From Microbial Fuel Cells to Biobatteries: Moving Toward On-Demand Micropower Generation for Small-Scale Single-Use Applications

PROGRESS REPORT

Biobatteries www.advmattechnol.de From Microbial Fuel Cells to Biobatteries: Moving toward On-Demand Micropower Generation for Small-Scale Single-Use Applications

Yang Gao, Maedeh Mohammadifar, and Seokheun Choi*

and point-of-care diagnostics, allowing Microbial fuel cells (MFCs) that generate electricity generation from a broad for immediate actions to be taken with diversity of biomass and organic substrates through microbial metabolism critical healthcare information available have attracted considerable research interest as an alternative clean energy at accident sites, in doctors’ offices and in ambulances.[11,12] Furthermore, minia- technology and energy-efficient wastewater treatment method. Despite turized disposable device technology has encouraging successes and auspicious pilot-scale experiments of the MFCs, been used in transient electronics which is increasing doubts about their viability for practical large-scale applications an emerging technology with the unique are being raised. Low performance, expensive core parts and materials, characteristic of physically disappearing [13,14] energy-intensive operation, and scaling bottlenecks question a sustainable on demand. The small-scale devices development. Instead, special MFCs for low-power battery-reliant devices can be ubiquitously deployed in our environment to temporarily collect real- might be more applicable and potentially realizable. Such bacteria-powered time information for human safety and biobatteries would enable i) a truly stand-alone device platform suitable for security,[15,16] revolutionizing the fields use in resource-limited and remote regions, ii) simple, on-demand power of temporary biomedical implants,[17,18] generation within a programmed period of time, and iii) a tracelessly biode- environmentally friendly electronics,[19] [20] gradable battery due to the use of the bacteria used for power generation. The data-secure memory devices, and disposable consumer electronics.[21] After biobattery would be an excellent power solution for small-scale, on-demand, their operation, the devices are prefer- single-use, and disposable electronics. Recent progress of small-scale MFC- ably designed to biodegrade without any based biobatteries is critically reviewed with specific attention toward various environmental and public health issues. device platforms. Furthermore, comments and outlook related to the potential Despite the huge potential of the small- directions and challenges of the biobatteries are discussed to offer inspiration scale disposable devices in diagnostics to the community and induce fruitful future research. and next-generation electronics, however, significant challenges still remain in developing those devices at a system level that contains an integrated, on-demand power 1. Introduction source.[22–24] The key challenge is to develop a miniaturized on-chip power source for those diagnostic and transient devices Small-scale, single-use, disposable electronic devices have in a more effective and efficient way. Power autonomy is one recently received tremendous attention in diagnostic indus- of the most crucial elements of the devices for them to work tries and transient electronics.[1–6] The single-use technique independently and self-sustainably, even in resource-limited significantly reduces the risk of cross-contamination,[1] opera- environments where a stable electrical supply is not avail- tion and manufacturing costs,[2] and information leakage[7] able.[4] Even standard batteries are not suitable owing to their while the device miniaturization offers low power require- cost, incompatibility with miniaturized device platforms, dis- ment, high speed, and good reliability.[8–10] The small-scale, posal difficulties, and potential danger to the environment.[25,26] single-use devices enable the creation of low-cost, easy-to-use, Also, conventional energy harvesting technologies (e.g., solar, thermal, mechanical, chemical energy) are too overqualified and expensive to be used as a power source for single- Y. Gao, M. Mohammadifar, Prof. S. Choi use, disposable electronic applications, which require only Bioelectronics and Microsystems Laboratory small amounts of power consumption for a relatively short Department of Electrical and Computer Engineering time. What is necessary is a green, low-cost, and disposable State University of New York-Binghamton micropower source that can be easily incorporated into small, Binghamton, NY 13902, USA E-mail: [email protected] single-use applications for use in resource-limited environments. Among the many batteries and other energy storage The ORCID identification number(s) for the author(s) of this article can be found under https://doi.org/10.1002/admt.201900079. devices, a microbial fuel cell (MFC) based biobattery is the most underdeveloped.[27] Nonetheless, excitement is growing, as DOI: 10.1002/admt.201900079 microorganisms can generate electrical power from wastewater

