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Effects of encapsulation of microorganisms on product formation during microbial fermentations

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Abstract

This paper reviews the latest developments in microbial products by encapsulated microorganisms in a liquid core surrounded by natural or synthetic membranes. Cells can be encapsulated in one or several steps using liquid droplet formation, pregel dissolving, coacervation, and interfacial polymerization. The use of encapsulated yeast and bacteria for fermentative production of ethanol, lactic acid, biogas, l-phenylacetylcarbinol, 1,3-propanediol, and riboflavin has been investigated. Encapsulated cells have furthermore been used for the biocatalytic conversion of chemicals. Fermentation, using encapsulated cells, offers various advantages compared to traditional cultivations, e.g., higher cell density, faster fermentation, improved tolerance of the cells to toxic media and high temperatures, and selective exclusion of toxic hydrophobic substances. However, mass transfer through the capsule membrane as well as the robustness of the capsules still challenge the utilization of encapsulated cells. The history and the current state of applying microbial encapsulation for production processes, along with the benefits and drawbacks concerning productivity and general physiology of the encapsulated cells, are discussed.

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References

  • Abelyan V (2000) A new method for immobilization of microbial cells by cross-linking. Appl Biochem Microbiol 36(3):310–314. doi:10.1007/bf02742586

    Article  Google Scholar 

  • Alosta HA (2007) Riboflavin production by encapsulated Candida flareri. PhD thesis, Oklahoma State University, Stillwater

  • Anal AK, Singh H (2007) Recent advances in microencapsulation of probiotics for industrial applications and targeted delivery. Trends Food Sci Tech 18(5):240–251. doi:10.1016/j.tifs.2007.01.004

    Article  CAS  Google Scholar 

  • Argüelles JC (2000) Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 174(4):217–224. doi:10.1007/s002030000192

    Article  Google Scholar 

  • Bhatia SR, Khattak SF, Roberts SC (2005) Polyelectrolytes for cell encapsulation. Curr Opin Colloid In 10:45–51. doi:10.1016/j.cocis.2005.05.004

    Article  CAS  Google Scholar 

  • Boender LGM, de Hulster EAF, van Maris AJA, Daran-Lapujade PAS, Pronk JT (2009) Quantitative physiology of Saccharomyces cerevisiae at near-zero specific growth rates. Appl Environ Microbiol 75(17):5607–5614. doi:10.1128/aem.00429-09

    Article  CAS  Google Scholar 

  • Boender LGM, van Maris AJA, de Hulster EAF, Almering MJH, van der Klei IJ, Veenhuis M, de Winde JH, Pronk JT, Daran-Lapujade P (2011) Cellular responses of Saccharomyces cerevisiae at near-zero growth rates: transcriptome analysis of anaerobic retentostat cultures. FEMS Yeast Res 11(8):603–620. doi:10.1111/j.1567-1364.2011.00750.x

    Article  CAS  Google Scholar 

  • Brandberg T, Karimi K, Taherzadeh MJ, Franzén CJ, Gustafsson L (2007) Continuous fermentation of wheat-supplemented lignocellulose hydrolysate with different types of cell retention. Biotechnol Bioeng 98(1):80–90. doi:10.1002/bit.21410

    Article  CAS  Google Scholar 

  • Bučko M, Vikartovská A, Lacík I, Kolláriková G, Gemeiner P, Pätoprstý V, Brygin M (2005) Immobilization of a whole-cell epoxide-hydrolyzing biocatalyst in sodium alginate-cellulose sulfate-poly(methylene-co-guanidine) capsules using a controlled encapsulation process. Enzym Microb Tech 36(1):118–126. doi:10.1016/j.enzmictec.2004.07.006

    Article  Google Scholar 

  • Bučko M, Vikartovská A, Gemeiner P, Lacík I, Kolláriková G, Marison IW (2006) Nocardia tartaricans cells immobilized in sodium alginate–cellulose sulfate–poly(methylene-co-guanidine)capsules: mechanical resistance and operational stability. J Chem Technol Biotechnol 81(4):500–504. doi:10.1002/jctb.1466

