Cell-free spent media obtained from Bifidobacterium bifidum and Bifidobacterium crudilactis grown in media supplemented with 3’-sialyllactose modulate virulence gene expression in Escherichia coli O157:H7 and Salmonella Typhimurium
Bondue, Pauline ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Département de sciences des denrées alimentaires (DDA)
Crevecoeur, Sébastien ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Brose, François ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Département de sciences des denrées alimentaires (DDA)
Daube, Georges ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Delcenserie, Véronique ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Gestion de la qualité dans la chaîne alimentaire
Language :
English
Title :
Cell-free spent media obtained from Bifidobacterium bifidum and Bifidobacterium crudilactis grown in media supplemented with 3’-sialyllactose modulate virulence gene expression in Escherichia coli O157:H7 and Salmonella Typhimurium
Publication date :
2016
Journal title :
Frontiers in Microbiology
eISSN :
1664-302X
Publisher :
Frontiers Research Foundation, Lausanne, Switzerland
Arrieta, M. C., Stiemsma, L. T., Amenyogbe, N., Brown, E. M., and Finlay, B. (2014). The intestinal microbiome in early life: health and disease. Front. Immunol. 5:427. doi: 10.3389/fimmu.2014.00427
Asakuma, S., Hatakeyama, E., Urashima, T., Yoshida, E., Katayama, T., Yamamoto, K., et al. (2011). Phisiology of the consumption of human milk oligosaccharides by infant-gut associated bifidobacteria. J. Biol. Chem. 40, 34583-34592. doi: 10.1074/jbc.M111.248138
Barile, D., and Rastall, R. A. (2013). Human milk and related oligosaccharides as prebiotics. Curr. Opin. Biotechnol. 24, 214-219. doi: 10.1016/j.copbio.2013.01.008
Barile, D., Tao, N., Lebrilla, C. B., Coisson, J. D., Arlorio, M., and German, J. B. (2009). Permeate from cheese whey ultrafiltration is a source of milk oligosaccharides. Int. Dairy J. 19, 524-530. doi: 10.1016/j.idairyj.2009.03.008
Bayoumi, M. A., and Griffiths, M. W. (2010). Probiotics down-regulate genes in Salmonelle enterica serovar Typhimurium pathogenicity islands 1 and 2. J. Food Prot. 73, 452-460.
Bayoumi, M. A., and Griffiths, M. W. (2012). In vitro inhibition of expression of virulence genes responsible for colonization and systemic spread of enteric pathogens using Bifidobacterium bifidum secreted molecules. Int. J. Food Microbiol. 156, 255-263. doi: 10.1016/j.ijfoodmicro.2012.03.034
Bondue, P., and Delcenserie, V. (2015). Genome of bifidobacteria and carbohydrate metabolism. Korean J. Food Sci. Anim. Resour. 35, 1-9. doi: 10.5851/kosfa.2015.35.1.1
Botteldoorn, N., Van Coillie, E., Grijspeerrdt, K., Werbrouck, H., Haesebrouck, F., Donné, E., et al. (2006). Real-time reverse transcription PCR for the quantification of the mntH expression of Salmonella enterica as a functiun of growth phase and phagosome-like conditions. J. Microbiol. Methods 66, 125-135. doi: 10.1016/j.mimet.2005.11.003
Carey, C. M., Kostrzynska, M., and Thompson, S. (2009). Escherichia coli O157:H7 stress and virulence gene expression on romaine lettuce using comparative real-time PCR. J. Microbiol. Methods 2, 235-242. doi: 10.1016/j.mimet.2009.02.010
Champagne, C. P., Raymond, Y., Pouliot, Y., Gauthier, S. F., and Lessard, M. (2014). Effect of bovine colostrum, cheese whey, and spray-dried porcine plasma on the in vitro growth of probiotic bacteria and Escherichia coli. Can. J. Microbiol. 60, 287-295. doi: 10.1139/cjm-2014-0130
Chichlowski, M., German, J. B., Lebrilla, C. B., and Mills, D. A. (2011). The influence of milk oligosaccharides on microbiota of infants: opportunities for formulas. Annu. Rev. Food Sci. Technol. 2, 331-351. doi: 10.1146/annurev-food-022510-133743
Daube, G., Delcenserie, V., and Gavini, F. (2006). Probiotic Bifidobacterial Species. PCT/EP2006/061247, US 20080274085, WO 2006/122850, 31-03-2006. European Patent Office, European Union.
