Abstract
Propionibacteria are actinobacteria consisting of two principal groups: cutaneous and dairy. Cutaneous propionibacteria are considered primary pathogens to humans, whereas dairy propionibacteria are widely used in the food and pharmaceutical industries. Increasing attention has been focused on improving the performance of dairy propionibacteria for the production of industrially important chemicals, and significant advances have been made through strain engineering and process optimization in the production of flavor compounds, nutraceuticals, and antimicrobial compounds. In addition, genome sequencing of several propionibacteria species has been completed, deepening understanding of the metabolic and physiological features of these organisms. However, the metabolic engineering of propionibacteria still faces several challenges owing to the lack of efficient genome manipulation tools and the existence of various types of strong restriction-modification systems. The emergence of systems and synthetic biology provides new opportunities to overcome these bottlenecks. In this review, we first introduce the major species of propionibacteria and their properties and provide an overview of their functions and applications. We then discuss advances in the genome sequencing and metabolic engineering of these bacteria. Finally, we discuss systems and synthetic biology approaches for engineering propionibacteria as efficient and robust cell factories for the production of industrially important chemicals.
Similar content being viewed by others
References
Ali MN, Mohd MK (2011) Enhancement in vitamin B12 production by mutant strains of Propionibacterium freudenreichii. Int J Eng Sci 3:4921–4925
Ammar EM, Wang Z, Yang ST (2013) Metabolic engineering of Propionibacterium freudenreichii for n-propanol production. Appl Microbiol Biotechnol 97:4677–4690
Barbirato F, Chedaille D, Bories A (1997) Propionic acid fermentation from glycerol: comparison with conventional substrates. Appl Microbiol Biotechnol 47:441–446
Barefoot SF, Ratnam P (1999) Composition and method for treating acne. US Patents 5,981,473
Barker BM, Kroll K, Vödisch M, Mazurie A, Kniemeyer O, Cramer RA (2012) Transcriptomic and proteomic analyses of the Aspergillus fumigatus hypoxia response using an oxygen-controlled fermenter. BMC Genomics 13:62–86
Bernard K, Shuttleworth L, Munro C, Forbes-Faulkner J, Pitt D, Norton J, Thomas A (2002) Propionibacterium australiense sp. nov. derived from granulomatous bovine lesions. Anaerobe 8:41–47
Beuvier E, Berthaud K, Cegarra S, Dasen A, Pochet S, Buchin S, Duboz G (1997) Ripening and quality of Swiss-type cheese made from raw, pasteurized or microfiltered milk. Int Dairy J 7:311–323
Blount BC, Mack MM, Wehr CM, MacGregor JT, Hiatt RA, Wang G, Wickramasinghe SN, Everson RB, Ames BN (1997) Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc Natl Acad Sci U S A 94:3290–3295
Boyaval P, Corre C (1987) Continuous fermentation of sweet whey permeate for propionic acid production in a CSTR with UF recycle. Biotechnol Lett 9:801–806
Brede DA, Faye T, Johnsborg O, Ødegård I, Nes IF, Holo H (2004) Molecular and genetic characterization of propionicin F, a bacteriocin from Propionibacterium freudenreichii. Appl Environ Microbiol 70:7303–7310
Brede DA, Faye T, Stierli MP, Dasen G, Theiler A, Nes IF, Meile L, Holo H (2005) Heterologous production of antimicrobial peptides in Propionibacterium freudenreichii. Appl Environ Microbiol 71:8077–8084
Britz T, Riedel K (1994) Propionibacterium species diversity in Leerdammer cheese. Int J Food Microbiol 22:257–267