    Article  Google Scholar 

  • Bučko M, Schenkmayerová A, Gemeiner P, Vikartovská A, Mihovilovič MD, Lacík I (2011) Continuous testing system for Baeyer–Villiger biooxidation using recombinant Escherichia coli expressing cyclohexanone monooxygenase encapsulated in polyelectrolyte complex capsules. Enzym Microb Tech 49(3):284–288. doi:10.1016/j.enzmictec.2011.05.013

    Article  Google Scholar 

  • Butler MF, Ng Y-F, Pudney PDA (2003) Mechanism and kinetics of the crosslinking reaction between biopolymers containing primary amine groups and genipin. J Polym Sci Pol Chem 41(24):3941–3953. doi:10.1002/pola.10960

    Article  CAS  Google Scholar 

  • Carstensen F, Apel A, Wessling M (2012) In situ product recovery: submerged membranes vs. external loop membranes. J Membr Sci 394–395(0):394–395. doi:10.1016/j.memsci.2011.11.029

    Google Scholar 

  • Chai Y, Mei L-H, Wu G-L, Lin D-Q, Yao S-J (2004) Gelation conditions and transport properties of hollow calcium alginate capsules. Biotechnol Bioeng 87(2):228–233. doi:10.1002/bit.20144

    Article  CAS  Google Scholar 

  • Chandy T, Mooradian Daniel L, Rao Gundu HR (1999) Evaluation of modified alginate–chitosan–polyethylene glycol microcapsules for cell encapsulation. Artif Organs 23(10):894–903. doi:10.1046/j.1525-1594.1999.06244.x

    Article  CAS  Google Scholar 

  • Chang TMS (1964) Semipermeable microcapsules. Science 146:524–525. doi:10.1126/science.146.3643.524

    Article  CAS  Google Scholar 

  • Chang HN, Seong GH, Yoo I-K, Park JK, Seo J-H (1996) Microencapsulation of recombinant Saccharomyces cerevisiae cells with invertase activity in liquid-core alginate capsules. Biotechnol Bioeng 51:157–162. doi:10.1002/(SICI)1097-0290(19960720)51:2<157::AID-BIT4>3.0.CO;2-I

    Article  Google Scholar 

  • Chang HN, Seong GH, Yoo I-K, Park JK, Seo J-H (1998) Method for immobilization of whole microbial cells in calcium alginate capsules. US patent 5,766,907, 16 Jun 1998

  • Chen H, Ouyang W, Jones M, Metz T, Martoni C, Haque T, Cohen R, Lawuyi B, Prakash S (2007) Preparation and characterization of novel polymeric microcapsules for live cell encapsulation and therapy. Cell Biochem Biophys 47:159–167. doi:10.1385/CBB:47:1:159

    Article  CAS  Google Scholar 

  • Cheong SH, Park JK, Kim BS, Chang HN (1993) Microencapsulation of yeast cells in the calcium alginate membrane. Biotechnol Tech 7(12):879–884. doi:10.1007/BF00156366

    Article  CAS  Google Scholar 

  • Cheryan M, Mehaia MA (1983) A high-performance membrane bioreactor for continuous fermentation of lactose to ethanol. Biotechnol Lett 5(8):519–524. doi:10.1007/bf01184942

    Article  CAS  Google Scholar 

  • de Vos P, Bučko M, Gemeiner P, Navrátil M, Svitel J, Faas M, Strand BL, Skjak-Bræk G, Morch YA, Vikartovská A, Lacík I, Kolláriková G, Orive G, Poncelet D, Pedraz JL, Ansorge-Schumacher MB (2009) Multiscale requirements for bioencapsulation in medicine and biotechnology. Biomaterials 30:2559–2570. doi:10.1016/j.biomaterials.2009.01.014

    Article  Google Scholar 

  • Dembczynski R, Jankowski T (2000) Characterisation of small molecules diffusion in hydrogel-membrane liquid-core capsules. Biochem Eng J 6(1):41–44. doi:10.1016/S1369-703X(00)00070-X

