Towards patterned bioelectronics: facilitated immobilization of exoelectrogenic Escherichia coli with heterologous pili

Lienemann, Michael; TerAvest, Michaela A.; Pitkänen, Juha‐Pekka; Stuns, Ingmar; Penttilä, Merja; Ajo‐Franklin, Caroline M.; Jäntti, Jussi

doi:10.1111/1751-7915.13309

Title: Towards patterned bioelectronics: facilitated immobilization of exoelectrogenic Escherichia coli with heterologous pili

Journal Article · Mon Sep 17 00:00:00 EDT 2018 · Microbial Biotechnology (Online)

DOI:https://doi.org/10.1111/1751-7915.13309· OSTI ID:1471141

^[1]; TerAvest, Michaela A. ^[2]; Pitkänen, Juha‐Pekka ^[3]; Stuns, Ingmar ^[1]; Penttilä, Merja ^[1]; Ajo‐Franklin, Caroline M. ^[4]; Jäntti, Jussi ^[1]

VTT Technical Research Centre of Finland Ltd Espoo Finland
Department of Biochemistry and Molecular Biology Michigan State University East Lansing MI USA, The Molecular Foundry Lawrence Berkeley National Laboratory Molecular Biophysics and Integrated Bioimaging Division Synthetic Biology Institute Berkeley CA USA
VTT Technical Research Centre of Finland Ltd Espoo Finland, Current affiliation: Solar Foods Ltd Helsinki Finland
The Molecular Foundry Lawrence Berkeley National Laboratory Molecular Biophysics and Integrated Bioimaging Division Synthetic Biology Institute Berkeley CA USA

Summary Biosensors detect signals using biological sensing components such as redox enzymes and biological cells. Although cellular versatility can be beneficial for different applications, limited stability and efficiency in signal transduction at electrode surfaces represent a challenge. Recent studies have shown that the Mtr electron conduit from Shewanella oneidensis MR ‐1 can be produced in Escherichia coli to generate an exoelectrogenic model system with well‐characterized genetic tools. However, means to specifically immobilize this organism at solid substrates as electroactive biofilms have not been tested previously. Here, we show that mannose‐binding Fim pili can be produced in exoelectrogenic E. coli and can be used to selectively attach cells to a mannose‐coated material. Importantly, cells expressing fim genes retained current production by the heterologous Mtr electron conduit. Our results demonstrate the versatility of the exoelectrogenic E. coli system and motivate future work that aims to produce patterned biofilms for bioelectronic devices that can respond to various biochemical signals.

View Journal Article

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); Office of Naval Research (ONR) (United States); The Finnish Funding Agency for Technology and Innovation (Tekes) (Finland); Academy of Finland

Grant/Contract Number:: 287011; DE‐AC02‐05CH11231; AC02-05CH11231; N000141310551; 2299/31/2012; 40044/13; 277121; 272569

OSTI ID:: 1471141

Alternate ID(s):: OSTI ID: 1472156; OSTI ID: 1483273

Journal Information:: Microbial Biotechnology (Online), Journal Name: Microbial Biotechnology (Online) Vol. 11 Journal Issue: 6; ISSN 1751-7915

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 18 works

Citation information provided by
Web of Science

References (55)