Brüggemann H, Henne A, Hoster F, Liesegang H, Wiezer A, Strittmatter A, Hujer S, Dürre P, Gottschalk G (2004) The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305:671–673
Brzuszkiewicz E, Weiner J, Wollherr A, Thürmer A, Hüpeden J, Lomholt HB, Kilian M, Gottschalk G, Daniel R, Mollenkopf HJ (2011) Comparative genomics and transcriptomics of Propionibacterium acnes. PLoS ONE 6:e21581
Burgess C, Smid E, Rutten G, Van Sinderen D (2006) A general method for selection of riboflavin-overproducing food grade micro-organisms. Microbiol Cell Fact 5:24
Burgess CM, Smid EJ, van Sinderen D (2009) Bacterial vitamin B2, B11 and B12 overproduction: an overview. Int J Food Microbiol 133:1–7
Cardoso FS, Gaspar P, Hugenholtz J, Ramos A, Santos H (2004) Enhancement of trehalose production in dairy propionibacteria through manipulation of environmental conditions. Int J Food Microbiol 91:195–204
Cardoso FS, Castro RF, Borges N, Santos H (2007) Biochemical and genetic characterization of the pathways for trehalose metabolism in Propionibacterium freudenreichii, and their role in stress response. Microbiology 153:270–280
Carrondo MJ, Crespo JP, Moura M (1988) Production of propionic acid using a xylose utilizing Propionibacterium. Appl Biochem Biotechnol 17:295–312
Chamba J-F, Perreard É (2002) Contribution of propionic acid bacteria to lipolysis of Emmental cheese. Lait 82:33–44
Charfreitag O, Collins M, Stackebrandt E (1988) Reclassification of Arachnia propionica as Propionibacterium propionicus comb. nov. Int J Syst Bacteriol 38:354–357
Chen F, Feng XH, Xu H, Zhang D, Ouyang PK (2012) Propionic acid production in a plant fibrous-bed bioreactor with immobilized Propionibacterium freudenreichii CCTCC M207015. J Biotechnol 164:202–210
Chen F, Feng X, Liang J, Xu H, Ouyang P (2013) An oxidoreduction potential shift control strategy for high purity propionic acid production by Propionibacterium freudenreichii CCTCC M207015 with glycerol as sole carbon source. Bioprocess Biosyst Eng 36:1165–1176
Cheong DE, Lee H-I, So JS (2008) Optimization of electrotransformation conditions for Propionibacterium acnes. J Microbiol Meth 72:38–41
Chiliveri SR, Yeruva T, Panda SH, Linga VR (2010) Optimization of fermentation parameters for vitamin B12 production using Propionibacterium freudertreichii sub sp shermanii OLP-5 by Taguchi method. J Pure Appl Microbiol 4:647–658
Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823
Coral J, Karp SG, de Souza Vandenberghe LP, Parada JL, Pandey A, Soccol CR (2008) Batch fermentation model of propionic acid production by Propionibacterium acidipropionici in different carbon sources. Appl Biochem Biotechnol 151:333–341
Cousin FJ, Mater DD, Foligne B, Jan G (2011) Dairy propionibacteria as human probiotics: a review of recent evidence. Dairy Sci Technol 91:1–26
Dalmasso M, Aubert J, Briard-Bion V, Chuat V, Deutsch SM, Even S, Falentin H, Jan G, Jardin J, Maillard MB (2012a) A temporal-omic study of Propionibacterium freudenreichii CIRM-BIA1T adaptation strategies in conditions mimicking cheese ripening in the cold. PLoS ONE 7:e29083
Dalmasso M, Aubert J, Even S, Falentin H, Maillard M-B, Parayre S, Loux V, Tanskanen J, Thierry A (2012b) Accumulation of intracellular glycogen and trehalose by Propionibacterium freudenreichii under conditions mimicking cheese ripening in the cold. Appl Environ Microbiol 78:6357–6364
Deborde C, Corre C, Rolin D, Nadal L, De Certaines J, Boyaval P (1996) Trehalose biosynthesis in dairy Propionibacterium. J Magn Reson Anal 2:297–304
