Escherichia coli-Derived Uracil Increases the Antibacterial Activity and Growth Rate of Lactobacillus plantarum

Eun-Mi  Ha

doi:10.4014/jmb.1601.01063

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Research article

Molecular and Cellular Microbiology (MCM) | Pathogenesis and Host-Microbial interactions

Escherichia coli-Derived Uracil Increases the Antibacterial Activity and Growth Rate of Lactobacillus plantarum

Eun-Mi Ha ^1*

Department of Pharmacology, College of Pharmacy, Catholic University of Daegu, Gyeongsan 38430, Republic of Korea

Received: January 25, 2016; Accepted: March 18, 2016

J. Microbiol. Biotechnol. 2016; 26(5): 975-987

Published May 28, 2016 https://doi.org/10.4014/jmb.1601.01063

Abstract

Lactobacillus plantarum (L. plantarum) is a representative probiotic. In particular, L. plantarum is the first commensal bacterium to colonize the intestine of infants. For this reason, the initial settlement of L. plantarum can play an important role in determining an infant’s health as well as their eventual health status as an adult. In addition, L. plantarum combats pathogenic infections (such as Escherichia coli (E. coli), one of the early pathogenic colonizers in an unhealthy infant gut) by secreting antimicrobial substances. The aim of this research was to determine how L. plantarum combats E. coli infection and why it is a representative probiotic in the intestine. Consequently, this research observed that E. coli releases uracil. L. plantarum specifically recognizes E. coli-derived uracil, which increases the growth rate and production of antimicrobial substance of L. plantarum. In addition, through the inhibitory activity test, this study postulates that the antimicrobial substance is a protein and can be considered a bacteriocin-like substance. Therefore, this research assumes that L. plantarum exerts its antibacterial ability by recognizing E. coli and increasing its growth rate as a result, and this phenomenon could be one of the reasons for L. plantarum settling in the intestine of infants as a beneficial bacterium.

Keywords

Lactobacillus plantarum, uracil, Escherichia coli, antibacterial activity, growth rate, probiotics

