Encapsulation of cells within silica matrixes: Towards a new advance in the conception of living hybrid materials.

Living cells can be considered as a highly efficient molecular engines spatially enclosed, remaining however fragile. By combining cells with silica materials in an appropriate way, novel living hybrid material technologies can be designed. After showing the real interplay between silica species and living organisms in nature, this featuring article summarizes the considerable progress in cell encapsulation into silica matrixes. Generally speaking, bioencapsulation allows protecting cells from harsh environment and controlling their surrounding as well as their concentration. This combination produces ultimately a device that can be oriented to drive the desired biochemical reactions. Particularly, this article highlights that functional living matters are very promising in the development of new eco-friendly processes. Compared to conventional chemical process, these hybrid systems would be enabled to use greater and in more efficient way renewable resources (i.e. solar energy) to produce a vast array of chemicals. Additionally, encapsulated cell technology has opened the possibility to design various other kinds of bioactive materials such as cleaning systems, biosensors and artificial organs. Through different examples, including the immobilization of microorganisms, photosynthetic organelles, plant cells and animal cells, the interests and the preparation methods of these living hybrid materials are discussed.

[1]  S. Dirè,et al.  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 , 1989 .

[2]  Jan Roelof van der Meer,et al.  Whole-cell living biosensors—are they ready for environmental application? , 2006, Applied Microbiology and Biotechnology.

[3]  C. Exley.  Silicon in life : A bioinorganic solution to bioorganic essentiality , 1998 .

[4]  Mercedes Perullini,et al.  Cell Growth at Cavities Created Inside Silica Monoliths Synthesized by Sol−Gel , 2005 .

[5]  Eric C. Carnes,et al.  Cell-directed localization and orientation of a functional foreign transmembrane protein within a silica nanostructure. , 2009, Journal of the American Chemical Society.

[6]  M. Abdel-Latif,et al.  Bioaccumulation of some hazardous metals by sol–gel entrapped microorganisms , 1999 .

[7]  Eric C. Carnes,et al.  Cell-directed assembly of bio/nano interfaces-a new scheme for cell immobilization. , 2007, Accounts of chemical research.

[8]  O. Belykh,et al.  Silicon mineralization in the culture of cyanobacteria from hot springs , 2006, Doklady Biological Sciences.

[9]  G. Carturan,et al.  Production of Valuable Drugs from Plant Cells Immobilized by Hybrid Sol-Gel SiO2 , 1998 .

[10]  C. Xia,et al.  Efficient immobilization of whole cells of Methylomonas sp. strain GYJ3 by sol–gel entrapment , 2004 .

[11]  E. Malchiodi,et al.  Production of recombinant proteins by sol–gel immobilized Escherichia coli , 2006 .

[12]  Swapnil Chhabra,et al.  Aqueous sol-gel encapsulation of genetically engineered Moraxella spp. cells for the detection of organophosphates. , 2005, Biosensors & bioelectronics.

[13]  B. Su,et al.  Targeting photobioreactors: Immobilisation of cyanobacteria within porous silica gel using biocompatible methods , 2008 .

[14]  O. Lev,et al.  Encapsulation of luminous recombinant E. coli in sol-gel silicate films , 2001 .

[15]  T. Brányik,et al.  The use of silica gel prepared by sol-gel method and polyurethane foam as microbial carriers in the continuous degradation of phenol , 2000, Applied Microbiology and Biotechnology.

[16]  F. Lim,et al.  Microencapsulated islets as bioartificial endocrine pancreas. , 1980, Science.

[17]  O. Pines,et al.  Conversion of Fumaric Acid to l‐Malic by Sol‐Gel Immobilized Saccharomyces cerevisiae in a Supported Liquid Membrane Bioreactor , 2002, Biotechnology progress.

[18]  Xiao-Dong Zhou,et al.  In vitro toxicity of silica nanoparticles in human lung cancer cells. , 2006, Toxicology and applied pharmacology.

[19]  J. Bartlett,et al.  Encapsulation of sulfate-reducing bacteria in a silica host , 2000 .

[20]  C. Canlet,et al.  Metabolism of [14C]-2,4,6-trinitrotoluene in tobacco cell suspension cultures. , 2005, Environmental science & technology.

