Abstract
Human gastrointestinal microbiota (HGIM) incorporate a large number of microbes from different species. Anaerobic bacteria are the dominant organisms in this microbial consortium and play a crucial role in human health. In addition to their functional role as the main source of many essential metabolites for human health, they are considered as biotherapeutic agents in the regulation of different human metabolites. They are also important in the prevention and in the treatment of different physical and mental diseases. Bifidobacteria are the dominant anaerobic bacteria in HGIM and are widely used in the development of probiotic products for infants, children and adults. To develop bifidobacteria-based bioproducts, therefore, it is necessary to develop a large-scale biomass production platform based on a good understanding of the ideal medium and bioprocessing parameters for their growth and viability. In addition, high cell viability should be maintained during downstream processing and storage of probiotic cell powder or the final formulated product. In this work we review the latest information about the biology, therapeutic activities, cultivation and industrial production of bifidobacteria.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsAbbreviations
- ASD:
-
Autism spectrum disorders
- ATCC:
-
American type culture collection
- ATP:
-
Adenosine triphosphate
- BSH:
-
Bile salt hydrolase
- CAGR:
-
Compound annual growth rate
- CFU:
-
Colony forming unit
- CLB:
-
Liver cysteine lactose
- FDA:
-
Food and Drug Administration
- FOS:
-
Fructooligosaccharides
- GIT:
-
Gastro intestinal tract
- GRAS:
-
Generally regarded as safe
- HGIM:
-
Human gastrointestinal microbiota
- IBS:
-
Irritable bowel syndrome
- LAB:
-
Lactic acid bacteria
- MERCOSUR:
-
Mercado Común del Sur (Common Market of South)
- MRS:
-
Man–Rogosa–Sharp medium
- NYA:
-
National Yoghurt Association
- NRSP:
-
Natural rubber serum powder
- RCM:
-
Reinforced clostridia medium
- sEPS:
-
Surface exopolysaccharides
- SMF:
-
Submerged fermentation
- SSF:
-
Solid state fermentation
- TPY:
-
Trypticase-phytone-yeast extract
- WHO:
-
World Health Organization
References
Ley RE, Peterson DA, Gordon JL (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848
Sekirov I, Russell SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904
Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104:13780–13785
Fuller R (1989) A review: probiotics in man and animals. J Appl Bacteriol 66:365–378
Fooks LJ, Gibson GR (2002) Probiotics as modulators of the gut flora. Brit J Nutr 88:S39–S49
Leahy SC, Higgins DG, Fitzgerald GF, van Sinderen D (2005) Getting better with bifidobacteria. J Appl Microbiol 98:1303–1315
Muller JA, Ross RP, Fitzgerald GF, Stanton C (2009) Manufacture of probiotic bacteria. In: Charalampopulos D, Rastall R (eds) Prebiotics and probiotics science and technology. Springer, Heidelberg, pp 725–759
Sarmidi MR, El Enshasy HA (2012) Biotechnology for wellness industry: concepts and biofactories. Int J Biotechnol Well Ind 1:3–28
Shah NP (2007) Functional cultures and health benefits. Int Dairy J 17:1262–1277
Forssten SD, Sindelar CW, Ouwehand AC (2011) Probiotics from an industrial perspective. J Clin Microbiol 17:410–413
Salminen S, Isolauri E, Salminen E (1996) Clinical uses of probiotics for stabilizing the gut mucosal barrier: successful strains and future challenges. Antonie van Leeuwenhoek 70:347–358
Salminen S, Bouley C, Boutron-Ruault MC, Cummings JH, Franck A, Gibson GR, Isolauri E, Moreau M-C, Roberfroid M, Rowland I (1998) Functional food science and gastrointestinal physiology and function. Brit J Nutr 80(Suppl 1):S147–S171
BourliouxP KB, Guarner F, Braesco B (2003) The intestine and its microflora are partners for the protection of the host. Am J Clin Nutr 78:675–683
Villena J, Salva S, Nuñez M, Corzo J, Tolaba R, Faedda J, Font G, Alvarez S (2012) Probiotics for everyone! The novel immunobiotic Lactobacillus rhamnosus CRL1505 and the beginning of social probiotic programs in Argentina. Int J Biotechnol Well Ind 1:189–198
Heyman M, Menard S (2002) Probiotic microorganisms: how they affect intestinal pathophysiology. Cell Mol Life Sci 59:1–15
Foster JA, McVey Neufeld KA (2013) Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36:305–312
Steenbergen L, Sellaro R, van Hemert S, Bosch JA, Colzato LS (2015) A randomized controlled trial to test the effect of multi species probiotics on cognitive reactivity to sad mood. Brain Behav Immunity 48:258–264