Tuning Promoter Strengths for Improved Synthesis and Function of Electron Conduits in Escherichia coli Goldbeck, Cheryl P.; Jensen, Heather M.; TerAvest, Michaela A. ACS Synthetic Biology, Vol. 2, Issue 3 https://doi.org/10.1021/sb300119v	journal	August 2012
Ferrozine---a new spectrophotometric reagent for iron Stookey, Lawrence L. Analytical Chemistry, Vol. 42, Issue 7, p. 779-781 https://doi.org/10.1021/ac60289a016	journal	June 1970
An arsenic-specific biosensor with genetically engineered Shewanella oneidensis in a bioelectrochemical system Webster, Dylan P.; TerAvest, Michaela A.; Doud, Devin F. R. Biosensors and Bioelectronics, Vol. 62 https://doi.org/10.1016/j.bios.2014.07.003	journal	December 2014
Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli: Stick-and-roll bacterial adhesion Thomas, Wendy E.; Nilsson, Lina M.; Forero, Manu Molecular Microbiology, Vol. 53, Issue 5 https://doi.org/10.1111/j.1365-2958.2004.04226.x	journal	August 2004
Electrochemical Analysis of Shewanella oneidensis Engineered To Bind Gold Electrodes Kane, Aunica L.; Bond, Daniel R.; Gralnick, Jeffrey A. ACS Synthetic Biology, Vol. 2, Issue 2 https://doi.org/10.1021/sb300042w	journal	August 2012
Cryo-Transmission Electron Microscopy of Frozen-Hydrated Sections of Escherichia coli and Pseudomonas aeruginosa Matias, V. R. F.; Al-Amoudi, A.; Dubochet, J. Journal of Bacteriology, Vol. 185, Issue 20 https://doi.org/10.1128/JB.185.20.6112-6118.2003	journal	October 2003
Organization and expression of genes responsible for type 1 piliation in Escherichia coli. Orndorff, P. E.; Falkow, S. Journal of Bacteriology, Vol. 159, Issue 2 https://doi.org/10.1128/JB.159.2.736-744.1984	journal	January 1984
Transforming exoelectrogens for biotechnology using synthetic biology: Synthetic Biology of Exoelectrogens TerAvest, Michaela A.; Ajo-Franklin, Caroline M. Biotechnology and Bioengineering, Vol. 113, Issue 4 https://doi.org/10.1002/bit.25723	journal	September 2015
Formate Metabolism in Shewanella oneidensis Generates Proton Motive Force and Prevents Growth without an Electron Acceptor Kane, Aunica L.; Brutinel, Evan D.; Joo, Heena Journal of Bacteriology, Vol. 198, Issue 8 https://doi.org/10.1128/JB.00927-15	journal	February 2016
Interaction of Gold Nanoparticles with Common Human Blood Proteins Lacerda, Silvia H. De Paoli; Park, Jung Jin; Meuse, Curt ACS Nano, Vol. 4, Issue 1 https://doi.org/10.1021/nn9011187	journal	December 2009
The electrically conductive pili of Geobacter species are a recently evolved feature for extracellular electron transfer Holmes, Dawn E.; Dang, Yan; Walker, David J. F. Microbial Genomics, Vol. 2, Issue 8 https://doi.org/10.1099/mgen.0.000072	journal	August 2016
CymA and Exogenous Flavins Improve Extracellular Electron Transfer and Couple It to Cell Growth in Mtr-Expressing Escherichia coli Jensen, Heather M.; TerAvest, Michaela A.; Kokish, Mark G. ACS Synthetic Biology, Vol. 5, Issue 7 https://doi.org/10.1021/acssynbio.5b00279	journal	April 2016
Dissimilatory Fe(III) and Mn(IV) reduction. Lovley, D. R. Microbiological Reviews, Vol. 55, Issue 2 https://doi.org/10.1128/MMBR.55.2.259-287.1991	journal	January 1991
Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities Breuer, Marian; Rosso, Kevin M.; Blumberger, Jochen Journal of The Royal Society Interface, Vol. 12, Issue 102 https://doi.org/10.1098/rsif.2014.1117	journal	January 2015
Single-Walled Carbon Nanotube as a Unique Scaffold for the Multivalent Display of Sugars Gu, Lingrong; Luo, Pengju G.; Wang, Haifang Biomacromolecules, Vol. 9, Issue 9 https://doi.org/10.1021/bm800395e	journal	September 2008