[21]  Wayne Ouellette,et al.  Cytotoxicity of mesoporous silica nanomaterials. , 2008, Journal of inorganic biochemistry.

[22]  C. Peterson,et al.  Silica Sol-Gel Encapsulation of Pancreatic Islets , 1998, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[23]  M. Tan,et al.  Bioencapsulation of living yeast (Pichia pastoris) with silica after transformation with lysozyme gene , 2008 .

[24]  K. Konhauser,et al.  DIVERSITY OF IRON AND SILICA PRECIPITATION BY MICROBIAL MATS IN HYDROTHERMAL WATERS, ICELAND : IMPLICATIONS FOR PRECAMBRIAN IRON FORMATIONS , 1996 .

[25]  G. Carturan,et al.  Production of Enzymes by Plant Cells Immobilized by Sol-Gel Silica , 2003 .

[26]  D. Avnir,et al.  Recent bio-applications of sol–gel materials , 2006 .

[27]  M. Sastry,et al.  Bacterial synthesis of silicon/silica nanocomposites , 2008 .

[28]  H. Ijima,et al.  Synthesis and transport characterization of alginate/aminopropyl-silicate/alginate microcapsule: application to bioartificial pancreas. , 2001, Biomaterials.

[29]  W. Pompe,et al.  Biosorption of Heavy Metals by Sol-Gel Immobilized Bacillus sphaericus Cells, Spores and S-Layers , 2003 .

[30]  H. Chang,et al.  Microencapsulation of microbial cells. , 2000, Biotechnology advances.

[31]  E. Arcalis,et al.  Plants as bioreactors: a comparative study suggests that Medicago truncatula is a promising production system. , 2005, Journal of biotechnology.

[32]  D. Ronen,et al.  Atrazine degradation by Pseudomonas strain ADP entrapped in sol-gel glass , 1996 .

[33]  Roberto C. Dante,et al.  Hypotheses for direct PEM fuel cells applications of photobioproduced hydrogen by Chlamydomonas reinhardtii , 2005 .

[34]  H. Sarmento,et al.  Photosynthesis within porous silica gel: viability and activity of encapsulated cyanobacteria , 2008 .

[35]  K. Schwarz,et al.  Growth-promoting Effects of Silicon in Rats , 1972, Nature.

[36]  C. Peterson,et al.  Bioartificial organs I: Silica gel encapsulated pancreatic islets for the treatment of diabetes mellitus , 1997 .

[37]  Shimshon Belkin,et al.  Fluorescence and bioluminescence reporter functions in genetically modified bacterial sensor strains , 2003 .

[38]  W. Pompe,et al.  Biosorption of Uranium and Copper by Biocers , 2003 .

[39]  N. Nassif,et al.  Bacteria quorum sensing in silica matrices , 2004 .

[40]  Shimshon Belkin,et al.  Advances in preservation methods: keeping biosensor microorganisms alive and active. , 2006, Current opinion in biotechnology.

[41]  T. Coradin,et al.  Sol–gel encapsulation of bacteria: a comparison between alkoxide and aqueous routes , 2001 .

[42]  Stephen Mann,et al.  Sol−Gel Synthesis of Organized Matter , 1997 .

[43]  P. Aebischer,et al.  The Dawn of Biotechnology in Artificial Organs , 1995, ASAIO journal.

[44]  Colin R. Janssen,et al.  Ecotoxicity of silica nanoparticles to the green alga pseudokirchneriella subcapitata: Importance of surface area , 2008, Environmental toxicology and chemistry.

[45]  M. Jobbágy,et al.  Optimizing silica encapsulation of living cells: in situ evaluation of cellular stress , 2008 .

[46]  R. Campostrini,et al.  Immobilization of plant cells in hybrid sol-gel materials , 1996 .

[47]  K. Konhauser,et al.  Experimental study of iron and silica immobilization by bacteria in mixed Fe-Si systems: implications for microbial silicification in hot springs , 2003 .

[48]  H. Böttcher,et al.  Utilization of sol–gel ceramics for the immobilization of living microorganisms , 2008 .

[49]  Victor Smetacek,et al.  Architecture and material properties of diatom shells provide effective mechanical protection , 2003, Nature.