Lew L-C, Gan C-Y, Liong M-T (2013) Dermal bioactives from lactobacilli and bifidobacteria. Ann Microbiol 63:1047–1055
Raja BR, Arunachalam KD (2011) Market potential for probiotic nutritional supplements in India. Afr J Business Manag 5:5418–5423
Markets and Markets (2014) Global probiotics market worth US$32.6 billion by 2014. http://www.prnewswire.com/news-releases/marketsandmarkets-global-probiotics-market-worth-us326-billion-by-2014-62565667.html. Accessed 10 June 2015
Saxelin M, Tynkkynen S, Mattila-Sandholom T, de Vos WM (2005) Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 16:204–211
Mättö J, Alakomi H-L, Vaari A, Virkajärvi I, Saarela M (2006) Influence of processing conditions on Bifidobacterium animalis subsp. lactis functionality with a special focus on acid tolerance and factors affecting it. Int Dairy J 16:1029–1037
Vergari F, Tibuzzi A, Basile G (2010) An overview of the functional food market: from marketing issues and commercial players to future demand from life in space, “Bio-farms for nutraceuticals”. In: Giardi MT, Rea G, Berra B (eds) Advances in experimental medicine and biology. Springer, Berlin, pp 308–321
Meena GS, Gupta S, Majumdar GC, Banerjee R (2011) Growth characteristics modelling of Bifidobacterium bifidum using RSM and ANN. Braz Arch Biol Technol 54:1357–1366
Bhadoria PBS, Mahapatra SC (2011) Prospects, technological aspects and limitations of probiotics – a worldwide review. Eur J Food Res Rev 1:23–42
Philippe D, Heupel E, Blum-Sperisen S, Riedel CU (2011) Treatment with Bifidobacterium bifidum 17 partially protects mice from Th1-driven inflammation in a chemically induced model of colitis. Int J Food Microbiol 149:45–49
Jalili H, Razavi SH, Safari M, Malcata FX (2009) Enhancement of growth rate and β-galactosidase activity, and variation in organic acid profile of Bifidobacterium animalis subsp. lactis Bb 12. Enz Microb Technol 45:469–476
Kabeerdoss J, Devi RS, Mary RR, Prabhavathi D, Vidya R, Mechenro J, Mahendri NV, Pugazhendhi S, Ramakrishna BS (2011) Effect of yoghurt containing Bifidobacterium lactis Bb12® on faecal excretion of secretory immunoglobulin A and human beta-defensin 2 in healthy adult volunteers. Nutr J 23; 10:138.
Su P, Henriksson A, Mitchell H (2007) Selected prebiotics support the growth of prebiotic mono-cultures in vitro. Anaerobe 13:134–139
Siro I, Kápolna E, Kápolna B, Lugasi A (2008) Functional food: product development, marketing and consumer acceptance – a review. Appetite 51:456–467
Mayer HK, Amtmann E, Philippi E, Steinegger G, Mayrhofer S, Kneifel W (2007) Molecular discrimination of new isolates of Bifidobacterium animalis subsp lactis from reference strains and commercial probiotic strains. Int Dairy J 17:565–573
Bonannoxs A (2012) Some like it healthy: demand for functional and conventional yogurts in the Italian market. Agribusiness 28:67–85
Grmanová M, Vlková E, Rada V, Homutová I (2010) Survival of Bifidobacteria in adult intestinal tract. Folia Microbiol 55:281–285
Kopećnỳ J, Mrázek J, Killer J (2010) The presence of Bifidobacteria in social insects, fish and reptiles. Folia Microbiol 55:336–339
Buchanan RE (1974) Bergey’s manual of determinative bacteriology, 8th edn. NEE Gibbons, Williams and Wilkins, Baltimore
Mitsuoka T (1992) The human gastrointestinal tract. In: Wood BJB (ed) The lactic acid bacteria in health and disease. Elsevier, Amsterdam, pp 69–114
Reimann S, Grattepanche F, Benz R, Mozetti V, Rezzonico E, Berger B, Lacroix C (2011) Improved tolerance to bile salts aggregated Bifidobacterium longum produced during continuous culture with immobilized cells. Bioresour Technol 102:4559–4567
Bottacini F, Ventura M, van Sinderen D, Motherway MO (2014) Diversity, ecology and intestinal function of bifidobacteria. Microb Cell Fact 13(Suppl 1):S4
Ventura M, van Sinderen D, Fitzgerald GF, Zink R (2004) Insights into the taxonomy, genetics and physiology of bifidobacteria. Antoine Van Leeuwenhoek 86:205–223
Ventura M, Canchaya C, Dei Casale A, Dellaglio F, Neviani E, Fitzgerald GF, van Sinderen D (2006) Analysis of bifidobacterial evolution using a multilocus approach. Int J Syst Evol Microbiol 56:2783–2792
Hughes D, Hoover DG (1991) Bifidobacteria their potential for use in American dairy products. J Food Technol 45:74–80
Kim HS (1988) Characterization of lactobacilli and bifidobacteria as applied to dietary adjuncts. Cult Dair Prod J 23:6–9
Ballongue J (1998) Bifidobacteria and probiotic action. In: Salminen S, von Wright A (eds) Lactic Acid Bacteria. Marcel Dekker, New York, pp 519–587