References

Atrih A, Rekhif N, Michel M, Lefebvre G. 1993. Detection of bacteriocins produced by Lactobacillus plantarum strains isolated from different foods. Microbios 75: 117-123.
Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Systems Biol. 2: 2006 0008.
Bedford Russell AR, Murch SH. 2006. Could peripartum antibiotics have delayed health consequences for the infant? BJOG 113: 758-765.
Benor S, Marom R, Ben Tov A, Armoni Domany K, Zaidenberg-Israeli G, Dollberg S. 2014. Probiotic supplementation in mothers of very low birth weight infants. Am. J. Perinatol. 31: 497-504.
Biasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C. 2010. Mode of delivery affects the bacterial community in the newborn gut. Early Hum. Dev. 86 Suppl. 1: 13-15.
Bjorksten B. 2006. The gut microbiota: a complex ecosystem. Clinical and experimental allergy. Clin. Exper. Allergy 36:1215-1217.
Bjorksten B, Naaber P, Sepp E, Mikelsaar M. 1999. The intestinal microflora in allergic Estonian and Swedish 2year-old children. Clin. Exper. Allergy 29: 342-346.
Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M. 2001. Allergy development and the intestinal microflora during the first year of life. J. Allergy Clin. Immunol. 108: 516-520.
Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC. 2006. Adenosine 5’-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 112: 358-404.
Debley JS, Smith JM, Redding GJ, Critchlow CW. 2005. Childhood asthma hospitalization risk after cesarean delivery in former term and premature infants. Ann. Allergy Asthma Immunol. 94: 228-233.
Duncan SH, Flint HJ. 2013. Probiotics and prebiotics and health in ageing populations. Maturitas 75: 44-50.
Dunne C, O’Mahony L, Murphy L, Thornton G, Morrissey D, O’Halloran S, et al. 2001. In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am. J. Clin. Nutr. 73: 386S-392S.
Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. 2005. Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
Eltzschig HK, Macmanus CF, Colgan SP. 2008. Neutrophils as sources of extracellular nucleotides: functional consequences at the vascular interface. Trends Cardiovasc. Med. 18: 103-107.
Eltzschig HK, Sitkovsky MV, Robson SC. 2012. Purinergic signaling during inflammation. N. Engl. J. Med. 367: 23222333.
Fallani M, Amarri S, Uusijarvi A, Adam R, Khanna S, Aguilera M, et al. 2011. Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres. Microbiology 157: 1385-1392.
Fukuda S, Ishikawa H, Koga Y, Aiba Y, Nakashima K, Cheng L, Shirakawa T. 2004. Allergic symptoms and microflora in schoolchildren. J. Adolesc. Health 35: 156-158.
Gamelin E, Boisdron-Celle M, Turcant A, Larra F, Allain P, Robert J. 1997. Rapid and sensitive high-performance liquid chromatographic analysis of halogenopyrimidines in plasma. J. Chromatogr. B Biomed. Sci. Appl. 695: 409-416.
Gewolb IH, Schwalbe RS, Taciak VL, Harrison TS, Panigrahi P. 1999. Stool microflora in extremely low birthweight infants. Arch. Dis. Child. Fetal Neonatal Ed. 80: F167-F173.
Gibson GR, Roberfroid MB. 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutrit. 125: 1401-1412.
Gronlund MM, Lehtonen OP, Eerola E, Kero P. 1999. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J. Pediatric Gastroenterol. Nutr. 28: 19-25.
Ha EM. 2015. Growth rate and antimicrobial activity of Lactobacillus plantarum reacting with bacterial culture supernatant. Microbiol. Biotechnol. Lett. 43: 187-194
Hallstrom M, Eerola E, Vuento R, Janas M, Tammela O. 2004. Effects of mode of delivery and necrotising enterocolitis on the intestinal microflora in preterm infants. Eur. J. Clin. Microbiol. Infect. Dis. 23: 463-470.
Iebba V, Aloi M, Civitelli F, Cucchiara S. 2011. Gut microbiota and pediatric disease. Dig. Dis. 29: 531-539.
Isolauri E, Arvola T, Sutas Y, Moilanen E, Salminen S. 2000. Probiotics in the management of atopic eczema. Clin. Exper. Allergy 30: 1604-1610.
Isolauri E, Juntunen M, Rautanen T, Sillanaukee P, Koivula T. 1991. A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88: 90-97.
Jack RW, Tagg JR, Ray B. 1995. Bacteriocins of grampositive bacteria. Microbiol. Rev. 59: 171-200.
Junger WG. 2011. Immune cell regulation by autocrine purinergic signalling. Nat. Rev. Immunol. 11: 201-212.
Kalliomaki M, Isolauri E. 2002. Pandemic of atopic diseases - a lack of microbial exposure in early infancy? Curr. Drug Targets Infect. Disord. 2: 193-199.
Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. 2001. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J. Allergy Clin. Immunol. 107: 129-134.
Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. 2001. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357: 1076-1079.