Ding M, Wang X, Yang Y, Yuan Y (2012) Comparative metabolic profiling of parental and inhibitors—tolerant yeasts during lignocellulosic ethanol fermentation. Metabolomics 8:232–243
Dishisha T, Alvarez MT, Hatti-Kaul R (2012) Batch- and continuous propionic acid production from glycerol using free and immobilized cells of Propionibacterium acidipropionici. Bioresour Technol 118:553–562
Downes J, Wade WG (2009) Propionibacterium acidifaciens sp. nov., isolated from the human mouth. Int J Syst Bacteriol 59:2778–2781
Doyle MP, Meng J (2006) Bacteria in food and beverage production. In: Dworkin M, Falkow S, Schleifer KH, Stackerbrandt E (eds) Prokaryotes. Springer, New York, pp 797–811
Ekinci F, Barefoot S (2006) Fed-batch enhancement of jenseniin G, a bacteriocin produced by Propionibacterium thoenii (jensenii) P126. Food Microbiol 23:325–330
Falentin H, Deutsch SM, Jan G, Loux V, Thierry A, Parayre S, Maillard MB, Dherbécourt J, Cousin FJ, Jardin J (2010) The complete genome of Propionibacterium freudenreichii CIRM-BIA1T, a hardy actinobacterium with food and probiotic applications. PLoS ONE 5:e11748
Faye T, Langsrud T, Nes IF, Holo H (2000) Biochemical and genetic characterization of propionicin T1, a new bacteriocin from Propionibacterium thoenii. Appl Environ Microbiol 66:4230–4236
Faye T, Brede DA, Langsrud T, Nes IF, Holo H (2002) An antimicrobial peptide is produced by extracellular processing of a protein from Propionibacterium jensenii. J Bacteriol 184:3649–3656
Faye T, Holo H, Langsrud T, Nes IF, Brede DA (2011) The unconventional antimicrobial peptides of the classical propionibacteria. Appl Microbiol Biotechnol 89:549–554
Feng X, Chen F, Xu H, Wu B, Li H, Li S, Ouyang P (2011) Green and economical production of propionic acid by Propionibacterium freudenreichii CCTCC M207015 in plant fibrous-bed bioreactor. Bioresour Technol 102:6141–6146
Fitz-Gibbon S, Tomida S, Chiu B-H, Nguyen L, Du C, Liu M, Elashoff D, Erfe MC, Loncaric A, Kim J (2013) Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Investig Dermatol 133:2152–2160
Foligne B, Breton J, Mater D, Jan G (2013) Tracking the microbiome functionality: focus on Propionibacterium species. Gut 62:1227–1228
Fujimura S, Nakamura T (1978) Purification and properties of a bacteriocin-like substance (acnecin) of oral Propionibacterium acnes. Antimicrob Agents Chemother 14:893–898
Gagnaire V, Piot M, Camier B, Vissers JP, Jan G, Léonil J (2004) Survey of bacterial proteins released in cheese: a proteomic approach. Int J Food Microbiol 94:185–201
Grinstead D, Barefoot S (1992) Jenseniin G, a heat-stable bacteriocin produced by Propionibacterium jensenii P126. Appl Environ Microbiol 58:215–220
Guan N, Liu L, Zhuge X, Xu Q, Li J, Du C, Chen J (2012) Genome-shuffling improves acid tolerance of Propionibacterium acidipropionici and propionic acid production. Adv Chem Res 15:143–152
Guan N, Liu L, H-d S, Chen RR, Zhang J, Li J, Du G, Shi Z, Chen J (2013) Systems-level understanding how Propionibacterium acidipropionici respond to propionic acid stress at the microenvironment levels: mechanism and application. J Biotechnol 167:56–63
Higaki S, Morohashi M, Yamagishi T (2003) Anti-lipase activity of unsei-in against Propionibacterium avidum in the human axilla. Int J Antimicrob Agents 21:597–599
Higashiyama T (2002) Novel functions and applications of trehalose. Pure Appl Chem 74:1263–1269
Himmi E, Bories A, Boussaid A, Hassani L (2000) Propionic acid fermentation of glycerol and glucose by Propionibacterium acidipropionici and Propionibacterium freudenreichii ssp. shermanii. Appl Microbiol Biotechnol 53:435–440