Chen B, Wang X, Zhang L (2010) Culture medium for Bifidobacterium longum, composition comprising the same and preparation method. USP, US 2010/0098667 A1
Mandar R, Mikelsaar M (1996) Transmission of mother’s microflora to the newborn at birth. Biol Neonate 96:30–35
Huurre A, Kalliomaki M, Rautava S, Rinne M, Salminen S, Isolauri E (2008) Mode of delivery on gut microbiota and humoral immunity. Neonatol 93:236–240
Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. PNAS 107:11971–11975
Othman NZ, El Enshasy HA, Abdel Malek R, Sarmidi MR, Aziz RA (2009) Kinetics of cell growth and functional characterization of probiotic strains Lactobacillus delbrueckii and Lactobacillus paracasei isolated from breast milk. Deut Lebensmittel Rund 105:444–450
Elsayed EA, Othman NZ, Malek R, Tang T, El Enshasy HA (2014) Improvement of cell mass production of Lactobacillus delbrueckii sp. bulgaricus WICC-B-02: a newly isolated probiotic strain from mother’s milk. J Appl Pharmceut Sci 4:8–14
Solís G, de los Reyes-Gavilan CG, Fernández N, Margolles A, Gueimonde M (2010) Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe 16:307–310
Gueimonde M, Laitinen K, Salminen S, Isolauri E (2007) Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology 92:64–66
Putignani L, Del Chierico F, Petrucca A, Vernocchi P, Dallapiccola B (2014) The human gut microbiota: a dynamic interplay with the host from birth to senescence settled during childhood. Pediat Res 76:2–10
Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1402
Harmsen HJM, Wildeboer-Veloo ACM, Raangs GC, Wagendorp AA, Klijn N, Bindels JG (2000) Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30:61–67
Hopkins MJ, Cummings JH, Macfarlane GT (1998) Inter-species differences in maximum specific growth rates and cell yields of Bifidobacteria cultured on oligosaccharides and other simple carbohydrate sources. J Appl Microbiol 85:381–386
Reuter G (2001) The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. Curr Issues Intest Microbiol 2:43–53
Lacroix C, Yildirim S (2007) Fermentation technologies for the production of probiotics with high viability and functionality. J Biotechnol 18:176–183
Shimamura S, Abe F, Ishibashi N, Miyakawa H, Yaeshima T, Tomita M (1990) Endogenous oxygen uptake and polysaccharide accumulation in Bifidobacterium. Agric Biol Chem 54:2869–2874
Simpson PJ, Stanton C, Fitzgerald OF, Ross RP (2005) Intrinsic tolerance of Bifidobacterium longum species to heat and following spray drying and storage. J Appl Microbiol 99:493–501
Andriantsoanirina V, Allano S, Butel MJ, Aries J (2013) Tolerance of Bifidobacterium human isolates to bile, acid and oxygen. Anaerobe 21:39–42
Meile L, Ludwig W, Rueger U, Gut C, Kaufmann P, Dasen G, Wenger S, Teuber M (1997) Bifidobacterium lactis sp. nov., a moderately oxygen tolerant species isolated from fermented milk. Syst Appl Microbiol 20:57–64
Ninomiya K, Matsuda K, Kawahat T, Kanaya T, Kohno M, Katakura Y, Masanori A, Shioya S (2009) Effect of CO2 concentration on the growth and exopolysaccharide production of Bifidobacterium longum cultivated under anaerobic conditions. J Biosci Bioeng 107:535–537
Kleerebezem M, Vaughan EE (2009) Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 63:269–290
Tanaka H (2000) Bile salts hydrolase of Bifidobacterium longum-biochemical and genetic characterization. Appl Environ Microbiol 66:2502–2512
Krasaekoopt W, Bhandari B, Deeth H (2004) The influence of coating materials on some properties of alginate beads and survivability of microencapsulated probiotic bacteria. Int Dairy J 14:737–743
Takahashi N, Xiao JZ, Miyaji K, Yaeshiima T, Hiramatsu A, Iwatsuki K, Kokubo S, Hosono A (2004) Selection of acid tolerant bifidobacteria and evidence for a low-pH-inducible acid tolerance response in Bifidobacterium longum. J Dairy Res 71:340–345
Tham CSC, Peh KK, Bhat R, Liong MT (2011) Probiotic properties of bifidobacteria and lactobacilli isolated from local dairy products. Ann Microbiol 62:1079–1087
Sonnenburg ED, Sonnenburg JL, Manchester JK, Hansen EE, Chiang HC, Gordon JI (2006) A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing in vivo to carbohydrate metabolism. Proc Natl Acad Sci USA 103:8834–8839
Rautava S, Walker WA (2007) Commensal bacteria and epithelial cross talk in the developing intestine. Curr Gastroenterol Rep 9:385–392
Guglielmetti S, De Noni I, Caracciolo F, Molinari F, Parini C, Mora D (2008) Bacterial cinnamoyl esterase activity screening for the production of a novel functional food product. Appl Environ Microbiol 74:1284–1288