    Article  CAS  Google Scholar 

  • Dembczynski R, Jankowski T (2002) Growth characteristics and acidifying activity of Lactobacillus rhamnosus in alginate/starch liquid-core capsules. Enzym Microb Tech 31:111–115. doi:10.1016/S0141-0229(02)00080-7

    Article  CAS  Google Scholar 

  • Galazzo JL, Bailey JE (1990) Growing Saccharomyces cerevisiae in calcium-alginate beads induces cell alterations which accelerate glucose conversion to ethanol. Biotechnol Bioeng 36:417–426. doi:10.1002/bit.260360413

    Article  CAS  Google Scholar 

  • Gasch AP, Werner-Washburne M (2002) The genomics of yeast responses to environmental stress and starvation. Funct Integr Genomics 2:181–192

    Article  CAS  Google Scholar 

  • Gåserød O, Smidsrød O, Skjåk-Bræk G (1998) Microcapsules of alginate–chitosan—I. A quantitative study of the interaction between alginate and chitosan. Biomaterials 19:1815–1825. doi:10.1016/S0142-9612(98)00073-8

    Article  Google Scholar 

  • Gåserød O, Sannes A, Skjåk-Bræk G (1999) Microcapsules of alginate–chitosan. II. A study of capsule stability and permeability. Biomaterials 20:773–783. doi:10.1016/S0142-9612(98)00230-0

    Article  Google Scholar 

  • Ge XM, Zhang L, Bai FW (2006) Impacts of yeast floc size distributions on their observed rates for substrate uptake and product formation. Enzym Microb Tech 39:289–295. doi:10.1016/j.enzmictec.2005.10.026

    Article  CAS  Google Scholar 

  • Ghidoni I, Chlapanidas T, Bucco M, Crovato F, Marazzi M, Vigo D, Torre M, Faustini M (2008) Alginate cell encapsulation: new advances in reproduction and cartilage regenerative medicine. Cytotechnology 58(1):49–56. doi:10.1007/s10616-008-9161-0

    Article  CAS  Google Scholar 

  • Gill I, Ballesteros A (2000) Bioencapsulation within synthetic polymers (part 1): sol–gel encapsulated biologicals. Trends Biotechnol 18(7):282–296. doi:10.1016/S0167-7799(00)01457-8

    Article  CAS  Google Scholar 

  • Goosen MFA, O’Shea GM, Gharapetian HM, Chou S, Sun AM (1985) Optimization of microencapsulation parameters: semipermeable microcapsules as a bioartificial pancreas. Biotechnol Bioeng 27(2):146–150. doi:10.1002/bit.260270207

    Article  CAS  Google Scholar 

  • Green KD, Gill IS, Khan JA, Vulfson EN (1996) Microencapsulation of yeast cells and their use as a biocatalyst in organic solvents. Biotechnol Bioeng 49:535–543. doi:10.1002/(SICI)1097-0290(19960305)49:5<535::AID-BIT6>3.0.CO;2-K

    Article  CAS  Google Scholar 

  • Groboillot AF, Champagne CP, Darling GD, Poncelet D, Neufeld RJ (1993) Membrane formation by interfacial cross-linking of chitosan for microencapsulation of Lactococcus lactis. Biotechnol Bioeng 42(10):1157–1163. doi:10.1002/bit.260421005

    Article  CAS  Google Scholar 

  • Hsu Y-L, Chu I-M (1992) Poly(ethylenimine)-reinforced liquid-core capsules for the cultivation of hybridoma cells. Biotechnol Bioeng 40(11):1300–1308. doi:10.1002/bit.260401103

    Article  CAS  Google Scholar 

  • Hucík M, Bučko M, Gemeiner P, Štefuca V, Vikartovská A, Mihovilovič M, Rudroff F, Iqbal N, Chorvát D, Lacík I (2010) Encapsulation of recombinant E. coli expressing cyclopentanone monooxygenase in polyelectrolyte complex capsules for Baeyer–Villiger biooxidation of 8-oxabicyclo[3.2.1]oct-6-en-3-one. Biotechnol Lett 32(5):675–680. doi:10.1007/s10529-010-0203-2

