Alginate/porous silica matrices for the
encapsulation of living organisms: tunable
properties for biosensors, modular bioreactors,
and bioremediation devices

• Authors: Mercedes Perullini , Mariano Calcabrini , Matías Jobbágy , Sara A. Bilmes
• Languages of publication: EN

Abstracts

EN

The encapsulation of living cells within inorganic
silica hydrogels is a promising strategy for the design
of biosensors, modular bioreactors, and bioremediation
devices, among other interesting applications, attracting
scientific and technological interest. These hostguest
multifunctional materials (HGFM) combine synergistically
specific biologic functions of their guest with
those of the host matrix enhancing their performance.
Although inorganic immobilization hosts present several
advantages over their (bio)polymer-based counterparts in
terms of chemical and physical stability, the direct contact
of cells with silica precursors during synthesis and
the constraints imposed by the inorganic host during operating
conditions have proved to influence their biological
response. Recently, we proposed an alternative two-step
procedure including a pre-encapsulation in biocompatible
polymers such as alginates in order to confer protection
to the biological guest during the inorganic and more cytotoxic
synthesis. By means of this procedure, whole cultures
of microorganisms remain confined in small liquid
volumes generated inside the inorganic host, providing
near conventional liquid culture conditions.Moreover, the
fact of protecting the biological guest during the synthesis
of the host, allows extending the synthesis parameters
beyond biocompatible conditions, tuning the microstructure
of the matrix. In turn, the microstructure (porosity at
the nanoscale, radius of gyration of particles composing
the structure, and fractal dimension of particle clusters)
is determinant of macroscopic parameters, such as optical
quality and transport properties that govern the encapsulation
material’s performance. Here, we review the most
interesting applications of the two-step procedure, making
special emphasis on the optimization of optical, transport
and mechanical properties of the host as well as in the interaction
with the guest during operation conditions.

Keywords

EN

Sol-gel; whole-culture encapsulation; mesoporous; bioremediation; biosensing; bioreactors

• Publisher: De Gruyter Open
• Journal: Mesoporous Biomaterials
• Year: 2015
• Volume: 2
• Issue: 1

Dates

accepted

22 - 7 - 2015

online

28 - 8 - 2015

received

5 - 6 - 2015

Contributors

author

Mercedes Perullini

• INQUIMAE-DQIAQF,
  Facultad de Ciencias Exactas y Naturales, Universidad de Buenos
  Aires. Ciudad Universitaria, Pab. II, C1428EHA, Buenos Aires, Argentina

author

Mariano Calcabrini

• INQUIMAE-DQIAQF,
  Facultad de Ciencias Exactas y Naturales, Universidad de Buenos
  Aires. Ciudad Universitaria, Pab. II, C1428EHA, Buenos Aires, Argentina

author

Matías Jobbágy

• INQUIMAE-DQIAQF,
  Facultad de Ciencias Exactas y Naturales, Universidad de Buenos
  Aires. Ciudad Universitaria, Pab. II, C1428EHA, Buenos Aires, Argentina

author

Sara A. Bilmes

• INQUIMAE-DQIAQF,
  Facultad de Ciencias Exactas y Naturales, Universidad de Buenos
  Aires. Ciudad Universitaria, Pab. II, C1428EHA, Buenos Aires, Argentina