Serafini F, StratiF R-MP, Turroni F, Foroni E, Duranti S, Milano F, Perotti A, Viappiani A, Guglielmetti S, Buschini A, Margolles A, van Sinderen D, Ventura M (2013) Evaluation of adhesion properties and antibacterial activities of the infant gut commensal Bifidobacterium bifidum PRL2010. Anaerobe 21:9–17
Rahman MM, Kim W-S, Kumura H, Shimazaki K-I (2008) Auto aggregation and surface hydrophobicity of bifidobacteria. World J Microbiol Biotechnol 24:1593–1598
O’Connell Motherway M, Zomer A, Leathy SC, Reunanen J, Bottacini F, Claesson MJ, O’Brien F, Flynn K, Casey PG, Munoz JAM, Bearney B, Houston AM, O’Mahony C, Higgins DG, Shanahan F, Palva A, de Vos WM, Fitzgerald GF, Ventura M, O’Toole PW, van Sinderen D (2011) Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci USA 108:11217–11222
Fanning S, Hall IJ, Cronin M, Zomer A, MacSharry J, Goulding D, Motherway MO, Shanahan F, Nally K, Dougan K, Dougan G, van Sinderen D (2012) Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci USA 109:2108–2113
Fanning S, Hall LJ, van Sinderen D (2012) Bifidobacterium breve UCC2003 surface exopolysaccharide production is a beneficial trait mediating commensal-host interaction through immune modulation and pathogen protection. Gut Microbes 3:420–425
Hidalgo-Cantabrana C, Sánchez B, Milani C, Ventura M, Margolles A, Ruas-Madiedo P (2014) Genomic overview and biological function of exopolysaccahride biosynthesis in Bifodobacterium spp. Appl Env Microbiol 80:9–18
Ebhodaghe SO, Abiose SH, Adeniran HA (2012) Assessment of physico-chemical characteristics, viability and inhibitory effect of Bifidobacteria in soymilk. J Food Res 1:159–170
Cheikhyoussef A, Cheikhyoussef N, Chen H, Zhao J, Tang J, Zhang H, Chen W (2010) Bifidin 1 - a new bacteriocin produced by Bifidobacterium infantis BCRC 14602: purification and partial amino acid sequence. Food Control 21:746–753
Yildirim Z, Winters D, Johnson M (1999) Purification, amino acid sequence and mode of action of bifidocin B produced by Bifidobacterium bifidum NCFB 1454. J Appl Microbiol 86:45–54
Lee JH, Li X, O’Sullivan DJ (2011) Transcription analysis of a lantibiotic gene cluster from Bifidobacterium longum DJO10A. Appl Environ Microbiol 77:5879–5887
Martinez FAC, Balciunas EM, Converti A, Cotter PD, de Souza Oliveira RP (2013) Bacteriocin production by Bifidobacterium spp. A review. Biotechnol Adv 31:482–488
Arora M, Sharma S, Baldi A (2013) Comparative insight of regulatory guidelines for probiotics in USA, India and Malaysia: a critical review. Int J Biotechnol Well Ind 2:51–64
Talwalkar A, Kailasapathy K (2004) A review of oxygen toxicity in probiotic yogurts: influence on the survival of probiotic bacteria and protective technique. Comp Rev Food Sci Food Safety 13:117–124
Guarner F, Malagelada JR (2003) Gut flora in health and disease. Lancet 361:512–519
Jose NM, Bunt CR, Hussain MA (2015) Comparison of microbiological and probiotic characteristics of Lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms 3:198–212
Vandamme TF, Lenourry A, Charrueau C, Chaumeil J-C (2002) The use of polysaccharides to target drugs to the colon. Carbohyd Polym 48:219–231
Fallingborg J (1999) Intraluminal pH of the human gastrointestinal tract. Dan Med Bull 46:183–196
Mozzetti V, Grattepanche F, Moine D, Berger B, Rezzonico E (2010) New method for selection of hydrogen peroxide adapted bifidobacteria cells using continuous culture and immobilized cell technology. Microb Cell Fact 9:60
Lui LS, Fishman ML, Kost J, Hicks KB (2003) Pectin-based systems for colon specific drug delivery via oral route. Biomaterials 24:3333–3343
Gomes AMP, Malcata FX (1999) Bifidobacterium sp. and Lactobacillus acidophilus: biological, biochemical, technological and therapeutical properties relevant for use as probiotics. Trends Food Sci Technol 10:139–157
Singh J (1997) Bifidobacterium longum, a lactic acid-producing intestinal bacterium inhibits colon cancer and modulates the intermediate biomarkers of colon carcinogenesis. Carcinogenesis 18:833–841
Her SL, Duan KJ, Sheu DC, Lin CT (2004) A repeated batch process for cultivation of Bifidobacterium longum. J Ind Microbiol Biotechnol 31:427–432
O’Mahony D, Murphy S, Boileau T, Park JS, O’Brien F, Groeger D, Konileczna P, Ziegler M, Scully P, Shanahan F, Kiely B, O’Mahony L (2010) Bifidobacterium animalis AHC7 protects against pathogen-induced NF-κB activation in vivo. BMC Immunol 11:63
Donkor ON, Vasiljevic T, Gill HS (2010) Probiotics and immunomodulation. In: Watson RR, Zibadi S, Preedy VR (eds) Dietary components and immune function, Nutrition and Health Series. Springer, New York, pp 625–655