    Article  Google Scholar 

  • Hyndman CL, Groboillot AF, Poncelet D, Champagne CP, Neufeld RJ (1993) Microencapsulation of Lactococcus lactis within cross-linked gelatin membranes. J Chem Technol Biotechnol 56(3):259–263. doi:10.1002/jctb.280560307

    Article  CAS  Google Scholar 

  • Jankowski T, Zielinska M, Wysakowska A (1997) Encapsulation of lactic acid bacteria with alginate/starch capsules. Biotechnol Tech 11(1):31–34. doi:10.1007/BF02764447

    Article  CAS  Google Scholar 

  • Kean T, Roth S, Thanou M (2005) Trimethylated chitosans as non-viral gene delivery vectors: cytotoxicity and transfection efficiency. J Control Release 103(3):643–653. doi:10.1016/j.jconrel.2005.01.001

    Article  CAS  Google Scholar 

  • Kim S-K, Yu S-H, Son J-H, Hübner H, Buchholz R (1998) Calculations on O2 transfer in capsules with animal cells for the determination of maximum capsule size without O2 limitation. Biotechnol Lett 20(6):549–552. doi:10.1023/A:1005341526365

    Article  CAS  Google Scholar 

  • Klinke HB, Thomsen AB, Ahring BK (2004) Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 66(1):10–26. doi:10.1007/s00253-004-1642-2

    Article  CAS  Google Scholar 

  • Krasaekoopt W, Bhandari B, Deeth H (2003) Evaluation of encapsulation techniques of probiotics for yoghurt. Int Dairy J 13(1):3–13. doi:10.1016/S0958-6946(02)00155-3

    Article  CAS  Google Scholar 

  • Kubota M, Matsui M, Chiku H, Kasashima N, Shimojoh M, Sakaguchi K (2005) Cell adsorption and selective desorption for separation of microbial cells by using chitosan-immobilized silica. Appl Environ Microbiol 71(12):8895–8902. doi:10.1128/aem.71.12.8895-8902.2005

    Article  CAS  Google Scholar 

  • Kunioka M (1997) Biosynthesis and chemical reactions of poly(amino acid)s from microorganisms. Appl Microbiol Biotechnol 47:469–475. doi:10.1007/s002530050958

    Article  CAS  Google Scholar 

  • Kurayama F, Suzuki S, Oyamada T, Furusawa T, Sato M, Suzuki N (2010) Facile method for preparing organic/inorganic hybrid capsules using amino-functional silane coupling agent in aqueous media. J Colloid Interf Sci 349(1):70–76. doi:10.1016/j.jcis.2010.05.039

    Article  CAS  Google Scholar 

  • Larisch BC (1990) Microencapsulation of Lactococcus lactis subsp. cremoris for application in the dairy industry. MSc thesis, McGill University, Montreal

  • Larisch BC, Poncelet D, Champagne CP, Neufeld RJ (1994) Microencapsulation of Lactococcus lactis subsp. cremoris. J Microencapsul 11(2):189–195. doi:10.3109/02652049409040450

    Article  CAS  Google Scholar 

  • Lee BH, Park JK (1996) Encapsulation of whole cell β-galactosidase of Escherichia coli. Korean J Biotechnol Bioeng 11:398–404

    Google Scholar 

  • Leveque I, Rhodes KH, Mann S (2002) Biomineral-inspired fabrication of semi-permeable calcium phosphate–polysaccharide microcapsules. J Mater Chem 12(8):2178–2180. doi:10.1039/B204599K

    Article  CAS  Google Scholar 

  • Lin J, Yu W, Liu X, Xie H, Wang W, Ma X (2008) In vitro and in vivo characterization of alginate-chitosan-alginate artificial microcapsules for therapeutic oral delivery of live bacterial cells. J Biosci Bioeng 105(6):660–665. doi:10.1263/jbb.105.660

    Article  CAS  Google Scholar 

  • Liouni M, Drichoutis P, Nerantzis ET (2008) Studies of the mechanical properties and the fermentation behavior of double layer alginate–chitosan beads, using Saccharomyces cerevisiae entrapped cells. World J Microbiol Biotechnol 24:281–288. doi:10.1007/s11274-007-9467-7