Adv. Mater. Technol. 2019, 1900079 1900079 (1 of 26) © 2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.advancedsciencenews.com www.advmattechnol.de or biomass, if available in resource-limited settings.[28,29] Furthermore, the biobattery can be decomposed by the on-chip Yang Gao received his microorganisms, promoting device biodegradability.[30,31] B.Sc. degree at Sichuan Here, we highlight the latest progress in the development University in China in 2011. of the bacteria-powered biobatteries and their applications. We After graduation, he was an will first discuss the MFC technology and its limitation as a electrical engineer in the practical power source. Then, we will introduce a novel MFC- R&D Department at Sinovel based biobattery platform as a new avenue for the MFC, which Wind Group Co., Ltd in China include the working mechanisms, configurations, and compo- between 2011 and 2013. nents. Details of the frontier research of flexible biobatteries, Then, he worked at the Hong biodegradable biobatteries, and long-lasting biobatteries will Kong Polytechnic University be discussed. Lastly, we will provide a critical perspective on on microgrid implementation strategic future applications. between 2014 and 2015. He is currently a Ph.D. student in the Electrical and Computer Engineering Department at State University of New York 2. Limitations in Microbial Fuel Cells (SUNY) at Binghamton, NY, USA. His research interests include paper-based and textile-based biobatteries. Even a few years ago, no one doubted that the next generation of renewable energy could come through electroactive microorganisms (cf. also known as exoelectrogens, electrochemically active Maedeh Mohammadifar bacteria, anode respiring bacteria, and electricigens) because of received her B.Sc. degree their extraordinary ability to extracellularly transfer electrons from Khajeh Nasir Toosi from renewable organic matter to external electrodes.[32] This University of Technology, biological renewable energy technology looked fascinating as Tehran, Iran, in 2008, and a solution for environmental preservation and sustainability her M.Sc. degree from by generating renewable bioelectricity with abundant organic Amirkabir University of waste in nature.[33–35] Time selected this technique as the “The Technology, Tehran, Iran, in 50 Best Inventions for 2009.”[36] Furthermore, its considerable 2010. After graduation, she progress arisen from revolutionizing MFCs strengthened our was a research engineer at beliefs that this bacterial energy production could alleviate the Technology Incubator energy crises and environmental pollution. Notwithstanding Center of Tehran University the continuous governmental, academic and industrial efforts of Medical Sciences between 2011 and 2014. She is and money spent for the last decade, MFC techniques have not currently a Ph.D. student in the Electrical and Computer been able to go further than pilot-scale tests. The question has Engineering Department at State University of New York been raised by many leading researchers as to whether MFCs (SUNY) at Binghamton, NY, USA. Her research interests can be a future alternative energy technology and an energy- include paper-based, biodegradable, and transient efficient wastewater treatment method,[37,38] while leaving some biobatteries, and self-powered biosensors. possibilities of its practical use for powering small-scale electronics in sediment environments.[39–41] Rather, there has been a significant shift in research toward bacterial electrosynthesis Seokheun Choi received his by using bidirectional bacterial electron exchange, producing B.Sc. and M.Sc. degrees in value-added chemicals,[42–45] or biofuels,[46–48] or performing electrical engineering from many other environmentally important functions, such as Sungkyunkwan University, water desalination,[49,50] bioremediation,[51,52] and toxicity detec- Korea, in 2003 and 2004, tion.[53,54] This is because of several critical issues that prevent respectively. He received his MFC technology from becoming a practical real system for Ph.D. degree in electrical power production at larger scales. First, the power output of the engineering from Arizona MFC (i.e., only several thousand mW m−2) is still too low for State University, USA, in practical applications other than powering low-power sensing 2011. He was a research devices.[55,56] Significant research efforts in exploring MFC engineer with LG Chem, Ltd., architectures, materials, electroactive bacteria, and operating Korea, from 2004–2006. From conditions have been made to improve the power performance 2011–2012, he was a research professor at the University of MFCs, but the outputs are not even comparable to other of Cincinnati, USA. He is currently an associate professor energy technological results.[56–59] Second, the amount of power in the Department of Electrical & Computer Engineering generated by MFCs is not a linear function of their size. Even at SUNY-Binghamton. Also, he is serving as an associate if the MFCs can be fabricated for large-scale applications, their director of the Center for Research in Advanced Sensing power output and wastewater treatment capacity do not increase Technologies and Environmental Sustainability at proportionally.[60] Although scaling up by incorporating minia- SUNY-Binghamton. turized MFC units could lead to linear or super-linear increase

of the output power with stack size/volume,[61] oftentimes, the power density and treatment efficiency of the MFC stacks degrade while the total cost of materials, operation, and maintenance increases significantly.[62,63] Last but not least, long-term operation of the living bacteria in a continuous MFC system requires multilevel complex feedback controls to optimize conditions, such as[64,65]temperature,[66] pH,[67] gas,[68] and rate of substrate loading,[69,70] resulting to higher energy costs than the MFC produces.[58] Moreover, during the operation, many other issues including material degradation, system malfunc- tion, and biofouling, relegate this promising energy harvesting technology to the status of a laboratory curiosity.[38] Sediment and benthic MFCs are the few types of bacteria- powered electricity harvesting platforms thus far demonstrated as practical power sources.[71–73] As sediment MFCs use natural bacteria and in situ nutrients continuously renewed by natural processes, these MFCs have been considered an alternative energy harvesting technique for long-term, consistent, main- Figure 1. Conceptual illustration of the biobattery and its potential tenance-free and cost-effective use without any power-required application. feeding system. Moreover, since the anoxic sediment naturally offers anaerobic conditions for the bacteria resides on the anode, occupying habitats with extreme conditions of temperature, there is no need to hermetically seal the device to promote the pH, salt concentration, radiation, and different air gas compo- bacterial electron transfer for the power production. During the sitions.[79–82] As an energy harvesting technique, if the biggest last decade, sediment MFCs have been intensively investigated issues for MFC are low power density, scaling-up bottleneck, to provide a practical power source and some of them were suc- and maintenance-dependent operation, then, a small-power, cessfully demonstrated to operate remote wireless sensors.[41,74] miniaturized, and disposable battery-type MFC platform for However, our ability to harness the potential of sediment MFC short-term standalone operation will be more applicable and technology lags from fundamental factors that maximize its potentially realizable (Figure 1).[38] While the bacteria-powered performance capability. The overall output voltage of the device battery (or biobattery) is similar to the MFC that converts does not increase because all the anodes are embedded in the biochemical energy to electrical power, the battery stores its same electrolyte solution, forming a short circuit.[75,76] This reactants and products internally without replenishing the limits the device potential to just around 500 mV.[40,77] Its overall reactant and withdrawing the products. Therefore, the biobat- power output is also low and cannot provide continuously reli- tery will be used to power battery-reliant devices that require able power for applications. Moreover, scaling-up the MFC does only minimal amounts of energy for a relatively short-term not guarantee increases in power production and rather leads period. The beauty of the biobattery, then, is that electricity can to difficulties in anchoring, operating, and maintaining the be extracted from almost limitless environmental or biological large anode in the sediment.[72] To alleviate these limitations, a liquids that are readily available even in the most resource- unique solution has been to intermittently provide short bursts constrained settings. of high power and voltage by using an efficient power manage- As a newly developed platform, the term “biobattery” will be ment interface.[39,78] However, this approach will never be a used in this progress report interchangeably with “the small- fundamental breakthrough that can maximize the MFC power scale MFCs operating in batch mode” during the discussion of generating capabilities. Above all, since the sediment MFCs are prior arts in the next section, because the MFC without organic deployed under the seafloor and riverbeds, their applications substrate replenishment could be considered as a biobattery. will be very limited or require much more power for signal communication from the deep water. 3.1. Biobattery Configuration and Operation

