Living electronics

  • Yixin Zhang
  • Leo Huan-Hsuan Hsu
  • Xiaocheng JiangEmail author
Review Article


Living electronics that converges the unique functioning modality of biological and electrical circuits has the potential to transform both fundamental biophysical/biochemical inquiries and translational biomedical/engineering applications. This article will review recent progress in overcoming the intrinsic physiochemical and signaling mismatches at biological/electronic interfaces, with specific focus on strategic approaches in forging the functional synergy through: (1) biohybrid electronics, where genetically encoded bio-machineries are hybridized with electronic transducers to facilitate the translation/interpretation of biologically derived signals; and (2) biosynthetic electronics, where biogenic electron pathways are designed and programmed to bridge the gap between internal biological and external electrical circuits. These efforts are reconstructing the way that artificial electronics communicate with living systems, and opening up new possibilities for many cross-disciplinary applications in biosynthesis, sensing, energy transduction, and hybrid information processing.


bioelectronics signaling biohybrid synthetic biology extracellular electron transfer electrochemically active bacteria 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



X. J. acknowledges the funding support from National Science Foundation (DMR-1652095, CBET-1803907) and Air Force Office of Scientifc Research (FA9550-18-1-0128).


  1. [1]
    Sarpeshkar, R. The big picture. In Ultra Low Power Bioelectronics: Fundamentals, Biomedical Applications, and Bioinspired Systems. Sarpeshkar, R., Ed.; Cambridge University Press: Cambridge, 2010; pp 3–27.CrossRefGoogle Scholar
  2. [2]
    Sarpeshkar, R. Feedback systems: Fundamentals, benefits, and root-locus analysis. In Ultra Low Power Bioelectronics: Fundamentals, Biomedical Applications, and Bioinspired Systems. Sarpeshkar, R., Ed.; Cambridge University Press: Cambridge, 2010; pp 28–56.CrossRefGoogle Scholar
  3. [3]
    Kim, D. H.; Viventi, J.; Amsden, J. J.; Xiao, J. L.; Vigeland, L.; Kim, Y. S.; Blanco, J. A.; Panilaitis, B.; Frechette, E. S.; Contreras, D. et al. Dissolvable films of silk fibroin for ultrathin conformal bio-integrated electronics. Nat. Mater.2010, 9, 511–517.CrossRefGoogle Scholar
  4. [4]
    Rotenberg, M. Y.; Tian, B. Z. Bioelectronic devices: Long-lived recordings. Nat. Biomed. Eng.2017, 1, 0048.Google Scholar
  5. [5]
    Lacour, S. P.; Courtine, G.; Guck, J. Materials and technologies for soft implantable neuroprostheses. Nat. Rev. Mater.2016, 1, 16063.Google Scholar
  6. [6]
    Tian, B. Z.; Lieber, C. M. Synthetic nanoelectronic probes for biological cells and tissues. Annu. Rev. Anal. Chem. (Palo Alto Calif)2013, 6, 31–51.CrossRefGoogle Scholar
  7. [7]
    Zhang, A. Q.; Lieber, C. M. Nano-bioelectronics. Chem. Rev.2016, 116, 215–257.CrossRefGoogle Scholar
  8. [8]
    Tian, B. Z.; Cohen-Karni, T.; Qing, Q.; Duan, X. J.; Xie, P.; Lieber, C. M. Three-dimensional, flexible nanoscale field-effect transistors as localized bioprobes. Science2010, 329, 830–834.CrossRefGoogle Scholar
