Abstract
Natural materials, such as biofilms and tissues, sense and respond to environmental signals using genetic, metabolic, and proteomic machinery. This machinery allows natural materials to actuate changes with unmatched spatiotemporal precision. However, natural materials are relatively limited in morphology and functionality compared to synthetic materials. In an effort to enhance synthetic materials with the capabilities of living systems, we describe recent efforts to control synthetic polymerizations using live cells as actuators. Both microbes and eukaryotic cells have been employed in radical and oxidative polymerizations, significantly expanding the synthetic scope available to living systems. In addition, these mechanisms have enabled construction of polymer networks and hydrogels that resemble natural materials like tissues. Future efforts in synthetic biology, combined with new methods for reprogramming metabolism to control abiotic chemistry, will enable more platforms that synergistically enhance synthetic materials with living functions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Bennett MR, Gurnani P, Hill PJ, Alexander C, Rawson FJ (2020) Iron-catalysed radical polymerisation by living bacteria. Angewandte Chemie-German Edition 132:4780–4785. https://doi.org/10.1002/ange.201915084
Bond DR, Lovley DR (2003) Electricity production by geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555. https://doi.org/10.1128/aem.69.3.1548-1555.2003
Brutinel ED, Gralnick JA (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biotechnol 93:41–48. https://doi.org/10.1007/s00253-011-3653-0
Corts AD, Thomason LC, Gill RT, Gralnick JA (2019) A new recombineering system for precise genome-editing in Shewanella oneidensis strain MR-1 using single-stranded oligonucleotides. Sci Rep 9:39. https://doi.org/10.1038/s41598-018-37025-4
Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 55:995–1008. https://doi.org/10.1111/j.1365-2958.2010.07266.x
Coursolle D, Baron DB, Bond DR, Gralnick JA (2009) The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. J Bacteriol 192:467–474. https://doi.org/10.1128/jb.00925-09
Dundas CM, Graham AJ, Romanovicz DK, Keitz BK (2018) Extracellular electron transfer by Shewanella oneidensis controls palladium nanoparticle phenotype. ACS Synth Biol 7:2726–2736. https://doi.org/10.1021/acssynbio.8b00218
Dundas CM, Walker DJF, Keitz BK (2020) Tuning extracellular electron transfer by Shewanella oneidensis using transcriptional logic gates. ACS Synth Biol 9:2301–2315. https://doi.org/10.1021/acssynbio.9b00517
Fan G, Dundas CM, Graham AJ, Lynd NA, Keitz BK (2018) Shewanella oneidensis as a living electrode for controlled radical polymerization. Proc Natl Acad Sci U S A 115:4559–4564. https://doi.org/10.1073/pnas.1800869115
Fan G, Graham AJ, Kolli J, Lynd NA, Keitz BK (2020) Aerobic radical polymerization mediated by microbial metabolism. Nat Chem 12:638–646. https://doi.org/10.1038/s41557-020-0460-1
Fantin M, Isse AA, Gennaro A, Matyjaszewski K (2015) Understanding the fundamentals of aqueous ATRP and defining conditions for better control. Macromolecules 48:6862–6875. https://doi.org/10.1021/acs.macromol.5b01454
Furubayashi M, Wallace AK, González LM, Jahnke JP, Hanrahan BM, Payne AL, Stratis-Cullum DN, Gray MT, Liu H, Rhoads MK, Voigt CA (2021) Genetic tuning of iron oxide nanoparticle size, shape, and surface properties in Magnetospirillum magneticum. Adv Funct Mater 31:2004813. https://doi.org/10.1002/adfm.202004813
Geng J, Li W, Zhang Y, Thottappillil N, Clavadetscher J, Lilienkampf A, Bradley M (2019) Radical polymerization inside living cells. Nat Chem 11:578–586. https://doi.org/10.1038/s41557-019-0240-y
Gilbert C, Tang T-C, Ott W, Dorr BA, Shaw WM, Sun GL, Lu TK, Ellis T (2021) Living materials with programmable functionalities grown from engineered microbial co-cultures. Nat Mater 20:691–700. https://doi.org/10.1038/s41563-020-00857-5