3. Biobatteries: a New Avenue for Microbial An MFC, consisting of an anode, cathode, and ion exchange Fuel Cells membrane, is an electrochemical energy conversion device that can generate electrical power through microbial anode respira- Then, should it be a science fiction to translate the MFC technology tion (Figure 2A). A specialized subset of microorganisms (i.e., to practical real-world applications? Although a macrolevel or electroactive bacteria) in the MFC make their own energy by mesolevel MFC system for power generation and wastewater generating a proton gradient across the cell membrane through treatment or a benthic MFC for long-term and high-power extracellular electron transfer (EET) in the anoxic or anaerobic generation in the sediment environment may not be practically environment, establishing electrical contact with the external realized in the short term, the revolutionary microbial elec- anode. The transferred electrons move along the external trogenicity is still attractive and can be the most promising circuit to produce an electrical current and reach the cathode source of energy in harsh and resource-limited environ- while the produced protons travel to the cathode through the ments. This is because microorganisms are ubiquitous, ion exchange membrane.[83]

The bacteria-powered biobatteries have the same device configuration and operating principle as the MFCs except for the active feeding system with the inlet and outlet (Figure 2B,C). The biobatteries are working as a primary cell, designed to be discarded once the internally stored organic fuel is depleted. The microorganisms as a biocatalyst can be ideally introduced upon operation or be preloaded in the battery before use. The environmental liquid in river, ocean, or pond water generally consists various microorganisms, some of which have the ability to generate the electric current by transferring electrons across the cell membrane to external electrodes. Ideally, the bacteria- powered battery can be made operable by dropping any liquid that is readily available in local settings. Then, it might be important to find out the types of electroactive bacteria that are present in various types of liquid in nature, and how much power each of these bacteria can generate.[84–86] These studies may uncover distinct electroactive bacterial communities in our environment and aid in the development of various strategies to use the bacteria-powered battery in resource-limited settings.[85,87] However, preloading the biocatalytic microorganisms in the device before use is more preferable because the environmental sample generally does not include enough electroactive bacteria that can operate as a biobattery energy source.[27,88,89] For practical battery use, the environmental sample requires several hours of bacterial culturing and selecting processes to have a desired power. Yet still, liquid samples may not be available in certain circumstances. For example in dry and desert climates, the lack of liquids would prevent the battery from on-site operation.[90] Therefore, the preloading technique to store enough well-cultured electroactive anodophiles as a self-contained device until use will be more realistic and practical for the battery-type MFC platforms. Once the device fabrication is completed, the electroactive bacteria as a biocatalyst is immobilized in the anodic chamber. Then, the device is entirely sealed so that the bacterial cells are confined in the device not to negatively affect our environment while being protected from outside not to be contaminated.[91] The bacterial cells preinoculated in the device can be lyophilized for long-term storage and be readily rehydrated for on-demand power generation.[27,91] With this technique, the biobatteries need to be stored with an optimized condition before being dispensed while the electric bacterial metabolism is held. Freeze-drying, or lyophilization, is widely used for the long-term preservation of bioactive materials. By rapidly freezing the materials and subsequent lowering of the pressure, ice crystals are converted directly from the solid phase to the gas [92] phase. This dehydration ensures minimal shrinkage and gen- Figure 2. A) Schematic representation of the common extracellular elec- erates a completely soluble product that is readily rehydrated. tron transfer (EET) pathways of microorganisms. B) Illustration of the Instead of freeze-drying and dehydration process for on- configuration and operation principles of a microbial fuel cell (MFC). demand power generation, the biobattery can be alternatively C) Illustration of the configuration and operation principles of biobattery. constructed by using a concentrated solid-state anolyte, sustaining the microbial activity and generating the electrical and materials,[97,98] anodic conditions (e.g., overall volume, current for an extended period. A slow release of bacterial nutri- oxygen concentration),[68,88] and device operations (power ents from the synthetic solid anolyte enables slow, efficient, and management circuits).[99,100] continuous mass transfer and significantly contributes to the long-lasting microbial biobattery.[93] Therefore, the solid phase device provides a long-term operational capability while the 3.2. Biobattery Components and Their Requirements freeze-dried technique demonstrates short battery operation. Of note, the longevity of the biobattery can be further controlled by The biobattery consists of four functional components: manipulating type of microorganisms,[94–96] device structures a) anode, b) anodic chamber, c) ion exchange membrane, and