References

• [1] Blondeau, M. and T. Coradin, Living materials from sol-gelchemistry: current challenges and perspectives. Journal ofMaterials Chemistry, 2012. 22(42): p. 22335-22343.[Crossref]
• [2] Kuncová, G. and J. Trögl, Physiology of microorganisms immobilizedinto inorganic polymers, in Handbook of Inorganic ChemistryResearch. 2011. p. 53-101.
• [3] Coradin, T., N. Nassif, and J. Livage, Silica-alginate compositesfor microencapsulation. Applied Microbiology and Biotechnology,2003. 61(5-6): p. 429-434.[Crossref]
• [4] Depagne, C., C. Roux, and T. Coradin, How to design cell-basedbiosensors using the sol-gel process. Analytical BioanalyticalChemistry, 2011. 400(4): p. 965-976.
• [5] Brinker, C.J. and G.W. Scherrer, Sol-Gel Science, 1990.
• [6] Nassif, N. and J. Livage, From diatoms to silica-based biohybrids.Chemical Society Reviews, 2011. 40(2): p. 849-859.[Crossref]
• [7] Gill, I. and A. Ballesteros, Bioencapsulation within syntheticpolymers (Part 1): Sol-gel encapsulated biologicals. Trends inBiotechnology, 2000. 18(7): p. 282-296.[Crossref]
• [8] Livage, J., T. Coradin, and C. Roux, Encapsulation ofbiomolecules in silica gels. Journal of Physics CondensedMatter, 2001. 13(33): p. R673-R691.[Crossref]
• [9] Carturan, G., et al., Encapsulation of functional cells by sol-gelsilica: Actual progress and perspectives for cell therapy. Journalof Materials Chemistry, 2004. 14(14): p. 2087-2098.[Crossref]
• [10] Vallet-Regí, M. and E. Ruiz-Hernández, Bioceramics: From boneregeneration to cancer nanomedicine. Advanced Materials,2011. 23(44): p. 5177-5218.[Crossref]
• [11] Ferrer, M.L., F. Del Monte, and D. Levy, A novel and simplealcohol-free sol-gel route for encapsulation of labile proteins.Chemistry of Materials, 2002. 14(9): p. 3619-3621.[Crossref]
• [12] Meunier, C.F., et al., Living hybrid materials capable of energyconversion and CO2 assimilation Chemical Communications,2010. 46: p. 3843-3859.
• [13] Nassif, N., et al., A sol-gel matrix to preserve the viability ofencapsulated bacteria. Journal of Materials Chemistry, 2003.13(2): p. 203-208.[Crossref]
• [14] Perullini, M., et al., Improving silica matrices for encapsulationof Escherichiacoli using osmoprotectors. Journal of MaterialsChemistry. 21(12): p. 4546-4552.
• [15] Perullini, M., et al., Cell growth at cavities created inside silicamonoliths synthesized by sol-gel. Chemistry ofMaterials, 2005.17(15): p. 3806-3808.
• [16] De Vos, P., et al., Polymers in cell encapsulation from anenveloped cell perspective. Advanced Drug Delivery Reviews,2014. 67-68: p. 15-34.
• [17] Zimmermann, H., S.G. Shirley, and U. Zimmermann, Alginatebasedencapsulation of cells: Past, present, and future. CurrentDiabetes Reports, 2007. 7(4): p. 314-320.[Crossref]
• [18] Boninsegna, S., R. Dal Toso, and R. Dal Monte, Alginate microspheresloaded with animal cells and coated by a siliceouslayer. Journal of Sol-Gel Science and Technology, 2003. 26(1-3):p. 1151-1157.[Crossref]
• [19] Perullini, M., et al., Silica-alginate-fungi biocomposites for remediationof polluted water. Journal of Materials Chemistry.20(31): p. 6479-6483.
• [20] Duarte, K.R., et al., Treatment of olive oil mill wastewater bysilica-alginate-fungi biocomposites. Water, Air, and Soil Pollution,2012. 223(7): p. 4307-4318.
• [21] Perullini, M., et al., Plant cell proliferation inside an inorganichost. Journal of Biotechnology, 2007. 127(3): p. 542-548.[Crossref]
• [22] Perullini, M., et al., Sol-gel silica platforms for microalgaebasedoptical biosensors. Journal of Biotechnology, 2014.179(1): p. 65-70.[Crossref]
• [23] Perullini, M., et al., Co-encapsulation of Daphnia magna and microalgaein silica matrices, a stepping stone toward a portablemicrocosm. Biotechnology Reports, 2014. 4(1): p. 147-150.[Crossref]
• [24] Kieran, P.M., P.F. MacLoughlin, and D.M. Malone, Plant cell suspensioncultures: some engineering considerations. Journal ofBiotechnology, 1997. 59(1–2): p. 39-52.[Crossref]
• [25] Eleftheriou, N.M., et al., Entrapment of living bacterial cells inlow-concentration silica materials preserves cell division andpromoter regulation. Chemistry of Materials, 2013. 25(23): p.4798-4805.[Crossref]