  9. [9]
    Cohen-Karni, T.; Timko, B. P.; Weiss, L. E.; Lieber, C. M. Flexible electrical recording from cells using nanowire transistor arrays. Proc. Natl. Acad. Sci. USA2009, 106, 7309–7313.CrossRefGoogle Scholar
  10. [10]
    Robinson, J. T.; Jorgolli, M.; Shalek, A. K.; Yoon, M. H.; Gertner, R. S.; Park, H. Vertical nanowire electrode arrays as a scalable platform for intracellular interfacing to neuronal circuits. Nat. Nanotechnol.2012, 7, 180–184.CrossRefGoogle Scholar
  11. [11]
    Xie, C.; Lin, Z. L.; Hanson, L.; Cui, Y.; Cui, B. X. Intracellular recording of action potentials by nanopillar electroporation. Nat. Nanotechnol.2012, 7, 185–190.CrossRefGoogle Scholar
  12. [12]
    Qing, Q.; Pal, S. K.; Tian, B. Z.; Duan, X. J.; Timko, B. P.; Cohen-Karni, T.; Murthy, V. N.; Lieber, C. M. Nanowire transistor arrays for mapping neural circuits in acute brain slices. Proc. Natl. Acad. Sci. USA2010, 107, 1882–1887.CrossRefGoogle Scholar
  13. [13]
    Liu, J.; Fu, T. M.; Cheng, Z. G.; Hong, G. S.; Zhou, T.; Jin, L. H.; Duvvuri, M.; Jiang, Z.; Kruskal, P.; Xie, C. et al. Syringe-injectable electronics. Nat. Nanotechnol.2015, 10, 629–636.CrossRefGoogle Scholar
  14. [14]
    Fu, T. M.; Hong, G. S.; Zhou, T.; Schuhmann, T. G.; Viveros, R. D.; Lieber, C. M. Stable long-term chronic brain mapping at the single-neuron level. Nat. Methods2016, 13, 875–882.CrossRefGoogle Scholar
  15. [15]
    Cui, Y.; Wei, Q. Q.; Park, H.; Lieber, C. M. Nanowire nanosensors for highly sensitive and selective detection of biological and chemical species. Science2001, 293, 1289–1292.CrossRefGoogle Scholar
  16. [16]
    Wang, W. U.; Chen, C.; Lin, K. H.; Fang, Y.; Lieber, C. M. Label-free detection of small-molecule-protein interactions by using nanowire nanosensors. Proc. Natl. Acad. Sci. USA2005, 102, 3208–3212.CrossRefGoogle Scholar
  17. [17]
    Hahm, J. I.; Lieber, C. M. Direct ultrasensitive electrical detection of DNA and DNA sequence variations using nanowire nanosensors. Nano Lett.2004, 4, 51–54.CrossRefGoogle Scholar
  18. [18]
    Patolsky, F.; Zheng, G. F.; Hayden, O.; Lakadamyali, M.; Zhuang, X. W.; Lieber, C. M. Electrical detection of single viruses. Proc. Natl. Acad. Sci. USA2004, 101, 14017–14022.CrossRefGoogle Scholar
  19. [19]
    Luo, Z. Q.; Jiang, Y. W.; Myers, B. D.; Isheim, D.; Wu, J. S.; Zimmerman, J. F.; Wang, Z. A.; Li, Q. Q.; Wang, Y. C.; Chen, X. Q. et al. Atomic gold-enabled three-dimensional lithography for silicon mesostructures. Science2015, 348, 1451–1455.CrossRefGoogle Scholar
  20. [20]
    Jiang, Z.; Qing, Q.; Xie, P.; Gao, R. X.; Lieber, C. M. Kinked p-n junction nanowire probes for high spatial resolution sensing and intracellular recording. Nano Lett.2012, 12, 1711–1716.CrossRefGoogle Scholar
  21. [21]
    Tian, B. Z.; Lieber, C. M. Nanowired bioelectric interfaces. Chem. Rev.2019, 119, 9136–9152.CrossRefGoogle Scholar
  22. [22]
    Wang, C. F.; Wang, C. G.; Huang, Z. L.; Xu, S. Materials and structures toward soft electronics. Adv. Mater.2018, 30, 1801368.CrossRefGoogle Scholar
  23. [23]
