Abstract
The aim of this study was to evaluate the fermentation of dietary fiber from green bean (Phaseolus vulgaris) and prickly pear shell (Opuntia ficus-indica) by Lactobacillus acidophilus LA-5 and Bifidobacterium bifidum 450B growing as mono-culture and co-culture, the fermentation products, and proteins expressed during this process. The analysis of the fermentation profile showed a major growth of bacteria in the culture media of each dietary fiber supplemented with glucose, and particularly B. bifidum 450B at 48 h showed the highest growth. In the case of the co-culture, the growth was lower indicating the possible negative interaction between L. acidophilus LA-5 and B. bifidum 450B and may be due to the less amount of carbohydrates and the high content of non-soluble fiber that affected the nutrients availability for the bacterial strains. The pH changes indicated the presence of short-chain fatty acids (SCFAs), being acetate (46–100%) the main SCFA. Changes in the proteome concerned proteins that are involved in carbohydrate and other carbohydrate pathways. The characterization of the bacteria according to the growth, metabolites, and proteins expressed allows understanding the response to the change of environmental conditions and could be useful to understand L. acidophilus LA-5 and B. bifidum 450B strains’ adaptation to specific applications.
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Al-Sheraji, SH, Ismail A, Manap MY, Mustafa S, Yusof RM, Hassan FA (2012) Fermentation and non-digestibility of Mangifera Pajang fibrous pulp and its polysaccharides. J Funct Foods 4:933–940
Angelis M, Calasso M, Cavallo N, Cagno RD, Gobbetti M (2016) Functional proteomics within the genus Lactobacillus. Proteomics 16(6):946–962
Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157:121–141
Bloemen JG, Venema K, van de Poll MC, SWO Damink, WA Buurman, CH Dejong (2009) Short chain fatty acids exchange across the gut and liver in humans measured at surgery. Clin Nutr 28:657–661
Bove CG, Angelis MD, Gatti M, Calasso M, Neviani E, Gobbetti M (2012) Metabolic and proteomic adaptation of Lactobacillus rhamnosus strains during growth under cheese-like environmental conditions compared to de Man, Rogosa, and Sharpe medium. Proteomics 12:3206–3218
Buck BL, Azcarate-Peril MA, Klaenhammer TR (2009) Role of autoinducer-2 on the adhesion ability of Lactobacillus acidophilus. J Appl Microbiol 107:269–279
Canducci F, Armuzzi A, Cremonini F, Cammarota G, Bartolozzi F, Pola P, Gasbarrini G, Gasbarrini A (2000) A lyophilized and inactivated culture of Lactobacillus acidophilus increases Helicobacter pylori eradication rates. Aliment Pharmacol Ther 14:1625–1629
Cleusix, V, Lacroix C, Vollenweider S, Duboux M, Le Blay G (2007) Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol 7:1
Coconnier, MH, Lievin V, Hemery E, Servin AL (1998) Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl Environ Microbiol 64:4573–4580
Cohen D, Renes J, Bouwman FG, Zoetendal EG, Mariman E, de Vos WM, Vaughan EE (2006) Proteomic analysis of log to stationary growth phase Lactobacillus plantarum cells and a 2-DE database. Proteomics 6:6485–6493
Costabile, A, Kolida S, Klinder A, Gietl E, Bäuerlein M, Frohberg C, Landschütze V, Gibson GR (2010) A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects. Br J Nutr 104:1007–1017
den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54:2325–2340
Di Cagno R, De Angelis M, Calasso M, Vincentini O, Vernocchi P, Ndagijimana M, De Vincenzi M, Dessì MR, Guerzoni ME, Gobbetti M (2010) Quorum sensing in sourdough Lactobacillus plantarum Dc400: induction of plantaricin a (Plna) under co-cultivation with other lactic acid bacteria and effect of Plna on bacterial and Caco-2 cells. Proteomics 10:2175–2190
Di Cagno R, De Angelis M, Coda R, Minervini F, Gobbetti M (2009) Molecular adaptation of sourdough Lactobacillus plantarum Dc400 under co-cultivation with other lactobacilli. Res Microbiol 160:358–366
Di Cagno R, De Angelis M, Limitone A, Minervini F, Simonetti MC, Buchin S, Gobbetti M (2007) Cell–cell communication in sourdough lactic acid bacteria: a proteomic study in Lactobacillus sanfranciscensis Cb1. Proteomics 7:2430–2446
Álvarez EE, Sánchez PG (2006) La fibra dietética. Nutr Hosp 21:61–72
