Eric VanArsdale

University of Maryland, College Park

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William E. Bentley

University of Maryland, College Park

Gregory F. Payne

University of Maryland, College Park

Eunkyoung Kim

University of Maryland, College Park

Chen‐Yu Chen

University of Maryland, College Park

Jinyang Li

Wenzhou Medical University

Gregory F. Payne

University of Maryland, College Park

Juliana Pitzer

University of Maryland, College Park

Kristina Stephens

Oak Ridge National Laboratory

Chen‐Yu Tsao

University of Maryland, College Park

Sally Wang

Institute for Bioscience and Biotechnology Research

Cooperative Institutions

University of Maryland, College Park

Institute for Bioscience and Biotechnology Research

Chinese Academy of Sciences

RWTH Aachen University

Biocat

University of Maryland, Baltimore

Advanced Bioscience Laboratories (United States)

Cell Biotech (South Korea)

John Wiley & Sons (United States)

Hudson Institute

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A redox-based electrogenetic CRISPR system to connect with and control biological information networks

Nature Communications (2020)

Narendranath Bhokisham Eric VanArsdale Kristina Stephens Pricila Hauk Gregory F. Payne

Electronic information can be transmitted to cells directly from microelectronics via electrode-activated redox mediators. These transmissions are decoded by redox-responsive promoters which enable user-specified control over biological function. Here, we build on this redox communication modality by establishing an electronic eCRISPR conduit of information exchange. This system acts as a biological signal processor, amplifying signal reception and filtering biological noise. We electronically amplify bacterial quorum sensing (QS) signaling by activating LasI, the autoinducer-1 synthase. Similarly, we filter out unintended noise by inhibiting the native SoxRS-mediated oxidative stress response regulon. We then construct an eCRISPR based redox conduit in both E. coli and Salmonella enterica. Finally, we display eCRISPR based information processing that allows transmission of spatiotemporal redox commands which are then decoded by gelatin-encapsulated E. coli. We anticipate that redox communication channels will enable biohybrid microelectronic devices that could transform our abilities to electronically interpret and control biological function.

10.1038/s41467-020-16249-x

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Citations (60)

Electrogenetic Signal Transmission and Propagation in Coculture to Guide Production of a Small Molecule, Tyrosine

ACS Synthetic Biology (2022)

Eric VanArsdale Juliana Pitzer Sally Wang Kristina Stephens Chen‐Yu Chen

There are many strategies to actuate and control genetic circuits, including providing stimuli like exogenous chemical inducers, light, magnetic fields, and even applied voltage, that are orthogonal to metabolic activity. Their use enables actuation of gene expression for the production of small molecules and proteins in many contexts. Additionally, there are a growing number of reports wherein cocultures, consortia, or even complex microbiomes are employed for the production of biologics, taking advantage of an expanded array of biological function. Combining stimuli-responsive engineered cell populations enhances design space but increases complexity. In this work, we co-opt nature's redox networks and electrogenetically route control signals into a consortium of microbial cells engineered to produce a model small molecule, tyrosine. In particular, we show how electronically programmed short-lived signals (i.e., hydrogen peroxide) can be transformed by one population and propagated into sustained longer-distance signals that, in turn, guide tyrosine production in a second population building on bacterial quorum sensing that coordinates their collective behavior. Two design methodologies are demonstrated. First, we use electrogenetics to transform redox signals into the quorum sensing autoinducer, AI-1, that, in turn, induces a tyrosine biosynthesis pathway transformed into a second population. Second, we use the electrogenetically stimulated AI-1 to actuate expression of ptsH, boosting the growth rate of tyrosine-producing cells, augmenting both their number and metabolic activity. In both cases, we show how signal propagation within the coculture helps to ensure tyrosine production. We suggest that this work lays a foundation for employing electrochemical stimuli and engineered cocultures for production of molecular products in biomanufacturing environments.

Autoinducer

Synthetic Biology

Cell Signaling

10.1021/acssynbio.1c00522

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Citations (16)

Redox-enabled electronic interrogation and feedback control of hierarchical and networked biological systems

Nature Communications (2023)

Sally Wang Chen‐Yu Chen John R. Rzasa Chen‐Yu Tsao Jinyang Li

Abstract Microelectronic devices can directly communicate with biology, as electronic information can be transmitted via redox reactions within biological systems. By engineering biology’s native redox networks, we enable electronic interrogation and control of biological systems at several hierarchical levels: proteins, cells, and cell consortia. First, electro-biofabrication facilitates on-device biological component assembly. Then, electrode-actuated redox data transmission and redox-linked synthetic biology allows programming of enzyme activity and closed-loop electrogenetic control of cellular function. Specifically, horseradish peroxidase is assembled onto interdigitated electrodes where electrode-generated hydrogen peroxide controls its activity. E. coli ’s stress response regulon, oxyRS , is rewired to enable algorithm-based feedback control of gene expression, including an eCRISPR module that switches cell-cell quorum sensing communication from one autoinducer to another—creating an electronically controlled ‘bilingual’ cell. Then, these disparate redox-guided devices are wirelessly connected, enabling real-time communication and user-based control. We suggest these methodologies will help us to better understand and develop sophisticated control for biology.