    Rogers, J. A.; Someya, T.; Huang, Y. G. Materials and mechanics for stretchable electronics. Science2010, 327, 1603–1607.CrossRefGoogle Scholar
  24. [24]
    Yang, X.; Zhou, T.; Zwang, T. J.; Hong, G. S.; Zhao, Y. L.; Viveros, R. D.; Fu, T. M.; Gao, T.; Lieber, C. M. Bioinspired neuron-like electronics. Nat. Mater.2019, 18, 510–517.CrossRefGoogle Scholar
  25. [25]
    Hong, G. S.; Fu, T. M.; Qiao, M.; Viveros, R. D.; Yang, X.; Zhou, T.; Lee, J. M.; Park, H. G.; Sanes, J. R.; Lieber, C. M. A method for single-neuron chronic recording from the retina in awake mice. Science2018, 360, 1447–1451.CrossRefGoogle Scholar
  26. [26]
    Xie, C.; Liu, J.; Fu, T. M.; Dai, X. C.; Zhou, W.; Lieber, C. M. Three-dimensional macroporous nanoelectronic networks as minimally invasive brain probes. Nat. Mater.2015, 14, 1286–1292.CrossRefGoogle Scholar
  27. [27]
    Inal, S.; Rivnay, J.; Suiu, A. O.; Malliaras, G. G.; McCulloch, I. Conjugated polymers in bioelectronics. Acc. Chem. Res.2018, 51, 1368–1376.CrossRefGoogle Scholar
  28. [28]
    Kozai, T. D. Y.; Catt, K.; Du, Z. H.; Na, K.; Srivannavit, O.; Haque, R. U. M.; Seymour, J.; Wise, K. D.; Yoon, E.; Cui, X. T. Chronic in vivo evaluation of PEDOT/CNT for stable neural recordings. IEEE Trans. Biomed. Eng.2016, 63, 111–119.CrossRefGoogle Scholar
  29. [29]
    Choi, S.; Lee, H.; Ghaffari, R.; Hyeon, T.; Kim, D. H. Recent advances in flexible and stretchable bio-electronic devices integrated with nanomaterials. Adv. Mater.2016, 28, 4203–4218.CrossRefGoogle Scholar
  30. [30]
    Liu, G. Z.; Qi, M.; Hutchinson, M. R.; Yang, G. F.; Goldys, E. M. Recent advances in cytokine detection by immunosensing. Biosens. Bioelectron.2016, 79, 810–821.CrossRefGoogle Scholar
  31. [31]
    Ronkainen, N. J.; Halsall, H. B.; Heineman, W. R. Electrochemical biosensors. Chem. Soc. Rev.2010, 39, 1747–1763.CrossRefGoogle Scholar
  32. [32]
    Sarkar, D.; Liu, W.; Xie, X. J.; Anselmo, A. C.; Mitragotri, S.; Banerjee, K. MoS2 field-effect transistor for next-generation label-free biosensors. ACS Nano2014, 8, 3992–4003.CrossRefGoogle Scholar
  33. [33]
    Allen, B. L.; Kichambare, P. D.; Star, A. Carbon nanotube field-effect-transistor-based biosensors. Adv. Mater.2007, 19, 1439–1451.CrossRefGoogle Scholar
  34. [34]
    Pappa, A. M.; Parlak, O.; Scheiblin, G.; Mailley, P.; Salleo, A.; Owens, R. M. Organic electronics for point-of-care metabolite monitoring. Trends Biotechnol.2018, 36, 45–59.CrossRefGoogle Scholar
  35. [35]
    Stenken, J. A.; Poschenrieder, A. J. Bioanalytical chemistry of cytokines-a review. Anal. Chim. Acta2015, 853, 95–115.CrossRefGoogle Scholar
  36. [36]
    Moon, J. M.; Thapliyal, N.; Hussain, K. K.; Goyal, R. N.; Shim, Y. B. Conducting polymer-based electrochemical biosensors for neuro-transmitters: A review. Biosens. Bioelectron.2018, 102, 540–552.CrossRefGoogle Scholar
  37. [37]
    Perry, M.; Li, Q.; Kennedy, R. T. Review of recent advances in analytical techniques for the determination of neurotransmitters. Anal. Chim. Acta2009, 653, 1–22.CrossRefGoogle Scholar
  38. [38]
    Nguyen, H. H.; Lee, S. H.; Lee, U. J.; Fermin, C. D.; Kim, M. Immobilized enzymes in biosensor applications. Materials (Basel) 2019, 12, 121.CrossRefGoogle Scholar