Holo H, Faye T, Brede DA, Nilsen T, Ødegård I, Langsrud T, Brendehaug J, Nes IF (2002) Bacteriocins of propionic acid bacteria. Lait 82:59–68
Honore A, Thorsen M, Skov T (2013) Liquid chromatography-mass spectrometry for metabolic footprinting of co-cultures of lactic and propionic acid bacteria. Anal Bioanal Chem 405:8151–8170
Horváth B, Hunyadkürti J, Vörös A, Fekete C, Urbán E, Kemény L, Nagy I (2012) Genome sequence of Propionibacterium acnes type II strain ATCC 11828. J Bacteriol 194:202–203
Hsu ST, Yang ST (1991) Propionic acid fermentation of lactose by Propionibacterium acidipropionici: effects of pH. Biotechnol Bioeng 38:571–578
Huang YL, Wu Z, Zhang L, Ming Cheung C, Yang ST (2002) Production of carboxylic acids from hydrolyzed corn meal by immobilized cell fermentation in a fibrous-bed bioreactor. Bioresour Technol 82:51–59
Hugenholtz J, Hunik J, Santos H, Smid E (2002) Nutraceutical production by propionibacteria. Lait 82:103–112
Hugenschmidt S, Schwenninger SM, Lacroix C (2011) Concurrent high production of natural folate and vitamin B12 using a co-culture process with Lactobacillus plantarum SM39 and Propionibacterium freudenreichii DF13. Process Biochem 46:1063–1070
Hunyadkürti J, Feltóti Z, Horváth B, Nagymihály M, Vörös A, McDowell A, Patrick S, Urbán E, Nagy I (2011) Complete genome sequence of Propionibacterium acnes type IB strain 6609. J Bacteriol 193:4561–4562
Imhof R, Glättli H, Bosset J (1995) Volatile organic compounds produced by thermophilic and mesophilic single strain dairy starter cultures. LWT Food Sci Technol 28:78–86
Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31:233–239
Jin Z, Yang ST (1998) Extractive fermentation for enhanced propionic acid production from lactose by Propionibacterium acidipropionici. Biotechnol Prog 14:457–465
Jore J, Van Luijk N, Luiten R, Van der Werf M, Pouwels P (2001) Efficient transformation system for Propionibacterium freudenreichii based on a novel vector. Appl Environ Microbiol 67:499–503
Khanal R (2004) Potential health benefits of conjugated linoleic acid (CLA): a review. Asian Aust J Anim 17:1315–1328
Kiatpapan P, Murooka Y (2001) Construction of an expression vector for propionibacteria and its use in production of 5-aminolevulinic acid by Propionibacterium freudenreichii. Appl Microbiol Biotechnol 56:144–149
Kiatpapan P, Murooka Y (2002) Genetic manipulation system in propionibacteria. J Biosci Bioeng 93:1–8
Kiatpapan P, Hashimoto Y, Nakamura H, Piao YZ, Ono H, Yamashita M, Murooka Y (2000) Characterization of pRGO1, a plasmid from Propionibacterium acidipropionici, and its use for development of a host-vector system in propionibacteria. Appl Environ Microbiol 66:4688–4695
Kitano H (2002) Systems biology: a brief overview. Science 295:1662–1664
Klantschitsch T, Bachmann HP, Puhan Z (2000) Influence of milk treatment and ripening conditions on quality of Raclette cheese. Lait 80:51–67
Klappenbach JA, Dunbar JM, Schmidt TM (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66:1328–1333
Kośmider A, Białas W, Kubiak P, Drożdżyńska A, Czaczyk K (2012) Vitamin B12 production from crude glycerol by Propionibacterium freudenreichii ssp. shermanii: optimization of medium composition through statistical experimental designs. Bioresour Technol 105:128–133
Kourkoutas Y, Xolias V, Kallis M, Bezirtzoglou E, Kanellaki M (2005) Lactobacillus casei cell immobilization on fruit pieces for probiotic additive, fermented milk and lactic acid production. Process Biochem 40:411–416