Delcenserie, V., Gavini, F., Beerens, H., Tresse, O., Franssen, C., and Daube, G. (2007). Description of a new species, Bifidobacterium crudilactis sp. nov., isolated from raw milk and raw milk cheeses. Syst. Appl. Microbiol. 30, 381-389. doi: 10.1016/j.syapm.2007.01.004
Delcenserie, V., Lapointe, G., Charaslertrangsi, T., Rabalski, A., and Griffiths, M. W. (2012). Glucose decreases virulence gene expression of Escherichia coli O17:H7. J. Food Prot. 75. 748-752. doi: 10.4315/0362-028X.JFP-11-384
Delcenserie, V., Taminiau, B., Gavini, F., de Schaetzen, M. A., Cleenwerck, I., Theves, M., et al. (2013). Detection and characterization of Bifidobacterium crudilactis and B. mongoliense able to grow during the manufacturing process of French raw milk cheeses. BMC Microbiol. 13:239. doi: 10.1186/1471-2180-13-239
De Vuyst, L., Moens, F., Selak, M., Riviere, A., and Leroy, F. (2013). Summer Meeting 2013: growth and physiology of bifidobacteria. J. Appl. Microbiol. 116, 477-491. doi: 10.1111/jam.12415
Di Gioia, D., Aloisio, I., Mazzola, G., and Biavati, B. (2014). Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants. Appl. Microbiol. Biotechnol. 98, 563-577. doi: 10.1007/s00253-013-5405-9
Dotz, V., Rudloff, S., Meyer, C., Lochnit, G., and Kunz, C. (2014). Metabolic fate of neutral human milk oligosaccharides in exclusively breastfed infants. Mol. Nutr. Food Res. 59, 355-364. doi: 10.1002/mnfr.201400160
Ebbensgaard, A., Mordhorst, H., Overgaard, M. T., Nielsen, C. G., Aarestrup, F. M., and Hansen, E. B. (2015). Comparative evaluation of antimicrobial activity of different antimicrobial peptides against a range of pathogenic bacteria. PLoS ONE 10:e0144611. doi: 10.1371/journal.pone.0144611
Falcao, J. P., Falcao, D. P., and Gomes, T. A. T. (2004). Ice as a vehicle for diarrheagenic Escherichia coli. Int. J. Food Microbiol. 91, 99-103. doi: 10.1016/S0168-1605(03)00327-1
Food Agriculture Organization/Organisation Mondiale de la Santé (FAO/OMS) (1998). Le lait et les Produits Laitiers dans la Nutrition Humaine. Available online at: http://www.fao.org/docrep/t4280f/t4280f0h.htm (Accessed June 16, 2016).
Garrido, D., Dallas, D. C., and Mills, D. A. (2013). Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications. Microbiology 159, 649-664. doi: 10.1099/mic.0.064113-0
Guri, A., Paligot, M., Crèvecoeur, S., Piedboeuf, B., Claes, J., Daube, G., et al. (2016). In vitro screening of mare's milk antimicrobial effect and antiproliferative activity. FEMS Microbiol. Lett. 363, 1-7. doi: 10.1093/femsle/fnv234
Henke, J. B., and Bassler, B. (2004). Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J. Bacteriol. 186, 3794-3805. doi: 10.1128/JB.186.12.3794-3805.2004
Kaper, J. B., Nataro, J. P., and Mobley, H. L. (2004). Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2. 123-140. doi: 10.1038/nrmicro818
Kelly, V., Davis, S., Berry, S., Melis, J., Spelman, R., Snell, R., et al. (2013). Rapid, quantitative analysis of 3'-and 6'-sialyllactose in milk by flow-injection analysis-mass spectrometry: screening of milks for naturally elevated sialyllactose concentration. J. Dairy Sci. 96, 7684-7691. doi: 10.3168/jds.2013-6972
Medellin-Pena, M. J., and Griffiths, M. W. (2009). Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157:H7 colonization. Appl. Environ. Microbiol. 75, 1165-1172. doi: 10.1128/AEM.01651-08
Medellin-Pena, M. J., Wang, H., Johnson, R., Anand, S., and Griffiths, M. W. (2007). Probiotics affect virulence-related gene expression in Escherichia coli O157:H7. Appl. Environ. Microbiol. 73, 4259-4267. doi: 10.1128/AEM.00159-07
Mei, G. Y., Tang, J., Carey, C., Bach, S., and Kostrzynska, M. (2015). The effect of oxidative stress on gene expression of Shiga toxin-producing Escherichia coli (STEC) O157:H7 and non-O157 serotypes. Int. J. Food Microbiol. 215, 7-15. doi: 10.1016/j.ijfoodmicro.2015.07.029
