulatory properties. J. Cell.Physiol. 234(6), 8008-8018.

Zhang, D., Li, R., Li, J., 2012. Lactobacillus reuteri ATCC 55730 and L22 display probiotic potential in vitro and protect against Salmonella-induced pullorum disease in a chick model of infection. Res. Vet. Sci. 93(1), 366-373.

Zhang, S., Hu, H., Wang, L., Liu, F., Pan, S., 2018. Preparation and prebiotic potential of pectin oligosaccharides obtained from citrus peel pectin. Food.Chem. 244, 232-237.

Zou, Y.J., Xu, J.J., Wang, X., Zhu, Y.H., Wu, Q., Wang, J.F., 2020. Lactobacillus johnsonii l531 ameliorates Escherichia coli-induced cell damage via inhibiting NLRP3 inflammasome activity and promoting ATG5/ATG16L1-mediated autophagy in porcine mammary epithelial cells. Vet. Sci. 7(3), 112.