Koussémon M, Combet-Blanc Y, Patel BK, Cayol JL, Thomas P, Garcia JL, Ollivier B (2001) Propionibacterium microaerophilum sp. nov., a microaerophilic bacterium isolated from olive mill wastewater. Int J Syst Evol Microbiol 51:1373–1382
Kusano K, Yamada H, Niwa M, Yamasato K (1997) Propionibacterium cyclohexanicum sp. nov., a new acid-tolerant ω-cyclohexyl fatty acid-containing propionibacterium isolated from spoiled orange juice. Int J Syst Bacteriol 47:825–831
LeBlanc JG, Rutten G, Bruinenberg P, Sesma F, de Giori GS, Smid EJ (2006) A novel dairy product fermented with Propionibacterium freudenreichii improves the riboflavin status of deficient rats. Nutrition 22:645–651
Lee ZM-P, Bussema C, Schmidt TM (2009) rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucleic Acids Res 37:D489–D493
Leverrier P, Dimova D, Pichereau V, Auffray Y, Boyaval P, Jan G (2003) Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: physiological and proteomic analysis. Appl Environ Microbiol 69:3809–3818
Lewis VP, Yang ST (1992) A novel extractive fermentation process for propionic acid production from whey lactose. Biotechnol Prog 8:104–110
Liu L, Zhu Y, Li J, Wang M, Lee P, Du G, Chen J (2012) Microbial production of propionic acid from propionibacteria: current state, challenges and perspectives. Crit Rev Biotechnol 32:374–381
Lu P, Ma D, Chen Y, Guo Y, Chen GQ, Deng H, Shi Y (2013) L-glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia. Cell Res 23:635–644
Lyon WJ, Glatz BA (1993) Isolation and purification of propionicin PLG-1, a bacteriocin produced by a strain of Propionibacterium thoenii. Appl Environ Microbiol 59:83–88
Mak TN, Schmid M, Brzuszkiewicz E, Zeng G, Meyer R, Sfanos KS, Brinkmann V, Meyer TF, Brüggemann H (2013) Comparative genomics reveals distinct host-interacting traits of three major human-associated propionibacteria. BMC Genomics 14:640
Malik A, Reinbold G, Vedamuthu E (1968) An evaluation of the taxonomy of Propionibacterium. Can J Microbiol 14:1185–1191
Mantere-Alhonen S (1995) Propionibacteria used as probiotics—a review. Lait 75:447–452
Marraffini LA, Sontheimer EJ (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11:181–190
Martens J, Barg H, Warren M, Jahn D (2002) Microbial production of vitamin B12. Appl Microbiol Biotechnol 58:275–285
Marwaha S, Sethi R, Kennedy J (1983) Influence of 5,6-dimethylbenzimidazole (DMB) on vitamin B12 biosynthesis by strains of Propionibacterium. Enzym Microb Technol 5:361–364
Meile L, Le Blay G, Thierry A (2008) Safety assessment of dairy microorganisms: Propionibacterium and Bifidobacterium. Int J Food Microbiol 126:316–320
Meynial-Salles I, Dorotyn S, Soucaille P (2008) A new process for the continuous production of succinic acid from glucose at high yield, titer and productivity. Biotechnol Bioeng 99:129–135
Miescher S, Stierli MP, Teuber M, Meile L (2000) Propionicin SM1, a bacteriocin from Propionibacterium jensenii DF1: isolation and characterization of the protein and its gene. Syst Appl Microbiol 23:174–184
Murooka Y, Piao Y, Kiatpapan P, Yamashita M (2005) Production of tetrapyrrole compounds and vitamin B12 using genetically engineering of Propionibacterium freudenreichii. An overview. Lait 85:9–22
Nouaille S, Even S, Charlier C, Le Loir Y, Cocaign-Bousquet M, Loubière P (2009) Transcriptomic response of Lactococcus lactis in mixed culture with Staphylococcus aureus. Appl Environ Microbiol 75:4473–4482