Kelly D, King T, Aminov R. 2007. Importance of microbial colonization of the gut in early life to the development of immunity. Mutat. Res. 622: 58-69.
Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, et al. 2007. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446: 1091-1095.
Kreda SM, Okada SF, van Heusden CA, O’Neal W, Gabriel S, Abdullah L, et al. 2007. Coordinated release of nucleotides and mucin from human airway epithelial Calu-3 cells. J. Physiol. 584: 245-259.
Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, et al. 2007. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases:a randomized, double-blind, placebo-controlled trial. J. Allergy Clin. Immunol. 119: 192-198.
Lang JR, Bolton S. 1991. A comprehensive method validation strategy for bioanalytical applications in the pharmaceutical industry. Experimental considerations. J. Pharm. Biomed. Anal. 9: 357-361.
Laubereau B, Filipiak-Pittroff B, von Berg A, Grubl A, Reinhardt D, Wichmann HE, Koletzko S. 2004. Caesarean section and gastrointestinal symptoms, atopic dermatitis, and sensitization during the first year of life. Arch. Dis. Child. 89: 993-997.
Lazarowski ER. 2012. Vesicular and conductive mechanisms of nucleotide release. Purinergic Signal. 8: 359-373.
Lazarowski ER, Boucher RC. 2001. UTP as an extracellular signaling molecule. News Physiol. Sci. 16: 1-5.
Lazarowski ER, Boucher RC, Harden TK. 2003. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64: 785-795.
Lazarowski ER, Homolya L, Boucher RC, Harden TK. 1997. Direct demonstration of mechanically induced release of cellular UTP and its implication for uridine nucleotide receptor activation. J. Biol. Chem. 272: 24348-24354.
Lee KA, Kim SH, Kim EK, Ha EM, You H, Kim B, et al. 2013. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153: 797-811.
Lewus CB, Kaiser A, Montville TJ. 1991. Inhibition of food-borne bacterial pathogens by bacteriocins from lactic acid bacteria isolated from meat. Appl. Environ. Microbiol. 57: 1683-1688.
Lohner S, Kullenberg D, Antes G, Decsi T, Meerpohl JJ. 2014. Prebiotics in healthy infants and children for prevention of acute infectious diseases: a systematic review and metaanalysis. Nutr. Rev. 72: 523-531.
Mackie RI, Sghir A, Gaskins HR. 1999. Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69: 1035S-1045S.
Majamaa H, Isolauri E. 1997. Probiotics: a novel approach in the management of food allergy. J. Allergy Clin. Immunol. 99: 179-185.
Maldonado A, Ruiz-Barba JL, Jimenez-Diaz R. 2004. Production of plantaricin NC8 by Lactobacillus plantarum NC8 is induced in the presence of different types of gram-positive bacteria. Arch. Microbiol. 181: 8-16.
Masters M, Colloms MD, Oliver IR, He L, Macnaughton EJ, Charters Y. 1993. The pcnB gene of Escherichia coli, which is required for ColE1 copy number maintenance, is dispensable. J. Bacteriol. 175: 4405-4413.
Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118.
Messi P, Bondi M, Sabia C, Battini R, Manicardi G. 2001. Detection and preliminary characterization of a bacteriocin (plantaricin 35d) produced by a Lactobacillus plantarum strain. Int. J. Food Microbiol. 64: 193-198.
Negele K, Heinrich J, Borte M, von Berg A, Schaaf B, Lehmann I, et al. 2004. Mode of delivery and development of atopic disease during the first 2 years of life. Pediatr. Allergy Immunol. 15: 48-54.
Orrhage K, Nord CE. 1999. Factors controlling the bacterial colonization of the intestine in breastfed infants. Acta Paediatr. Suppl. 88: 47-57.
Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. 2007. Development of the human infant intestinal microbiota. PLoS Biol. 5: e177.
Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, et al. 2007. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 56: 661-667.
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
Rautava S, Isolauri E. 2002. The development of gut immune responses and gut microbiota: effects of probiotics in prevention and treatment of allergic disease. Curr. Issues Intest. Microbiol. 3: 15-22.
Rinas U, Hellmuth K, Kang R, Seeger A, Schlieker H. 1995. Entry of Escherichia coli into stationary phase is indicated by endogenous and exogenous accumulation of nucleobases. Appl. Environ. Microbiol. 61: 4147-4151.
Rook GA, Brunet LR. 2005. Microbes, immunoregulation, and the gut. Gut 54: 317-320.
Ruiz-Barba JL, Caballero-Guerrero B, Maldonado-Barragan A, Jimenez-Diaz R. 2010. Coculture with specific bacteria enhances survival of Lactobacillus plantarum NC8, an autoinducerregulated bacteriocin producer, in olive fermentations. Food Microbiol. 27: 413-417.
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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(5): 975-987