• [26] Perullini, M., et al., Optimizing silica encapsulation of livingcells: In situ evaluation of cellular stress. Chemistry ofMaterials, 2008. 20(9): p. 3015-3021.[Crossref]
• [27] Kuncova, G., et al., Monitoring of the viability of cells immobilizedby sol-gel process. Journal of Sol-Gel Science and Technology,2004. 31(1-3 SPEC.ISS.): p. 335-342.[Crossref]
• [28] Perullini, M., et al., Optimizing silica encapsulation of livingcells: In situ evaluation of cellular stress. Chemistry ofMaterials, 2008. 20(9): p. 3015-3021.[Crossref]
• [29] Sakai, S., et al., Newly Developed Aminopropyl-Silicate ImmunoisolationMembrane for a Microcapsule-Shaped Bioarti ficial Pancreas. Annals of the New York Academy of Sciences,2001. 944(1): p. 277-283.
• [30] Perullini, M., et al., Improving bacteria viability in metal oxidehosts via an alginate-based hybrid approach. Journal ofMaterials Chemistry, 2011. 21(12): p. 8026-8031.[Crossref]
• [31] Amoura, M., et al., Bacteria encapsulation in colloidal inorganicmatrices: is it a general method? Comptes Rendus del’Academie des Sciences - Series IIc: Chemistry, 2010. 13: p. 52-57.
• [32] Sicard, C., et al., CeO2 Nanoparticles for the Protection of PhotosyntheticOrganisms Immobilized in Silica Gels. Chemistry ofMaterials, 2011. 23(6): p. 1374-1378.[Crossref]
• [33] Perullini, M., et al., Rhodamine B doped silica encapsulationmatrices for the protection of photosynthetic organisms. Journalof Biotechnology, 2014. 184: p. 94-99.
• [34] Perullini, M., et al., Effect of synthesis conditions on the microstructureof TEOS derived silica hydrogels synthesized by thealcohol-free sol-gel route. Journal of Sol-Gel Science and Technology,2011. 59(1): p. 174-180.[Crossref]
• [35] Perullini, M., et al., New method for the simultaneous determinationof diffusion and adsorption of dyes in silica hydrogels.Journal of Colloid and Interface Science, 2014. 425: p. 91-95.
• [36] Perullini, M., Levinson, N., Jobbágy, M., Bilmes, S. A., ComprehensiveSAXS based microstructure and transport propertiescharacterization of biocompatible silica hydrogels, in press.
• [37] Perullini, M., et al., Improving silica matrices for encapsulationof Escherichia coli using osmoprotectors. Journal of MaterialsChemistry, 2011. 21(12): p. 4546-4552.[Crossref]
• [38] Drury, J.L. and D.J. Mooney, Hydrogels for tissue engineering:scaffold design variables and applications. Biomaterials, 2003.24(24): p. 4337-4351.[Crossref]
• [39] Gombotz, W.R. and S.F. Wee, Protein release from alginate matrices.Advanced Drug Delivery Reviews, 1998. 31(3): p. 267-285.[Crossref]
• [40] Smidsrod, O. and G. Skjakbraek, Alginate as ImmobilizationMatrix for Cells. Trends in Biotechnology, 1990. 8(3): p. 71-78.[Crossref]
• [41] Rowley, J.A., G.Madlambayan, and D.J. Mooney, Alginate hydrogelsas synthetic extracellular matrix materials. Biomaterials,1999. 20(1): p. 45-53.[Crossref]
• [42] Smidsrod, O., Properties of Poly(1,4-Hexuronates) in Gel State.2. Comparison of Gels of Different Chemical Composition. ActaChemica Scandinavica, 1972. 26(1): p. 79-88.
• [43] Brayner, R., et al., Alginate-Mediated Growth of Co, Ni, and CoNiNanoparticles: Influence of the Biopolymer Structure. Chemistryof Materials, 2007. 19(5): p. 1190-1198.[Crossref]
• [44] Agulhon, P., et al., Controlled synthesis from alginate gelsof cobalt–manganese mixed oxide nanocrystals with peculiarmagnetic properties. Catalysis Today, 2012. 189(1): p. 49-54.
• [45] Monakhova, Y., et al., Newmixed lanthanum- and alkaline-earthcation-containing basic catalysts obtained by an alginate route.Catalysis Today, 2012. 189(1): p. 28-34.
• [46] Liu, F., et al., Photoluminescent porous alginate hybridmaterials containing lanthanide ions. Biomacromolecules,2008. 9(7): p. 1945-50.[Crossref]
• [47] Haug, A. and O. Smidsrřd, Strontium–Calcium Selectivity of Alginates.Nature, 1967. 215(5102): p. 757-757.
• [48] Draget, K.I., G.S. Braek, and O. Smidsrod, Alginic Acid Gels - theEffect of Alginate Chemical-Composition andMolecular-Weight.Carbohydrate Polymers, 1994. 25(1): p. 31-38.[Crossref]