Ördögh L, Hunyadkürti J, Vörös A, Horváth B, Szűcs A, Urbán E, Kereszt A, Kondorosi É, Nagy I (2013) Complete genome sequence of Propionibacterium avidum strain 44067, isolated from a human skin abscess. Genome Announc 1:e00337–00313
Orla-Jensen O (1909) Die hauptlinien des naturlichen bakteriensystems. Zentbl Bakteriol Parasitenkd Infektkrank Hyg Abt 22:305–346
Paik HD, Glatz BA (1997) Enhanced bacteriocin production by Propionibacterium thoenii in fed-batch fermentation. J Food Protect 60:1529–1533
Parizzi L, Grassi M, Llerena L, Carazzolle M, Queiroz V, Lunardi I, Zeidler A, Teixeira P, Mieczkowski P, Rincones J, Pereira G (2012) The genome sequence of Propionibacterium acidipropionici provides insights into its biotechnological and industrial potential. BMC Genomics 13:562–581
Pérez-Clemente RM, Vives V, Zandalinas SI, López-Climent MF, Muñoz V, Gómez-Cadenas A (2012) Biotechnological approaches to study plant responses to stress. BioMed Res Int 2013:1–10
Perry A, Lambert PA (2006) Propionibacterium acnes. Lett Appl Microbiol 42:185–188
Piao Y, Kiatpapan P, Yamashita M, Murooka Y (2004a) Effects of expression of hemA and hemB genes on production of porphyrin in Propionibacterium freudenreichii. Appl Environ Microbiol 70:7561–7566
Piao Y, Yamashita M, Kawaraichi N, Asegawa R, Ono H, Murooka Y (2004b) Production of vitamin B12 in genetically engineered Propionibacterium freudenreichii. J Biosci Bioeng 98:167–173
Pitcher DG, Collins MD (1991) Phylogenetic analysis of some LL-diaminopimelic acid-containing coryneform bacteria from human skin: description of Propionibacterium innocuum sp. nov. FEMS Microbiol Lett 84:295–300
Pophaly S, Tomar S, De S, Singh R (2012) Multifaceted attributes of dairy propionibacteria: a review. World J Microbiol Biotechnol 28:3081–3095
Preininger M, Rychlik M, Grosch W (1994) Potent odorants of the neutral volatile fraction of Swiss cheese (Emmentaler). In: Maarse H, van der Meij OG (eds) Trends in flavour research. Elsevier, Amsterdam, pp 267–270
Preininger M, Warmke R, Grosch W (1996) Identification of the character impact flavour compounds of Swiss cheese by sensory studies of models. Z Lebensm Unters Forsch 202:30–34
Quesada-Chanto A, Wagner F (1994) Microbial production of propionic acid and vitamin B12 using molasses or sugar. Appl Microbiol Biotechnol 41:378–383
Quesada-Chanto A, Schmid-Meyer A, Schroeder A, Carvalho-Jonas M, Blanco I, Jonas R (1998) Effect of oxygen supply on biomass, organic acids and vitamin B12 production by Propionibacterium shermanii. World J Microbiol Biotechnol 14:843–846
Rainio A, Vahvaselkä M, Suomalainen T, Laakso S (2001) Reduction of linoleic acid inhibition in production of conjugated linoleic acid by Propionibacterium freudenreichii ssp. shermanii. Can J Microbiol 47:735–740
Rainio A, Vahvaselkä M, Suomalainen T, Laakso S (2002) Production of conjugated linoleic acid by Propionibacterium freudenreichii ssp. shermanii. Lait 82:91–101
Ramsay J, Aly Hassan M, Ramsay B (1998) Biological conversion of hemicellulose to propionic acid. Enzym Microb Technol 22:292–295
Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8:2281–2308
Ratnam P, Barefoot SF, Prince LD, Bodine AB, McCaskill LH (1999) Partial purification and characterization of the bacteriocin produced by Propionibacterium jensenii B1264. Lait 79:125–136
Rehberger TG, Glatz BA (1990) Characterization of Propionibacterium plasmids. Appl Environ Microbiol 56:864–871
Roessner CA, Huang KX, Warren MJ, Raux E, Scott AI (2002) Isolation and characterization of 14 additional genes specifying the anaerobic biosynthesis of cobalamin (vitamin B12) in Propionibacterium freudenreichii (P. shermanii). Microbiology 148:1845–1853
