Creating biological nanomaterials using synthetic biology

Abstract Synthetic biology is a new discipline that combines science and engineering approaches to precisely control biological networks. These signaling networks are especially important in fields such as biomedicine and biochemical engineering. Additionally, biological networks can also be critical to the production of naturally occurring biological nanomaterials, and as a result, synthetic biology holds tremendous potential in creating new materials. This review introduces the field of synthetic biology, discusses how biological systems naturally produce materials, and then presents examples and strategies for incorporating synthetic biology approaches in the development of new materials. In particular, strategies for using synthetic biology to produce both organic and inorganic nanomaterials are discussed. Ultimately, synthetic biology holds the potential to dramatically impact biological materials science with significant potential applications in medical systems.

[1]  J J Collins,et al.  A theory for controlling cell cycle dynamics using a reversibly binding inhibitor. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Joao B Xavier,et al.  The Evolution of Quorum Sensing in Bacterial Biofilms , 2008, PLoS biology.

[3]  J. C. Liao,et al.  Engineered Synthetic Pathway for Isopropanol Production in Escherichia coli , 2007, Applied and Environmental Microbiology.

[4]  M. Bennett,et al.  A fast, robust, and tunable synthetic gene oscillator , 2008, Nature.

[5]  R S Wolfe,et al.  Magnetite in Freshwater Magnetotactic Bacteria , 1979, Science.

[6]  R. Blakemore.  Magnetotactic bacteria , 1975, Science.

[7]  Martin Fussenegger,et al.  Design and construction of synthetic gene networks in mammalian cells. , 2012, Methods in molecular biology.

[8]  J. Costerton,et al.  The involvement of cell-to-cell signals in the development of a bacterial biofilm. , 1998, Science.

[9]  M. Davison,et al.  Magnetoreception and its trigeminal mediation in the homing pigeon , 2004, Nature.

[10]  Shigeru Kondo,et al.  Reaction-Diffusion Model as a Framework for Understanding Biological Pattern Formation , 2010, Science.

[11]  A. Turing.  The chemical basis of morphogenesis , 1990 .

[12]  M. Fussenegger,et al.  Genetically programmed superparamagnetic behavior of mammalian cells. , 2012, Journal of biotechnology.

[13]  H. Bujard,et al.  Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. , 1997, Nucleic acids research.

[14]  G. Church,et al.  Synthetic Gene Networks That Count , 2009, Science.

[15]  James J. Collins,et al.  Iterative plug-and-play methodology for constructing and modifying synthetic gene networks , 2012, Nature Methods.

[16]  Bonnie L Bassler,et al.  Quorum sensing controls biofilm formation in Vibrio cholerae , 2003, Molecular microbiology.

[17]  Mauricio S. Antunes,et al.  Programmable Ligand Detection System in Plants through a Synthetic Signal Transduction Pathway , 2011, PloS one.

[18]  Wilfried Weber,et al.  Synthetic biology for mammalian cell technology and materials sciences. , 2013, Biotechnology advances.

[19]  Christopher A. Voigt,et al.  A Synthetic Genetic Edge Detection Program , 2009, Cell.

[20]  William I. Bacchus,et al.  Increasing the dynamic control space of mammalian transcription devices by combinatorial assembly of homologous regulatory elements from different bacterial species. , 2013, Metabolic engineering.

[21]  Wilson W Wong,et al.  Single-cell zeroth-order protein degradation enhances the robustness of synthetic oscillator , 2007, Molecular systems biology.

[22]  A. Turing,et al.  The chemical basis of morphogenesis. 1953. , 1990, Bulletin of mathematical biology.

[23]  Danielle Tullman-Ercek,et al.  Engineering nanoscale protein compartments for synthetic organelles. , 2013, Current opinion in biotechnology.

[24]  Yun Jung Lee,et al.  Fabricating Genetically Engineered High-Power Lithium-Ion Batteries Using Multiple Virus Genes , 2009, Science.

[25]  M. Fussenegger,et al.  A novel reporter system for bacterial and mammalian cells based on the non-ribosomal peptide indigoidine. , 2012, Metabolic engineering.

[26]  Bernhard O. Palsson,et al.  Metabolic flux balance analysis and the in silico analysis of Escherichia coli K-12 gene deletions , 2000, BMC Bioinformatics.