Graham AJ, Dundas CM, Hillsley A, Kasprak DS, Rosales AM, Keitz BK (2020) Genetic control of radical cross-linking in a semisynthetic hydrogel. ACS Biomater Sci Eng 6:1375–1386. https://doi.org/10.1021/acsbiomaterials.9b01773
Graham AJ, Gibbs SL, Cabezas CAS, Wang Y, Green AM, Milliron DJ, Keitz BK (2021) In Situ optical quantification of extracellular electron transfer using plasmonic metal oxide nanocrystals. ChemElectroChem. https://doi.org/10.1002/celc.202101423
Guzman MS, Rengasamy K, Binkley MM, Jones C, Ranaivoarisoa TO, Singh R, Fike DA, Meacham JM, Bose A (2019) Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris. Nat Commun 10:1355. https://doi.org/10.1038/s41467-019-09377-6
Hay JJ, Rodrigo-Navarro A, Petaroudi M, Bryksin AV, GarcÃa AJ, Barker TH, Dalby MJ, Salmeron-Sanchez M (2018) Bacteria-based materials for stem cell engineering. Adv Mater 30:1804310. https://doi.org/10.1002/adma.201804310
Hu Y, Yang Y, Katz E, Song H (2015) Programming the quorum sensing-based AND gate in Shewanella oneidensis for logic gated-microbial fuel cells. Chem Commun 51:4184–4187. https://doi.org/10.1039/c5cc00026b
Johnston TG, Yuan S-F, Wagner JM, Yi X, Saha A, Smith P, Nelson A, Alper HS (2020) Compartmentalized microbes and co-cultures in hydrogels for on-demand bioproduction and preservation. Nat Commun 11:563. https://doi.org/10.1038/s41467-020-14371-4
Kamigaito M, Ando T, Sawamoto M (2001) Metal-catalyzed living radical polymerization. Chem Rev 101:3689–3746. https://doi.org/10.1021/cr9901182
Li F-H, Tang Q, Fan Y-Y, Li Y, Li J, Wu J-H, Luo C-F, Sun H, Li W-W, Yu H-Q (2020) Develo** a population-state decision system for intelligently reprogramming extracellular electron transfer in Shewanella oneidensis. Proc Natl Acad Sci U S A 117:23001–23010. https://doi.org/10.1073/pnas.2006534117
Liu J, Kim YS, Richardson CE, Tom A, Ramakrishnan C, Birey F, Katsumata T, Chen S, Wang C, Wang X, Joubert L-M, Jiang Y, Wang H, Fenno LE, Tok JB-H, Pașca SP, Shen K, Bao Z, Deisseroth K (2020) Genetically targeted chemical assembly of functional materials in living cells, tissues, and animals. Science 367:1372–1376. https://doi.org/10.1126/science.aay4866
Lorandi F, Fantin M, Shanmugam S, Wang Y, Isse AA, Gennaro A, Matyjaszewski K (2019) Toward electrochemically mediated reversible addition–fragmentation chain-transfer (e RAFT) polymerization: can propagating radicals be efficiently electrogenerated from RAFT agents? Macromolecules 52:1479–1488. https://doi.org/10.1021/acs.macromol.9b00112
Lu Y, Li H, Wang J, Yao M, Peng Y, Liu T, Li Z, Luo G, Deng J (2021a) Engineering bacteria-activated multifunctionalized hydrogel for promoting diabetic wound healing. Adv Funct Mater 2105749. https://doi.org/10.1002/adfm.202105749
Lu H, Huang Y, Lv F, Liu L, Ma Y, Wang S (2021b) Living bacteria-mediated aerobic photo-induced radical polymerization for in-situ bacterial encapsulation and differentiation. CCS Chemistry 3:1296–1305. https://doi.org/10.31635/ccschem.021.202100957
Luo Y, Gu Y, Feng R, Brash J, Eissa AM, Haddleton DM, Chen G, Chen H (2019) Synthesis of glycopolymers with specificity for bacterial strains via bacteria-guided polymerization. Chem Sci 10:5251–5257. https://doi.org/10.1039/c8sc05561k
Magennis EP, Fernandez-Trillo F, Sui C, Spain SG, Bradshaw DJ, Churchley D, Mantovani G, Winzer K, Alexander C (2014) Bacteria-instructed synthesis of polymers for self-selective microbial binding and labelling. Nat Mater 13:748–755. https://doi.org/10.1038/nmat3949
Matyjaszewski K (2012) Atom transfer radical polymerization (ATRP): current status and future perspectives. Macromolecules 45:4015–4039. https://doi.org/10.1021/ma3001719
Meng F, Ellis T (2020) The second decade of synthetic biology: 2010–2020. Nat Commun 11:5174. https://doi.org/10.1038/s41467-020-19092-2