[50]  S. Dirè,et al.  Entrapment of viable microorganisms by SiO2 sol-gel layers on glass surfaces: trapping, catalytic performance and immobilization durability of Saccharomyces cerevisiae. , 1993, Journal of Biotechnology.

[51]  N. Nassif,et al.  A sol–gel matrix to preserve the viability of encapsulated bacteria , 2003 .

[52]  P. V. Cutsem,et al.  Thylakoids entrapped within porous silica gel: towards living matter able to convert energy , 2009 .

[53]  J. Raven.  THE TRANSPORT AND FUNCTION OF SILICON IN PLANTS , 1983 .

[54]  J. Yun,et al.  Inside Cover: Catalytic Asymmetric Boration of Acyclic α,β‐Unsaturated Esters and Nitriles (Angew. Chem. Int. Ed. 1/2008) , 2008 .

[55]  M. Ferrer,et al.  Biocompatible Sol−Gel Route for Encapsulation of Living Bacteria in Organically Modified Silica Matrixes , 2003 .

[56]  Shinji Sakai,et al.  In vitro and in vivo evaluation of alginate/sol-gel synthesized aminopropyl-silicate/alginate membrane for bioartificial pancreas. , 2002, Biomaterials.

[57]  P. V. Cutsem,et al.  Investigation of different silica precursors: Design of biocompatible silica gels with long term bio-activity of entrapped thylakoids toward artificial leaf , 2009 .

[58]  W. Lutze.  Nuclear Waste Management in Europe , 1987 .

[59]  E. Pope.  Gel encapsulated microorganisms: Saccharomyces cerevisiae—Silica gel biocomposites , 1995 .

[60]  O. Lev,et al.  Fluorescent Bacteria Encapsulated in Sol−Gel Derived Silicate Films , 2002 .

[61]  D. Hall,et al.  The potential applications of cyanobacterial photosynthesis for clean technologies , 1995, Photosynthesis Research.

[62]  E. G. Vrieling,et al.  Diatom silicon biomineralization as an inspirational source of new approaches to silica production , 1999 .

[63]  M. Jobbágy,et al.  Plant cell proliferation inside an inorganic host. , 2007, Journal of biotechnology.

[64]  D. Koch,et al.  Freeze gelation: a new option for the production of biological ceramic composites (biocers) , 2003 .

[65]  E. Epstein.  The anomaly of silicon in plant biology. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[66]  E. Ryan,et al.  Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. , 2000, The New England journal of medicine.

[67]  D. G. Adams,et al.  Cyanobacterial viability during hydrothermal biomineralisation , 2000 .

[68]  Mamiko Sato,et al.  Size-dependent toxicity of silica nano-particles to Chlorella kessleri , 2008, Journal of environmental science and health. Part A, Toxic/hazardous substances & environmental engineering.

[69]  H. Ijima,et al.  Aminopropyl-silicate membrane for microcapsule-shaped bioartificial organs: control of molecular permeability , 2002 .

[70]  A. Granato,et al.  Encapsulation of hepatocytes by SiO2 , 2000 .

[71]  G. H. Algire,et al.  The diffusion-chamber technique applied to a study of the nature of homograft resistance. , 1954, Journal of the National Cancer Institute.

[72]  P. Vos,et al.  Cell encapsulation: Promise and progress , 2003, Nature Medicine.

[73]  Shimshon Belkin,et al.  Sol–gel luminescence biosensors: Encapsulation of recombinant E. coli reporters in thick silicate films , 2002 .

[74]  E. Zwierkowska,et al.  Application of cell-based biosensors for the detection of bacterial elicitor flagellin. , 2007, Bioelectrochemistry.

[75]  K. Konhauser,et al.  The effect of cyanobacteria on silica precipitation at neutral pH: implications for bacterial silicification in geothermal hot springs , 2003 .

[76]  I. Moreno-Garrido.  Microalgae immobilization: current techniques and uses. , 2008, Bioresource technology.

[77]  R. Newton,et al.  Growth enhancement of loblolly pine (Pinus taeda L.) seedlings by silicon , 1989 .

[78]  M. Power,et al.  Aerogels as biosensors: viral particle detection by bacteria immobilized on large pore aerogel , 2001 .