d) air-cathode or solid-state cathode (Figure 2C). The anode is Thermoelectric generators (TEG) were developed to har- critical in providing the overall power generation by allowing vest energy from heat flow between the human body and the the actual accessible area for bacteria to attach and deter- ambient environment.[127] As the constant temperature differ- mining the efficiencies of the bacterial extracellular electron ence provides a reliable source of power, flexible TEG could transfer. Recently, many unconventional 3D microscale anode be integrated into smart textiles or wearable electronic skins materials for MFCs have been explored to increase surface providing unlimited electricity.[128] Also, piezoelectric nano- area,[101,102] bioaffinity,[103,104] porosity,[105,106] conductivity[107,108] generators (PENGs) and triboelectric nanogenerators (TENGs) and biocompatibility,[109,110] and the studies can be applied for gained tremendous attention during the recent decade. These biobatteries. The anodic chamber is to contain the bacterial techniques have been widely developed for applications such organic food for oxidization, determining the operating time of as ambient vibration energy harvester,[129] self-powered wear- power generation. Once the organic food is depleted, the power able biomedical systems,[117] or in vivo energy harvesting generation of the biobattery stops. Therefore, in order to pre- for implantable devices.[130–133] For light energy conversion, cisely control the battery runtime, the total volume of the anodic ultrathin and flexible photovoltaic cells were also created for chamber and initial organic substrate concentration needs to be powering various medical implants[134,135] carefully designed according to the number of bacterial cells While those energy harvesting techniques can be advanta- and their organic concentration tolerance. The ion exchange geous for some specific applications, they are overqualified in membrane physically separates the anode compartment from terms of power rating and device lifespan and too expensive as the cathode, maintaining a potential difference between them. a power source for single-use, disposable applications, which The important roles of the ion exchange membrane are to only require a minimal amount of energy for a short period of i) preserve the electrochemical neutrality in the battery by time. Moreover, these energy harvesting devices are nonbiode- allowing the exchange of ions, ii) minimize oxygen invasion gradable with toxic inorganic materials which can leave adverse from the cathode, and iii) block the media crossover between effects on the environment and public health. The MFC-based the anode and cathode. The cathode is an important factor biobattery has competitive advantages over those conventional limiting the overall biobattery performance.[111,112] Electron power solutions as i) the material and fabrication are cost-effec- acceptors are used at the cathode for the reduction process, as tive, ii) the device structure is much simpler than others and electrons and protons diffuse from the anode to the cathode in easily integrative into other applications, iii) the biobattery is order to maintain charge neutrality. In two-chambered MFC biodegradable, biocompatible, and environmentally friendly, so configurations, potassium ferricyanide, potassium permanga- it can be decomposed by the on-chip bacteria, iv) it is capable nate, or manganese dioxide have often been used as cathodic of harvesting electricity from miscellaneous organic fuels electron acceptors. However, using cathodic chemicals are not including body fluids, sewage sludge, wastewater and any applicable for actual disposable applications in a resource-lim- environmental liquid, and v) the self-regenerating microbial ited setting because their toxicity and cost. The air-cathode or biocatalyst could provide resilient and adaptive power genera- solid-state cathode offers the better promise and sustainability tion with self-repairing and self-adjusting capabilities.[136] for the battery-type MFC platforms.[27] Oxygen is readily acces- Recent microfabrication and microfluidic advances success- sible, sustainable, and environmentally friendly while the solid- fully made small-scale MFCs suitable for portable devices or lab- state cathode, such as a silver oxide/silver or a Prussian Blue on-chip systems.[90,137] The small-scale MFCs inherently provide (PB), is stable under conditions favorable for microbial growth beneficial conditions for high power generation because of a large and provides versatile device architectures.[113,114] surface-to-volume ratio, fast reaction time, short proton traveling distance, and effective mass transport. However, the miniaturized MFCs have not been translated into practical power applications 3.3. Merits and Challenges of Biobatteries because of their energy-intensive operation requiring microfluidic tubes and fluidic manipulation. The external energy for the Currently, primary and secondary batteries are being used as fluidic control is at the tens of mW to several Ws level, which is the main power sources for small single-use devices such as much higher than the power generated from the MFC itself.[38,93] biomedical systems,[115] ingestible biosensors,[116] implantable On the other hand, the biobatteries take advantage of the fab- devices[115] and various wearable electronics.[24,117] Despite the rication techniques for the small MFCs while avoiding those wide applications of these batteries, they will not be practical practical issues. For example, the solid-anolytes (e.g., nutrients power solutions for the future generation of electronics because embedded in an agar gel) that slowly release highly concentrated of the major drawbacks including toxicity, short lifespan, bulky organic substrates could dramatically reduce the anodic chamber size, and high cost.[57,118] Instead, a variety of energy harvesting dimensions while eliminating the power consumption from strategies for powering those small-scale applications have been fluidic pumps.[35,93] Moreover, the immobilization techniques proposed, including, but not limited to, electrochemical, ther- of bacteria or biofilm on the anode (e.g., bacterial encapsula- moelectric, mechanical, and photovoltaic energy harvesters. tion) can empower the precise control over the anodic bacterial For instance, enzymatic fuel cells (EFCs) were integrated community, activity, and stability.[88,138,139] into a tattoo-based biosensor as a power source for epidermal Although the overall biobattery components and their func- monitoring, oxidizing sweat lactate to generate electricity.[119] tions are the same as the MFCs’, however, the development Furthermore, EFCs have been demonstrated as implantable requirements for the components are more difficult to be met power sources in various living organisms such as rabbit,[120] because of the miniaturized size of the biobattery with com- rat,[121,122] cockroaches,[123] snails,[124] clams[125] and lobsters.[126] pactness, and its disposable use. The size of the biobattery is at