Characterization of the Shewanella oneidensis MR-1 Decaheme Cytochrome MtrA : EXPRESSION IN Pitts, Katy E.; Dobbin, Paul S.; Reyes-Ramirez, Francisca Journal of Biological Chemistry, Vol. 278, Issue 30 https://doi.org/10.1074/jbc.M302582200	journal	May 2003
Electrode-assisted acetoin production in a metabolically engineered Escherichia coli strain Förster, Andreas H.; Beblawy, Sebastian; Golitsch, Frederik Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0745-9	journal	March 2017
Bacteria-based AND logic gate: a decision-making and self-powered biosensor Li, Zhongjian; Rosenbaum, Miriam A.; Venkataraman, Arvind Chemical Communications, Vol. 47, Issue 11 https://doi.org/10.1039/c0cc05037g	journal	January 2011
The sweet connection: Solving the riddle of multiple sugar-binding fimbrial adhesins in Escherichia coli: Multiple E. coli fimbriae form a versatile arsenal of sugar-binding lectins potentially involved in surface-colonisation and tissue tropism Korea, Charalampia-Georgia; Ghigo, Jean-Marc; Beloin, Christophe BioEssays, Vol. 33, Issue 4 https://doi.org/10.1002/bies.201000121	journal	February 2011
A New Strain Collection for Improved Expression of Outer Membrane Proteins Meuskens, Ina; Michalik, Marcin; Chauhan, Nandini Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00464	journal	November 2017
Engineering of a synthetic electron conduit in living cells Jensen, H. M.; Albers, A. E.; Malley, K. R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 45 https://doi.org/10.1073/pnas.1009645107	journal	October 2010
Three promising applications of microbial electrochemistry for the water sector Modin, Oskar; Aulenta, Federico Environmental Science: Water Research & Technology, Vol. 3, Issue 3 https://doi.org/10.1039/C6EW00325G	journal	January 2017
Microbial electron transport and energy conservation â€“ the foundation for optimizing bioelectrochemical systems Kracke, Frauke; Vassilev, Igor; KrÃ¶mer, Jens O. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00575	journal	June 2015
Rational design of quinones for high power density biofuel cells Milton, Ross D.; Hickey, David P.; Abdellaoui, Sofiene Chemical Science, Vol. 6, Issue 8 https://doi.org/10.1039/C5SC01538C	journal	January 2015
Electroactive Biofilms for Sensing: Reflections and Perspectives Prévoteau, Antonin; Rabaey, Korneel ACS Sensors, Vol. 2, Issue 8 https://doi.org/10.1021/acssensors.7b00418	journal	July 2017
Influences of Aerobic Respiration on Current Generation by Shewanella oneidensis MR-1 in Single-Chamber Microbial Fuel Cells Kouzuma, Atsushi; Hashimoto, Kazuhito; Watanabe, Kazuya Bioscience, Biotechnology, and Biochemistry, Vol. 76, Issue 2 https://doi.org/10.1271/bbb.110633	journal	February 2012
Shewanella secretes flavins that mediate extracellular electron transfer Marsili, E.; Baron, D. B.; Shikhare, I. D. Proceedings of the National Academy of Sciences, Vol. 105, Issue 10 https://doi.org/10.1073/pnas.0710525105	journal	March 2008
A whole-cell electrochemical biosensing system based on bacterial inward electron flow for fumarate quantification Si, Rong-Wei; Zhai, Dan-Dan; Liao, Zhi-Hong Biosensors and Bioelectronics, Vol. 68 https://doi.org/10.1016/j.bios.2014.12.035	journal	June 2015
Long-term arsenic monitoring with an Enterobacter cloacae microbial fuel cell Rasmussen, Michelle; Minteer, Shelley D. Bioelectrochemistry, Vol. 106 https://doi.org/10.1016/j.bioelechem.2015.03.009	journal	December 2015
Programming the quorum sensing-based AND gate in Shewanella oneidensis for logic gated-microbial fuel cells Hu, Yidan; Yang, Yun; Katz, Evgeny Chemical Communications, Vol. 51, Issue 20 https://doi.org/10.1039/C5CC00026B	journal	January 2015