[27]  J. Liao,et al.  Engineering synthetic recursive pathways to generate non-natural small molecules. , 2012, Nature chemical biology.

[28]  Douglas Densmore,et al.  The Eugene language for synthetic biology. , 2011, Methods in enzymology.

[29]  J. Keasling,et al.  High-level semi-synthetic production of the potent antimalarial artemisinin , 2013, Nature.

[30]  Markus Wieland,et al.  Engineering of ribozyme-based riboswitches for mammalian cells. , 2012, Methods.

[31]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[32]  Christopher A. Voigt,et al.  Environmental signal integration by a modular AND gate , 2007, Molecular systems biology.

[33]  J. Liao,et al.  A synthetic gene–metabolic oscillator , 2005, Nature.

[34]  F. Crick.  Central Dogma of Molecular Biology , 1970, Nature.

[35]  Timothy K Lu,et al.  Synthetic circuits integrating logic and memory in living cells , 2013, Nature Biotechnology.

[36]  J. Collins,et al.  DIVERSITY-BASED, MODEL-GUIDED CONSTRUCTION OF SYNTHETIC GENE NETWORKS WITH PREDICTED FUNCTIONS , 2009, Nature Biotechnology.

[37]  S. Basu,et al.  A synthetic multicellular system for programmed pattern formation , 2005, Nature.

[38]  Minami Yoda,et al.  Towards an in vivo biologically inspired nanofactory. , 2007, Nature nanotechnology.

[39]  Xing‐dong Zhang,et al.  Computer simulation of biomolecule–biomaterial interactions at surfaces and interfaces , 2015, Biomedical materials.

[40]  M. Fussenegger,et al.  Regulated multicistronic expression technology for mammalian metabolic engineering , 1998, Cytotechnology.

[41]  Grant J. Jensen,et al.  Magnetosomes Are Cell Membrane Invaginations Organized by the Actin-Like Protein MamK , 2006, Science.

[42]  Christopher A. Voigt,et al.  Multichromatic control of gene expression in Escherichia coli. , 2011, Journal of molecular biology.

[43]  D. G. Gibson,et al.  Enzymatic assembly of DNA molecules up to several hundred kilobases , 2009, Nature Methods.

[44]  A. Griffin,et al.  Social evolution theory for microorganisms , 2006, Nature Reviews Microbiology.

[45]  Pamela A Silver,et al.  Parts plus pipes: synthetic biology approaches to metabolic engineering. , 2012, Metabolic engineering.

[46]  D. Belin,et al.  Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter , 1995, Journal of bacteriology.

[47]  Martin Fussenegger,et al.  A synthetic low-frequency mammalian oscillator , 2010, Nucleic acids research.

[48]  J. Stelling,et al.  A tunable synthetic mammalian oscillator , 2009, Nature.

[49]  Clément Sanchez,et al.  Biomimetism and bioinspiration as tools for the design of innovative materials and systems , 2005, Nature materials.

[50]  J. Keasling,et al.  Homogeneous expression of the P(BAD) promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter. , 2001, Microbiology.

[51]  Christopher A. Voigt,et al.  Robust multicellular computing using genetically encoded NOR gates and chemical ‘wires’ , 2011, Nature.

[52]  J. Keasling,et al.  Regulatable Arabinose-Inducible Gene Expression System with Consistent Control in All Cells of a Culture , 2000, Journal of bacteriology.

[53]  Drew Endy,et al.  A survey of enabling technologies in synthetic biology , 2013, Journal of biological engineering.

[54]  Y. Chiang,et al.  Virus-Enabled Synthesis and Assembly of Nanowires for Lithium Ion Battery Electrodes , 2006, Science.

[55]  Farren J. Isaacs,et al.  Programming cells by multiplex genome engineering and accelerated evolution , 2009, Nature.

[56]  J. Collins,et al.  Construction of a genetic toggle switch in Escherichia coli , 2000, Nature.

[57]  Claudia Schmidt-Dannert,et al.  Engineered Protein Nano-Compartments for Targeted Enzyme Localization , 2012, PloS one.

[58]  T. Yeates,et al.  Atomic-Level Models of the Bacterial Carboxysome Shell , 2008, Science.

[59]  M. Elowitz,et al.  A synthetic oscillatory network of transcriptional regulators , 2000, Nature.

[60]  S. Ho,et al.  Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. , 1989, Gene.