Figure 3. A) Schematic illustration of the flexible tube MFC. B) Photoimages of the carbon sleeve electrode being pushed (up) and pulled (down). C) Photoimage of the bending of the flexible tube MFC. D) SEM image of the N-MoO3−x coated carbon fiber bundle. E) SEM images of the close-up views of the highly open structure of the N-MoO3−x nanowire treated under 700 °C. F) Schematic illustration of the fiber-shaped MFC. G) Polarization curve and power density of the fiber-shaped MFC under both flat and bent conditions. H) Power density generated for the fiber-shaped MFC versus time. A–C) Reproduced with permission.[163] Copyright 2014, Wiley-VCH. D–H) Reproduced with permission.[164] Copyright 2016, Wiley-VCH. most in several centimeters for powering portable small-scale to their highly conductive, chemically stable, biologically com- electronic applications, requiring the significant reduction of the patible features having a large surface area.[158–160] Carbon components’ thicknesses and dimensions without scarifying the nanotubes (CNT) and carbon fibers have widely been used as performance. Furthermore, biodegradability or disposability is a an anodic material of the MFC to boost the sluggish bacterial required feature of the biobatteries because of the one-time use. extracellular electron transfer while providing a macroscopic porous scaffold for enhanced biocatalytic loading volume and chemical fluxes.[107,161,162] In a pioneering study, Ieropoulos and 4. Recent Advances in MFC-Based Biobatteries co-workers proposed a flexible tube-shaped MFC with carbon fiber sleeves as electrodes (Figure 3A–C).[163] In their later work, 4.1. Flexible Biobatteries twelve of these MFCs were paired to form a wearable sock for powering an integrated wireless transmitter.[90] This system was Flexible electronics have received intensive attention because of self-sustainable for a day with a bioinspired foot-pump to cir- the demand for intimate human-machine interface,[140,141] geo- culate anolyte (i.e., urine). The MFC was reset with fresh urine metrically compatible military and environmental sensing,[142–144] once a day. Every 2 min, a message of “World’s first wearable and wearable biomedical care.[145–147] To realize the stand-alone MFC” was transmitted to a computer with the device wearer and sustainable functions of these electronics, flexible energy gaiting at a speed of 88 steps min−1. Such a urine activated supplying devices are highly required. Traditional battery-oper- system could be modified to transmit the person’s coordinates ated flexible electronics cannot offer long-standing operation due in emergency situations. Another design for the flexible MFC, to the finite energy budgets available from those batteries.[148,149] demonstrated by Yang and co-workers in 2016, was based on Moreover, the conventional batteries are too heavy, rigid, thick, a carbon fiber anode with modified surface properties.[164] and bulky to be integrated into thin, light-weight, and flexible The environmental benign molybdenum trioxide (MoO3) electronics.[150–152] Even the latest lithium-ion batteries[153–155] and was selected as the modifier because its high work function supercapacitors[156,157] suffered from low energy storage capacity (6.9 eV) and rough surface are favorable for asymmetric super- [57,135] and frequent recharging requirements. All things consid- capacitors and biobatteries. The MoO3 nanowires were grown ered, a flexible, small-scale MFC biobattery has the potential to on the carbon fiber surface via a seed-assisted hydrothermal become a truly useful energy technology because of its renew- method. Then, nitrogen (N) and low-valance-state Mo dual able, sustainable, cost-effective, and eco-friendly capabilities. doping was introduced by thermally reducing the nanowires in ammonia atmosphere under 700 °C, denoted as N-MoO3−x-7. The resulted surface was a conductive, hydrophilic and highly 4.1.1. Carbon-Based Biobatteries open structure, providing multitudinous active sites for electrochemical reactions (Figure 3D,E). The N-MoO3−x-7 fiber was With the dramatic innovation of carbon-based materials, flexible used as an MFC anode. Constructed inside a heat-shrinkable biobatteries have witnessed tremendous advancement owning tube, the fiber-shaped MFC employed Pt-based air-cathode and