  39. [39]
    Willner, I.; Willner, B. Biomaterials integrated with electronic elements: En route to bioelectronics. Trends Biotechnol.2001, 19, 222–230.CrossRefGoogle Scholar
  40. [40]
    Yates, N. D. J.; Fascione, M. A.; Parkin, A. Methodologies for “wiring” redox proteins/enzymes to electrode surfaces. Chem. -Eur. J.2018, 24, 12164–12182.CrossRefGoogle Scholar
  41. [41]
    Saboe, P. O.; Conte, E.; Farell, M.; Bazan, G. C.; Kumar, M. Biomimetic and bioinspired approaches for wiring enzymes to electrode interfaces. Energy Environ. Sci.2017, 10, 14–42.CrossRefGoogle Scholar
  42. [42]
    Nöll, T.; Nöll, G. Strategies for “wiring” redox-active proteins to electrodes and applications in biosensors, biofuel cells, and nanotechnology. Chem. Soc. Rev.2011, 40, 3564–3576.CrossRefGoogle Scholar
  43. [43]
    Ghorbani Zamani, F.; Moulahoum, H.; Ak, M.; Odaci Demirkol, D.; Timur, S. Current trends in the development of conducting polymers-based biosensors. TrAC Trends Anal. Chem.2019, 118, 264–276.CrossRefGoogle Scholar
  44. [44]
    Yuan, M. W.; Minteer, S. D. Redox polymers in electrochemical systems: From methods of mediation to energy storage. Curr. Opin. Electrochem.2019, 15, 1–6.CrossRefGoogle Scholar
  45. [45]
    Hasan, K.; Milton, R. D.; Grattieri, M.; Wang, T.; Stephanz, M.; Minteer, S. D. Photobioelectrocatalysis of intact chloroplasts for solar energy conversion. ACS Catal.2017, 7, 2257–2265.CrossRefGoogle Scholar
  46. [46]
    Kim, E.; Archibald, J. M. Diversity and evolution of plastids and their genomes. In The Chloroplast: Interactions with the Environment. Sandelius, A. S.; Aronsson, H., Eds.; Springer: Berlin, Heidelberg, 2009; pp 1–39.Google Scholar
  47. [47]
    Kulbacka, J.; Choromanska, A.; Rossowska, J.; Wezgowiec, J.; Saczko, J.; Rols, M. P. Cell membrane transport mechanisms: Ion channels and electrical properties of cell membranes. In Transport Across Natural and Modified Biological Membranes and Its Implications in Physiology and Therapy. Kulbacka, J.; Satkauskas, S., Eds.; Springer: Cham, 2017; pp 39–58.CrossRefGoogle Scholar
  48. [48]
    Stern, E.; Wagner, R.; Sigworth, F. J.; Breaker, R.; Fahmy, T. M.; Reed, M. A. Importance of the debye screening length on nanowire field effect transistor sensors. Nano Lett.2007, 7, 3405–3409.CrossRefGoogle Scholar
  49. [49]
    Dai, X. C.; Vo, R.; Hsu, H. H.; Deng, P.; Zhang, Y. X.; Jiang, X. C. Modularized field-effect transistor biosensors. Nano Lett.2019, 19, 6658–6664.CrossRefGoogle Scholar
  50. [50]
    Gao, N.; Zhou, W.; Jiang, X. C.; Hong, G. S.; Fu, T. M.; Lieber, C. M. General strategy for biodetection in high ionic strength solutions using transistor-based nanoelectronic sensors. Nano Lett.2015, 15, 2143–2148.CrossRefGoogle Scholar
  51. [51]
    Bay, H. H.; Vo, R.; Dai, X. C.; Hsu, H. H.; Mo, Z. M.; Cao, S. R.; Li, W. Y.; Omenetto, F. G.; Jiang, X. C. Hydrogel gate graphene field-effect transistors as multiplexed biosensors. Nano Lett.2019, 19, 2620–2626.CrossRefGoogle Scholar
  52. [52]
    Liu, Q. J.; Wu, C. S.; Cai, H.; Hu, N.; Zhou, J.; Wang, P. Cell-based biosensors and their application in biomedicine. Chem. Rev.2014, 114, 6423–6461.CrossRefGoogle Scholar