[61]  G. J. Velicer.  Social strife in the microbial world. , 2003, Trends in microbiology.

[62]  Martin Fussenegger,et al.  The use of light for engineered control and reprogramming of cellular functions. , 2012, Current opinion in biotechnology.

[63]  Jeremy Minshull,et al.  Engineering the Salmonella type III secretion system to export spider silk monomers , 2009, Molecular systems biology.

[64]  Jeremy Shaw,et al.  Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons , 2012, Nature.

[65]  J. Collins,et al.  Synthetic Biology Moving into the Clinic , 2011, Science.

[66]  E. Greenberg,et al.  A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. , 2006, International journal of medical microbiology : IJMM.

[67]  D. Endy,et al.  Rewritable digital data storage in live cells via engineered control of recombination directionality , 2012, Proceedings of the National Academy of Sciences.

[68]  L. V. Doronina-Amitonova,et al.  Neurophotonics: optical methods to study and control the brain , 2015 .

[69]  P. Silver,et al.  Modularity of a carbon-fixing protein organelle , 2011, Proceedings of the National Academy of Sciences.

[70]  Dong Soo Yun,et al.  Virus-templated iridium oxide-gold hybrid nanowires for electrochromic application. , 2012, Nanoscale.

[71]  Rahul Sarpeshkar,et al.  Synthetic analog computation in living cells , 2013, Nature.

[72]  T. Seo,et al.  In vivo synthesis of diverse metal nanoparticles by recombinant Escherichia coli. , 2010, Angewandte Chemie.

[73]  J. Bailey,et al.  Toward a science of metabolic engineering , 1991, Science.

[74]  P. Silver,et al.  Induction of Biogenic Magnetization and Redox Control by a Component of the Target of Rapamycin Complex 1 Signaling Pathway , 2012, PLoS biology.

[75]  Christopher A. Voigt,et al.  Automated design of synthetic ribosome binding sites to control protein expression , 2016 .

[76]  Ahmad S. Khalil,et al.  A Synthetic Biology Framework for Programming Eukaryotic Transcription Functions , 2012, Cell.

[77]  M. Silverman,et al.  Identification of genes and gene products necessary for bacterial bioluminescence. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[78]  George Georgiou,et al.  Virus-Based Toolkit for the Directed Synthesis of Magnetic and Semiconducting Nanowires , 2004, Science.

[79]  B. Palsson,et al.  In silico predictions of Escherichia coli metabolic capabilities are consistent with experimental data , 2001, Nature Biotechnology.

[80]  C. Bashor,et al.  References and Notes Supporting Online Material Using Engineered Scaffold Interactions to Reshape Map Kinase Pathway Signaling Dynamics , 2022 .

[81]  Emma M. B. Weeding,et al.  Eugene – A Domain Specific Language for Specifying and Constraining Synthetic Biological Parts, Devices, and Systems , 2011, PloS one.

[82]  W. Wiltschko,et al.  The Role of the Magnetite-Based Receptors in the Beak in Pigeon Homing , 2010, Current Biology.

[83]  J. Keasling,et al.  Modulation of gene expression from the arabinose-inducible araBAD promoter , 2002, Journal of Industrial Microbiology and Biotechnology.

[84]  Swapnil Bhatia,et al.  Developer's and user's guide to Clotho v2.0 A software platform for the creation of synthetic biological systems. , 2011, Methods in enzymology.

[85]  Farshid Guilak,et al.  A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. , 2007, Nature materials.

[86]  R. Weiss,et al.  A universal RNAi-based logic evaluator that operates in mammalian cells , 2007, Nature Biotechnology.

[87]  Christopher A. Voigt,et al.  Synthetic biology: Engineering Escherichia coli to see light , 2005, Nature.

[88]  M. Fussenegger,et al.  Optogenetic therapeutic cell implants. , 2012, Gastroenterology.

[89]  Robert M. Horton,et al.  Gene splicing by overlap extension. , 1990 .

[90]  George Georgiou,et al.  Viral assembly of oriented quantum dot nanowires , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[91]  A. Komeili.  Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria. , 2012, FEMS microbiology reviews.

[92]  Ying Zhang,et al.  Artificial cells: building bioinspired systems using small-scale biology. , 2008, Trends in biotechnology.

[93]  H. Nakazawa,et al.  Formation of magnetite by bacteria and its application , 2008, Journal of The Royal Society Interface.