    Article  CAS  Google Scholar 

  • Lu Y, Mei L (2007) Production of indigo by immobilization of E. coli BL21 (DE3) cells in calcium-alginate gel capsules. Chin J Chem Eng 15(3):387–390. doi:10.1016/S1004-9541(07)60096-2

    Article  CAS  Google Scholar 

  • Ma J, Qi WT, Yang LN, Yu WT, Xie YB, Wang W, Ma XJ, Xu F, Sun LX (2007) Microcalorimetric study on the growth and metabolism of microencapsulated microbial cell culture. J Microbiol Meth 68:172–177. doi:10.1016/j.mimet.2006.07.007

    Article  CAS  Google Scholar 

  • Mei L-H, Yao S-J (2002) Cultivation and modelling of encapsulated Saccharomyces cerevisiae in NaCS-PDMDAAC polyelectrolyte complexes. J Microencapsul 19(4):397–405. doi:10.1080/02652040210141101

    Article  CAS  Google Scholar 

  • Mogensen AO, Vieth WR (1973) Mass transfer and biochemical reaction with semipermeable microcapsules. Biotechnol Bioeng 15:467–481. doi:10.1002/bit.260150304

    Article  CAS  Google Scholar 

  • Murua A, Portero A, Orive G, Hernández RM, Md C, Pedraz JL (2008) Cell microencapsulation technology: towards clinical application. J Control Release 132:76–83. doi:10.1016/j.jconrel.2008.08.010

    Article  CAS  Google Scholar 

  • Nigam SC, Tsao I-F, Sakoda A, Wang HY (1988) Techniques for preparing hydrogel membrane capsules. Biotechnol Lett 2(4):271–276. doi:10.1007/BF01875541

    CAS  Google Scholar 

  • Norton S, Watson K, D’Amore T (1995) Ethanol tolerance of immobilized brewers’ yeast cells. Appl Microbiol Biotechnol 43(1):18–24. doi:10.1007/BF00170616

    Article  CAS  Google Scholar 

  • Oh CY, Park JK (1998) The characteristics of encapsulated whole cell β-galactosidase. Bioprocess Eng 19:419–425. doi:10.1007/PL00009027

    Article  CAS  Google Scholar 

  • Orive G, Gascón AR, Hernández RM, Igartua M, Pedraz JL (2003) Cell microencapsulation technology for biomedical purposes: novel insights and challenges. Trends Pharmacol Sci 24(5):207–210. doi:10.1016/S0165-6147(03)00073-7

    Article  CAS  Google Scholar 

  • Orive G, Hernández RM, Gascón AR, Calafiore R, Chang TMS, Pd V, Hortelano G, Hunkeler D, Lacík I, Pedraz JL (2004) History, challenges and perspectives of cell microencapsulation. Trends Biotechnol 22(2):87–92. doi:10.1016/j.tibtech.2003.11.004

    Article  CAS  Google Scholar 

  • Park JK, Chang HN (2000) Microencapsulation of microbial cells. Biotechnol Adv 18:303–319

    Article  CAS  Google Scholar 

  • Park JK, Jung JY (2002) Production of benzaldehyde by encapsulated whole-cell benzoylformate decarboxylase. Enzym Microb Tech 30(6):726–733

    Article  CAS  Google Scholar 

  • Park JK, Lee KD (2001) Production of l-phenylacetylcarbinol (l-PAC) by encapsulated Saccharomyces cerevisiae cells. Korean J Chem Eng 18(3):363–370. doi:10.1007/bf02699179

    Article  CAS  Google Scholar 

  • Park JK, Jeong GS, Chang HN (1997a) The effect of oxygen transfer on the activity of encapsulated whole cell ß-galactosidase. Bioproc Biosyst Eng 17(4):197–202. doi:10.1007/pl00008964

    CAS  Google Scholar 

  • Park JK, Jin YB, Park HW (1997b) The recovery of heavy metals using encapsulated microbial cells. Biotechnol Bioprocess Eng 2:132–135