  53. [53]
    Stern, E.; Steenblock, E. R.; Reed, M. A.; Fahmy, T. M. Label-free electronic detection of the antigen-specific T-cell immune response. Nano Lett.2008, 8, 3310–3314.CrossRefGoogle Scholar
  54. [54]
    Pham, T. D.; Pham, P. Q.; Li, J. F.; Letai, A. G.; Wallace, D. C.; Burke, P. J. Cristae remodeling causes acidification detected by integrated graphene sensor during mitochondrial outer membrane permeabilization. Sci. Rep.2016, 6, 35907.Google Scholar
  55. [55]
    Kumar, A.; Hsu, L. H. H.; Kavanagh, P.; Barrière, F.; Lens, P. N. L.; Lapinsonnière, L.; Lienhard V. J. H.; Schröder, U.; Jiang, X. C.; Leech, D. The ins and outs of microorganism-electrode electron transfer reactions. Nat. Rev. Chem.2017, 1, 0024.Google Scholar
  56. [56]
    Yang, Y. G.; Xu, M. Y.; Guo, J.; Sun, G. P. Bacterial extracellular electron transfer in bioelectrochemical systems. Process Biochem.2012, 47, 1707–1714.CrossRefGoogle Scholar
  57. [57]
    Snider, R. M.; Strycharz-Glaven, S. M.; Tsoi, S. D.; Erickson, J. S.; Tender, L. M. Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven. Proc. Natl. Acad. Sci. USA2012, 109, 15467–15472.CrossRefGoogle Scholar
  58. [58]
    Jiang, X. C.; Hu, J. S.; Petersen, E. R.; Fitzgerald, L. A.; Jackan, C. S.; Lieber, A. M.; Ringeisen, B. R.; Lieber, C. M.; Biffinger, J. C. Probing single- to multi-cell level charge transport in Geobacter sulfurreducens DL-1. Nat. Commun.2013, 4, 2751.Google Scholar
  59. [59]
    Shi, L.; Dong, H. L.; Reguera, G.; Beyenal, H.; Lu, A. H.; Liu, J.; Yu, H. Q.; Fredrickson, J. K. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol.2016, 14, 651–662.CrossRefGoogle Scholar
  60. [60]
    Santos, T. C.; Silva, M. A.; Morgado, L.; Dantas, J. M.; Salgueiro, C. A. Diving into the redox properties of Geobacter sulfurreducens cytochromes: A model for extracellular electron transfer. Dalton Trans.2015, 44, 9335–9344.CrossRefGoogle Scholar
  61. [61]
    Gorby, Y. A.; Yanina, S.; McLean, J. S.; Rosso, K. M.; Moyles, D.; Dohnalkova, A.; Beveridge, T. J.; Chang, I. S.; Kim, B. H.; Kim, K. S. et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl. Acad. Sci. USA2006, 103, 11358–11363.CrossRefGoogle Scholar
  62. [62]
    Reguera, G.; McCarthy, K. D.; Mehta, T.; Nicoll, J. S.; Tuominen, M. T.; Lovley, D. R. Extracellular electron transfer via microbial nanowires. Nature2005, 435, 1098–1101.CrossRefGoogle Scholar
  63. [63]
    Marsili, E.; Baron, D. B.; Shikhare, I. D.; Coursolle, D.; Gralnick, J. A.; Bond, D. R. Shewanella secretes flavins that mediate extracellular electron transfer. Proc. Natl. Acad. Sci. USA2008, 105, 3968–3973.CrossRefGoogle Scholar
  64. [64]
    Newman, D. K.; Kolter, R. A role for excreted quinones in extracellular electron transfer. Nature2000, 405, 94–97.CrossRefGoogle Scholar
  65. [65]
    Jiang, X. C.; Hu, J. S.; Fitzgerald, L. A.; Biffinger, J. C.; Xie, P.; Ringeisen, B. R.; Lieber, C. M. Probing electron transfer mechanisms in Shewanella oneidensis MR-1 using a nanoelectrode platform and single-cell imaging. Proc. Natl. Acad. Sci. USA2010, 107, 16806–16810.CrossRefGoogle Scholar
  66. [66]