Mellies, J. L., Barron, A. M. S., and Carmona, A. M. (2007). Enteropathogenic and enterrohemorrhagic Escherichia coli virulence gene regulation. Infect. Inmmun. 75. 4199-4210. doi: 10.1128/IAI.01927-06
Milani, C., Lugli, G. A., Duranti, S., Turroni, F., Bottacini, F., Mangifesta, M., et al. (2014). Genomic encyclopedia of type strains of the genus bifidobacterium. Appl. Environ. Microbiol. 80, 6290-6302. doi: 10.1128/AEM.02308-14
Milani, C., Lugli, G. A., Duranti, S., Turroni, F., Mancabelli, L., Ferrario, C., et al. (2015). Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci. Rep. 5:15782. doi: 10.1038/srep15782
Mith, H., Clinquart, A., Zhiri, A., Daube, G., and Delcenserie, V. (2014). The impact of oregano (Origanum heracleoticum) essential oil and carvacrol on virulence gene transcription by Escherichia coli O157:H7. FEMS Microbiol. Lett. 362. 1-7. doi: 10.1093/femsle/fnu021
Momose, Y., and Hirayama, K. (2008). Effect of organic acids on inhibition of Escherichia coli O157:H7 colonization in gnobiotic mice associated with infant intestinal microbiota. Anton. Leeuw. Int. J. G. 93. 141-149. doi: 10.1007/s10482-007-9188-9
Mundi, A., Delcenserie, V., Amiri-Jami, M., Moorhead, S., and Griffiths, M. W. (2013). Cell-free preparations of Lactobacillus acidophilus strain La-5 and Bifidobacterium longum strain NCC2705 affect virulence gene expression in Campylobacter jejuni. J. Food Prot. 76, 1740-1746. doi: 10.4315/0362-028X.JFP-13-084
Nakamura, T., Kawase, H., Kimura, K., Watanabe, Y., Ohtani, M., Arai, I., et al. (2003). Concentrations of sialyloligosaccharides in bovine colostrum and milk during the prepartum and early lactation. J. Dairy Sci. 86, 1315-1320. doi: 10.3168/jds.S0022-0302(03)73715-1
Nakanishi, N., Abe, H., Ogura, Y., Hayashi, T., Tashiro, K., Kuhara, S., et al. (2006). ppGpp with DksA controls gene expression in the locus of enterocyte effacement (LEE) pathogenicity island of enterohaemorrhagic Escherichia coli through activation of two virulence regulatory genes. Mol. Microbiol. 61. 194-205. doi: 10.1111/j.1365-2958.2006.05217.x
Pacheco, A. R., Barile, D., Underwood, M. A., and Mills, D. A. (2015). The impact of the milk glycobiome on the neonate gut microbiota. Annu. Rev. Anim. Biosci. 3, 419-445. doi: 10.1146/annurev-animal-022114-111112
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 2002-2007. doi: 10.1093/nar/29.9.e45
Rashid, R. A., Tabata, T. A., Oatley, M. J., Besser, T. E., Tarr, P. I., and Moseley, S. L. (2006). Expression of putative virulence factors of Escherichia coli O157:H7 differs in bovine and human infections. Infect. Immun. 74, 4142-4148. doi: 10.1128/IAI.00299-06
Sakarya, S., Göktürk, C., Öztürk, T., and Ertugrul, M. B. (2010). Sialic acid is required for nonspecific adherence of Salmonella enterica ssp. enterica serovar Typhi on Caco-2cells. FEMS Immunol. Med. Microbiol. 58. 330-335. doi: 10.1111/j.1574-695X.2010.00650.x
Scholtens, P. A. (2014). Stool characteristics of infants receiving short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides: a review. World, J. Gastroenterol. 20:13446. doi: 10.3748/wjg.v20.i37.13446
Scott, K. P., Antoine, J., Midtvedt, T., and Van Hemert, S. (2015). Manipulating the gut microbiota to maintain health and treat disease. Microb. Ecol. Health Dis. 1, 1-10. doi: 10.3402/mehd.v26.25877
Sela, D. A. (2011). Bifidobacterial utilization of human milk oligosaccharides. Int. J. Food Microbiol. 149, 58-64. doi: 10.1016/j.ijfoodmicro.2011.01.025
Sela, D. A., Chapman, J., Adeuya, A., Kim, J. H., Chen, F., Whitehead, T. R., et al. (2008). The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. U.S.A. 105, 18964-18969. doi: 10.1073/pnas.0809584105