    Article  Google Scholar 

  • Park JK, Park HW, Lee YH (2000) Production of glucosyl–xylitol using encapsulated whole cell CGTase. Korean J Biotechnol Bioeng 15(1):35–41

    Google Scholar 

  • Park J-K, Sohn J-H, Park H-W, Lee Y-H (2001) Encapsulation of whole cell CGTase from concentrated broth solution. Biotechnol Bioprocess Eng 6(1):67–71. doi:10.1007/BF02942253

    Article  CAS  Google Scholar 

  • Pourbafrani M, Talebnia F, Niklasson C, Taherzadeh MJ (2007) Protective effect of encapsulation in fermentation of limonene-contained media and orange peel hydrolyzate. Int J Mol Sci 8:777–787

    Article  CAS  Google Scholar 

  • Prokop A, Hunkeler D, Powers AC, Whitesell RR, Wang TG (1998) Water soluble polymers for immunoisolation II: evaluation of multicomponent microencapsulation systems. Advances in Polymer Science 136:53–73. doi:10.1007/3-540-69682-2_2

    Google Scholar 

  • Purwadi R, Brandberg T, Taherzadeh MJ (2007) A possible industrial solution to ferment lignocellulosic hydrolyzate to ethanol: continuous cultivation with flocculating yeast. Int J Mol Sci 8:920–932. doi:10.3390/i8090920

    Article  CAS  Google Scholar 

  • Qi W-t, Yu W-t, Xie Y-b, Ma X (2005) Optimization of Saccharomyces cerevisiae culture in alginate–chitosan–alginate microcapsule. Biochem Eng J 25:151–157. doi:10.1016/j.bej.2005.04.019

    Article  CAS  Google Scholar 

  • Riley M, Muzzio F, Reyes S (1999) Experimental and modeling studies of diffusion in immobilized cell systems. Appl Biochem Biotechnol 80(2):151–188. doi:10.1385/ABAB:80:2:151

    Article  CAS  Google Scholar 

  • Sakai S, Ono T, Ijima H, Kawakami K (2002) Aminopropyl-silicate membrane for microcapsule-shaped bioartificial organs: control of molecular permeability. J Membr Sci 202(1–2):73–80. doi:10.1016/S0376-7388(01)00731-1

    Article  CAS  Google Scholar 

  • Sakai S, Hashimoto I, Kawakami K (2008) Production of cell-enclosing hollow-core agarose microcapsules via jetting in water-immiscible liquid paraffin and formation of embryoid body-like spherical tissues from mouse ES cells enclosed within these microcapsules. Biotechnol Bioeng 99(1):235–243. doi:10.1002/bit.21624

    Article  CAS  Google Scholar 

  • Schenkmayerová A, Bučko M, Gemeiner P, Chorvát D, Lacík I (2012) Viability of free and encapsulated Escherichia coli overexpressing cyclopentanone monooxygenase monitored during model Baeyer–Villiger biooxidation by confocal laser scanning microscopy. Biotechnol Lett 34(2):309–314. doi:10.1007/s10529-011-0765-7

    Article  Google Scholar 

  • Seong G-H, Han SJ, Chang H-N, Lee J (1997) Whole cell enzyme microencapsulation of Escherichia coli with oxygendependent inducible nar promoter. Biotechnol Lett 19(9):881–884. doi:10.1023/A:1018341705134

    Article  CAS  Google Scholar 

  • Serp D, Cantana E, Heinzen C, von Stockar U, Marison IW (2000) Characterization of an encapsulation device for the production of monodisperse alginate beads for cell immobilization. Biotechnol Bioeng 70(1):41–53. doi:10.1002/1097-0290(20001005)70:1<41::AID-BIT6>3.0.CO;2-U

    Article  CAS  Google Scholar 

  • Sheldon RA (2007) Enzyme immobilization: the quest for optimum performance. Adv Synth Catal 349(8–9):1289–1307. doi:10.1002/adsc.200700082