Microbial fuel cell biosensor for in situ assessment of microbial activity Tront, J. M.; Fortner, J. D.; Plötze, M. Biosensors and Bioelectronics, Vol. 24, Issue 4 https://doi.org/10.1016/j.bios.2008.06.006	journal	December 2008
Efficient Immobilization and Patterning of Live Bacterial Cells Suo, Zhiyong; Avci, Recep; Yang, Xinghong Langmuir, Vol. 24, Issue 8 https://doi.org/10.1021/la7038653	journal	April 2008
Mind the gap: cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1 Fonseca, Bruno M.; Paquete, Catarina M.; Neto, Sónia E. Biochemical Journal, Vol. 449, Issue 1 https://doi.org/10.1042/BJ20121467	journal	December 2012
Periplasmic Electron Transfer via the c-Type Cytochromes MtrA and FccA of Shewanella oneidensis MR-1 Schuetz, B.; Schicklberger, M.; Kuermann, J. Applied and Environmental Microbiology, Vol. 75, Issue 24 https://doi.org/10.1128/AEM.01834-09	journal	October 2009
Is there a Specific Ecological Niche for Electroactive Microorganisms? Koch, Christin; Harnisch, Falk ChemElectroChem, Vol. 3, Issue 9 https://doi.org/10.1002/celc.201600079	journal	July 2016
Dissimilatory iron reduction in Escherichia coli: identification of CymA of Shewanella oneidensis and NapC of E. coli as ferric reductases Gescher, Johannes S.; Cordova, Carmen D.; Spormann, Alfred M. Molecular Microbiology, Vol. 68, Issue 3 https://doi.org/10.1111/j.1365-2958.2008.06183.x	journal	May 2008
Tools for resolving complexity in the electron transfer networks of multiheme cytochromes c Firer-Sherwood, Mackenzie A.; Bewley, Kathryn D.; Mock, Jee-Young Metallomics, Vol. 3, Issue 4 https://doi.org/10.1039/c0mt00097c	journal	January 2011
Blue Light Switchable Bacterial Adhesion as a Key Step toward the Design of Biofilms Chen, Fei; Wegner, Seraphine V. ACS Synthetic Biology, Vol. 6, Issue 12 https://doi.org/10.1021/acssynbio.7b00197	journal	August 2017
Microbial Biofilm Voltammetry: Direct Electrochemical Characterization of Catalytic Electrode-Attached Biofilms Marsili, E.; Rollefson, J. B.; Baron, D. B. Applied and Environmental Microbiology, Vol. 74, Issue 23 https://doi.org/10.1128/AEM.00177-08	journal	October 2008
Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella Brutinel, Evan D.; Gralnick, Jeffrey A. Applied Microbiology and Biotechnology, Vol. 93, Issue 1 https://doi.org/10.1007/s00253-011-3653-0	journal	November 2011
Genomic reconstruction of Shewanella oneidensis MR-1 metabolism reveals a previously uncharacterized machinery for lactate utilization Pinchuk, Grigory E.; Rodionov, Dmitry A.; Yang, Chen Proceedings of the National Academy of Sciences, Vol. 106, Issue 8 https://doi.org/10.1073/pnas.0806798106	journal	February 2009
The Mtr Pathway of Shewanella oneidensis MR-1 Couples Substrate Utilization to Current Production in Escherichia coli TerAvest, Michaela A.; Zajdel, Tom J.; Ajo-Franklin, Caroline M. ChemElectroChem, Vol. 1, Issue 11 https://doi.org/10.1002/celc.201402194	journal	August 2014
Partial Functional Replacement of CymA by SirCD in Shewanella oneidensis MR-1 Cordova, C. D.; Schicklberger, M. F. R.; Yu, Y. Journal of Bacteriology, Vol. 193, Issue 9 https://doi.org/10.1128/JB.01355-10	journal	March 2011
Biofilm Lithography enables high-resolution cell patterning via optogenetic adhesin expression Jin, Xiaofan; Riedel-Kruse, Ingmar H. Proceedings of the National Academy of Sciences, Vol. 115, Issue 14 https://doi.org/10.1073/pnas.1720676115	journal	March 2018