Synthetic Biology

10.1038/s41467-023-44223-w

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Citations (11)

Electronic signals are electrogenetically relayed to control cell growth and co-culture composition

Metabolic Engineering Communications (2021)

Kristina Stephens Fauziah Rahma Zakaria Eric VanArsdale Gregory F. Payne William E. Bentley

There is much to be gained by enabling electronic interrogation and control of biological function. While the benefits of bioelectronics that rely on potential-driven ionic flows are well known (electrocardiograms, defibrillators, neural prostheses, etc) there are relatively few advances targeting nonionic molecular networks, including genetic circuits. Redox activities combine connectivity to electronics with the potential for specific genetic control in cells. Here, electrode-generated hydrogen peroxide is used to actuate an electrogenetic "relay" cell population, which interprets the redox cue and synthesizes a bacterial signaling molecule (quorum sensing autoinducer AI-1) that, in turn, signals increased growth rate in a second population. The dramatically increased growth rate of the second population is enabled by expression of a phosphotransferase system protein, HPr, which is important for glucose transport. The potential to electronically modulate cell growth via direct genetic control will enable new opportunities in the treatment of disease and manufacture of biological therapeutics and other molecules.

Bioelectronics

Autoinducer

10.1016/j.mec.2021.e00176

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Citations (13)

Catechol‐Based Molecular Memory Film for Redox Linked Bioelectronics

Advanced Electronic Materials (2020)

Si Wu Eunkyoung Kim Chen‐Yu Chen Jinyang Li Eric VanArsdale

Abstract Redox is emerging as an alternative modality for bio‐device communication. In contrast to the more familiar ionic electrical modality: (i) redox involves the flow of electrons through oxidation–reduction reactions; (ii) the aqueous medium is an “insulator” to this electron flow since free electrons do not normally exist in water; and (iii) redox states are intrinsically digital (oxidized and reduced). By exploiting these unique features, a catechol‐based molecular memory film is reported. This memory is fabricated by electrochemically grafting catechol to a chitosan–agarose polysaccharide network to generate a redox‐active but non‐conducting matrix. The redox state of the grafted catechol moieties serves as the 2‐state memory. It is shown that these redox states: can be repeatedly switched by diffusible mediators (electron shuttles); can be easily read electrically or optically; are stable for at least 2 h in the absence of energy; are sensitive to biologically relevant oxidizing and reducing contexts; and can be switched enzymatically. This catechol‐based molecular memory film is a simple circuit element for redox linked bioelectronics.

Bioelectronics

Catechol

Oxidizing agent

10.1002/aelm.202000452

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Citations (22)

Assessing electrogenetic activation via a network model of biological signal propagation

Frontiers in Systems Biology (2024)

Kayla Chun Eric VanArsdale Elebeoba May Gregory F. Payne William E. Bentley

Introduction: Molecular communication is the transfer of information encoded by molecular structure and activity. We examine molecular communication within bacterial consortia as cells with diverse biosynthetic capabilities can be assembled for enhanced function. Their coordination, both in terms of engineered genetic circuits within individual cells as well as their population-scale functions, is needed to ensure robust performance. We have suggested that “electrogenetics,” the use of electronics to activate specific genetic circuits, is a means by which electronic devices can mediate molecular communication, ultimately enabling programmable control. Methods: Here, we have developed a graphical network model for dynamically assessing electronic and molecular signal propagation schemes wherein nodes represent individual cells, and their edges represent communication channels by which signaling molecules are transferred. We utilize graph properties such as edge dynamics and graph topology to interrogate the signaling dynamics of specific engineered bacterial consortia. Results: We were able to recapitulate previous experimental systems with our model. In addition, we found that networks with more distinct subpopulations (high network modularity) propagated signals more slowly than randomized networks, while strategic arrangement of subpopulations with respect to the inducer source (an electrode) can increase signal output and outperform otherwise homogeneous networks. Discussion: We developed this model to better understand our previous experimental results, but also to enable future designs wherein subpopulation composition, genetic circuits, and spatial configurations can be varied to tune performance. We suggest that this work may provide insight into the signaling which occurs in synthetically assembled systems as well as native microbial communities.