    Babauta, J.; Renslow, R.; Lewandowski, Z.; Beyenal, H. Electro-chemically active biofilms: Facts and fiction. A review. Biofouling2012, 28, 789–812.CrossRefGoogle Scholar
  67. [67]
    Selberg, J.; Gomez, M.; Rolandi, M. The potential for convergence between synthetic biology and bioelectronics. Cell Syst.2018, 7, 231–244.CrossRefGoogle Scholar
  68. [68]
    Scognamiglio, V.; Antonacci, A.; Lambreva, M. D.; Litescu, S. C.; Rea, G. Synthetic biology and biomimetic chemistry as converging technologies fostering a new generation of smart biosensors. Biosens. Bioelectron.2015, 74, 1076–1086.CrossRefGoogle Scholar
  69. [69]
    Leang, C.; Malvankar, N. S.; Franks, A. E.; Nevin, K. P.; Lovley, D. R. Engineering Geobacter sulfurreducens to produce a highly cohesive conductive matrix with enhanced capacity for current production. Energy Environ. Sci.2013, 6, 1901–1908.CrossRefGoogle Scholar
  70. [70]
    Tan, Y.; Adhikari, R. Y.; Malvankar, N. S.; Pi, S.; Ward, J. E.; Woodard, T. L.; Nevin, K. P.; Xia, Q. F.; Tuominen, M. T.; Lovley, D. R. Synthetic biological protein nanowires with high conductivity. Small2016, 12, 4481–4485.CrossRefGoogle Scholar
  71. [71]
    Altamura, L.; Horvath, C.; Rengaraj, S.; Rongier, A.; Elouarzaki, K.; Gondran, C.; Maçon, A. L. B.; Vendrely, C.; Bouchiat, V.; Fontecave, M. et al. A synthetic redox biofilm made from metalloprotein-prion domain chimera nanowires. Nat. Chem.2017, 9, 157–163.CrossRefGoogle Scholar
  72. [72]
    Matsuda, S.; Liu, H.; Kouzuma, A.; Watanabe, K.; Hashimoto, K.; Nakanishi, S. Electrochemical gating of tricarboxylic acid cycle in electricity-producing bacterial cells of Shewanella. PLoS One2013, 8, e72901.CrossRefGoogle Scholar
  73. [73]
    Kato, S. Influence of anode potentials on current generation and extracellular electron transfer paths of Geobacter species. Int. J. Mol. Sci.2017, 18, 108.CrossRefGoogle Scholar
  74. [74]
    Grobbler, C.; Virdis, B.; Nouwens, A.; Harnisch, F.; Rabaey, K.; Bond, P. L. Effect of the anode potential on the physiology and proteome of Shewanella oneidensis MR-1. Bioelectrochemistry2018, 119, 172–179.CrossRefGoogle Scholar
  75. [75]
    Hsu, L.; Deng, P.; Zhang, Y. X.; Nguyen, H. N; Jiang, X. C. Nanostructured interfaces for probing and facilitating extracellular electron transfer. J. Mater. Chem. B2018, 6, 7144–7158.CrossRefGoogle Scholar
  76. [76]
    Xie, X.; Hu, L. B.; Pasta, M.; Wells, G. F.; Kong, D. S.; Criddle, C. S.; Cui, Y. Three-dimensional carbon nanotube-textile anode for high-performance microbial fuel cells. Nano Lett.2011, 11, 291–296.CrossRefGoogle Scholar
  77. [77]
    Bian, R. X.; Jiang, Y; Wang, Y; Sun, J. K.; Hu, J. S.; Jiang, L.; Liu, H. Highly boosted microbial extracellular electron transfer by semiconductor nanowire array with suitable energy level. Adv. Funct. Mater.2018, 28, 1707408.CrossRefGoogle Scholar
  78. [78]
    Nakamura, R.; Okamoto, A.; Tajima, N.; Newton, G. J.; Kai, F.; Takashima, T.; Hashimoto, K. Biological iron-monosulfide production for efficient electricity harvesting from a deep-sea metal-reducing bacterium. ChemBioChem2010, 11, 643–645.CrossRefGoogle Scholar
  79. [79]