Published online May 28, 2016 https://doi.org/10.4014/jmb.1601.01063

Escherichia coli-Derived Uracil Increases the Antibacterial Activity and Growth Rate of Lactobacillus plantarum

Eun-Mi Ha ^1*

Department of Pharmacology, College of Pharmacy, Catholic University of Daegu, Gyeongsan 38430, Republic of Korea

Received: January 25, 2016; Accepted: March 18, 2016

Abstract

Lactobacillus plantarum (L. plantarum) is a representative probiotic. In particular, L. plantarum is
the first commensal bacterium to colonize the intestine of infants. For this reason, the initial
settlement of L. plantarum can play an important role in determining an infant’s health as well
as their eventual health status as an adult. In addition, L. plantarum combats pathogenic
infections (such as Escherichia coli (E. coli), one of the early pathogenic colonizers in an
unhealthy infant gut) by secreting antimicrobial substances. The aim of this research was to
determine how L. plantarum combats E. coli infection and why it is a representative probiotic in
the intestine. Consequently, this research observed that E. coli releases uracil. L. plantarum
specifically recognizes E. coli-derived uracil, which increases the growth rate and production
of antimicrobial substance of L. plantarum. In addition, through the inhibitory activity test, this
study postulates that the antimicrobial substance is a protein and can be considered a
bacteriocin-like substance. Therefore, this research assumes that L. plantarum exerts its
antibacterial ability by recognizing E. coli and increasing its growth rate as a result, and this
phenomenon could be one of the reasons for L. plantarum settling in the intestine of infants as a
beneficial bacterium.

Keywords: Lactobacillus plantarum, uracil, Escherichia coli, antibacterial activity, growth rate, probiotics

