Synthesis and patterning of tunable multiscale materials with engineered cells

Many natural biological systems - such as biofilms, shells and skeletal tissues - are able to assemble multifunctional and environmentally responsive multiscale assemblies of living and non-living components. Here, by using inducible genetic circuits and cellular communication circuits to regulate Escherichia coli curli amyloid production, we show that E. coli cells can organize self-assembling amyloid fibrils across multiple length scales, producing amyloid-based materials that are either externally controllable or undergo autonomous patterning. We also interfaced curli fibrils with inorganic materials, such as gold nanoparticles (AuNPs) and quantum dots (QDs), and used these capabilities to create an environmentally responsive biofilm-based electrical switch, produce gold nanowires and nanorods, co-localize AuNPs with CdTe/CdS QDs to modulate QD fluorescence lifetimes, and nucleate the formation of fluorescent ZnS QDs. This work lays a foundation for synthesizing, patterning, and controlling functional composite materials with engineered cells.

[1]  J. Northrop,et al.  Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[2]  X. H. Wu,et al.  Control of crystal phase switching and orientation by soluble mollusc-shell proteins , 1996, Nature.

[3]  N. Seeman,et al.  Design and self-assembly of two-dimensional DNA crystals , 1998, Nature.

[4]  C. Prigent-Combaret,et al.  Isolation of an Escherichia coli K-12 Mutant Strain Able To Form Biofilms on Inert Surfaces: Involvement of a New ompR Allele That Increases Curli Expression , 1998, Journal of bacteriology.

[5]  Steve Weiner,et al.  THE MATERIAL BONE: Structure-Mechanical Function Relations , 1998 .

[6]  G. Whitesides,et al.  Unconventional Methods for Fabricating and Patterning Nanostructures. , 1999, Chemical reviews.

[7]  G. Whitesides,et al.  Unconventional Methods for Fabricating and Patterning Nanostructures , 1999 .

[8]  R. Kolter,et al.  Biofilm formation as microbial development. , 2000, Annual review of microbiology.

[9]  C. Prigent-Combaret,et al.  Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. , 2000, Environmental microbiology.

[10]  Michael Pepper,et al.  Electrically Driven Single-Photon Source , 2001, Science.

[11]  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.

[12]  H. Jaeger,et al.  Conducting nanowires built by controlled self-assembly of amyloid fibers and selective metal deposition , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Shuguang Zhang Fabrication of novel biomaterials through molecular self-assembly , 2003, Nature Biotechnology.

[14]  A. Heuer,et al.  Tissue Regeneration in the Shell of the Giant Queen Conch, Strombus gigas , 2004 .

[15]  Molly M Stevens,et al.  Exploring and engineering the cell surface interface. , 2011, Science.

[16]  J. Hubbell,et al.  Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering , 2005, Nature Biotechnology.

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

[18]  Julian H. George,et al.  Exploring and Engineering the Cell Surface Interface , 2005, Science.

[19]  J. Aizenberg,et al.  Skeleton of Euplectella sp.: Structural Hierarchy from the Nanoscale to the Macroscale , 2005, Science.

[20]  Rein V. Ulijn,et al.  Peptide-based stimuli-responsive biomaterials. , 2006, Soft matter.

[21]  Arul Jayaraman,et al.  Indole is an inter-species biofilm signal mediated by SdiA , 2007, BMC Microbiology.

[22]  Matthew R Chapman,et al.  Curli biogenesis and function. , 2006, Annual review of microbiology.

[23]  P. Rothemund Folding DNA to create nanoscale shapes and patterns , 2006, Nature.

[24]  Christopher M Dobson,et al.  Characterization of the nanoscale properties of individual amyloid fibrils , 2006, Proceedings of the National Academy of Sciences.

[25]  Richard Weinkamer,et al.  Nature’s hierarchical materials , 2007 .

[26]  Ron Weiss,et al.  Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium , 2007, Proceedings of the National Academy of Sciences.

[27]  K. M. Yu,et al.  Direct digital manufacturing of three-dimensional functionally graded material objects , 2008, Comput. Aided Des..

[28]  M. Chapman,et al.  The Molecular Basis of Functional Bacterial Amyloid Polymerization and Nucleation* , 2008, Journal of Biological Chemistry.