    Nakamura, R.; Kai, F.; Okamoto, A.; Newton, G. J.; Hashimoto, K. Self-constructed electrically conductive bacterial networks. Angew. Chem., Int. Ed.2009, 48, 508–511.CrossRefGoogle Scholar
  80. [80]
    Kalathil, S.; Katuri, K. P.; Alazmi, A. S.; Pedireddy, S.; Kornienko, N; Costa, P. M. F. J.; Saikaly, P. E. Bioinspired synthesis of reduced graphene oxide-wrapped Geobacter sulfurreducens as a hybrid electrocatalyst for efficient oxygen evolution reaction. Chem. Mater. als2019, 31, 3686–3693.CrossRefGoogle Scholar
  81. [81]
    Jiang, X. C; Hu, J. S.; Lieber, A. M.; Jackan, C. S.; Biffinger, J. C; Fitzgerald, L. A.; Ringeisen, B. R.; Lieber, C. M. Nanoparticle facilitated extracellular electron transfer in microbial fuel cells. Nano Lett.2014, 14, 6737–6742.CrossRefGoogle Scholar
  82. [82]
    Chong, G W.; Karbelkar, A. A.; El-Naggar, M. Y. Nature’s conductors: What can microbial multi-heme cytochromes teach us about electron transport and biological energy conversion? Curr. Opin. Chem. Biol.2018, 47, 7–17.CrossRefGoogle Scholar
  83. [83]
    Ueki, T.; Walker, D. J. F; Tremblay, P. L.; Nevin, K. P.; Ward, J. E.; Woodard, T. L.; Nonnenmann, S. S.; Lovley, D. R. Decorating the outer surface of microbially produced protein nanowires with peptides. ACS Synth. Biol.2019, 8, 1809–1817.CrossRefGoogle Scholar
  84. [84]
    Dai, J. C; Liu, Y. Q.; Liu, S. Y; Li, S. Y; Gao, N; Wang, J.; Zhou, J. Z.; Qiu, D. R. Differential gene content and gene expression for bacterial evolution and speciation of Shewanella in terms of biosynthesis of heme and heme-requiring proteins. BMC Microbiol.2019, 19, 173.Google Scholar
  85. [85]
    Deutschbauer, A.; Price, M. N; Wetmore, K. M.; Shao, W. J.; Baumohl, J. K; Xu, Z. C; Nguyen, M.; Tamse, R.; Davis, R W.; Arkin, A. P. Evidence-based annotation of gene function in Shewanella oneidensis MR-1 using genome-wide fitness profiling across 121 conditions. PLoS Genet.2011, 7, e1002385.CrossRefGoogle Scholar
  86. [86]
    Coppi, M. V.; Leang, C; Sandler, S. J.; Lovley, D. R. Development of a genetic system for Geobacter sulfurreducens. Appl. Environ. Microbiol.2001, 67, 3180–3187.CrossRefGoogle Scholar
  87. [87]
    Nguyen, P. Q.; Courchesne, N. M. D.; Duraj-Thatte, A; Praveschotinunt, P.; Joshi, N. S. Engineered living materials: Prospects and challenges for using biological systems to direct the assembly of smart materials. Adv. Mater.2018, 30, 1704847.CrossRefGoogle Scholar
  88. [88]
    Webster, D. P.; TerAvest, M. A.; Doud, D. F. R.; Chakravorty, A.; Holmes, E. C.; Radens, C. M.; Sureka, S.; Gralnick, J. A.; Angenent, L. T. An arsenic-specific biosensor with genetically engineered Shewanella oneidensis in a bioelectrochemical system. Biosens. Bioelectron.2014, 62, 320–324.CrossRefGoogle Scholar
  89. [89]
    Tschirhart, T.; Kim, E.; McKay, R.; Ueda, H.; Wu, H. C.; Pottash, A. E.; Zargar, A.; Negrete, A.; Shiloach, J.; Payne, G. F. et al. Electronic control of gene expression and cell behaviour in Escherichia coli through redox signalling. Nat. Commun.2017, 8, 14030.CrossRefGoogle Scholar
  90. [90]