Escherichia coli as a biocatalyst (Figure 3F). A maximum power paper reservoir (Whatman #1 filter paper; pore size 10 µm) density of 0.76 µW cm−2 was produced by the MFC under a for holding the anolyte and catholyte for an extended period flat condition, and no noticeable performance degradation was of time, and iii) commercially available Nafion 117 PEM.[198] observed under a mechanically bent condition (Figure 3G). This was the first bacteria-powered battery fabricated on paper With a batch operation mode, the device lasted for up to 50 h material, but the commercial Nafion 117 used as the PEM was and it was able to immediately restore full power generation expensive, and unacceptably increased the total production capacity once the anolyte was replenished (Figure 3H). cost (>$5 per device). Moreover, using Nafion 117 led to low proton conductivity at low humidity levels and significant volumetric size change with increased humidity. To address these 4.1.2. Paper-Based Biobatteries issues, we developed a paper-based PEM by infiltrating sodium polystyrene sulfonate (Figure 4B).[199] Sodium polystyrene sul- Paper, by far the cheapest and most widely used flexible fonate (Na-PSS) is a polyelectrolyte capable of conducting ions. substrate, has renewed the interest in fields of electronics, The water wicked through the Na-PSS embedded paper mem- medical care, and energy.[3,165–167] These natural cellulose fibers brane, allowing efficient proton transfer while minimizing are flexible, porous, lightweight, environmentally friendly, exhib- substrate cross-over between the anode and cathode chamber. iting good mechanical strength, high surface-to-volume ratio Unfortunately, however, because of the permeation issue and unrivaled availability.[168] Basic electronic components and through the PEM, this battery could not provide power high devices, such as diodes,[169] transistors,[170] displays,[171] memo- enough to run other practical devices.[199] ries,[172] fluidic valves[173,174] and mechanical actuators,[175,176] To further improve the performance of paper-based have been realized on paper substrates. In particular, a variety of biobatteries and reduce the cost, we created a simple tech- paper-based systems for real-time monitoring[177,178] and rapid nique for microfabricating the PEM by using a hydrophobic diagnostics[179–181] in healthcare applications were demonstrated wax (Figure 4C).[200] A commercially available wax printer was with great promises. Furthermore, a plurality of techniques has used to easily print the hydrophobic wax-based membrane been introduced to transform or create papers with favorable and heat was applied in controlled manner to get the desir- functionalities including high transparency,[168,182] superior able depths of wax penetration. The melted wax functioned mechanical and thermal properties,[170,183] tunable surface phys- as the membrane separating the anode and cathode while icochemical characteristics,[184–186] and ion-conductivity.[183] allowing protons and cations in the electrolyte to pass through The fabrication processes range from fiber-level approaches efficiently. Incorporating wax-based PEM in paper-based bio- like nanofibrillation to physically or chemically disintegrate the batteries significantly reduced the total material cost to about fiber,[182,187] or regenerate nanofiber from various sources such $0.1, while the Nafion-based MFC cost about $2.5. The power as microbial cellulose[188] or chitin,[189,190] to blending func- performance of the wax-based PEM was comparable to the tionalized materials such as metals,[191] semiconductors,[192] commercial Nafion PEM. insulator,[183] nanoparticles,[193] synthetic polymers,[173,194] and Although we realized more efficient and cost-effective PEM biomolecules[195–197] into the paper substrate. for paper-based biobatteries, several challenges remained, Recently, electroactive bacteria have been merged with including that i) we needed to add potassium ferricyanide as an paper,[27] offering a simple yet powerful energy source for paper- electron acceptor to the device. Although this chemical has the based devices, especially in remote and resource-limited set- advantages of fast cathodic reaction and low overpotential, its tings as these microorganisms can harvest electric power from high cost and toxicity render it inadequate for actual application various organic substrates available in those challenging fields. in a resource-limited setting. On the other hand, oxygen from Furthermore, the paper device can be affordable, equipment ambient air is the most commonly used electron acceptor due free, easy-to-use, deliverable to end users, and easily integrated to its low cost, sustainability, and lack of waste product. For this into structurally simple designs in a cost-effective and eco- reason, devices operated with oxygen hold excellent potential friendly manner. Both the surface roughness and porosity of for practical applications. Moreover, ii) using carbon cloth as an paper can be beneficial to bacterial accommodation and mass anode is not preferable for easy system integrations onto paper. transfer relative to the bio-electricity generation while its hydro- Instead, an entirely paper-based battery would be ideal for philic feature readily absorbs and holds bacterial media without developing on-chip, paper-based disposable biosensors. Finally, additional volumetric chamber or an external fluidic control iii) paper-based biobatteries are limited to a low-output working system. Therefore, a paper-based, MFC-type biobattery offers voltage of about 0.3 V at maximum power delivery. To produce the transformative potential for the use of low-power, simple, higher power output and operating voltages without additional inexpensive, and disposable electronics in resource-limited cost and energy loss from the booster circuits, stacking batteries environments, ultimately realizing a truly stand-alone and self- in series and/or in parallel is essential. Simple electrical con- sustainable device platform that does not rely on a well-estab- nections between single biobattery units cannot be assembled lished power grid or commercial batteries can be developed. into compact and simple paper systems because the biobattery Our group, Bioelectronics and Microsystems Lab, pioneered array requires a large footprint and each unit needs an inlet for paper-based MFC-type biobatteries and initiated the field of inoculation. paper bioenergy. The 1st generation version of our paper- An entirely paper-based battery platform with an air- based biobattery is best illustrated by the schematic dia- breathing cathode resolved the challenges identified in our 1st gram and photo in Figure 4A. The paper battery consisted of generation battery platform and further simplified the battery i) a flexible carbon cloth anode for bacterial attachment, ii) a operation with only a single drop of bacteria-containing liquid.

