Abstract
Cyanobacteria inhabit nearly every ecosystem on earth, play a vital role in nutrient cycling, and are useful as model organisms for fundamental research in photosynthesis and carbon and nitrogen fixation. In addition, they are important for several established biotechnologies for producing food additives, nutritional and pharmaceutical compounds, and pigments, as well as emerging biotechnologies for biofuels and other products. Encapsulation of living cyanobacteria into a porous silica gel matrix is a recent approach that may dramatically improve the efficiency of certain production processes by retaining the biomass within the reactor and modifying cellular metabolism in helpful ways. Although encapsulation has been explored empirically in the last two decades for a variety of cell types, many challenges remain to achieving optimal encapsulation of cyanobacteria in silica gel. Recent evidence with Synechocystis sp. PCC 6803, for example, suggests that several unknown or uncharacterized proteins are dramatically upregulated as a result of encapsulation. Also, additives commonly used to ease stresses of encapsulating living cells, such as glycerol, have detrimental impacts on photosynthesis in cyanobacteria. This mini-review is intended to address the current status of research on silica sol-gel encapsulation of cyanobacteria and research areas that may further the development of this approach for biotechnology applications.
Similar content being viewed by others
References
Armanini L, Carturan G, Boninsegna S, dal Monte R, Muraca M (1999) SiO2 entrapment of animal cells. Part 2: protein diffusion through collagen membranes coated with SiO2. J Mater Chem 9:3057–3060
Armon R (2000) Sol-gel as reaction matrix for bacterial enzymatic activity. J Sol-Gel Sci Technol 19:289–292
Assink RA, Kay BD (1991) Study of sol-gel chemical reaction kinetics by NMR. Annu Rev Mater Res 21:491–513
Avnir D, Coradin T, Lev O, Livage J (2006) Recent bio-applications of sol-gel materials. J Mater Chem 16:1013–1030
Bagshaw SA, Prouzet E, Pinnavaia TJ (1995) Templating of mesoporous molecular sieves by nonionic polyethylene oxide surfactants. Science 269(5228):1242–1244
Bechtold MF, Vest RD, Plambeck L Jr (1968) Silicic acid from tetraethyl silicate hydrolysis. Polymerization and properties. J Am Chem Soc 90(17):4590–4598
Bergogne L, Fennouh S, Guyon S, Roux C, Livage J (2000) Sol-gel entrapment of enzymes. Mater Res Soc Symp Proc 628:10.12.11–10.12.16
Bhatia RB, Brinker CJ (2000) Aqueous sol-gel process for protein encapsulation. Chem Mater 12(8):2434–2441
Boninsegna S, Bosetti P, Carturan G, Dellagiacoma G, Monte RD, Rossi M (2003) Encapsulation of individual pancreatic islets by sol-gel SiO2: a novel procedure for perspective cellular grafts. J Biotechnol 100:277–286
Bottcher H, Soltmann U, Mertig M, Pompe W (2004) Biocers: ceramics with incorporated microorganisms for biocatalytic, biosorptive and functional materials development. J Mater Chem 14:2176–2188
Brasack I, Bottcher H (2000) Biocompatibility of modified silica-protein composite layers. J Sol-Gel Sci Technol 19:479–482
Brennan L, Owende (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustain Energy Rev 14(2):557–577
Brinker CJ (1994) Sol-gel processing of silica. In: Bergna HE (ed) The colloid chemistry of silica. American Chemical Society, Washington, D.C, pp 361–402
Brinker CJ, Scherer GW (1990) Sol-gel science. Academic, San Diego
Brinker CJ, Keefer KD, Schaefer DW, Ashley CS (1982) Sol-gel transition in simple silicates. J Non-Cryst Solids 48:47–64
Brinker CJ, Keefer KD, Schaefer DW, Assink RA, Kay BD, Ashley CS (1984) Sol-gel transition in simple silicates II. J Non-Cryst Solids 63:45–59
Carturan G, Campostrini R, Dire S, Scardi V, Alteriis ED (1989) Inorganic gels for immobilization of biocatalysts: inclusion of invertase-active whole cells of yeast (Saccharomyces cerevisiae) into thin layers of SiO2 gel deposited on glass sheets. J Mol Catal 57:L13–L16
