Influence of silica matrix composition and functional component additives on the bioactivity and viability of encapsulated living cells

Savage, Travis J.; Dunphy, Darren R.; Harbaugh, Svetlana; Kelley-Loughnane, Nancy; Harper, Jason C.; Brinker, C. Jeffrey

doi:10.1021/acsbiomaterials.5b00261

Title: Influence of silica matrix composition and functional component additives on the bioactivity and viability of encapsulated living cells

Journal Article · Fri Nov 06 00:00:00 EST 2015 · ACS Biomaterials Science & Engineering

DOI:https://doi.org/10.1021/acsbiomaterials.5b00261· OSTI ID:1340691

Savage, Travis J. ^[1]; Dunphy, Darren R. ^[1]; Harbaugh, Svetlana ^[2]; Kelley-Loughnane, Nancy ^[2]; Harper, Jason C. ^[3]; Brinker, C. Jeffrey ^[4]

Univ. of New Mexico, Albuquerque, NM (United States)
Wright Patterson Air Force Base, Dayton, OH (United States)
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Univ. of New Mexico, Albuquerque, NM (United States); Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

The remarkable impact encapsulation matrix chemistry can have on the bioactivity and viability of integrated living cells is reported. Two silica chemistries (aqueous silicate and alkoxysilane), and a functional component additive (glycerol), are employed to generate three distinct silica matrices. These matrices are used to encapsulate living E. coli cells engineered with a synthetic riboswitch for cell-based biosensing. Following encapsulation, membrane integrity, reproductive capability, and riboswitch-based protein expression levels and rates are measured over a 5 week period. Striking differences in E. coli bioactivity, viability, and biosensing performance are observed for cells encapsulated within the different matrices. E. coli cells encapsulated for 35 days in aqueous silicate-based (AqS) matrices showed relatively low membrane integrity, but high reproductive capability in comparison to cells encapsulated in glycerol containing sodium silicate-based (AqS + g) and alkoxysilane-based (PGS) gels. Further, cells in sodium silicate-based matrices showed increasing fluorescence output over time, resulting in a 1.8-fold higher fluorescence level, and a faster expression rate, over cells free in solution. Furthermore, this unusual and unique combination of biological properties demonstrates that careful design of the encapsulation matrix chemistry can improve functionality of the biocomposite material, and result in new and unexpected physiological states.

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Research Organization:: Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC04-94AL85000

OSTI ID:: 1340691

Report Number(s):: SAND-2017-0555J; 650542

Journal Information:: ACS Biomaterials Science & Engineering, Vol. 1, Issue 12; ISSN 2373-9878

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 11 works

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References (47)