[79]  Stephen Mann,et al.  Life as a nanoscale phenomenon. , 2008, Angewandte Chemie.

[80]  R. Ely,et al.  Photobiological hydrogen production from Synechocystis sp. PCC 6803 encapsulated in silica sol–gel , 2009 .

[81]  G. Barrett,et al.  Genetically engineered whole-cell sensing systems: coupling biological recognition with reporter genes. , 2000, Chemical reviews.

[82]  M. Ferrer,et al.  Bacteria Viability in Sol−Gel Materials Revisited: Cryo-SEM as a Suitable Tool To Study the Structural Integrity of Encapsulated Bacteria , 2006 .

[83]  Deng-Fwu Hwang,et al.  In vitro cytotoxicitiy of silica nanoparticles at high concentrations strongly depends on the metabolic activity type of the cell line. , 2007, Environmental science & technology.

[84]  Eric C. Carnes,et al.  Cell-Directed Assembly of Lipid-Silica Nanostructures Providing Extended Cell Viability , 2006, Science.

[85]  E. M. Carlisle.  Silicon: An Essential Element for the Chick , 1972, Science.

[86]  E. M. Carlisle.  Silicon as a trace nutrient. , 1988, The Science of the total environment.

[87]  M. H. Adatia,et al.  The effects of silicon on cucumber plants grown in recirculating nutrient solution , 1986 .

[88]  Vincenzo Bisceglie,et al.  Über die antineoplastische Immunität , 1934, Zeitschrift für Krebsforschung.

[89]  R. Guzzon,et al.  Immobilization of yeast and bacteria cells in alginate microbeads coated with silica membranes: procedures, physico-chemical features and bioactivity , 2008 .

[90]  J. Trevors,et al.  Environmental applications of immobilized microbial cells: A review , 1996, Journal of Industrial Microbiology.

[91]  G. Gadd,et al.  Microbial treatment of metal pollution--a working biotechnology? , 1993, Trends in biotechnology.

[92]  N. Rivera,et al.  The effect of Fe on Si adsorption by Bacillus subtilis cell walls: insights into non-metabolic bacterial precipitation of silicate minerals , 2002 .

[93]  E. Malchiodi,et al.  Efficient preservation in a silicon oxide matrix of Escherichia coli, producer of recombinant proteins , 2005, Applied Microbiology and Biotechnology.

[94]  William A. Jacoby,et al.  Immobilized algal cells used for hydrogen production , 2007 .

[95]  J. Trevors.  Bacterial evolution and silicon , 1997, Antonie van Leeuwenhoek.

[96]  Carole C. Perry,et al.  Biosilicification: the role of the organic matrix in structure control , 2000, JBIC Journal of Biological Inorganic Chemistry.

[97]  N. Kröger,et al.  Silica deposition by a strongly cationic proline-rich protein from systemically resistant cucumber plants. , 2003, The Plant journal : for cell and molecular biology.

[98]  P. Kieran,et al.  Plant cell suspension cultures: some engineering considerations. , 1997, Journal of biotechnology.

[99]  S. Schultes,et al.  Grazing-induced changes in cell wall silicification in a marine diatom. , 2007, Protist.

[100]  D. Fiedler,et al.  Algae biocers: astaxanthin formation in sol–gel immobilised living microalgae , 2007 .

[101]  K. Konhauser,et al.  The dynamics of cyanobacterial silicification: an infrared micro-spectroscopic investigation 1 1 Associate editor: J. P. Amend , 2004 .

[102]  Peter T. Shepherd,et al.  Focus on biotechnology , 1982 .

[103]  N. Mallick.  Biotechnological potential of immobilized algae for wastewater N, P and metal removal: A review , 2002, Biometals.

[104]  J. Meunier.  Le rôle des plantes dans le transfert du silicium à la surface des continents , 2003 .

[105]  N. Nassif,et al.  Living bacteria in silica gels , 2002, Nature materials.

[106]  P. Lopez,et al.  Sol-gel encapsulation extends diatom viability and reveals their silica dissolution capability. , 2006, Chemical communications.

[107]  R. Buchholz,et al.  New processes and actual trends in biotechnology , 1995 .