SIGNAL (programming language)

10.3389/fsysb.2024.1291293

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Interactive Materials for Bidirectional Redox‐Based Communication

Advanced Materials (2021)

Jinyang Li Sally P. Wang Guanghui Zong Eunkyoung Kim Chen‐Yu Tsao

Abstract Emerging research indicates that biology routinely uses diffusible redox‐active molecules to mediate communication that can span biological systems (e.g., nervous and immune) and even kingdoms (e.g., a microbiome and its plant/animal host). This redox modality also provides new opportunities to create interactive materials that can communicate with living systems. Here, it is reported that the fabrication of a redox‐active hydrogel film can autonomously synthesize a H 2 O 2 signaling molecule for communication with a bacterial population. Specifically, a catechol‐conjugated/crosslinked 4‐armed thiolated poly(ethylene glycol) hydrogel film is electrochemically fabricated in which the added catechol moieties confer redox activity: the film can accept electrons from biological reductants (e.g., ascorbate) and donate electrons to O 2 to generate H 2 O 2 . Electron‐transfer from an Escherichia coli culture poises this film to generate the H 2 O 2 signaling molecule that can induce bacterial gene expression from a redox‐responsive operon. Overall, this work demonstrates that catecholic materials can participate in redox‐based interactions that elicit specific biological responses, and also suggests the possibility that natural phenolics may be a ubiquitous biological example of interactive materials.

Catechol

10.1002/adma.202007758

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Citations (24)

Hydrogel Patterning with Catechol Enables Networked Electron Flow

Advanced Functional Materials (2021)

Si Wu Zhiling Zhao John R. Rzasa Eunkyoung Kim Jinyang Li

Abstract Reduction–oxidation (redox) reactions provide a distinct modality for biological communication that is fundamentally different from the more‐familiar ion‐based electrical modality. Biology uses these two modalities for communication through different systems (immune versus nervous), and uses different mechanisms to control the flow of the charge carriers: the flow of soluble ions is controlled using structural barriers (i.e., membranes) and gates (e.g., membrane‐spanning protein channels), while the flow of insoluble electrons is controlled using redox‐reaction networks. Here, a simple electrochemical approach to pattern catechols onto a flexible polysaccharide hydrogel is reported and it is demonstrated that the patterned catechol regions serve as nodes for the mediated flow of electrons through redox reactions. Electron flow through this node involves the switching of binary redox states (oxidized and reduced) and this node's redox state can be detected (i.e., “read”) by passively observing its optical absorbance, or actively switching its redox‐state electrochemically. Further, this catechol node can be switched through biological mechanisms, and this enables the fabricated catechol node to be embedded within biochemical redox reaction networks to facilitate the spanning of bio‐electronic communication. Thus, it is envisioned that catechols can emerge as a molecular equivalent to a transistor for miniaturize‐able, deployable and sustainable redox‐linked bioelectronics.

Bioelectronics

Catechol

10.1002/adfm.202007709

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Citations (33)

Rapid, high-titer biosynthesis of melanin using the marine bacterium Vibrio natriegens

Frontiers in Bioengineering and Biotechnology (2023)

Aaron D. Smith Tanya Tschirhart Jaimee R. Compton Tiffany M. Hennessa Eric VanArsdale

Melanin is one of the most abundant natural biomolecules on Earth. These macromolecular biopolymers display several unique physical and chemical properties and have garnered interest as biomaterials for various commercial and industrial applications. To this end, extensive research has gone into refining methods for the synthesis and extraction of melanin from natural and recombinant sources. In this study, we developed and refined a procedure using a recombinant microbial system for the biosynthesis of melanin using the tyrosinase enzyme Tyr1 and tyrosine as a substrate. Using the emergent microbial chassis organisms Vibrio natriegens , we achieved maximal yields of 7.57 g/L, and one of the highest reported volumetric productivities of 473 mg L −1 h −1 with 100% conversion rates in an optimized, minimally defined medium. Additionally, we identified and investigated the use of a native copper responsive promoter in V. natriegens for stringent regulation of heterologous protein expression as a cost effective alternative to traditional IPTG-based induction. This research represents a promising advancement towards a green, rapid, and economical alternative for the biomanufacture of melanin.

Heterologous

Marine bacteriophage

10.3389/fbioe.2023.1239756

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Citations (5)

Enhanced Electrochemical Measurement of β-galactosidase Activity in Whole Cells by Coexpression of Lactose Permease, LacY

BioTechniques (2022)

Eric VanArsdale Juliana Pitzer Sally Wang Kristina Stephens Chen‐Yu Chen

Whole-cell biosensing links the sensing and computing capabilities of microbes to the generation of a detectable reporter. Whole cells enable dynamic biological computation (filtered noise, amplified signals, logic gating etc.). Enzymatic reporters enable in situ signal amplification. Electrochemical measurements are easily quantified and work in turbid environments. In this work we show how the coexpression of the lactose permease, LacY, dramatically improves electrochemical sensing of β-galactosidase (LacZ) expressed as a reporter in whole cells. The permease facilitates transport of the LacZ substrate, 4-aminophenyl β-d-galactopyranoside, which is converted to redox active p-aminophenol, which, in turn, is detected via cyclic voltammetry or chronocoulometry. We show a greater than fourfold improvement enabled by lacY coexpression in cells engineered to respond to bacterial signal molecules, pyocyanin and quorum-sensing autoinducer-2.

Lactose permease

10.2144/btn-2022-0090

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Citations (4)