Bifidobacterium from infant stool: the diversity and potential screening
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Abstract. Kusharyati DF, Pramono H, Ryandini D, Manshur TA, Dewi MA, Khatimah K, Rovik A. 2020. Bifidobacterium from infant stool: the diversity and potential screening. Biodiversitas 21: 2506-2513. Bifidobacteria spp. are a group of Lactic Acid Bacteria commonly found in the gastrointestinal tract of adults and infants. LAB are known as probiotics and have many health benefits. This research aimed to isolate Bifidobacteria from infant stool, identify, explore their diversity, and screen their potential as probiotics. Stool samples were collected from 3 healthy infants in Banyumas Regency. The potential screening included lysozyme resistance, antimicrobial activity, and exopolysaccharide production. A total of 7 Bifidobacterium species were isolated from infant stool: B. catenulatum, B. minimum, B. indicum, B. dentium, B. asteroides, B. galicum, and B. coerinum. B. indicum isolates (Bb3F and Bb1B) had the greatest inhibition activity against Escherichia coli and Candida albicans with 10.80 and 9.70 mm, respectively. Bifidobacteria isolates were resistant to lysozyme from egg whites up to 200 µg.mL-1. B. catenulatum Bb1A isolate had the highest yield of exopolysaccharide production with 74 mg.L-1. Among them, three Bifidobacterium strains (Bb1B, Bb2A, and Bb2E) were considered potentially as probiotics.
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References
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Biasucci G, Benenati B, Morelli L, Boehm G. 2008. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J. Nutr., 138 (9): 1796-1800.
Biavati B, Vescovo M, Torriani S, Bottazzi V. 2000. Bifidobacteria: history, ecology, physiology and applications. Ann. Microbiol., 50: 117-131.
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Cizeikiene D, Juodeikiene G, Paskevicius A, Bartkiene E. 2013. Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganisms isolated from food and their control in wheat bread. Food Control, 31: 539–545.
Degeest B, Vuyst L. 2000. Correlation of activities of the enzymes ?-phosphoglucomutase, UDP-galactose 4-epimerase, and UDP-glucose pyrophosphorylase with exopolysaccharide biosynthesis by Streptococcus thermophilus LY03. Appl. Environ. Microbiol., 66 (8): 3519-3527.
Deraz SF, Karlsson EN, Hedstrom M, Andersson MM, Mattiasson B. 2005. Purification and characterization of acidocin D20079, a bacteriocin produced by Lactobacillus acidophilus DSM 20079. J. Biotechnol., 117: 343-354.
Duranti S, Lugli GA, Mancabelli L, Armanini F, Turroni F, James K, Ferreti P, Gorfer V, Ferrario C, Milani C, Mangifesta M, Anzalone R, Zolfo M, Viappiani A, Pasolli E, Bariletti I, Canto R, Clementi R, Cologna M, Crifo T, Cusumano G, Fedi S, Gottardi S, Innamorati C, Mase C, Postai D, Savio D, Soffiati M, Tateo S, Pedrotti A, Segata N, Van-Sinderen D, Ventura M. 2017. Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission. Microbiome, 5 (66).
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Feliatra, Irwan E, Edwar S. 2004. Isolasi dan identifikasi bakteri probiotik dari ikan kerapu macan (Ephinephelus fuscogatus) dalam upaya efisiensi pakan ikan. J. Natur Indones., 6 (2): 75-80.
Gagnon M, Kheadr EE, Blay GL, Flissa I. 2004. In vitro inhibition of Escherichia coli O157:H7 by bifidobacterial strains of human origin. Int. J. Food Microbiol., 92 (1): 69-78.
Garrity GM, Brenner DJ, Kreig NR, Staley JT. 2005. Bergey’s Manual Systematics Bacteriology. 2nd Ed. Vol. 2. The Proteobacteria. Springer, United State of America.
Gilliland, SE. 2000. Health and nutritional benefits from lactic acid bacteria. FEMS Microbiol. Rev., 87: 175-188.
Hadadji M, Benama R., Saidi N, Henni E, Mebrouk K. 2005. Identification of cultivable bifidobacterium species isolated from breast-fed infants feces in West-Algeria. Afr. J. Biotechnol., 4 (5): 422-430.