    TerAvest, M. A.; Li, Z. J.; Angenent, L. T. Bacteria-based biocomputing with cellular computing circuits to sense, decide, signal, and act. Energy Environ. Sci.2011, 4, 4907–4916.CrossRefGoogle Scholar
  91. [91]
    Tamsir, A.; Tabor, J. J.; Voigt, C. A. Robust multicellular computing using genetically encoded NOR gates and chemical ‘wires’. Nature2011, 469, 212–215.CrossRefGoogle Scholar
  92. [92]
    Tabor, J. J.; Salis, H. M.; Simpson, Z. B.; Chevalier, A. A.; Levskaya, A.; Marcotte, E. M.; Voigt, C. A.; Ellington, A. D. A synthetic genetic edge detection program. Cell2009, 137, 1272–1281.CrossRefGoogle Scholar
  93. [93]
    Li, Z. J.; Rosenbaum, M. A.; Venkataraman, A.; Tam, T. K.; Katz, E.; Angenent, L. T. Bacteria-based AND logic gate: A decision-making and self-powered biosensor. Chem. Commun.2011, 47, 3060–3062.CrossRefGoogle Scholar
  94. [94]
    Schuergers, N.; Werlang, C.; Ajo-Franklin, C. M.; Boghossian, A. A. A synthetic biology approach to engineering living photovoltaics. Energy Environ. Sci.2017, 10, 1102–1115.CrossRefGoogle Scholar
  95. [95]
    Tolker-Nielsen, T.; Molin, S. Spatial organization of microbial biofilm communities. Microb. Ecol.2000, 40, 75–84.Google Scholar
  96. [96]
    Darch, S. E.; Simoska, O.; Fitzpatrick, M.; Barraza, J. P.; Stevenson, K. J.; Bonnecaze, R. T.; Shear, J. B.; Whiteley, M. Spatial determinants of quorum signaling in a Pseudomonas aeruginosa infection model. Proc. Natl. Acad. Sci. USA2018, 115, 4779–4784.CrossRefGoogle Scholar
  97. [97]
    Hsu, L.; Deng, P.; Zhang, Y. X.; Jiang, X. C. Core/shell bacterial cables: A one-dimensional platform for probing microbial electron transfer. Nano Lett.2018, 18, 4606–4610.CrossRefGoogle Scholar
  98. [98]
    Knowlton, S.; Onal, S.; Yu, C. H.; Zhao, J. J.; Tasoglu, S. Bioprinting for cancer research. Trends Biotechnol.2015, 33, 504–513.CrossRefGoogle Scholar
  99. [99]
    Gu, Q.; Tomaskovic-Crook, E.; Wallace, G. G.; Crook, J. M. 3D bioprinting human induced pluripotent stem cell constructs for in situ cell proliferation and successive multilineage differentiation. Adv. Healthc. Mater.2017, 6, 1700175.CrossRefGoogle Scholar
  100. [100]
    Espinosa-Hoyos, D.; Jagielska, A.; Homan, K. A.; Du, H. F.; Busbee, T.; Anderson, D. G.; Fang, N. X.; Lewis, J. A.; Van Vliet, K. J. Engineered 3D-printed artificial axons. Sci. Rep.2018, 8, 478.CrossRefGoogle Scholar
  101. [101]
    Kolesky, D. B.; Homan, K. A.; Skylar-Scott, M. A.; Lewis, J. A. Three-dimensional bioprinting of thick vascularized tissues. Proc. Natl. Acad. Sci. USA2016, 113, 3179–3184.CrossRefGoogle Scholar
  102. [102]
    Qian, F.; Zhu, C.; Knipe, J. M.; Ruelas, S.; Stolaroff, J. K.; DeOtte, J. R.; Duoss, E. B.; Spadaccini, C. M.; Henard, C. A.; Guarnieri, M. T. et al. Direct writing of tunable living inks for bioprocess intensification. Nano Lett.2019, 19, 5829–5835.CrossRefGoogle Scholar
  103. [103]
    Hsu, L.; Jiang, X. C. ‘Living’ inks for 3D bioprinting. Trends Biotechnol.2019, 37, 795–796.CrossRefGoogle Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yixin Zhang
    • 1
  • Leo Huan-Hsuan Hsu
    • 1
  • Xiaocheng Jiang
    • 1
    Email author
  1. 1.Department of Biomedical EngineeringTufts UniversityMedfordUSA

Personalised recommendations