Fernando, WMADB, Flint S, Zou M, Brennan CS, Ranaweera KK, Bamunuarachchi A (2011) The effect of rice fibre fractions on the growth of co-cultures of probiotics. J Food Sci Technol 48:14–25
Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6:121–131
Fritz JV, Desai MS, Shah P, Schneider JG, Wilmes P (2013) From meta-omics to causality: experimental models for human microbiome research. Microbiome 1:1
Goderska K, Nowak J, Czarnecki Z (2008) Comparision of growth of Lactobacillus acidophilus and Bifidobacterium bifidum species in media supplemented with selected saccharides including prebiotics. Acta Sci Polon Technol Aliment 7:5–20
Goh YJ, Klaenhammer TR (2013) A functional glycogen biosynthesis pathway in Lactobacillus acidophilus: expression and analysis of the glg operon. Mol Microbiol 89:1187–1200
Hamer HM, Jonkers DMAE, Venema K, Vanhoutvin SALW, Troost FJ, Brummer R-J (2008) Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27:104–119
Jin J, Liu S, Zhao L, Ge K, Mao X, Ren F (2011) Changes in ffh, uvra, groes and dnak mRNA abundance as a function of acid-adaptation and growth phase in Bifidobacterium longum Bbmn68 isolated from healthy centenarians. Curr Microbiol 62:612–617
Jin J, Qin Q, Guo H, Liu S, Ge S, Zhang H, Cui J, Ren F (2015) Effect of pre-stressing on the acid-stress response in Bifidobacterium revealed using proteomic and physiological approaches. PLoS ONE 10:e0117702
Kleessen B, Hartmann L, Blaut M (2001) Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Br J Nutr 86:291–300
Knudsen KB (2001) The nutritional significance of “dietary fibre”. Anim Feed Sci Technol 90:3–20
Koskenniemi K, Koponen J, Kankainen M, Savijoki K, Tynkkynen S, de Vos WM, Kalkkinen N, Varmanen P (2009) Proteome analysis of Lactobacillus rhamnosus Gg using 2-D dige and mass spectrometry shows differential protein production in laboratory and industrial-type growth media. J Proteom Res 8:4993–5007
Koskenniemi K, Lyra C, Rajaniemi-Wacklin P, Jokela J, Sivonen K (2007) Quantitative real-time pcr detection of toxic Nodularia cyanobacteria in the baltic sea. Appl Environ Microbiol 73:2173–2179
Laakso K, Koskenniemi K, Koponen J, Kankainen M, Surakka A, Salusjärvi T, Auvinen P, Savijoki K, Nyman TA, Kalkkinen N (2011) Growth phase-associated changes in the proteome and transcriptome of Lactobacillus rhamnosus Gg in industrial-type whey medium. Microbial Biotechnol 4:746–766
Lattimer JM, Haub MD(2010) Effects of dietary fiber and its components on metabolic health. Nutrients 2:1266–1289
Macfarlane GT, Gibson GR (1997) Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine. In: Macfarlane S, McBain AJ, Macfarlane GT (eds) Gastrointestinal microbiology. Springer, London, pp 269–318
Macfarlane, SMGT, Macfarlane GT, Cummings JHT (2006) Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther 24:701–714
Madhukumar MS, Muralikrishna G (2012) Fermentation of xylo-oligosaccharides obtained from wheat bran and Bengal gram husk by lactic acid bacteria and bifidobacteria. J Food Sci Technol 49:745–752
Metzler BU, Mosenthin R (2008) A review of interactions between dietary fiber and the gastrointestinal microbiota and their consequences on intestinal phosphorus metabolism in growing pigs. Asian Australas J Anim Sci 21:603
Morgan XC, Huttenhower C (2012) Human microbiome analysis. PLoS Comput Biol 8:e1002808
Nazzaro F, Fratianni F, Nicolaus B, Poli A, Orlando P (2012) The prebiotic source influences the growth, biochemical features and survival under simulated gastrointestinal conditions of the probiotic Lactobacillus acidophilus. Anaerobe 18:280–285
Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336:1262–1267
Otto A, Becher D, Schmidt F(2014) Quantitative proteomics in the field of microbiology. Proteomics 14:547–565
Plumed-Ferrer, Carme, Kaisa M Koistinen, Tiina L Tolonen, Satu J Lehesranta, Sirpa O Kärenlampi, Elina Mäkimattila, Vesa Joutsjoki, Vesa Virtanen, Atte Von Wright (2008) Comparative study of sugar fermentation and protein expression patterns of two Lactobacillus plantarum strains grown in three different media. Appl Environ Microbiol 74:5349–5358
Pokusaeva K, Fitzgerald GF, van Sinderen D (2011) Carbohydrate metabolism in bifidobacteria. Genes Nutr 6:285–306