Köhler GA, Assefa S, Reid, G. 2012. Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect. Dis. Obstet. Gynecol., 63-74.
Liu Z, Roy NC, Guo Y, Jia H, Ryan L, Samuelsson L, Thomas A, Plowman J, Clerens S, Day L. 2016. Human breast milk and infant formulas differentially modify the intestinal microbiota in human infants and host physiology in rats. J. Nutr., 146 (2): 191–199.
Lonnerdal B. 2003. Nutritional and physiological significance of human milk proteins. Am. J. Clin. Nutr., 77: 1537–1543.
Madiedo P, Hugenholltz J, Zoon P. 2002. An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int. Dairy J., 12: 163-171.
Mariat D, Firmesse O, Levenez F, Guimaraes VD, Sokol H, Dore J. 2009. The Firmicutes/Bacteriodes ration of the human microbiota changes with age. BMC Microbiol., 9: 123.
Martinez RCR, De-Martinis ECP. 2006. Effect of Leuconosoc mesenteroides 11 bacteriocin in the multiplication control of Listeria monocytogenes. Ciênc. Tecnol. Aliment., 26: 52-55.
Martinz FAC, Eduardo MB, Attilio C, Paul DC, Ricardo PSO. 2013. Bacteriocin production by Bifidobacterium spp. A Review. Biotechnol. Adv., 31: 482-488.
Narayanan R, Subramonian BS. 2015. Effect of prebiotics on bifidobacterial species isolated from infant feces. Indian J. Tradit. Know., 14 (2): 285-289.
Okamoto M, Benno Y, Leung KP, Maeda N. 2008. Bifidobacterium tsurumiense sp. Nov. from hamster dental plaque. Int. J. Syst. Evol. Microbiol., 58: 144-148.
Palmer C, Bik EM, Di-Giulio DB, Relman DA, Brown, PO. 2007. Development of the human infant intestinal microbiota. PLOS Biol., 5: e177.
Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, Brandt PAVD, Stobberingh EE. 2006. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics, 118: 511-521.
Phillips DC. 1966. The 3-dimensional structure of an enzyme molecule. Sci. Am., 215: 78–90.
Ramakrishna B. 2013. Role of the gut microbiota in human nutrition and metabolism. J. Gastroenterol. Hepatol., 28 (4): 9-17.
Sakurai T, Hashikura N, Minami J, Yamada A, Odamaki T, Xiao J. 2017. Tolerance mechanisms of human-residential bifidobacteria against lysozyme. Anaerobe, 47: 104-110.
Salazar N, Prieto A, Leal JA, Mayo B, Bada-Gancedo JC, de los Reyes-Gavilán CG, Ruas-Madiedo P. 2009. Production of exopolysaccharide by Lactobacillus and Bifidobacterium strains of human origin and metabolic activity of the producing bacteria in milk. J. Dairy Sci., 92: 4158-4168.
Schell M, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M, Pridmore DR, Arigoni F. 2002. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. P. Natl. Acad. Sci. USA., 99 (22): 14422-14427.
Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebrilla CB, German JB, Price NP, Richardson PM, Mills DA. 2008. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. P. Natl. Acad. Sci. USA., 105: 18964–18969.
Sirilun S, Takahashi H, Boonyaritichaikji S, Chaiyasuti C, Lertruangpanya P, Koga Y, Mikami K. 2015. Impact of maternal bifidobacteria and the mode of delivery on Bifidobacterium microbiota in infants. Benef. Microbes, 6 (6): 767-774.
Subijanto, Reza. 2006. Konsep dasar penggunaan prebiotik – probiotik di dalam susu formula bayi dan susu formula khusus alergi. Fakultas Kesehatan, Universitas Airlangga, Surabaya
Tallon R, Bressollier P, Urdaci M. 2003. Isolation and characterization of two exopolysaccharide produced by Lactobacillus plantarum EP56. Res. Microbiol., 154: 705-712.