Ruhal R, Choudhury B (2012a) Improved trehalose production from biodiesel waste using parent and osmotically sensitive mutant of Propionibacterium freudenreichii subsp. shermanii under aerobic conditions. J Ind Microbiol Biotechnol 39:1153–1160
Ruhal R, Choudhury B (2012b) Use of an osmotically sensitive mutant of Propionibacterium freudenreichii subspp. shermanii for the simultaneous productions of organic acids and trehalose from biodiesel waste based crude glycerol. Bioresour Technol 109:131–139
Ruhal R, Kataria R, Choudhury B (2013) Trends in bacterial trehalose metabolism and significant nodes of metabolic pathway in the direction of trehalose accumulation. Microb Biotechnol 6:493–502
Salih M, Sandine W, Ayres J (1990) Inhibitory effects of Microgard™ on yogurt and cottage cheese spoilage organisms. J Dairy Sci 73:887–893
Salminen S, von Wright A, Morelli L, Marteau P, Brassart D, de Vos WM, Fondén R, Saxelin M, Collins K, Mogensen G (1998) Demonstration of safety of probiotics—a review. Int J Food Microbiol 44:93–106
Seidametova E, Shakirzyanova M, Ruzieva D, Gulyamova T (2004) Isolation of cobalt-resistant strains of propionic acid bacteria, potent producers of vitamin B12. Appl Biochem Biotechnol 40:560–562
Singer MA, Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: the yin and yang of trehalose. Trends Biotechnol 16:460–468
Skerman VBD, McGowan V, Sneath PHA (1980) Approved lists of bacterial names. Int J Syst Bacteriol 30:225–230
Sonhom R, Thepsithar C, Jongsareejit B (2012) High level production of 5-aminolevulinic acid by Propionibacterium acidipropionici grown in a low-cost medium. Biotechnol Lett 34:1667–1672
Stierli MP (2002) DNA transformation of propionibacteria based on plasmids pLME106 and pLME108. Dissertation, Swiss Federal Institute of Technology
Suomalainen TH, Mäyrä Makinen AM (1999) Propionic acid bacteria as protective cultures in fermented milks and breads. Lait 79:165–174
Suwannakham S, Yang S (2005) Enhanced propionic acid fermentation by Propionibacterium acidipropionici mutant obtained by adaptation in a fibrous-bed bioreactor. Biotechnol Bioeng 91:325–337
Suwannakham S, Huang Y, Yang ST (2006) Construction and characterization of ack knock-out mutants of Propionibacterium acidipropionici for enhanced propionic acid fermentation. Biotechnol Bioeng 94:383–395
Thierry A, Maillard MB (2002) Production of cheese flavour compounds derived from amino acid catabolism by Propionibacterium freudenreichii. Lait 82:17–32
Thierry A, Maillard MB, Hervé C, Richoux R, Lortal S (2004a) Varied volatile compounds are produced by Propionibacterium freudenreichii in Emmental cheese. Food Chem 87:439–446
Thierry A, Richoux R, Kerjean JR (2004b) Isovaleric acid is mainly produced by Propionibacterium freudenreichii in Swiss cheese. Int Dairy J 14:801–807
Thierry A, Deutsch SM, Falentin H, Dalmasso M, Cousin FJ, Jan G (2011) New insights into physiology and metabolism of Propionibacterium freudenreichii. Int J Food Microbiol 149:19–27
Thirupathaiah Y, Rani CS, Reddy MS, Rao LV (2012) Effect of chemical and microbial vitamin B12 analogues on production of vitamin B12. World J Microbiol Biotechnol 28:2267–2271
Trojanowska K, Czaczyk K (1996) The effect of Co++, Mg++, Zn++, Mn++, Fe++ ions on the course of propionic acid fermentation. Ann Univ Agric Poznan 20:25–34
Van der Merwe I, Bauer R, Britz T, Dicks L (2004) Characterization of thoeniicin 447, a bacteriocin isolated from Propionibacterium thoenii strain 447. Int J Food Microbiol 92:153–160