Sela, D. A., and Mills, D. A. (2010). Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol. 18, 298-307. doi: 10.1016/j.tim.2010.03.008
Severi, E., Hood, D. W., and Thomas, G. H. (2007). Sialic acid utilization by bacterial pathogens. Microbiology 153, 2817-2822. doi: 10.1099/mic.0.2007/009480-0
Singh, R., and Jiang, X. (2015). Expression of stress and virulence genes in Escherichia coli O157:H7 heat shocked in fresh dairy compost. J. Food Prot. 78, 31-41. doi: 10.4315/0362-028X.JFP-13-529
Smilowitz, J. T., Lebrilla, C. B., Mills, D. A., German, J. B., and Freeman, S. L. (2014). Breast milk oligosaccharides: structure-function relationships in the neonate. Annu. Rev. Nutr. 34, 1-27. doi: 10.1146/annurev-nutr-071813-105721
Sumi, C. D., Yang, B. W., Yeo, I. C., and Hahm, Y. T. (2015). Antimicrobial peptides of the genus Bacillus: a new era for antibiotics. Can. J. Microbiol. 61, 93-103. doi: 10.1139/cjm-2014-0613
Takle, G. W., Toth, I. K., and Brurberg, M. B. (2007). Evaluation of reference genes for real-time RT-PCR expression studies in the plant pathogen Pectobacterium atrosepticum. BMC Plant Biol. 7:50. doi: 10.1186/1471-2229-7-50
Tanimomo, J., Delcenserie, V., Taminiau, B., Daube, G., Saint-Hubert, C., and Durieux, A. (2016). Growth and freeze-drying optimization of Bifidobacterium crudilactis. Food Nutr. Sci. 7, 616-626. doi: 10.4236/fns.2016.77063
Tao, N., DePeters, E. J., Freeman, S., German, J. B., Grimm, R., and Lebrilla, C. B. (2008). Bovine milk glycome. J. Dairy Sci. 91, 3768-3778. doi: 10.3168/jds.2008-1305
Tao, N., DePeters, E. J., German, J. B., Grimm, R., and Lebrilla, C. B. (2009). Variations in bovine milk oligosaccharides during early and middle lactation stages analyzed by high-performance liquid chromatography-chip/mass spectrometry. J. Dairy Sci. 92, 2991-3001. doi: 10.3168/jds.2008-1642
Tellez, A., Corredig, M., Guri, A., Zanabria, R., Griffiths, M. W., and Delcenserie, V. (2012). Bovine milk fat globule membrane affects virulence expression in Escherichia coli O157:H7. J. Dairy Sci. 95, 6313-6319. doi: 10.3168/jds.2012-5560
Underwood, M. A., German, J. B., Lebrilla, C. B., and Mills, D. A. (2015). Bifidobacterium longum subespecies infantis: champion colonizer in the infant gut. Pediatr. Res. 77, 229-235. doi: 10.1038/pr.2014.156
Urashima, T., Taufik, E., Fukuda, K., and Asakuma, S. (2013). Recent advances in studies on milk oligosaccharides of cows and other domestic farm animals. Biosci. Biotechnol. Biochem. 77, 455-466. doi: 10.1271/bbb.120810
Vimr, E. R., Kalivoda, K. A., Deszo, E. L., and Steenbergen, S. M. (2004). Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68, 132-153. doi: 10.1128/MMBR.68.1.132-153.2004
Wood, K. T., Gonzalez Barrios, A. F., Herzberg, M., and Lee, J. (2006). Motility influences biofilm architecture in Escherichia coli. Appl. Microbiol. Biotechnol. 72, 361-367. doi: 10.1007/s00253-005-0263-8
Xu, H., Lee, H. Y., and Ahn, J. (2010). Growth and virulence properties of biofilm-forming Salmonella enterica serovar Typhimurium under different acidic conditions. Appl. Environ. Microbiol. 76, 7910-7917. doi: 10.1128/AEM.01508-10
Zeinhom, M., Tellez, A. M., Delcenserie, V., El-Kholy, A. M., and El-Shinawy, Griffiths, M. W. (2012). Yoghurt containing bioactive molecules produced by Lactobacillus acidophilus La-5 exerts a protective effect against enterohaemorrhagic Escherichia coli (EHEC) in mice. J. Food Prot. 10, 1796-1805. doi: 10.4315/0362-028X.JFP-11-508
Zivkovic, A. M., and Barile, D. (2011). Bovine milk as a source of functional oligosaccharides for improving human health. Adv. Nutr. 2, 284-289. doi: 10.3945/an.111.000455