Thein ZM, Samaranayake YH, Samaranayake LP. 2006. Effect of oral bacteria on growth and survival of Candida albicans biofilms. Arch. Oral Biol., 51: 672–680.
Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, Gueimonde M, Margolles A, De-Bellis G, O’Toole PW, van Sinderen D, Marchesi JR, Ventura M. 2012. Diversity of bifidobacteria within the infant gut microbiota. PLoS One, 7: e36957.
Ujaoney S, Chandra J, Faddoul F. 2014. In vitro effect of over-the-counter probiotics on the ability of Candida albicans to form biofilm on denture strips. J. Dent. Hyg., 88: 183–189.
Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H. 2010. Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol. Evol., 2: 53–66.
Venkatesan S, Kirithika M, Roselin I, Ganesan R, Muthucelian K. 2012. Comparative in vitro and in vivo study of three probiotic organisms, Bifidobacterium sp., Lactobacillus sp., S. cerevisiae and analyzing its improvement with the supplementation of prebiotics. Int. J. Plant Anim. Environ. Sci., 2 (2): 94-106.
Vicariotto F, Del PM, Mogna L, Mogna G. 2012. Effectiveness of the association of 2 probiotic strains formulated in a slow release vaginal product, in women affected by vulvo-vaginal candidiasis: a pilot study. J. Clin. Gastroenterol., 46: 73-80.
Ward TL, Knights D, Gale CA. 2017. Infant fungal communities: current knowledge and research opportunities. BMC Med.: 15-30.
Wu MH, Pan TM, Wu YJ, Chang SJ, Chang SC, Hu CY. 2010. Exopolysaccharide activities from probiotic bifidobacterium: immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. J. Food Microbiol., 144: 104-110.
Yan S, Guozhong Z, Xiaoming L, Jianxin Z, Hao Z, Wei C. 2017. Production of exopolysaccharide by Bifidobacterium longum isolated from elderly and infant feces and analysis of priming glycosyltransferase genes. RSC Adv., 7: 31736-31744.
Zinedine A, Faid M. 2007. Isolation and characterization of strains of Bifidobacteria with probiotic properties in vitro. World J. Dairy Food Sci., 2 (1): 28-34.
Zubaidah E, Liasari Y, Saparianti E. 2012. Produksi eksopolisakarida oleh Lactobacillus plantarum B2 pada produk probiotik berbasis buah murbei. J. Teknol. Pertanian, 9 (1): 58-60.
Alp G, Aslim B. 2010. Relationship between the resistance to bile salts and low pH with exopolysaccharide (EPS) production of Bifidobacterium spp. isolated from infants feces and breast milk. Anaerobe, 16: 101-105.
Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S, Gómez-Llorente C, Gil A. 2012. Probiotic mechanisms of action. Ann. Nutr. Metab., 61: 160-174.
Biasucci G, Benenati B, Morelli L, Boehm G. 2008. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J. Nutr., 138 (9): 1796-1800.
Biavati B, Vescovo M, Torriani S, Bottazzi V. 2000. Bifidobacteria: history, ecology, physiology and applications. Ann. Microbiol., 50: 117-131.
Cintas LM, Herranz C, Hernández PE, Casaus MP, Nes LF. 2001. Review: bacteriocins of lactic acid bacteria. Int. J. Food Sci. Technol., 7: 281-305.
Cizeikiene D, Juodeikiene G, Paskevicius A, Bartkiene E. 2013. Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganisms isolated from food and their control in wheat bread. Food Control, 31: 539–545.
Degeest B, Vuyst L. 2000. Correlation of activities of the enzymes ?-phosphoglucomutase, UDP-galactose 4-epimerase, and UDP-glucose pyrophosphorylase with exopolysaccharide biosynthesis by Streptococcus thermophilus LY03. Appl. Environ. Microbiol., 66 (8): 3519-3527.
Deraz SF, Karlsson EN, Hedstrom M, Andersson MM, Mattiasson B. 2005. Purification and characterization of acidocin D20079, a bacteriocin produced by Lactobacillus acidophilus DSM 20079. J. Biotechnol., 117: 343-354.