Abstract

References

Atrih A, Rekhif N, Michel M, Lefebvre G. 1993. Detection of bacteriocins produced by Lactobacillus plantarum strains isolated from different foods. Microbios 75: 117-123.
Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Systems Biol. 2: 2006 0008.
Bedford Russell AR, Murch SH. 2006. Could peripartum antibiotics have delayed health consequences for the infant? BJOG 113: 758-765.
Benor S, Marom R, Ben Tov A, Armoni Domany K, Zaidenberg-Israeli G, Dollberg S. 2014. Probiotic supplementation in mothers of very low birth weight infants. Am. J. Perinatol. 31: 497-504.
Biasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C. 2010. Mode of delivery affects the bacterial community in the newborn gut. Early Hum. Dev. 86 Suppl. 1: 13-15.
Bjorksten B. 2006. The gut microbiota: a complex ecosystem. Clinical and experimental allergy. Clin. Exper. Allergy 36:1215-1217.
Bjorksten B, Naaber P, Sepp E, Mikelsaar M. 1999. The intestinal microflora in allergic Estonian and Swedish 2year-old children. Clin. Exper. Allergy 29: 342-346.
Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M. 2001. Allergy development and the intestinal microflora during the first year of life. J. Allergy Clin. Immunol. 108: 516-520.
Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC. 2006. Adenosine 5’-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 112: 358-404.
Debley JS, Smith JM, Redding GJ, Critchlow CW. 2005. Childhood asthma hospitalization risk after cesarean delivery in former term and premature infants. Ann. Allergy Asthma Immunol. 94: 228-233.
Duncan SH, Flint HJ. 2013. Probiotics and prebiotics and health in ageing populations. Maturitas 75: 44-50.
Dunne C, O’Mahony L, Murphy L, Thornton G, Morrissey D, O’Halloran S, et al. 2001. In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am. J. Clin. Nutr. 73: 386S-392S.
Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. 2005. Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
Eltzschig HK, Macmanus CF, Colgan SP. 2008. Neutrophils as sources of extracellular nucleotides: functional consequences at the vascular interface. Trends Cardiovasc. Med. 18: 103-107.
Eltzschig HK, Sitkovsky MV, Robson SC. 2012. Purinergic signaling during inflammation. N. Engl. J. Med. 367: 23222333.
Fallani M, Amarri S, Uusijarvi A, Adam R, Khanna S, Aguilera M, et al. 2011. Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres. Microbiology 157: 1385-1392.
Fukuda S, Ishikawa H, Koga Y, Aiba Y, Nakashima K, Cheng L, Shirakawa T. 2004. Allergic symptoms and microflora in schoolchildren. J. Adolesc. Health 35: 156-158.
Gamelin E, Boisdron-Celle M, Turcant A, Larra F, Allain P, Robert J. 1997. Rapid and sensitive high-performance liquid chromatographic analysis of halogenopyrimidines in plasma. J. Chromatogr. B Biomed. Sci. Appl. 695: 409-416.
Gewolb IH, Schwalbe RS, Taciak VL, Harrison TS, Panigrahi P. 1999. Stool microflora in extremely low birthweight infants. Arch. Dis. Child. Fetal Neonatal Ed. 80: F167-F173.
Gibson GR, Roberfroid MB. 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutrit. 125: 1401-1412.
Gronlund MM, Lehtonen OP, Eerola E, Kero P. 1999. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J. Pediatric Gastroenterol. Nutr. 28: 19-25.
Ha EM. 2015. Growth rate and antimicrobial activity of Lactobacillus plantarum reacting with bacterial culture supernatant. Microbiol. Biotechnol. Lett. 43: 187-194
Hallstrom M, Eerola E, Vuento R, Janas M, Tammela O. 2004. Effects of mode of delivery and necrotising enterocolitis on the intestinal microflora in preterm infants. Eur. J. Clin. Microbiol. Infect. Dis. 23: 463-470.
Iebba V, Aloi M, Civitelli F, Cucchiara S. 2011. Gut microbiota and pediatric disease. Dig. Dis. 29: 531-539.
Isolauri E, Arvola T, Sutas Y, Moilanen E, Salminen S. 2000. Probiotics in the management of atopic eczema. Clin. Exper. Allergy 30: 1604-1610.
Isolauri E, Juntunen M, Rautanen T, Sillanaukee P, Koivula T. 1991. A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88: 90-97.
Jack RW, Tagg JR, Ray B. 1995. Bacteriocins of grampositive bacteria. Microbiol. Rev. 59: 171-200.
Junger WG. 2011. Immune cell regulation by autocrine purinergic signalling. Nat. Rev. Immunol. 11: 201-212.
Kalliomaki M, Isolauri E. 2002. Pandemic of atopic diseases - a lack of microbial exposure in early infancy? Curr. Drug Targets Infect. Disord. 2: 193-199.
Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. 2001. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J. Allergy Clin. Immunol. 107: 129-134.
Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. 2001. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357: 1076-1079.