Carturan G, Monte RD, Pressi G, Secondin S, Verza P (1998) Production of valuable drugs from plant cells immobilized by hybrid sol-gel SiO2. J Sol-Gel Sci Technol 13:273–276
Chernev GE, Borisova BV, Kabaivanova LV, Salvado IM (2010) Silica hybrid biomaterials containing gelatin synthesized by sol-gel method. Cent Eur J Chem 8(4):870–876
Conroy J, Power ME, Martin J, Earp B, Hosticka B, Daitch CE, Norris PM (2000) Cells in sol-gels I: a cytocompatible route for the production of macroporous silica gels. J Sol-Gel Sci Technol 18:269–283
Coradin T, Livage J (2003) Synthesis and characterization of alginate/silica biocomposites. J Sol-Gel Sci Technol 26:1165–1168
Coradin T, Bah S, Livage J (2004) Gelatine/silicate interactions: from nanoparticles to composite gels. Colloids Surf B Biointerfaces 35:53–58
Davis PJ, Brinker CJ, Smith DM (1992a) Pore structure evolution in silica-gel during aging drying. 1. Temporal and thermal aging. J Non-Cryst Solids 142(3):189–196
Davis PJ, Brinker CJ, Smith DM (1992b) Pore structure evolution in silica-gel during aging drying. 2. Effect of pore fluids. J Non-Cryst Solids 142(3):197–207
Depagne C, Roux C, Coradin T (2011) How to design cell-based biosensors using the sol-gel process. Anal Bioanal Chem 400(4):965–976
Dickson DJ, Ely RL (2011) Evaluation of encapsulation stress and the effect of additives on viability and photosynthetic activity of Synechocystis sp. PCC 6803 encapsulated in silica gel. Appl Microbiol Biotechnol 91(6):1633–1646
Dickson DJ, Page CJ, Ely RL (2009) Photobiological hydrogen production from Synechocystis sp. PCC 6803 encapsulated in silica sol-gel. Int J Hydrog Energy 34(1):204–215
Dickson DJ, Luterra MD, Ely RL (2012a) Transcriptomic responses of Synechocystis sp. PCC 6803 encapsulated in silica gel. Appl Microbiol Biotechnol 96(1):183–196
Dickson DJ, Lassetter B, Glassy B, Page CJ, Yokochi AFT, Ely RL (2012b) Diffusion of dissolved ions from wet silica sol-gel monoliths: implications for biological encapsulation. Colloids Surf B Biointerfaces 102:611–619
Ducat DC, Avelar-Rivas JA, Way JC, Silver PA (2012) Rerouting carbon flux to enhance photosynthetic productivity. Appl Environ Microbiol 78(8):2660–2668
Eglin D, Mosser G, Giraud-Guille M-M, Livage J, Coradin T (2005) Type I collagen, a versatile liquid crystal biological template for silica structuration from nano- to microscopic scales. Soft Matter 1:129–131
Ellerby LM, Nashida CR, Nashida F, Yamanaka SA, Dunn B, Valentine JS, Zink JI (1992) Encapsulation of proteins in transparent porous silicate glasses prepared by the sol-gel method. Science 255(5048):1113–1115
Fahrenholtz WG, Smith DM, Hua D (1992) Formation of microporous silica gels from a modified silicon alkoxide. I. Base-catalyzed gels. J Non-Cryst Solids 144:45–52
Ferjani A, Mustardy L, Sulpice R, Marin K, Suzuki I, Hagemann M, Murata N (2003) Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131(4):1628–1637
Ferrer ML, Yuste L, Rojo F, Monte FD (2003) Biocompatible sol-gel route for encapsulation of living bacteria in organically modified silica matrices. Chem Mater 15(19):3614–3618
Fiedler D, Hager U, Franke H, Soltmann U, Bottcher H (2007) Algae biocers: astaxanthin formation in sol-gel immobilised living microalgae. J Mater Chem 17(3):261–266
Frenkel-Mullerad H, Avnir D (2005) Sol-gel materials as efficient enzyme protectors: preserving the activity of phosphatases under extreme pH conditions. J Am Chem Soc 127:8077–8081
Fu P (2008) Genome-scale modeling of Synechocystis sp. PCC 6803 and prediction of pathway insertion. J Chem Technol Biotechnol 84:473–483
Gadre SY, Gouma PI (2006) Biodoped ceramics: synthesis, properties, and applications. J Am Ceram Soc 89(10):2987–3002
Gautier C, Livage J, Coradin T, Lopez PJ (2006) Sol-gel encapsulation extends diatom viability and reveals their silica dissolution capability. Chem Commun 44:4611–4613
Glaser RH, Wilkes GL (1989) Solid-state 29Si NMR of TEOS-based multifunctional sol-gel materials. J Non-Cryst Solids 113:73–87