• [49] Korda, A., et al., Petroleumhydrobcarbon bioremediation: Samplingand analytical techniques, in situ treatments and commercialmicroorganisms currently used. Applied Microbiology andBiotechnology, 1997. 48(6): p. 677-686.[Crossref]
• [50] Farhadian, M., et al., In situ bioremediation of monoaromaticpollutants in groundwater: A review. Bioresource Technology,2008. 99(13): p. 5296-5308.[Crossref]
• [51] Ellis, D.E., et al., Bioaugmentation for accelerated in situ anaerobicbioremediation. Environmental Science and Technology,2000. 34(11): p. 2254-2260.[Crossref]
• [52] Cerqueira, V.S., et al., Comparison of bioremediation strategiesfor soil impacted with petrochemical oily sludge. InternationalBiodeterioration and Biodegradation, 2014. 95(PB): p. 338-345.[Crossref]
• [53] Sarkar, D., et al., Bioremediation of petroleum hydrocarbons incontaminated soils: Comparison of biosolids addition, carbonsupplementation, and monitored natural attenuation. EnvironmentalPollution, 2005. 136(1): p. 187-195.
• [54] Bento, F.M., et al., Comparative bioremediation of soils contaminatedwith diesel oil by natural attenuation, biostimulationand bioaugmentation. Bioresource Technology, 2005. 96(9): p.1049-1055.[Crossref]
• [55] Perullini, M., et al., Silica-alginate-fungi biocomposites for remediationof polluted water. Journal of Materials Chemistry,2010. 20(31): p. 6479-6483.[Crossref]
• [56] Carro, L., E. Hablot, and T. Coradin, Hybrids and biohybrids asgreen materials for a blue planet. Journal of Sol-Gel Science andTechnology, 2014. 70(2): p. 263-271.[Crossref]
• [57] Tuttolomondo, M.V., et al., Removal of azo dyes from water bysol-gel immobilized Pseudomonas sp. Journal of EnvironmentalChemical Engineering, 2014. 2(1): p. 131-136.
• [58] Alvarez, G.S., et al., A functional material that combines theCr(vi) reduction activity of Burkholderia sp. with the adsorbentcapacity of sol-gel materials. Journal of Materials Chemistry,2011. 21(17): p. 6359-6364.[Crossref]
• [59] Ramachandran, S., et al., Nostoc calcicola immobilized in silicacoatedcalcium alginate and silica gel for applications in heavymetal biosorption. Silicon, 2010. 1(4): p. 215-223.[Crossref]
• [60] Soltmann, U., Matys, S., Kieszig, G.. Pompe, W., Böttcher, H.,Algae-Silica HybridMaterials for Biosorption of Heavy Metals, J.Water Resource and Protection, 2010, 2, p. 115-122.
• [61] Duarte, K.R., et al., Removal of phenolic compounds in olivemill wastewater by silica-alginate-fungi biocomposites. InternationalJournal of Environmental Science and Technology, 2014.11(3): p. 589-596.[Crossref]
• [62] Premkumar, J.R., et al., Encapsulation of luminous recombinantE. coli in Sol-gel silicate films. AdvancedMaterials, 2001. 13(23):p. 1773.
• [63] Premkumar, J.R., et al., Sol-gel luminescence biosensors: Encapsulationof recombinant E. coli reporters in thick silicatefilms. Analytica Chimica Acta, 2002. 462(1): p. 11-23.
• [64] Nguyen-Ngoc, H. and C. Tran-Minh, Fluorescent biosensor usingwhole cells in an inorganic translucent matrix. Analytica ChimicaActa, 2007. 583(1): p. 161-165.
• [65] Peńa-Vázquez, E., et al., Microalgae fiber optic biosensors forherbicide monitoring using sol–gel technology. Biosensors andBioelectronics, 2009. 24(12): p. 3538-3543.[Crossref]
• [66] Ferro, Y., et al., Development of a biosensor for environmentalmonitoring based on microalgae immobilized in silica hydrogels.Sensors (Switzerland), 2012. 12(12): p. 16879-16891.[Crossref]
• [67] Pannier, A., et al., Alginate/silica hybrid materials for immobilizationof green microalgae Chlorella vulgaris for cell-basedsensor arrays. Journal of Materials Chemistry B, 2014. 2(45): p.7896-7909.[Crossref]
• [68] Kempf, B. and E. Bremer, Uptake and synthesis of compatiblesolutes as microbial stress responses to high-osmolality environments.Archives of Microbiology, 1998. 170(5): p. 319-330.[Crossref]
• [69] Sicard, C., et al., Nano-gold biosynthesis by silica-encapsulatedmicro-algae: A "living" bio-hybrid material. Journal of MaterialsChemistry, 2010. 20(42): p. 9342-9347.[Crossref]
• [70] Spedalieri, C., et al., Silica@proton-alginate microreactors: Aversatile platform for cell encapsulation. Journal of MaterialsChemistry B, 2015. 3(16): p. 3189-3194.[Crossref]

Identifiers

DOI

10.1515/mesbi-2015-0003