Duranti S, Lugli GA, Mancabelli L, Armanini F, Turroni F, James K, Ferreti P, Gorfer V, Ferrario C, Milani C, Mangifesta M, Anzalone R, Zolfo M, Viappiani A, Pasolli E, Bariletti I, Canto R, Clementi R, Cologna M, Crifo T, Cusumano G, Fedi S, Gottardi S, Innamorati C, Mase C, Postai D, Savio D, Soffiati M, Tateo S, Pedrotti A, Segata N, Van-Sinderen D, Ventura M. 2017. Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission. Microbiome, 5 (66).
Fanning S, Lindsay JH, Michelle C, Aldert Z, John MS, David G, Mary O’CM, Fergus S, Kenneth N, Gordon D, Douwe van S. 2012. Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. P. Natl. Acad. Sci. USA., 109 (6): 2108-2113.
Feliatra, Irwan E, Edwar S. 2004. Isolasi dan identifikasi bakteri probiotik dari ikan kerapu macan (Ephinephelus fuscogatus) dalam upaya efisiensi pakan ikan. J. Natur Indones., 6 (2): 75-80.
Gagnon M, Kheadr EE, Blay GL, Flissa I. 2004. In vitro inhibition of Escherichia coli O157:H7 by bifidobacterial strains of human origin. Int. J. Food Microbiol., 92 (1): 69-78.
Garrity GM, Brenner DJ, Kreig NR, Staley JT. 2005. Bergey’s Manual Systematics Bacteriology. 2nd Ed. Vol. 2. The Proteobacteria. Springer, United State of America.
Gilliland, SE. 2000. Health and nutritional benefits from lactic acid bacteria. FEMS Microbiol. Rev., 87: 175-188.
Hadadji M, Benama R., Saidi N, Henni E, Mebrouk K. 2005. Identification of cultivable bifidobacterium species isolated from breast-fed infants feces in West-Algeria. Afr. J. Biotechnol., 4 (5): 422-430.
Köhler GA, Assefa S, Reid, G. 2012. Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect. Dis. Obstet. Gynecol., 63-74.
Liu Z, Roy NC, Guo Y, Jia H, Ryan L, Samuelsson L, Thomas A, Plowman J, Clerens S, Day L. 2016. Human breast milk and infant formulas differentially modify the intestinal microbiota in human infants and host physiology in rats. J. Nutr., 146 (2): 191–199.
Lonnerdal B. 2003. Nutritional and physiological significance of human milk proteins. Am. J. Clin. Nutr., 77: 1537–1543.
Madiedo P, Hugenholltz J, Zoon P. 2002. An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int. Dairy J., 12: 163-171.
Mariat D, Firmesse O, Levenez F, Guimaraes VD, Sokol H, Dore J. 2009. The Firmicutes/Bacteriodes ration of the human microbiota changes with age. BMC Microbiol., 9: 123.
Martinez RCR, De-Martinis ECP. 2006. Effect of Leuconosoc mesenteroides 11 bacteriocin in the multiplication control of Listeria monocytogenes. Ciênc. Tecnol. Aliment., 26: 52-55.
Martinz FAC, Eduardo MB, Attilio C, Paul DC, Ricardo PSO. 2013. Bacteriocin production by Bifidobacterium spp. A Review. Biotechnol. Adv., 31: 482-488.
Narayanan R, Subramonian BS. 2015. Effect of prebiotics on bifidobacterial species isolated from infant feces. Indian J. Tradit. Know., 14 (2): 285-289.
Okamoto M, Benno Y, Leung KP, Maeda N. 2008. Bifidobacterium tsurumiense sp. Nov. from hamster dental plaque. Int. J. Syst. Evol. Microbiol., 58: 144-148.
Palmer C, Bik EM, Di-Giulio DB, Relman DA, Brown, PO. 2007. Development of the human infant intestinal microbiota. PLOS Biol., 5: e177.
Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, Brandt PAVD, Stobberingh EE. 2006. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics, 118: 511-521.
Phillips DC. 1966. The 3-dimensional structure of an enzyme molecule. Sci. Am., 215: 78–90.
Ramakrishna B. 2013. Role of the gut microbiota in human nutrition and metabolism. J. Gastroenterol. Hepatol., 28 (4): 9-17.