Ashraf R, Shah NP (2014) Immune system stimulation by probiotic microorganisms. Crit Rev Food Sci Nutr 54:938–956
Tannock GW (2004) A special fondness for Lactobacilli. Appl Environ Microbiol 70:3189–3194
Reid G (1999) The scientific basis for probiotic strains of Lactobacillus. Appl Environ Microbiol 65:3763–3766
Cryan JF, O’Mahony SM (2011) The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 23:187–192
Mayer EA (2011) Gut feelings: the emerging biology of gut-brain communication. Nat Rec Neurosci 12:453–466
Mayer EA, Knight R, Mazmanian SK, Gryan JF, Tillisch K (2014) Gut microbes and the brain: paradigm shift in neuroscience. J Neurosci 34:15490–15496
Bruce-Keller AJ, Salbaum JM, Luo M, Blanchard E IV, Taylor CM, Welsh DA, Berthoud HR (2015) Obese-type gut microbiota induce neurobehavioral changes in the absence of obesity. Biol Psychiatry 77:607–615
Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG (2008) The probiotic Bifidobacterium infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 43:164–174
Langkamp-Henken B, Rowe CC, Ford AL, Christman MC, Nieves C Jr, Khouri L, Specht GJ, Girard SA, Spaiser SJ, Dahl WJ (2015) Bifidobacterium bifidum R0071 results in a greater proportion of healthy days and a lower percentage of academically stressed students reporting a day of cold/flu: a randomized, double-blind, placebo-controlled study. Brit J Nutr 113:426–434
Hsiao EY (2014) Gastrointestinal issues in autism spectrum disorder. Harvard Rev Psych 22:104–111
Critchfield JW, van Hemert S, Ash M, Mulder L, Ashwood P (2011) The potential role of probiotics in the management of childhood autism spectrum disorders. Gastroenterol Res Pract 2011:161358
Iemoli E, Trabattoni D, Parisotto S, Borgonovo L, Toscano M, RizzaridiniG CM, Ricci E, Fusi A, De Vecchi E, Piconi S, Drago L (2012) Probiotics reduce gut microbial translocation and improve adult atopic dermatitis. J Clin Gastroenterol 46(Suppl):S33–S40
Yoshida Y, Seki T, Matsunaka H, Watanabe T, Shindo M, Yamada N, Yamamoto O (2010) Clinical effects of probiotic Bifidobacterium breve supplementation in adult patients with atopic dermatitis. Yonago Acta Medica 53:37–45
De Vrese M, Schrezenmeir J (2008) Probiotics, prebiotics, and synbiotics. Adv Biochem Eng/Biotechnol 111:1–66
Wang Y-C, Yu R-C, Chou C-C (2002) Growth and survival of bifidobacteria and lactic acid bacteria during the fermentation and storage of cultured soymilk drinks. Food Microbiol 19:501–508
Lin DC (2003) Probiotics as functional foods. Nutr Clin Pract 18:497–506
Gill H, Guarner F (2004) Probiotics and human health: a clinical perspective. Postgrad Med J 80:516–526
De Vrese M (2003) Effects of probiotic bacteria on gastrointestinal symptoms, Helicobacter pylori activity and antibiotics-induced diarrhoea. Gastroenterol 124:A560
Kwon SG, Son JW, Kim HJ, Park CS, Lee JK, Ji GE, Oh DK (2006) High concentration cultivation of Bifidobacterium bifidum in a submerged membrane bioreactor. Biotechnol Prog 22:1591–1597
Zampa A, Silvi S, Fabiani R, Morozzi G, Orpianesi C, Cresci A (2004) Effects of different digestible carbohydrates on bile acid metabolism and SCFA production by human gut micro-flora grown in an in vitro semi-continuous culture. Anaerobe 10:19–26
Martin R, Miquel S, Ulmer J, Kechaou N, Langella P, Bermúdez-Humaran LG (2013) Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease. Microb Cell Fact 12:71
LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 24:160–168
Gibson GR, Wang X (2008) Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J Appl Bacteriol 77:412–420
Jeon SG, Kayama H, Ueda Y, Takahashi T, Asahara T, Tsuji H, Tsuji NM, Kiyono H, Ma JS, Kusu T, Okumura R, Hara H, Yoshida H, Yamamoto M, Momoto T (2012) Probiotic Bifidobacterium breve induces IL-10-producing Tr1 cells in the colon. PLOS Pathog 8(5), e1002714
Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG (2010) Effects of the probiotic Bifodobacterium infantis in the materials separation model of depression. Neuroscience 170:1179–1188
Kaplan H, Hutkins RW (2000) Fermentation of fructooligosaccharides by lactic acid bacteria and Bifidobacteria. Appl Environ Microbiol 66:2682–2684
Han R, Ebert EC, Zhao Z, Li L, Zhang H, Ian R (2005) Novel characteristics of Bifidobacterium bifidum in solid state fermentation system. World J Micrbiol Biotechnol 21:1245–1248
Yu Z, Dong B, Lu W (2009) Dynamics of bacterial community in solid state fermented feed revealed by 16S rRNA. Lett Appl Microbiol 49:166–172