Van Luijk N, Stierli MP, Schwenninger SM, Hervé C, Dasen G, Jore JP, Pouwels PH, Van Der Werf MJ, Teuber M, Meile L (2002) Genetics and molecular biology of propionibacteria. Lait 82:45–57
Van Wyk J, Britz TJ (2012) A rapid high-performance liquid chromatography (HPLC) method for the extraction and quantification of folates in dairy products and cultures of Propionibacterium freudenreichii. Afr J Biotechnol 11:2087–2098
Van Wyk J, Witthuhn RC, Britz TJ (2011) Optimisation of vitamin B12 and folate production by Propionibacterium freudenreichii strains in kefir. Int Dairy J 21:69–74
Wang Z, Yang ST (2013) Propionic acid production in glycerol/glucose co-fermentation by Propionibacterium freudenreichii subsp. shermanii. Bioresour Technol 137:116–123
Wang Z, Sun J, Zhang A, Yang ST (2013) Propionic acid fermentation. In: Yang ST, El-Enshasy HA, Thongchul N (eds) Bioprocessing technologies in biorefinery for sustainable production of fuels, chemicals, and polymers. Wiley, New York, pp 331–334
Werkman C, Brown RW (1933) The propionic acid bacteria: II. Classification 1. J Bacteriol 26:393–417
Wood H (1981) Metabolic cycles in the fermentation by propionic acid bacteria. Curr Top Cell Regul 18:255
Ye K, Shijo M, Jin S, Shimizu K (1996) Efficient production of vitamin B12 from propionic acid bacteria under periodic variation of dissolved oxygen concentration. J Ferment Bioeng 82:484–491
Zhang A, Yang ST (2009) Engineering Propionibacterium acidipropionici for enhanced propionic acid tolerance and fermentation. Biotechnol Bioeng 104:766–773
Zhang Y, Liu J, Huang J, Mao Z (2010a) Genome shuffling of Propionibacterium shermanii for improving vitamin B12 production and comparative proteome analysis. J Biotechnol 148:139–143
Zhang Z, Cao J, Luo Y, Wu X, Wan Q (2010b) Study on CLA production from sesame oil by Propionibacterium shermanii. Food Sci Technol 1:13
Zhu Y, Li J, Tan M, Liu L, Jiang L, Sun J, Lee P, Du G, Chen J (2010) Optimization and scale-up of propionic acid production by propionic acid-tolerant Propionibacterium acidipropionici with glycerol as the carbon source. Bioresour Technol 101:8902–8906
Zhu L, Wei P, Cai J, Zhu X, Wang Z, Huang L, Xu Z (2012) Improving the productivity of propionic acid with FBB-immobilized cells of an adapted acid-tolerant Propionibacterium acidipropionici. Bioresour Technol 112:248–253
Zhuge X, Liu L, Shin HD, Chen RR, Li J, Du G, Chen J (2013) Development of a Propionibacterium-Escherichia coli shuttle vector as a useful tool for metabolic engineering of Propionibacterium jensenii, an efficient producer of propionic acid. Appl Environ Microbiol 80:4595–4602
Zhuge X, Liu L, Shin HD, Li J, Du G, Chen J (2014) Improved propionic acid production from glycerol with metabolically engineered Propionibacterium jensenii by integrating fed-batch culture with a pH-shift control strategy. Bioresour Technol 152:519–525
Acknowledgments
This work was supported financially by the Priority Academic Program Development of Jiangsu Higher Education Institutions, the 111 Project (111-2-06), 863 Program (2011AA100905), and 973 Program (2013CB733902).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Guan, N., Zhuge, X., Li, J. et al. Engineering propionibacteria as versatile cell factories for the production of industrially important chemicals: advances, challenges, and prospects. Appl Microbiol Biotechnol 99, 585–600 (2015). https://doi.org/10.1007/s00253-014-6228-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-014-6228-z