    Article  CAS  Google Scholar 

  • Shigeri Y, Koishi M, Kondo T, Shiba M, Tomioka S (1970) Studies on microcapsules. VI. Effect of variations in polymerization condition on microcapsule size. Can J Chem 48(13):2047–2051. doi:10.1139/v70-341

    Article  Google Scholar 

  • Stewart PS (2003) Diffusion in biofilms. J Bacteriol 185(5):1485–1491. doi:10.1128/jb.185.5.1485-1491.2003

    Article  CAS  Google Scholar 

  • Strøm AR, Kaasen I (1993) Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol Microbiol 8(2):205–210. doi:10.1111/j.1365-2958.1993.tb01564.x

    Article  Google Scholar 

  • Sun Z-J, Lv G-J, Li S-Y, Xie Y-B, Yu W-T, Wang W, Ma X-J (2007a) Probing the role of microenvironment for microencapsulated Sacchromyces cerevisiae under osmotic stress. J Biotechnol 128:150–161. doi:10.1016/j.jbiotec.2006.09.001

    Article  CAS  Google Scholar 

  • Sun Z-J, G-j L, Li S-y Y, W-t WW, Y-b X, Ma X (2007b) Differential role of microenvironment in microencapsulation for improved cell tolerance to stress. Appl Microbiol Biotechnol 75:1419–1427. doi:10.1007/s00253-007-0960-6

    Article  CAS  Google Scholar 

  • Sun Z-J, Li S-Y, Lv G-J, Zhu J, W-t Y, Wang W, Xie Y-B (2008) Metabolic response of different osmo-sensitive Sacchromyces cerevisiae to ACA microcapsule. Enzym Microb Tech 42:576–582. doi:10.1016/j.enzmictec.2008.01.021

    Article  CAS  Google Scholar 

  • Taherzadeh MJ, Millati R, Niklasson C (2001) Continuous cultivation of dilute-acid hydrolysates to ethanol by immobilized Saccharomyces cerevisiae. Appl Biochem Biotechnol 95:45–57. doi:10.1385/ABAB:95:1:45

    Article  CAS  Google Scholar 

  • Talebnia F, Taherzadeh MJ (2006) In situ detoxification and continuous cultivation of dilute-acid hydrolyzate to ethanol by encapsulated S. cerevisiae. J Biotechnol 125:377–384. doi:10.1016/j.jbiotec.2006.03.013

    Article  CAS  Google Scholar 

  • Talebnia F, Taherzadeh MJ (2007) Physiological and morphological study of encapsulated Saccharomyces cerevisiae. Enzym Microb Tech 41:683–688. doi:10.1016/j.enzmictec.2007.05.020

    Article  CAS  Google Scholar 

  • Talebnia F, Niklasson C, Taherzadeh MJ (2005) Ethanol production from glucose and dilute-acid hydrolyzates by encapsulated S. cerevisiae. Biotechnol Bioeng 90(3):345–353. doi:10.1002/bit.20432

    Article  CAS  Google Scholar 

  • Teixeira JA, Mota M (1990) Experimental assessment of internal diffusion limitations in yeast flocs. Chem Eng J 43(1):B13–B17. doi:10.1016/0300-9467(90)80047-G

    Article  CAS  Google Scholar 

  • Uludag H, De Vos P, Tresco PA (2000) Technology of mammalian cell encapsulation. Adv Drug Deliv Rev 42:29–64. doi:10.1016/S0169-409X(00)00053-3

    Article  CAS  Google Scholar 

  • Vicente AA, Dluhý M, Ferreira EC, Mota M, Teixeira JA (1998) Mass transfer properties of glucose and O2 in Saccharomyces cerevisiae flocs. Biochem Eng J 2:35–43

    Article  CAS  Google Scholar 

  • Voit EO (2003) Biochemical and genomic regulation of the trehalose cycle in yeast: review of observations and canonical model analysis. J Theor Biol 223(1):55–78

    Article  CAS  Google Scholar 

  • Wang FF, Wu CR, Wang YJ (1992) Preparation and application of poly(vinylamine)/alginate microcapsules to culturing of a mouse erythroleukemia cell line. Biotechnol Bioeng 40(9):1115–1118. doi:10.1002/bit.260400916