Unbalanced fermentation of glycerol in Escherichia coli via heterologous production of an electron transport chain and electrode interaction in microbial electrochemical cells Sturm-Richter, Katrin; Golitsch, Frederik; Sturm, Gunnar Bioresource Technology, Vol. 186 https://doi.org/10.1016/j.biortech.2015.02.116	journal	June 2015
Preferential Utilization of d-Lactate by Shewanella oneidensis Brutinel, Evan D.; Gralnick, Jeffrey A. Applied and Environmental Microbiology, Vol. 78, Issue 23 https://doi.org/10.1128/AEM.02183-12	journal	September 2012
Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1 Xu, Shuai; Jangir, Yamini; El-Naggar, Mohamed Y. Electrochimica Acta, Vol. 198 https://doi.org/10.1016/j.electacta.2016.03.074	journal	April 2016
Carboxyl functionalization of carbon fibers through a grafting reaction that preserves fiber tensile strength Ehlert, Gregory J.; Lin, Yirong; Sodano, Henry A. Carbon, Vol. 49, Issue 13 https://doi.org/10.1016/j.carbon.2011.05.057	journal	November 2011
A functional description of CymA, an electron-transfer hub supporting anaerobic respiratory flexibility in Shewanella Marritt, Sophie J.; Lowe, Thomas G.; Bye, Jordan Biochemical Journal, Vol. 444, Issue 3 https://doi.org/10.1042/BJ20120197	journal	May 2012
Proof of principle for an engineered microbial biosensor based on Shewanella oneidensis outer membrane protein complexes Golitsch, Frederik; Bücking, Clemens; Gescher, Johannes Biosensors and Bioelectronics, Vol. 47 https://doi.org/10.1016/j.bios.2013.03.010	journal	September 2013
Isotopic labeling of c-type multiheme cytochromes overexpressed in E. coli Fernandes, Ana P.; Couto, Isabel; Morgado, Leonor Protein Expression and Purification, Vol. 59, Issue 1 https://doi.org/10.1016/j.pep.2008.02.001	journal	May 2008
Hydrogen Metabolism in Shewanella oneidensis MR-1 Meshulam-Simon, G.; Behrens, S.; Choo, A. D. Applied and Environmental Microbiology, Vol. 73, Issue 4 https://doi.org/10.1128/AEM.01588-06	journal	December 2006
Dissimilatory Reduction of Extracellular Electron Acceptors in Anaerobic Respiration Richter, Katrin; Schicklberger, Marcus; Gescher, Johannes Applied and Environmental Microbiology, Vol. 78, Issue 4 https://doi.org/10.1128/AEM.06803-11	journal	December 2011
Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1: Modularity in S. oneidensis Coursolle, Dan; Gralnick, Jeffrey A. Molecular Microbiology https://doi.org/10.1111/j.1365-2958.2010.07266.x	journal	July 2010
Anaerobes unleashed: Aerobic fuel cells of Geobacter sulfurreducens Nevin, Kelly P.; Zhang, Pei; Franks, Ashley E. Journal of Power Sources, Vol. 196, Issue 18 https://doi.org/10.1016/j.jpowsour.2011.05.021	journal	September 2011

Similar Records

PEDOT:PSS-based Multilayer Bacterial-Composite Films for Bioelectronics

Journal Article · Tue Oct 16 00:00:00 EDT 2018 · Scientific Reports · OSTI ID:1471141

Zajdel, Tom J.; Baruch, Moshe; Méhes, Gábor; +5 more

Enhanced redox conductivity and enriched Geobacteraceae of exoelectrogenic biofilms in response to static magnetic field

Journal Article · Wed Jun 20 00:00:00 EDT 2018 · Applied Microbiology and Biotechnology · OSTI ID:1471141

Li, Cheng; Wang, Luguang; Liu, Hong

Comparative genomics of Geobacter chemotaxis genes reveals diverse signaling function

Journal Article · Tue Jan 01 00:00:00 EST 2008 · BMC Genomics · OSTI ID:1471141

Tran, Hoa T.; Krushkal, Julia; Antommattei, Frances M.; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Towards patterned bioelectronics: facilitated immobilization of exoelectrogenic Escherichia coli with heterologous pili

Citation Formats

References (55)

Similar Records

Related Subjects