Advances in Biomimetic and Nanostructured Biohybrid Materials Ruiz-Hitzky, Eduardo; Darder, Margarita; Aranda, Pilar Advanced Materials, Vol. 22, Issue 3 https://doi.org/10.1002/adma.200901134	journal	January 2010
Bio-inspired encapsulation and functionalization of living cells with artificial shells Wang, Sha; Guo, Zhiguang Colloids and Surfaces B: Biointerfaces, Vol. 113 https://doi.org/10.1016/j.colsurfb.2013.09.024	journal	January 2014
Whole-cell biochips for bio-sensing: integration of live cells and inanimate surfaces Ben-Yoav, Hadar; Melamed, Sahar; Freeman, Amihay Critical Reviews in Biotechnology, Vol. 31, Issue 4 https://doi.org/10.3109/07388551.2010.532767	journal	November 2010
From diatoms to silica-based biohybrids Nassif, Nadine; Livage, Jacques Chemical Society Reviews, Vol. 40, Issue 2 https://doi.org/10.1039/C0CS00122H	journal	January 2011
Whole-cell based hybrid materials for green energy production, environmental remediation and smart cell-therapy Léonard, Alexandre; Dandoy, Philippe; Danloy, Emeric Chemical Society Reviews, Vol. 40, Issue 2 https://doi.org/10.1039/c0cs00024h	journal	January 2011
Living hybrid materials capable of energy conversion and CO2 assimilation Meunier, Christophe F.; Rooke, Joanna C.; Léonard, Alexandre Chemical Communications, Vol. 46, Issue 22 https://doi.org/10.1039/c001799j	journal	January 2010
Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria Carnes, Eric C.; Lopez, DeAnna M.; Donegan, Niles P. Nature Chemical Biology, Vol. 6, Issue 1 https://doi.org/10.1038/nchembio.264	journal	November 2009
Microbial cells as catalysts for stereoselective red–ox reactions Carballeira, J. D.; Quezada, M. A.; Hoyos, P. Biotechnology Advances, Vol. 27, Issue 6 https://doi.org/10.1016/j.biotechadv.2009.05.001	journal	November 2009
Sol-gel Chemistry in Medicinal Science Coradin, Thibaud; Boissiere, Michel; Livage, Jacques Current Medicinal Chemistry, Vol. 13, Issue 1 https://doi.org/10.2174/092986706789803044	journal	January 2006
Immobilization of Biomolecules in Sol–Gels: Biological and Analytical Applications Kandimalla, Vivek Babu; Tripathi, Vijay Shyam; Ju, Huangxian Critical Reviews in Analytical Chemistry, Vol. 36, Issue 2 https://doi.org/10.1080/10408340600713652	journal	July 2006
Protein and cell micropatterning and its integration with micro/nanoparticles assembly Yap, F. L.; Zhang, Y. Biosensors and Bioelectronics, Vol. 22, Issue 6 https://doi.org/10.1016/j.bios.2006.03.016	journal	January 2007
Entrapment of biomolecules in sol–gel matrix for applications in biosensors: Problems and future prospects Gupta, R.; Chaudhury, N. K. Biosensors and Bioelectronics, Vol. 22, Issue 11 https://doi.org/10.1016/j.bios.2006.12.025	journal	May 2007
Bio-doped Nanocomposite Polymers: Sol−Gel Bioencapsulates Gill, Iqbal Chemistry of Materials, Vol. 13, Issue 10 https://doi.org/10.1021/cm0102483	journal	October 2001
Bioencapsulation within synthetic polymers (Part 1): sol–gel encapsulated biologicals Gill, Iqbal; Ballesteros, Antonio Trends in Biotechnology, Vol. 18, Issue 7 https://doi.org/10.1016/S0167-7799(00)01457-8	journal	July 2000
Enzymatic activity of glucose oxidase encapsulated in transparent glass by the sol-gel method Yamanaka, Stacey A.; Nishida, Fumito; Ellerby, Lisa M. Chemistry of Materials, Vol. 4, Issue 3 https://doi.org/10.1021/cm00021a001	journal	May 1992
Enzyme-functionalized mesoporous silica for bioanalytical applications Ispas, Cristina; Sokolov, Igor; Andreescu, Silvana Analytical and Bioanalytical Chemistry, Vol. 393, Issue 2 https://doi.org/10.1007/s00216-008-2250-2	journal	July 2008
Biofriendly Sol–Gel Processing for the Entrapment of Soluble and Membrane-Bound Proteins: Toward Novel Solid-Phase Assays for High-Throughput Screening Brennan, John D. Accounts of Chemical Research, Vol. 40, Issue 9 https://doi.org/10.1021/ar6000268	journal	April 2007