    Article  CAS  Google Scholar 

  • Westman JO, Manikondu RB, Franzén CJ, Taherzadeh MJ (2012a) Encapsulation-induced stress helps Saccharomyces cerevisiae resist convertible lignocellulose derived inhibitors. Int J Mol Sci 13(9):11881–11894. doi:10.3390/ijms130911881

    Article  CAS  Google Scholar 

  • Westman JO, Taherzadeh MJ, Franzén CJ (2012b) Proteomic analysis of the increased stress tolerance of Saccharomyces cerevisiae encapsulated in liquid core alginate–chitosan capsules. PLoS ONE (in press)

  • Xu L (2012) Bio-fuel production by using integrated anaerobic fermentation. PhD thesis, University of Minnesota, Minneapolis

  • Ylitervo P, Franzén CJ, Taherzadeh MJ (2011) Ethanol production at elevated temperatures using encapsulation of yeast. J Biotechnol 156(1):22–29. doi:10.1016/j.jbiotec.2011.07.018

    Article  CAS  Google Scholar 

  • Ylitervo P, Franzén CJ, Taherzadeh MJ (2012) Mechanically robust polysiloxane–ACA capsules for prolonged ethanol production. J Chem Technol Biotechnol. doi:10.1002/jctb.3944

  • Yoo I-K, Seong GH, Chang HN, Park JK (1996) Encapsulation of Lactobacillus casei cells in liquid-core alginate capsules for lactic acid production. Enzym Microb Tech 19(6):428–433. doi:10.1016/S0141-0229(96)00016-6

    Article  CAS  Google Scholar 

  • Yoshioka T, Hirano R, Shioya T, Kako M (1990) Encapsulation of mammalian cell with chitosan–CMC capsule. Biotechnol Bioeng 35(1):66–72. doi:10.1002/bit.260350110

    Article  CAS  Google Scholar 

  • Young T-H, Yao N-K, Chang R-F, Chen L-W (1996) Evaluation of asymmetric poly(vinyl alcohol) membranes for use in artificial islets. Biomaterials 17(22):2139–2145. doi:10.1016/0142-9612(96)00043-9

    Article  CAS  Google Scholar 

  • Youngsukkasem S, Rakshit SK, Taherzadeh MJ (2012) Biogas production by encapsulated methane-producing bacteria. BioResources 7(1):56–65

    CAS  Google Scholar 

  • Zhao Y-N, Chen G, Yao S-J (2006) Microbial production of 1,3-propanediol from glycerol by encapsulated Klebsiella pneumoniae. Biochem Eng J 32(2):93–99. doi:10.1016/j.bej.2006.09.007

    Article  CAS  Google Scholar 

  • Zou H, Wu S, Shen J (2008) Polymer/silica nanocomposites: preparation, characterization, properties, and applications. Chem Rev 108(9):3893–3957. doi:10.1021/cr068035q

    Article  CAS  Google Scholar 

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Acknowledgments

The authors appreciate financial support by the Swedish Research Council and the University of Borås in Sweden.

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Authors and Affiliations

  1. School of Engineering, University of Borås, 501 90, Borås, Sweden

    Johan O. Westman, Päivi Ylitervo & Mohammad J. Taherzadeh

  2. Chemical and Biological Engineering—Industrial Biotechnology, Chalmers University of Technology, 412 96, Gothenburg, Sweden

    Johan O. Westman, Päivi Ylitervo & Carl Johan Franzén

Authors
  1. Johan O. Westman
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  2. Päivi Ylitervo
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  3. Carl Johan Franzén
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  4. Mohammad J. Taherzadeh
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Correspondence to Mohammad J. Taherzadeh.

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Westman, J.O., Ylitervo, P., Franzén, C.J. et al. Effects of encapsulation of microorganisms on product formation during microbial fermentations. Appl Microbiol Biotechnol 96, 1441–1454 (2012). https://doi.org/10.1007/s00253-012-4517-y

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  • DOI: https://doi.org/10.1007/s00253-012-4517-y

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