[29]  Christopher R. So,et al.  Adsorption, diffusion, and self-assembly of an engineered gold-binding peptide on Au(111) investigated by atomic force microscopy. , 2009, Angewandte Chemie.

[30]  C. MacPhee,et al.  Efficient energy transfer within self-assembling peptide fibers: a route to light-harvesting nanomaterials. , 2009, Journal of the American Chemical Society.

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

[32]  Giorgio Volpe,et al.  Unidirectional Emission of a Quantum Dot Coupled to a Nanoantenna , 2010, Science.

[33]  L. D. Negro,et al.  Rapid Nanoimprinting of Silk Fibroin Films for Biophotonic Applications , 2010, Advanced materials.

[34]  Alexander K. Epstein,et al.  Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration , 2010, Proceedings of the National Academy of Sciences.

[35]  Lawrence Tamarkin,et al.  Phase I and Pharmacokinetic Studies of CYT-6091, a Novel PEGylated Colloidal Gold-rhTNF Nanomedicine , 2010, Clinical Cancer Research.

[36]  Roberto Kolter,et al.  d-Amino Acids Trigger Biofilm Disassembly , 2010, Science.

[37]  Yongdoo Choi,et al.  Gold nanorod-photosensitizer complex for near-infrared fluorescence imaging and photodynamic/photothermal therapy in vivo. , 2011, ACS nano.

[38]  T. Hwa,et al.  Sequential Establishment of Stripe Patterns in an Expanding Cell Population , 2011, Science.

[39]  Frances H. Arnold,et al.  Self-Organization, Layered Structure, and Aggregation Enhance Persistence of a Synthetic Biofilm Consortium , 2011, PloS one.

[40]  Philip Kollmannsberger,et al.  The physics of tissue patterning and extracellular matrix organisation: how cells join forces , 2011 .

[41]  Qun Ma,et al.  Engineering a novel c-di-GMP-binding protein for biofilm dispersal. , 2011, Environmental microbiology.

[42]  Samuel I Stupp,et al.  Supramolecular nanostructures that mimic VEGF as a strategy for ischemic tissue repair , 2011, Proceedings of the National Academy of Sciences.

[43]  Lauren A Austin,et al.  Small molecule-gold nanorod conjugates selectively target and induce macrophage cytotoxicity towards breast cancer cells. , 2012, Small.

[44]  Charles M. Lieber,et al.  Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. , 2012, Nature materials.

[45]  H. Atwater,et al.  Photonic design principles for ultrahigh-efficiency photovoltaics. , 2012, Nature materials.

[46]  B. Zakeri,et al.  Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin , 2012, Proceedings of the National Academy of Sciences.

[47]  U. Bach,et al.  A Solid‐State Plasmonic Solar Cell via Metal Nanoparticle Self‐Assembly , 2012, Advanced materials.

[48]  Manjunath Hegde,et al.  Synthetic quorum-sensing circuit to control consortial biofilm formation and dispersal in a microfluidic device , 2012, Nature Communications.

[49]  James J. Collins,et al.  Genetic switchboard for synthetic biology applications , 2012, Proceedings of the National Academy of Sciences.

[50]  Huanyu Cheng,et al.  A Physically Transient Form of Silicon Electronics , 2012, Science.

[51]  Martin Fussenegger,et al.  Synthetic two-way communication between mammalian cells , 2012, Nature Biotechnology.

[52]  D. Baker,et al.  Computational Design of Self-Assembling Protein Nanomaterials with Atomic Level Accuracy , 2012, Science.

[53]  J. Crowley,et al.  Escherichia coli Biofilms Have an Organized and Complex Extracellular Matrix Structure , 2013, mBio.

[54]  J. Friedrichs,et al.  Tightly anchored tissue-mimetic matrices as instructive stem cell microenvironments , 2013, Nature Methods.

[55]  Lingchong You,et al.  Temporal control of self-organized pattern formation without morphogen gradients in bacteria , 2013, Molecular systems biology.

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

[57]  Lingchong You,et al.  Engineered cell-cell communication and its applications. , 2014, Advances in biochemical engineering/biotechnology.