Kelly D, King T, Aminov R. 2007. Importance of microbial colonization of the gut in early life to the development of immunity. Mutat. Res. 622: 58-69.
Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, et al. 2007. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446: 1091-1095.
Kreda SM, Okada SF, van Heusden CA, O’Neal W, Gabriel S, Abdullah L, et al. 2007. Coordinated release of nucleotides and mucin from human airway epithelial Calu-3 cells. J. Physiol. 584: 245-259.
Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, et al. 2007. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases:a randomized, double-blind, placebo-controlled trial. J. Allergy Clin. Immunol. 119: 192-198.
Lang JR, Bolton S. 1991. A comprehensive method validation strategy for bioanalytical applications in the pharmaceutical industry. Experimental considerations. J. Pharm. Biomed. Anal. 9: 357-361.
Laubereau B, Filipiak-Pittroff B, von Berg A, Grubl A, Reinhardt D, Wichmann HE, Koletzko S. 2004. Caesarean section and gastrointestinal symptoms, atopic dermatitis, and sensitization during the first year of life. Arch. Dis. Child. 89: 993-997.
Lazarowski ER. 2012. Vesicular and conductive mechanisms of nucleotide release. Purinergic Signal. 8: 359-373.
Lazarowski ER, Boucher RC. 2001. UTP as an extracellular signaling molecule. News Physiol. Sci. 16: 1-5.
Lazarowski ER, Boucher RC, Harden TK. 2003. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64: 785-795.
Lazarowski ER, Homolya L, Boucher RC, Harden TK. 1997. Direct demonstration of mechanically induced release of cellular UTP and its implication for uridine nucleotide receptor activation. J. Biol. Chem. 272: 24348-24354.
Lee KA, Kim SH, Kim EK, Ha EM, You H, Kim B, et al. 2013. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153: 797-811.
Lewus CB, Kaiser A, Montville TJ. 1991. Inhibition of food-borne bacterial pathogens by bacteriocins from lactic acid bacteria isolated from meat. Appl. Environ. Microbiol. 57: 1683-1688.
Lohner S, Kullenberg D, Antes G, Decsi T, Meerpohl JJ. 2014. Prebiotics in healthy infants and children for prevention of acute infectious diseases: a systematic review and metaanalysis. Nutr. Rev. 72: 523-531.
Mackie RI, Sghir A, Gaskins HR. 1999. Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69: 1035S-1045S.
Majamaa H, Isolauri E. 1997. Probiotics: a novel approach in the management of food allergy. J. Allergy Clin. Immunol. 99: 179-185.
Maldonado A, Ruiz-Barba JL, Jimenez-Diaz R. 2004. Production of plantaricin NC8 by Lactobacillus plantarum NC8 is induced in the presence of different types of gram-positive bacteria. Arch. Microbiol. 181: 8-16.
Masters M, Colloms MD, Oliver IR, He L, Macnaughton EJ, Charters Y. 1993. The pcnB gene of Escherichia coli, which is required for ColE1 copy number maintenance, is dispensable. J. Bacteriol. 175: 4405-4413.
Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118.
Messi P, Bondi M, Sabia C, Battini R, Manicardi G. 2001. Detection and preliminary characterization of a bacteriocin (plantaricin 35d) produced by a Lactobacillus plantarum strain. Int. J. Food Microbiol. 64: 193-198.
Negele K, Heinrich J, Borte M, von Berg A, Schaaf B, Lehmann I, et al. 2004. Mode of delivery and development of atopic disease during the first 2 years of life. Pediatr. Allergy Immunol. 15: 48-54.
Orrhage K, Nord CE. 1999. Factors controlling the bacterial colonization of the intestine in breastfed infants. Acta Paediatr. Suppl. 88: 47-57.
Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. 2007. Development of the human infant intestinal microbiota. PLoS Biol. 5: e177.
Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, et al. 2007. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 56: 661-667.
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
Rautava S, Isolauri E. 2002. The development of gut immune responses and gut microbiota: effects of probiotics in prevention and treatment of allergic disease. Curr. Issues Intest. Microbiol. 3: 15-22.
Rinas U, Hellmuth K, Kang R, Seeger A, Schlieker H. 1995. Entry of Escherichia coli into stationary phase is indicated by endogenous and exogenous accumulation of nucleobases. Appl. Environ. Microbiol. 61: 4147-4151.
Rook GA, Brunet LR. 2005. Microbes, immunoregulation, and the gut. Gut 54: 317-320.
Ruiz-Barba JL, Caballero-Guerrero B, Maldonado-Barragan A, Jimenez-Diaz R. 2010. Coculture with specific bacteria enhances survival of Lactobacillus plantarum NC8, an autoinducerregulated bacteriocin producer, in olive fermentations. Food Microbiol. 27: 413-417.
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Escherichia coli-Derived Uracil Increases the Antibacterial Activity and Growth Rate of Lactobacillus plantarum

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