Gupta RP (1985) Electronic structure of crystalline and amorphous silicon dioxide. Phys Rev B 32(12):8278–8292
Gupta R, Chaudhury NK (2007) Entrapment of biomolecules in sol-gel matrix for applications in biosensors: problems and future prospects. Biosens Bioelectron 22(11):2387–2399
Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35(1):87–123
Hagemann M, Jeanjean R, Fulda S, Havaux M, Joset F, Erdmann N (1999) Flavodoxin accumulation contributes to enhanced cyclic electron flow around photosystem I in salt-stressed cells of Synechocystis sp. strain PCC 6803. Physiol Plant 105(4):670–678
Hench LL (1998) Sol-gel silica: properties, processing and technology transfer. Noyes Publications, Westwood
Ibach H (2006) Physics of surfaces and interfaces. Springer, Berlin
Iler RK (1979) The chemistry of silica. Wiley, New York
Jiang HM, Zheng Z, Li ZM, Wang XL (2006) Effects of temperature and solvent on the hydrolysis of alkoxysilane under alkaline conditions. Ind Eng Chem Res 45(25):8617–8622
Jin W, Brennan JD (2002) Properties and applications of proteins encapsulated within sol-gel derived materials. Anal Chim Acta 461:1–36
Kandimalla V, Tripathi V, Ju H (2006) Immobilization of biomolecules in sol-gels: biological and analytical applications. Crit Rev Anal Chem 36(2):73–106
Kay BD, Assink RA (1988) Sol-gel kinetics: II. Chemical speciation modeling. J Non-Cryst Solids 104(1):112–122
Kelts LW, Armstrong NJ (1989) A silicon-29 NMR study of the structural intermediates in low pH sol-gel reactions. J Mater Res 4(2):423–433
Klein LC (1985) Sol-gel processing of silicates. Annu Rev Mater Res 15:227–248
Kondo K, Ochiai Y, Katayama M, Ikeuchi M (2007) The membrane-associated CpcG2-phycobilisome in Synechocystis: a new photosystem I antenna. Plant Physiol 144(2):1200–1210
Kondo K, Mullineaux CW, Ikeuchi M (2009) Distinct roles of CpcG1-phycobilisome and CpcG2-phycobilisome in state transitions in a cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 99:217–225
Koslowski T, Kob W, Vollmayr K (1997) Numerical study of the electronic structure of amorphous silica. Phys Rev B 56(15):9469–9476
Kriegl JM, Forster FK, Nienhaus GU (2003) Charge recombination and protein dynamics in bacterial photosynthetic reaction centers entrapped in a sol-gel matrix. Biophys J 85:1851–1870
Kuncova G, Podrazky O (2004) Monitoring of the viability of cells immobilized by sol-gel process. J Sol-Gel Sci Technol 31:335–342
Laughlin RB, Joannopoulos JD, Chadi DJ (1979) Bulk electronic structure of SiO2. Phys Rev B 20(12):52285237
Leonard A, Rooke JC, Meunier CF, Sarmento H, Descy J-P, Su B-L (2010) Cyanobacteria immobilised in porous silica gels: exploring biocompatible synthesis routes for the development of photobioreactors. Energy Environ Sci 3(3):370–377
Leonard A, Dandoy P, Danloy E, Leroux G, Meunier CF, Rooke JC, Su B-L (2011) Whole-cell based hybrid materials for green energy production, environmental remediation and smart cell-therapy. Chem Soc Rev 40(2):860–885
Livage J, Coradin T, Roux C (2001) Encapsulation of biomolecules in silica gels. J Phys Condens Matter 13:R673–R691
Lu X (2010) A perspective: Photosynthetic production of fatty acid-based biofuels in genetically engineered cyanobacteria. Biotechnol Adv 28(6):742–746
Marin K, Huckauf J, Fulda S, Hagemann M (2002) Salt-dependent expression of glucosylglycerol-phosphate synthase, involved in osmolyte synthesis in the cyanobacterium Synechocystis sp. Strain PCC 6803. J Bacteriol 84(11):2870–2877
McCormick A (1994) Recent progress in the study of the kinetics of sol-gel SiO2 synthesis reactions. In: Attia YA (ed) Sol-gel processing and applications. Plenum, New York pp, pp 3–16
Meunier CF, Dandoy P, Su BL (2010) Encapsulation of cells within silica matrixes: towards a new advance in the conception of living hybrid materials. J Colloid Interface Sci 342:211–224
Muallem A, Bruce D, Hall DO (1983) Photoproduction of H-2 and NADPH2 by polyurethane-immobilized cyanobacteria. Biotechnol Lett 5(6):365–368