The paper-based bacteria-powered battery was designed to be the saliva-activated on-demand power generation strategy stackable, and integrative for low-cost, environmentally friendly from lyophilized electroactive bacteria.[91] The biobatteries and practical applications (Figure 4D).[201] The origami tech- were fabricated on a single-layer paper with lyophilized nique also allowed for a series connection of the paper-based Pseudomonas aeruginosa PAO1 in the anode (Figure 4J). batteries to produce the desired power output. When a single Conductive polymer poly(3,4-ethylenedioxythiophene) poly- drop of bacteria-containing liquid was added to the paper-based styrene sulfonate (PEDOT:PSS) was applied to the anodic battery, the liquid spread through 3D microfluidic pathways reservoir forming a 3D biocompatible and highly conduc- within the paper layers via simple capillary action (Figure 4E). tive paper matrix that facilitates bacterial adhesion and With the utilization of an air-cathode on paper, a novel bacteria- electron transfer to the anode.[203] A simple drop of liquid powered battery made entirely of paper substrates was created. (e.g., saliva) to the anode is sufficient to rehydrate the bac- We also created an origami battery that was based on a ninja teria and activate the battery. Maximum power densities of star-shaped design formed by eight serially connected biobat- 1.4 W m−2 and 1.1 W m−2 were obtained from rehydration teries as the modular blades(Figure 4F).[28] Each blade was a liquids of LB medium and artificial saliva with 19.4 mg dL−1 paper-based biobattery with 3D structures (i.e., anode, proton glucose, respectively (Figure 4K). Batteries stored at 22.8 °C exchange membrane, and air-cathode) created from 2D sheets and 45% relative humidity for up to 4 months were still able to through precise folding along predefined creases (Figure 4G). retain more than 30% of the original power output capacity. To The device was retractable, which allowed us to stack the eight further improve the practicality, increase the output power paper-based biobatteries in series, and transformed into a and reduce the cost of biobattery, a “squeeze-biobattery stack” sharp shuriken (closed) to a round frisbee (opened). To operate was developed.[27] As shown in Figure 4L, an easy-to-break liquid the device, a bacteria-containing liquid was added to the inlet pouch along with a paper-based battery stack was sealed inside of the closed battery stack (sharp shuriken), through which a low-density polyethylene (LDPE) cover. Electroactive bacteria, the liquid spread into each biobattery unit. Then, the battery Shewanella oneidensis, was preloaded to the batteries by lyophi- stack was converted into the round frisbee to connect the eight lization, while a simple squeeze by the fingers released the LB biobatteries in series. The series connection method improved medium from the pouch for device activation (Figure 4M). The the power output and the open state of the frisbee exposed all low-overpotential silver oxide solid-state cathode was used to elim- air-cathodes to the air for optimal cathodic reactions. The bat- inate the need for large area air-accessing, consequently allowing tery produced enough power to light up a red LED even with a the compact stacking of seven batteries in air-tight packaging. wastewater sample, which is readily accessible for on-site oper- Maximum power of 88.48 µW was achieved with a single biobat- ations in resource-limited and economically challenged regions tery pack (Figure 4N), and two-battery packs were connected in of the world. series to drive an electrical calculator (Figure 4L, inset). This paper- However, the device requires many paper layers to include based biobattery will provide a practical and accessible solution as all the components, such as the anode, cathode, and PEM, a novel bacterial power source that can empower a self-powered needed to function properly. This demands manual fabrica- paper-based diagnostic test for anyone, anywhere, and anytime. tion of the device, hindering batch production. Furthermore, potential issues such as misalignment of paper layers and vertical discontinuity between layers can ultimately decrease 4.1.3. Textile-Based Biobatteries the power output. In order to eliminate the major challenges, a massive research effort of our group focused on integrating Textile, with its interlacing fibers, offers more superior elasticity all the biobattery components into a single sheet of paper than paper. In general, textiles consist of fibers or yarns that (Figure 4H).[202] A nickel and polypyrrole/carbon black (Ppy/ are knitted, woven, or braided together. The yarns are com- CB) anode, a hydrophobic wax-based PEM, and an activated bined strands of fiber, and the building blocks of the fibers carbon-based air-cathode were all embedded in a single sheet are made up of highly oriented long molecular chains from of paper. In addition, an anodic chamber was introduced to nature (cotton, silk, asbestos, etc.) or man-made (graphene, the paper to act as a hydrophilic reservoir which could hold the polyethylene terephthalate, rayon, etc.) sources.[204] With anolyte including electroactive bacteria (Figure 4I). the forthcoming smart textiles, intensive efforts have been To further explorer the practicality and improve the per- devoted to developing general components such as conduc- formance of the biobattery, our group recently introduced tive circuitry,[205,206] transistors,[207,208] sensors,[209,210] energy

Figure 4. A) Photoimage and schematic illustration of the first generation paper-based biobattery with Nafion PEM. B) Schematic illustration of the paper-based biobattery with Na-PSS treated paper PEM. C) Photoimage and schematic illustration of the paper-based MFC with wax-based PEM. D) Inoculation and folding strategy of the entirely paper-based origami biobattery stack. E) Schematic illustration of the cross section of the battery stack. F) Inoculation and operating principle of the ninja star-shaped origami biobattery stack. G) Schematic diagram of the cross section of the individual battery module. H) Photoimage of the biobattery fabricated into a single sheet of paper. I) Microscopic image and schematic illustration of the single-sheet paper-based biobattery. J) Photoimage and schematic diagram of the saliva-activated paper biobattery with lyophilized exoelectrogens. K) Polarization curves and power density measured from the biobattery with different activation samples. L) Photoimage of the components of the squeeze biobattery stack. (inset: an electric calculator is powered by two battery stacks connected in series). M) Photoimage of the assembled squeeze biobattery stack. N) Polarization curve and output power of the battery pack. A) Reproduced with permission.[198] Copyright 2014, IEEE. B) Reproduced with permission.[199] Copyright 2013, Elsevier. C) Reproduced with permission.[200] Copyright 2018, Elsevier. D,E) Reproduced with permission.[201] Copy- right 2015, Elsevier. F,G) Reproduced with permission.[28] Copyright 2016, Elsevier. H,I) Reproduced with permission.[202] Copyright 2018, Wiley-VCH. J,K) Reproduced with permission.[91] Copyright 2017, Wiley-VCH. L–N) Reproduced with permission.[27] Copyright 2018, Wiley-VCH.