Rodriguez de Olmos A, Bru E, Garro MS (2015) Optimization of fermentation parameters to study the behavior of selected lactic cultures on soy solid state fermentation. Int J Food Microbiol 196:16–23
Kouya T, Ishiyama Y, Tanaka T, Taniguchi M (2013) Evaluation of positive interaction for cell growth between Bifidobacterium adolescentis and Propionibacterium freudenreichii using a co-cultivation system with two microfiltration modules. J Biosci Bioeng 115:189–192
Oliveira RPS, Perego P, Oliveira MN, Converti A (2012) Growth, organic acids profile and sugar metabolism of Bifidobacterium lactis in co-culture with Streptococcus thermophilus: the inulin effect. Food Res Int 48:21–27
Hsu CA, Yu RC, Lee SL, Chou CC (2007) Cultural condition affecting the growth and production of β-galactosidase by Bifidobacterium longum CCRC 15708 in a jar fermenter. Int J Food Microbiol 116:186–189
Doleyres Y (2002) Bifidobacterium longum ATCC 15707 Cell Production during free and immobilized cell cultures in MRS-whey permeate medium. Appl Microbiol Biotechnol 60:168–173
Roy D (2001) Media for the isolation and enumeration of bifidobacteria in dairy products. Int J Food Microbiol 69:167–182
Amaretti A, Bernardi T, Tamburini E, Zanoni S, Lomma M, Matteuzzi D, Rossi M (2007) Kinetics and metabolism of Bifidobacterium adolescentis MB 239 growing on glucose, galactose, lactose and galactooligosaccharides. Appl Environ Microbiol 73:3637–3644
Mlobeli NT, Gutierrez NA, Maddox IS (1998) Physiology and kinetics of Bifidobacterium bifidum during growth on different sugars. Appl Microbiol Biotechnol 50:125–128
Parche S, Amon J, Jankovic I, Rezzonico E, Beleut M, Barutçu H, Schendel I, Eddy MP, Burkovski A, Arigoni F, Titgemeyer F (2007) Sugar transport system of Bifidobacterium longum NCC2705. J Mol Microbiol Biotechnol 12:9–19
Kim TB, Song SH, Kang SC, Oh DK (2003) Quantitative comparison of lactose and glucose utilization in Bifidobacterium longum cultures. Biotechnol Prog 19:672–675
Etoh S, Sonomoto K, Ishizaki A (1999) Complementary effects of bifidogenic growth stimulators and ammonium sulfate in natural rubber serum powder on Bifidobacterium bifidum. J Biosci Biotechnol Biochem 63:627–631
Mayo B, Aleksandrzak-Piekarczyk T, Fernández M, Kowalczyk M, Pablo Álvarez-Martín P, Bardowski J (2010) Updates in the metabolism of lactic acid bacteria. In: Mozzi F, Raya RR, Vignolo GM (eds) Biotechnology of lactic acid bacteria: novel applications. Wiley-Blackwell, Iowa, pp 3–33
Fandi KG, Ghazali HM, YazidAM RAR (2001) Purification and N-terminal amino acid sequence of fructose-6-phosphate phosphoketolase from Bifidobacterium longum BB536. Lett Appl Microbiol 32:235–239
Pokusaeva K, Motherway MO, Zomer A, MacSharry J, Fitzgerald GF, Sinderen DV (2011) Cellodextrin utilization by Bifidobacterium breve UCC2003. Appl Environ Microbiol 77:1681–1690
Scardovi V (1986) Bifidobacterium. In: Sneath PH, Mair NS, Sharpe ME, Holt JG (eds) Bergey's Manual of Systematic Bacteriology, vol 2, 9th edn. Williams and Wilkins, Baltimore, p 1418
de Vries W, Stouthamer AH (1967) Pathway of glucose fermentation in relation to the taxonomy of Bifidobacteria. J Bacteriol 93:574–576
Cronin M, Ventura M, Fitzgerald GF, Sinderen DV (2011) Progress in genomics, metabolism, and biotechnology of bifidobacteria. Int J Food Microbiol 149:4–18
Gonzalez R, Blancas A, Santillana R, Azaola A, Wacher C (2004) Growth and final product formation by Bifidobacterium infantis in aerated fermentations. Appl Microbiol Biotechnol 65:606–610
Shene C, Mardones M, Zamora P, Bravo S (2005) Kinetics of Bifidobacterium longumATCC 15707 fermentations: effect of the dilution rate and carbon source. Appl Microbiol Biotechnol 67:623–630
Biavati B, Vescovo M, Torriani S, Bottazzi V (2000) Bifidobacteria: history, ecology, physiology and applications. Annals Microbiol 50:117–132
Nguyen TMP, Lee YK, Zhou W (2012) Effect of high intensity ultrasound on carbohydrate metabolism of bifidobacteria in milk fermentation. J food Chem 130:866–874
Caescu CI, Vidal O, Krzewinski F, Artenie V, Bouquelet S (2004) Bifidobacterium longum requires a fructokinase (Frk; ATP:D-fructorse 6-phosphotransferase, EC 2.7.1.4) for fructose catabolism. J Bacteriol 186:6515–6525
Thitaram SN, Siragusa GR, Hinton A Jr (2005) Bifidobacterium-selective isolation and enumeration from chicken caeca by a modified oligosaccharide antibiotic-selective agar medium. Lett Appl Microbiol 41:355–360
Poch M, Bezkorovainy A (1988) Growth-enhancing supplements for various species of the genus Bifidobacterium. J Dairy Sci 71:3214–3221