Properties and applications of proteins encapsulated within sol–gel derived materials Jin, Wen; Brennan, John D. Analytica Chimica Acta, Vol. 461, Issue 1 https://doi.org/10.1016/S0003-2670(02)00229-5	journal	June 2002
Cell-Directed Localization and Orientation of a Functional Foreign Transmembrane Protein within a Silica Nanostructure Carnes, Eric C.; Harper, Jason C.; Ashley, Carlee E. Journal of the American Chemical Society, Vol. 131, Issue 40 https://doi.org/10.1021/ja906055m	journal	October 2009
Aqueous Sol−Gel Process for Protein Encapsulation Bhatia, Rimple B.; Brinker, C. Jeffrey; Gupta, Alok K. Chemistry of Materials, Vol. 12, Issue 8 https://doi.org/10.1021/cm000260f	journal	August 2000
Encapsulation of cells within silica matrixes: Towards a new advance in the conception of living hybrid materials Meunier, Christophe F.; Dandoy, Philippe; Su, Bao-Lian Journal of Colloid and Interface Science, Vol. 342, Issue 2, p. 211-224 https://doi.org/10.1016/j.jcis.2009.10.050	journal	February 2010
Cell-Directed Integration into Three-Dimensional Lipid−Silica Nanostructured Matrices Harper, Jason C.; Khirpin, Constantine Y.; Carnes, Eric C. ACS Nano, Vol. 4, Issue 10, p. 5539-5550 https://doi.org/10.1021/nn101793u	journal	September 2010
Cell-Directed Assembly of Lipid-Silica Nanostructures Providing Extended Cell Viability Baca, Helen K.; Ashley, Carlee; Carnes, Eric Science, Vol. 313, Issue 5785, p. 337-341 https://doi.org/10.1126/science.1126590	journal	July 2006
Living Cells in Oxide Glasses Livage, J.; Coradin, T. Reviews in Mineralogy and Geochemistry, Vol. 64, Issue 1 https://doi.org/10.2138/rmg.2006.64.10	journal	January 2006
Sol-Gel Biopolymer/Silica Nanocomposites in Biotechnology Coradin, Thibaud; Allouche, Joachim; Boissiere, Michel Current Nanoscience, Vol. 2, Issue 3 https://doi.org/10.2174/1573413710602030219	journal	August 2006
Recent bio-applications of sol–gel materials Avnir, David; Coradin, Thibaud; Lev, Ovadia Journal of Materials Chemistry, Vol. 16, Issue 11, p. 1013-1030 https://doi.org/10.1039/B512706H	journal	January 2006
How to design cell-based biosensors using the sol–gel process Depagne, Christophe; Roux, Cécile; Coradin, Thibaud Analytical and Bioanalytical Chemistry, Vol. 400, Issue 4 https://doi.org/10.1007/s00216-010-4351-y	journal	November 2010
A sol–gel matrix to preserve the viability of encapsulated bacteria Nassif, Nadine; Roux, Cécile; Coradin, Thibaud Journal of Materials Chemistry, Vol. 13, Issue 2 https://doi.org/10.1039/b210167j	journal	January 2003
Cells in Sol-Gels I: A Cytocompatible Route for the Production of Macroporous Silica Gels Conroy, John F. T.; Power, Mary E.; Martin, Jason Journal of Sol-Gel Science and Technology, Vol. 18, Issue 3, p. 269-283 https://doi.org/10.1023/A:1008704208324	journal	August 2000
Bacteria Viability in Sol−Gel Materials Revisited: Cryo-SEM as a Suitable Tool To Study the Structural Integrity of Encapsulated Bacteria Ferrer, Maria L.; Garcia-Carvajal, Zaira Y.; Yuste, Luis Chemistry of Materials, Vol. 18, Issue 6 https://doi.org/10.1021/cm0522275	journal	March 2006
Living bacteria in silica gels Nassif, Nadine; Bouvet, Odile; Noelle Rager, Marie Nature Materials, Vol. 1, Issue 1 https://doi.org/10.1038/nmat709	journal	September 2002
Orthogonal Cell-Based Biosensing: Fluorescent, Electrochemical, and Colorimetric Detection with Silica-Immobilized Cellular Communities Integrated with an ITO-Glass/Plastic Laminate Cartridge Harper, Jason C.; Edwards, Thayne L.; Savage, Travis Small, Vol. 8, Issue 17, p. 2743-2751 https://doi.org/10.1002/smll.201200343	journal	June 2012
The differential fluorescence of bacteria stained with acridine orange and the effects of heat Back, J. P.; Kroll, R. G. Journal of Applied Bacteriology, Vol. 71, Issue 1 https://doi.org/10.1111/j.1365-2672.1991.tb04662.x	journal	July 1991