Sakurai T, Hashikura N, Minami J, Yamada A, Odamaki T, Xiao J. 2017. Tolerance mechanisms of human-residential bifidobacteria against lysozyme. Anaerobe, 47: 104-110.
Salazar N, Prieto A, Leal JA, Mayo B, Bada-Gancedo JC, de los Reyes-Gavilán CG, Ruas-Madiedo P. 2009. Production of exopolysaccharide by Lactobacillus and Bifidobacterium strains of human origin and metabolic activity of the producing bacteria in milk. J. Dairy Sci., 92: 4158-4168.
Schell M, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M, Pridmore DR, Arigoni F. 2002. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. P. Natl. Acad. Sci. USA., 99 (22): 14422-14427.
Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebrilla CB, German JB, Price NP, Richardson PM, Mills DA. 2008. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. P. Natl. Acad. Sci. USA., 105: 18964–18969.
Sirilun S, Takahashi H, Boonyaritichaikji S, Chaiyasuti C, Lertruangpanya P, Koga Y, Mikami K. 2015. Impact of maternal bifidobacteria and the mode of delivery on Bifidobacterium microbiota in infants. Benef. Microbes, 6 (6): 767-774.
Subijanto, Reza. 2006. Konsep dasar penggunaan prebiotik – probiotik di dalam susu formula bayi dan susu formula khusus alergi. Fakultas Kesehatan, Universitas Airlangga, Surabaya
Tallon R, Bressollier P, Urdaci M. 2003. Isolation and characterization of two exopolysaccharide produced by Lactobacillus plantarum EP56. Res. Microbiol., 154: 705-712.
Thein ZM, Samaranayake YH, Samaranayake LP. 2006. Effect of oral bacteria on growth and survival of Candida albicans biofilms. Arch. Oral Biol., 51: 672–680.
Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, Gueimonde M, Margolles A, De-Bellis G, O’Toole PW, van Sinderen D, Marchesi JR, Ventura M. 2012. Diversity of bifidobacteria within the infant gut microbiota. PLoS One, 7: e36957.
Ujaoney S, Chandra J, Faddoul F. 2014. In vitro effect of over-the-counter probiotics on the ability of Candida albicans to form biofilm on denture strips. J. Dent. Hyg., 88: 183–189.
Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H. 2010. Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol. Evol., 2: 53–66.
Venkatesan S, Kirithika M, Roselin I, Ganesan R, Muthucelian K. 2012. Comparative in vitro and in vivo study of three probiotic organisms, Bifidobacterium sp., Lactobacillus sp., S. cerevisiae and analyzing its improvement with the supplementation of prebiotics. Int. J. Plant Anim. Environ. Sci., 2 (2): 94-106.
Vicariotto F, Del PM, Mogna L, Mogna G. 2012. Effectiveness of the association of 2 probiotic strains formulated in a slow release vaginal product, in women affected by vulvo-vaginal candidiasis: a pilot study. J. Clin. Gastroenterol., 46: 73-80.
Ward TL, Knights D, Gale CA. 2017. Infant fungal communities: current knowledge and research opportunities. BMC Med.: 15-30.
Wu MH, Pan TM, Wu YJ, Chang SJ, Chang SC, Hu CY. 2010. Exopolysaccharide activities from probiotic bifidobacterium: immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. J. Food Microbiol., 144: 104-110.
Yan S, Guozhong Z, Xiaoming L, Jianxin Z, Hao Z, Wei C. 2017. Production of exopolysaccharide by Bifidobacterium longum isolated from elderly and infant feces and analysis of priming glycosyltransferase genes. RSC Adv., 7: 31736-31744.
Zinedine A, Faid M. 2007. Isolation and characterization of strains of Bifidobacteria with probiotic properties in vitro. World J. Dairy Food Sci., 2 (1): 28-34.
Zubaidah E, Liasari Y, Saparianti E. 2012. Produksi eksopolisakarida oleh Lactobacillus plantarum B2 pada produk probiotik berbasis buah murbei. J. Teknol. Pertanian, 9 (1): 58-60.
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