Giridhar R, Srivastava AK (2000) Fed-batch sorbose fermentation using pulse and multiple feeding strategies for productivity improvement. Biotechnol Bioprocess Eng 5:340–344
Guerra NP, Agrasar AT, Macias CL, Bernardez PF, Castro LP (2007) Dynamic mathematical models to describe the growth and nisin production by Lactococcuslactis subsp. lactis CECT 539 in both batch and re-alkalized fed-batch cultures. J Food Eng 82:103–113
Parada JL, Caron CR, Medeiros ABP, Soccol CR (2007) Bacteriocins from lactic acid bacteria: purification, properties and use as biopreservatives. Braz Arch Biol Technol 50:521–542
Jung I, Oh MK, Cho YC, Kong IS (2011) The viability to a wall shear stress and propagation of Bifidobacterium longum in the intensive membrane bioreactor. Appl Microbiol Biotechnol 92:939–949
Song S-H, Kim T-B, Oh H-I, Oh D-K (2003) Optimization of Bifidobacterium longum growth by use of calcium carbonate-alginate beads. World J Microbiol Biotechnol 19:727–731
Jalili H, Razavi H, Safari M, Amrane A (2010) Kinetic analysis and effect of culture medium and coating materials during free and immobilized cell cultures of Bifidobacterium animalis subsp. lactis Bb 12. Electron J Biotechnol 13:(3)http://www.ejbiotechnology.info/content/vol13/issue3/full/4/(2010)
Jalili H, Balannec B, Razavi H, Amrane A (2011) Unstructured model for free and immobilized cell culture without pH control of Bifidobacterium animalis subsp. lactis Bb 12-inhibitory effect of the undissociated organic acids. Biochem Eng J 58–59:184–188
Kongo JM, Gomes AM, Malcata FX (2006) Manufacturing of fermented goat milk with a mixed starter culture of Bifidobacterium animalis and Lactobacillus acidophilus in a controlled bioreactor. Lett Appl Microbiol 42:595–599
Mathys S, Meile L, Lacroix C (2009) Co-cultivation of a bacteriocin-producing mixed culture of Bifidobacterium thermophilum RBL67 and Pediococcus acidilactici UVA1 isolated from baby faeces. J Appl Microbiol 107:36–46
Goderska K (2012) Different methods of probiotics stabilization. In: Rigobelo EC (ed) Probiotics. InTech, Rijeka. doi:10.5772/50313
Meng XC, Stanton C, Fitzgerald GF, Daly C, Ross RP (2008) Anhydrobiotics: the challenges of drying probiotic cultures. Food Chem 106:1406–1416
Tymczyszyn EE, Diaz R, Pataro A, Sandonato N, Gomez-Zavaglia A, Disalvo EA (2008) Critical water activity for the preservation of Lactobacillus bulgaricus by vacuum drying. Int J Food Microbiol 128:342–347
Forest P, Kulozik U, Schmitt M, Bauer S, Santivarangkna C (2012) Storage stability of vacuum-dried probiotic bacterium Lactobacillus paracasei F19. Food Bioprod Process 90:295–300
Bauer SAW, Schneider S, Behr J, Kulozik U, Foerst P (2012) Combined influence of fermentation and drying conditions on survival and metabolic activity of starter and probiotic cultures after low-temperature vacuum drying. J Biotechnol 159:351–357
Nag A, Das S (2013) Improving ambient temperature stability of probiotics with stress adaptation and fluidized bed drying. J Func Foods 5:170–177
To BCS, Etzel MR (1997) Spray drying, freeze drying, or freezing of three different lactic acid bacteria species. J Food Sci 62:576–585
Saarela M, Virkajärvi I, Alakomi H-L, Mattila-Sandholm T, Vaari A, Suomalainen T, Mättö J (2005) Influence of fermentation time, cryoprotectant and neutralization of cell concentrate on freeze-drying survival, storage stability, and acid and bile exposure of Bifodobacterium animalis ssp. lactis cells produced without milk-based ingredients. J Appl Microbiol 99:1330–1339
Burns P, Vinderola G, Molinari F, Reinheimer J (2008) Suitability of whey and buttermilk for the growth and frozen storage of probiotic lactobacilli. Int J Dairy Technol 61:156–164
Celik OF, O’Sullivan JO (2013) Factors influencing the stability of freeze-dried stress-resilient and stress-sensitive strains of bifidobacteria. J Dairy Sci 96:3506–3516
Yang C, Zhu X, Fan D, Mi Y, Luo Y, Hui J, Su R (2012) Optimizing the chemical composition of protective agents for freeze-drying Bifidobacterium longum BIOMA 5920. Chin J Chem Eng 20:930–936
Modesto M, Mattarelli P, Biavati B (2004) Resistance to freezing and freeze-drying storage processes of potential probiotic bifidobacteria. Ann Microbiol 54:43–48
Bruno FA, Shah NP (2003) Viability of two freeze-dried strains of Bifidobacterium and of commercial preparation at various temperatures during prolonged storage. J Food Sci 68:2336–2339
Teixeria P, Castro H, Mohacsi-Frakas C, Kirby R (1997) Identification of sites of injury in Lactobacillus bulgaricus during heat stress. J Appl Microbiol 83:219–226