Roberfroid M (2007). Prebiotics: the concept revisited. J Nutr 137:830S–837S
Roediger WEW (1982) The effect of bacterial metabolites on nutrition and function of the colonic mucosa. Symbiosis between man and bacteria. In: Kaspar H, Goebell H (eds) Colon and Nutrition. MTP Press Ltd., Lancaster, pp 11–24
Roldána ML, Oterob JL, Villarreala F, Baronia MR, Carrascoc MS, Álvareza C, Russell-Whitec K, de los Ángeles Méndeza E, Simonettac AC (2011) Artículo original efecto inhibidor de Lactobacillus casei 206/1 contra Escherichia coli O157: H7. Revista de la Sociedad Venezolana de Microbiología 31:37–41
Roy CC, Kien CL, Bouthillier L, Levy E (2006) Short-chain fatty acids: ready for prime time?. Nutr Clin Pract 21:351–366
Sánchez B, Champomier-Vergès MC, del Carmen Collado M, Anglade P, Baraige F, Sanz Y, Clara G, Margolles A, Zagorec M (2007) Low-pH adaptation and the acid tolerance response of Bifidobacterium Longum biotype longum. Appl Environ Microbiol 73:6450–6459
Segata N, Boernigen D, Tickle TL, Morgan XC, Garrett WS, Huttenhower C (2013) Computational meta’omics for microbial community studies. Mol Syst Biol 9:666
Siciliano RA, Mazzeo MF (2012) Molecular mechanisms of probiotic action: a proteomic perspective. Curr Opin Microbiol 15:390–396
Simpson HL, Campbell BJ (2015) Review article: dietary fibre–microbiota interactions. Aliment Pharmacol Ther 42:158–179
Siragusa S, De Angelis M, Calasso M, Campanella D, Minervini F, Di Cagno R, Gobbetti M (2014) Fermentation and proteome profiles of Lactobacillus plantarum strains during growth under food-like conditions. J Proteom 96:366–380
Spina L, Cavallaro F, Fardowza NI, Lagoussis P, Bona D, Ciscato C, Rigante A, Vecchi M (2007) Butyric acid: pharmacological aspects and routes of administration. Dig Liver Dis Suppl 1:7–11
Tsukahara T, Koyama H, Okada M, Ushida K (2002) Stimulation of butyrate production by gluconic acid in batch culture of pig cecal digesta and identification of butyrate-producing bacteria. J Nutr 132:2229–2234
Varga GA, Kolver ES (1997) Microbial and animal limitations to fiber digestion and utilization. J Nutr 127:819S-823S
Waddington L, Cyr T, Hefford M, Truelstrup Hansen L, Kalmokoff M (2010) Understanding the acid tolerance response of Bifidobacteria. J Appl Microbiol 108:1408–1420
Wang X, Gibson GR (1993) Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol 75:373–380
Wei X, Wang S, Zhao X, Wang X, Li H, Lin W, Lu J, Zhurina D, Li B, Riedel CU (2016) Proteomic profiling of Bifidobacterium Bifidum S17 cultivated under in vitro conditions. Front Microbiol. doi:10.3389/fmicb.2016.00097
Weinstock GM (2012) Genomic approaches to studying the human microbiota. Nature 489:250–256
Winzer K, Hardie KR, Burgess N, Doherty N, Kirke D, Holden MTG, Linforth R, Cornell KA, Taylor AJ, Hill PJ (2002) Luxs: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3 (2h)-furanone. Microbiology 148:909–922
Wong JMW, De Souza R, Kendall CWC, Emam A, Jenkins DJA (2006) Colonic health: Fermentation and short chain fatty acids. J Clin Gastroenterol 40:235–243
Xiao M, Xu P, Zhao J, Wang Z, Zuo F, Zhang J, Ren F, Li P, Chen S, Ma H (2011) Oxidative stress-related responses of Bifidobacterium Longum subsp. longum Bbmn68 at the proteomic level after exposure to oxygen. Microbiology 157:1573–1588
Zhai Z, Douillard FP, An H, Wang G, Guo X, Luo Y, Hao Y (2014) Proteomic characterization of the acid tolerance response in Lactobacillus delbrueckii subsp. bulgaricus cauh1 and functional identification of a novel acid stress-related transcriptional regulator Ldb0677. Environ Microbiol 16:1524–1537
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Mora-Cura, Meléndez-Renteria, and Delgado-García would like to thank The National Council for Science and Technology (CONACYT), Mexico, for the financial support during their postgraduate studies.
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Mora-Cura, Y.N., Meléndez-Rentería, N.P., Delgado-García, M. et al. Fermentation of Dietetic Fiber from Green Bean and Prickly Pear Shell by Pure and Mixture Culture of Lactobacillus acidophilus LA-5 and Bifidobacterium bifidum 450B. Curr Microbiol 74, 691–701 (2017). https://doi.org/10.1007/s00284-017-1228-8
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DOI: https://doi.org/10.1007/s00284-017-1228-8