Nagahama K, Kimura Y, Takemoto A (2018) Living functional hydrogels generated by bioorthogonal cross-linking reactions of azide- modified cells with alkyne-modified polymers. Nat Commun 9:2195. https://doi.org/10.1038/s41467-018-04699-3
Nguyen PQ, Botyanszki Z, Tay PKR, Joshi NS (2014) Programmable biofilm-based materials from engineered curli nanofibres. Nat Commun 5:4945. https://doi.org/10.1038/ncomms5945
Niu J, Lunn DJ, Pusuluri A, Yoo JI, O’Malley MA, Mitragotri S, Soh HT, Hawker CJ (2017) Engineering live cell surfaces with functional polymers via cytocompatible controlled radical polymerization. Nat Chem 9:537–545. https://doi.org/10.1038/nchem.2713
Nothling MD, Cao H, McKenzie TG, Hocking DM, Strugnell RA, Qiao GG (2021) Bacterial redox potential powers controlled radical polymerization. J Am Chem Soc 143:286–293. https://doi.org/10.1021/jacs.0c10673
Rivera-Tarazona LK, Bhat VD, Kim H, Campbell ZT, Ware TH (2020) Shape-morphing living composites. Sci Adv 6:eaax8582. https://doi.org/10.1126/sciadv.aax8582
Rodrigo-Navarro A, Sankaran S, Dalby MJ, del Campo A, Salmeron-Sanchez M (2021) Engineered living biomaterials. Nat Rev Mater. https://doi.org/10.1038/s41578-021-00350-8
Sankaran S, Becker J, Wittmann C, del Campo A (2019) Optoregulated drug release from an engineered living material: self-replenishing drug depots for long-term, light-regulated delivery. Small 15:1804717. https://doi.org/10.1002/smll.201804717
Shaffner M, Rühs PA, Coulter F, Kilcher S, Studart AR (2017) 3D printing of bacteria into functional complex materials. Science. Advances 3:eaao6804. https://doi.org/10.1126/sciadv.aao6804
Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, Yu H-Q, Fredrickson JK (2016) Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 14:651–662. https://doi.org/10.1038/nrmicro.2016.93
Song R, Wu Y, Lin Z, **e J, Tan CH, Loo JSC, Cao B, Zhang J, Zhu J, Zhang Q (2017) Living and conducting: coating individual bacterial cells with in situ formed polypyrrole. Angew Chem Int Ed 56:10516–10520. https://doi.org/10.1002/anie.201704729
Springthorpe SK, Dundas CM, Keitz BK (2019) Microbial reduction of metal-organic frameworks enables synergistic chromium removal. Nat Commun 10:5212. https://doi.org/10.1038/s41467-019-13219-w
Szczepaniak G, Fu L, Jafari H, Kapil K, Matyjaszewski K (2021) Making ATRP more practical: oxygen tolerance. Acc Chem Res 54:1779–1790. https://doi.org/10.1021/acs.accounts.1c00032
Tang T-C, An B, Huang Y, Vasikaran S, Wang Y, Jiang X, Lu TK, Zhong C (2020) Materials design by synthetic biology. Nat Rev Mater. https://doi.org/10.1038/s41578-020-00265-w
Voigt CA (2020) Synthetic biology 2020–2030: six commercially-available products that are changing our world. Nat Commun 11:6379. https://doi.org/10.1038/s41467-020-20122-2
Wang Y, Fantin M, Park S, Gottlieb E, Fu L, Matyjaszewski K (2017) Electrochemically mediated reversible addition–fragmentation chain-transfer polymerization. Macromolecules 50:7872–7879. https://doi.org/10.1021/acs.macromol.7b02005
Workman DJ, Woods SL, Gorby YA, Fredrickson JK, Truex MJ (1997) Microbial reduction of vitamin B 12 by Shewanella alga strain BrY with subsequent transformation of carbon tetrachloride. Environ Sci Technol 31:2292–2297. https://doi.org/10.1021/es960880a
Xu S, Jangir Y, El-Naggar MY (2016) Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1. Electrochim Acta 198:49–55. https://doi.org/10.1016/j.electacta.2016.03.074
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Graham, A.J., Keitz, B.K. (2022). Living Synthetic Polymerizations. In: Srubar III, W.V. (eds) Engineered Living Materials. Springer, Cham. https://doi.org/10.1007/978-3-030-92949-7_2
Download citation
DOI: https://doi.org/10.1007/978-3-030-92949-7_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-92948-0
Online ISBN: 978-3-030-92949-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)