Linders LJM, Kets EPW, de Bont JAM, van’t Riet van K (1998) Combined influence of growth and drying conditions on the activity of dried Lactobacillus plantarum. Biotechnol Prog 14:537–539
Behdoudi-Jobbehdar S, Soukoulis C, Yonekura L, Fisk I (2013) Optimization of spray-drying process conditions for the production of maximally viable microencapsulated L. acidophilus NCIMB 701748. Drying Technol 31:1274–1283
Shokri Z, Fazeli MR, Ardjmand M, Mousavi SM, Gilani K (2015) Factors affecting viability of Bifidobacterium bifidum during spray drying. Daru 23:7
Corcoran BM, Ross RP, Fitzgerald GF, Stanton C (2004) Comparative survival of probiotic lactobacilli spray-dried in the presence of prebiotic substances. J Appl Microbiol 96:1024–1039
Prasad J, McJarrow P, Gopal P (2003) Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl Environ Microbiol 69:917–925
Santivarangkna C, Kulozika U, Poerst P (2007) Alternative drying processes for the industrial preservation of lactic acid starter cultures. Biotechnol Prog 23:302–315
Shamekhi F, Shuhaimi M, Ariff A, Manap YA (2013) Cell viability of microencapsulated Bifidobacterium animalis subsp. lactis under freeze-drying, storage and gastrointestinal tract simulation conditions. Folia Microbiol 58:91–101
Dianawati D, Shah NP (2011) Survival, acid and bile tolerance, and surface hydrophobicity of microencapsulated B. animalis ssp. lactis Bb12 during storage at room temperature. J Food Sci 76:M592–M599
Ding WK, Shah NP (2007) Acid, bile, and heat tolerance of free and microencapsulated probiotic bacteria. J Food Sci 72:M446–M450
Weinbreck F, Bodnár I, Marco ML (2010) Can encapsulation lengthen the shelf-life of probiotic bacteria in dry products? Int J Food Microbiol 136:364–367
Pop OL, Brandau T, Vodnar DC, Socaciu C (2012) Study of Bifidobacterium lactis 300b survival during encapsulation, coating and freeze-drying process and the release in alkaline media. Bull Univ Agric Sci Vet Med 69:372–379
Zhang F, Li XY, Park HJ, Zhao M (2013) Effect of microencapsulation methods on the survival of freeze-dried Bifidobacterium bifidum. J Microencapsul 30:511–518
Lian WC, Hsiao HC, Chou CC (2002) Survival of bifidobacteria after spray drying. Int J Food Biotechnol 74:79–86
Dianawati D, Shah NP (2011) Enzyme stability of microencapsulated Bifidobacterium animalis ssp. lactis Bb12 after freeze-drying and during storage in low water activity at room temperature. J Food Sci 76:M463–M471
Dianawati D, Mishra V, Shah NP (2012) Role of calcium alginate and mannitol in protecting Bifidobacterium. Appl Env Microbiol 78:6914–6921
Fávaro-Trindade CS, Grosso CR (2002) Microencapsulation of Lactobacillus acidophilus and Bifobacterium lactis and evaluation of their survival at pH values of the stomach and in bile. J Microencapsul 19:485–494
Saarela M, Rantala M, Hallamaa K, Nohynek L, Virkahärvi I, Mättö J (2004) Stationary phase acid and heat treatments for improvement of the viability of probiotic lactobacilli and bifidobacteria. J Appl Microbiol 96:1205–1214
Savijoki K, Suokko A, Palva A, Valmu L, Kalkkinen N, Varmanen P (2005) Effect of heat-shock and bile salts on protein synthesis of Bifodobacterium longum revealed by (35S) methionine labelling and two dimensional gel electrophoresis. FEMS Microbiol Lett 248:207–215
Ventura M, Canchaya C, Zhang Z, Fitzgerald GF, van Sinderen D (2007) Molecular characterization of hsp20, encoding a small heat shock protein of Bifidobacterium breve UCC2003. Appl Environ Microbiol 73:4695–4703
Ruiz L, Ruas-Madiedo P, Gueimonde M, de los Reyes-Gavilán CG, Margolles A, Sánchez B (2011) How do bifidobacteria counteract environmental challenges? Mechanisms involved and physiological consequences. Genes Nutr 6:307–318
Nguyen HT, Razafindralambo H, Blecker C, N’Yapo C, Thonart P, Delvigne F (2014) Stochastic exposure to sub-lethal high temperature enhances exopolysaccharides (EPS) excretion and improves Bifidobacterium bifidum cell survival to freeze-drying. Biochem Eng J 88:85–94
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
El Enshasy, H., Malik, K., Malek, R.A., Othman, N.Z., Elsayed, E.A., Wadaan, M. (2016). Anaerobic Probiotics: The Key Microbes for Human Health. In: Hatti-Kaul, R., Mamo, G., Mattiasson, B. (eds) Anaerobes in Biotechnology. Advances in Biochemical Engineering/Biotechnology, vol 156. Springer, Cham. https://doi.org/10.1007/10_2015_5008
Download citation
DOI: https://doi.org/10.1007/10_2015_5008
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-45649-2
Online ISBN: 978-3-319-45651-5
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)