Red but not dead? Membranes of stressed Saccharomyces cerevisiae are permeable to propidium iodide: Reversible membrane permeabilization in yeast Davey, H. M.; Hexley, P. Environmental Microbiology, Vol. 13, Issue 1 https://doi.org/10.1111/j.1462-2920.2010.02317.x	journal	August 2010
Encapsulation of S. cerevisiae in Poly(glycerol) Silicate Derived Matrices: Effect of Matrix Additives and Cell Metabolic Phase on Long-Term Viability and Rate of Gene Expression Harper, Jason C.; Lopez, DeAnna M.; Larkin, Elizabeth C. Chemistry of Materials, Vol. 23, Issue 10, p. 2555-2564 https://doi.org/10.1021/cm103525u	journal	May 2011
Correlating biological methods to assess Escherichia coli bacteria viability in silica gels Blondeau, M.; Brayner, R.; Guyot, F. Analytical Methods, Vol. 6, Issue 8 https://doi.org/10.1039/c4ay00111g	journal	January 2014
Resuscitation rate in different enterococcal species in the viable but non-culturable state Lleo, M. M.; Bonato, B.; Tafi, M. C. Journal of Applied Microbiology, Vol. 91, Issue 6 https://doi.org/10.1046/j.1365-2672.2001.01476.x	journal	December 2001
The Viable but Nonculturable State and Starvation Are Different Stress Responses of Enterococcus faecalis , as Determined by Proteome Analysis Heim, Sabina; Del Mar Lleo, Maria; Bonato, Barbara Journal of Bacteriology, Vol. 184, Issue 23 https://doi.org/10.1128/JB.184.23.6739-6745.2002	journal	December 2002
Spectral and structural comparison between bright and dim green fluorescent proteins in Amphioxus Bomati, Erin K.; Haley, Joy E.; Noel, Joseph P. Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep05469	journal	June 2014
Amphioxus encodes the largest known family of green fluorescent proteins, which have diversified into distinct functional classes Bomati, Erin K.; Manning, Gerard; Deheyn, Dimitri D. BMC Evolutionary Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2148-9-77	journal	January 2009
FRET-Based Optical Assay for Monitoring Riboswitch Activation Harbaugh, Svetlana; Kelley-Loughnane, Nancy; Davidson, Molly Biomacromolecules, Vol. 10, Issue 5 https://doi.org/10.1021/bm801117f	journal	April 2009
Cell-free protein synthesis: Applications come of age Carlson, Erik D.; Gan, Rui; Hodgman, C. Eric Biotechnology Advances, Vol. 30, Issue 5 https://doi.org/10.1016/j.biotechadv.2011.09.016	journal	September 2012
A cell-free protein-producing gel Park, Nokyoung; Um, Soong Ho; Funabashi, Hisakage Nature Materials, Vol. 8, Issue 5 https://doi.org/10.1038/nmat2419	journal	March 2009
Entrapment of Living Bacterial Cells in Low-Concentration Silica Materials Preserves Cell Division and Promoter Regulation Eleftheriou, Nikolas M.; Ge, Xin; Kolesnik, Julia Chemistry of Materials, Vol. 25, Issue 23 https://doi.org/10.1021/cm403198z	journal	November 2013
Sol–gel encapsulation of bacteria: a comparison between alkoxide and aqueous routes Coiffier, Anne; Coradin, Thibaud; Roux, Cécile Journal of Materials Chemistry, Vol. 11, Issue 8 https://doi.org/10.1039/b101308o	journal	January 2001
Production of Valuable Drugs from Plant Cells Immobilized by Hybrid Sol-Gel SiO2 Carturan, G.; Monte, R. Dal; Pressi, G. Journal of Sol-Gel Science and Technology, Vol. 13, Issue 1/3, p. 273-276 https://doi.org/10.1023/A:1008676904085	journal	January 1998
Immobilization of plant cells in hybrid sol-gel materials Campostrini, R.; Carturan, G.; Caniato, R. Journal of Sol-Gel Science and Technology, Vol. 7, Issue 1-2 https://doi.org/10.1007/BF00401888	journal	August 1996

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Title: Influence of silica matrix composition and functional component additives on the bioactivity and viability of encapsulated living cells

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