Nair BN, Elferink WJ, Keizer K, Verweij H (1996) Sol-gel synthesis and characterization of microporous silica membranes I: SAXS study on the growth of polymeric structures. J Colloid Interface Sci 178(2):565–570
Nassif N (2002) Living bacteria in silica gels. Nat Mater 1:42–44
Nassif N, Cc R, Coradin T, Rager M-N, Bouvet OMM, Livage J (2003) A sol-gel matrix to preserve the viability of encapsulated bacteria. J Mater Chem 13:203–208
Nassif N, Roux C, Coradin T, Bouvet OMM, Livage J (2004) Bacteria quorum sensing in silica matrices. J Mater Chem 14:2264–2268
Nguyen-Ngoc H, Tran-Minh C (2007a) Sol-gel process for vegetal cell encapsulation. Mater Sci Eng C 27(4):607–611
Nguyen-Ngoc H, Tran-Minh C (2007b) Fluorescent biosensor using whole cells in an inorganic translucent matrix. Anal Chim Acta 583(1):161–165
Nieto A, Areva S, Wilson T, Viitala R, Vallet-Regi M (2009) Cell viability in a wet silica gel. Acta Biomater 5(9):3478–3487
Pang JB, Qiu KY, Wei Y (2001) Preparation of mesoporous silica materials with non-surfactant hydroxy-carboxylic acid compounds as templates via sol-gel process. J Non-Cryst Solids 283(2–3):101–108
Parmer A, Singh NK, Pandey A, Gnansounou E, Madamwar D (2011) Cyanobacteria and microalgae: a positive prospect for biofuels. Bioresour Technol 102(22):10163–10172
Perullini M, Amoura M, Roux C, Coradin T, Livage J, Japas ML, Jobbagy M, Bilmes SA (2011) Improving silica matrices for encapsulation of Escherichia coli using osmoprotectors. J Mater Chem 21(12):4546–4552
Pierre AC (2004) The sol-gel encapsulation of enzymes. Biocat Biotrans 22(3):145–170
Pope EJA, Mackenzie JD (1986) Sol-gel processing of silica II: the role of the catalyst. J Non-Cryst Solids 87:185–198
Pope EJA, Braun K, Peterson CM (1997) Bioartificial organs I: Silica gel encapsulated pancreatic islets for the treatment of diabetes mellitus. J Sol-Gel Sci Technol 8:635–639
Pouxviel JC, Boilot JP, Beloeil JC, Lallemand JY (1987) NMR study of the sol-gel polymerization. J Non-Cryst Solids 89:345–360
Pressi G, Toso RD, Monte RD (2003) Production of enzymes by plant cells immobilized by sol-gel silica. J Sol-Gel Sci Technol 26:1189–1193
Raman NK, Wallace S, Brinker CJ (1996) Shrinkage and microstructural development during drying of organically modified silica xerogels. Mater Res Soc Symp Proc 435:6
Reetz MT, Tielmann P, Wiesenhofer W, Konen W, Zonta A (2003) Second generation sol-gel encapsulated lipases: robust heterogeneous biocatalysts. Adv Synth Catal 345:717–728
Ren L, Tsuru K, Hayakawa S, Osaka A (2001) Synthesis and characterization of gelatin-siloxane hybrids derived through sol-gel procedure. J Sol-Gel Sci Technol 21:115–121
Rooke JC, Leonard A, Su BL (2008) Targeting photobioreactors: Immobilisation of cyanobacteria within porous silica gel using biocompatible methods. J Mater Chem 18:1333–1341
Stephens E, Ross IL, Mussgnug JH, Wagner LD, Borowitzka MA, Posten C, Kruse O, Hankamer B (2010) Future prospects of microalgal biofuel production systems. Trends Plant Sci 15(10):554–564
Taylor A, Finnie KS, Bartlett JR, Holden PJ (2004) Encapsulation of viable aerobic microorganisms in silica gels. J Sol-Gel Sci Technol 32:223–228
Yoldas BE (1979) Monolithic glass formation by chemical polymerization. J Mater Sci 14(8):1843–1849
Yu D, Volponi J, Chhabra S, Brinker CJ, Mulchandani A, Singh AK (2005) Aqueous sol-gel encapsulation of genetically engineered Moraxella spp. cells for the detection of organophosphates. Biosens Bioelectron 20(7):1433–1437
Zadvorny OA, Barrows AM, Zorin NA, Peters JW, Elgren TE (2010) High level of hydrogen production activity achieved for hydrogenase encapsulated in sol–gel material doped with carbon nanotubes. J Mater Chem 20:1065–1067
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dickson, D.J., Ely, R.L. Silica sol-gel encapsulation of cyanobacteria: lessons for academic and applied research. Appl Microbiol Biotechnol 97, 1809–1819 (2013). https://doi.org/10.1007/s00253-012-4686-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-012-4686-8