Adv. Mater. Technol. 2019, 1900079 1900079 (9 of 26) © 2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.advancedsciencenews.com www.advmattechnol.de harvesting or storage devices,[211–213] and actuators.[214–216] made. Moreover, with the comparative advantages that include More specific yet integrated systems have been demonstrated, low cost, environmentally benign or biodegradable materials, including long-term electrocardiography for health moni- and wide-range of fuels applicable for electricity generation, a toring,[217] electromyography for sport and fitness training,[218] flexible biobattery can be especially beneficial for single-use or controlled drug delivery for wound healing and health care,[219] disposable applications. artificial muscles for rehabilitation,[220] intelligent textile for military,[142] or smart personal thermal management for energy conservation.[221–223] Compared with paper substrates, textiles 4.2. Biodegradable Biobatteries offer distinct characteristics such as elasticity, hierarchical morphologies, greater mechanical strength, and, most important, Rapid progress in the fields of material science, biology, chem- wearability.[224] The elasticity and good mechanical strength istry, and electrical engineering is ushering in a new class of allow textile-based devices to simultaneously withstand extreme materials and devices that are considered to be transient. This mechanical deformation and provide reliable contact with the new realm requires the devices to have a stable performance body contour. The wearability presents the feasibility for the during the designed lifetime and safely disappear without any integration into clothing, medical equipment, automobiles and discernable remnants afterward. From the functionality perspec- households, and the hierarchical morphologies, from a fabrica- tive, transient devices can be categorized as “implant-and-forget” tion point of view, opens up device design as yarns of different and “deploy-and-forget.” The “implant-and-forget” devices, being functionality could be precisely weaved, embroidered or knitted biocompatible and bioresorbable, have arisen from early biode- into the structured textiles.[225,226] gradable sutures, grafts or bioimaging markers to more active As a preliminary work, our group, for the first time, fabri- and multifunctional temporal devices such as vascular scaf- cated biobatteries with fabrics.[136,227] As shown in Figure 5A, folds with multisensory,[17] self-propelled drug delivery,[229,230] a membrane-less biobattery was integrated into a single fabric in vivo sensors (e.g., electrophysiological signal or intracra- layer with a top-down approach. The carbon-based anodes and nial pressure or temperature),[207,231] or therapeutic implants cathodes were sprayed on opposite sides of the fabric, while the that provide regenerative electrical or thermal stimulus.[232,233] anode side was treated with PEDOT:PSS to promote electron The “deploy-and-forget” sector, on the other hand, are more transfer from bacteria, the Ag/Ag2O redox couple was used involved with eco-friendliness and information security. These as the solid-state cathode (Figure 5B). While a hydrophobic devices and systems are designed to minimize their environ- pattern was precisely engineered on the anode side of the fabric mental effect by using fabrication processes and materials to control the anodic volume, the cathode was tightly placed on with low embodied energy,[234] switching away from nonre- the hydrophilic opposite side to reduce proton travel distance newable or toxic materials (e.g., gallium, indium, or arsenic), (Figure 5C). With Pseudomonas aeruginosa PAO1, a maximum and partially or completely disintegrating after use to reduce power density of 6.4 W m−2 and open circuit voltage (OCV) waste and the possibility of information leakage. With the fast of 0.4 V were reached. To examine the mechanical resiliency, advancing fundamental research on transient conducting,[6,235] the biobatteries were connected to a 10 kΩ load until a stable semiconducting,[19,236,237] and dielectric materials,[238–240] a wide current output was reached. Then, it was stretched to 150% variety of transient devices that use synthesized biocompatible of their original length for 70 times (Figure 5D), followed by a polymer-based organic semiconductors,[19] biodegradable silk 150% stretch and holding for 1 min (Figure 5E), and four 180° fibroin-based resistive memory[20] or other complex compo- longitudinal twists (Figure 5F). Afterward, the current density nents have been characterized in great detail. Thus, an energy recovered to 67% of the original value. In another approach, source for device powering during the operation and the subse- we used the hierarchical morphologies of the textile by weaving quent disintegration triggering is becoming increasingly urgent anodic and cathodic yarns in the weft direction.[228] As shown to fully accomplish the transient technology breakthrough. in Figure 5G,H, three yarns were combined as the anode: a Biodegradable biobatteries have been considered to augment a conductive current collector was sandwiched between two con- wide range of practical applications in transient devices. ductive and hydrophilic active yarns harboring an electricity- In 2015, Ieropoulos and co-workers developed completely generating bacteria Shewanella oneidensis. The cathodic yarn biodegradable MFCs that could use human urine as the fuel with silver oxide electron acceptor was passivated by a micropo- and keep operating for more than six months.[30] In their study, rous polytetrafluoroethylene (PTFE) membrane. A maximum an egg-yolk-based graphite powder mixture with a lanolin diffu- power density of 17 µW cm−3 was produced by this yarn- sion layer was selected as the cathode design rather than a con- stacked biobattery (Figure 5I). ductive synthetic latex (CSL)-based, gelatin-based, or nontoxic At present, the flexible biobatteries are immature compared conductive carbon-based materials because of the mixture’s to the well-commercialized primary batteries, and various superior biodegradability and performance stability. The MFCs aspects await future investigation. Specifically, the output power were constructed on a 3D printed polylactic acid (PLA) frame of flexible biobatteries are limited for more demanding applica- (Figure 6A, left). With a carbon veil anode warped around the tions, more efficient and robust electric connectors and circuit PLA frame (Figure 6A, middle) and a subsequent cover layer routing techniques are needed for the various flexible substrates of natural rubber (Figure 6A, right), the egg-based cathode with unique properties, and the health concerns about the bac- solution was brushed on the rubber, forming the cathode and, terial pathogenicity. Nevertheless various prototype flexible hence, the complete device. Five MFCs were connected in biobatteries have been successfully demonstrated on a plethora parallel as a single stack (Figure 6B). Although, when buried of flexible substrates and significant advancements have been underground, the cathode would be completely degraded after

Figure 5. Schematic illustrations of A) the textile-based biobattery array, batch-fabricated on a single-layer fabric, B) its operating principle, and C) photoimages and schematics of the individual biobattery. Current generated from the textile-based biobattery during D) stretching and relaxing, E) stretching and holding for 1 min, and F) twisting and relaxing for every 5 s. G) Photoimages of the woven yarn-based biobatteries during operation (inset: the magnified view of the four interlaced functional yarns for an individual battery). H) Schematic diagram of the operating principle of the yarn-based biobattery. I) Polarization curve and power density of the single yarn-based biobattery with bacterial inoculum. A–F) Reproduced with permission.[136] Copyright 2017, Wiley-VCH. G–I) Reproduced with permission.[228] Copyright 2018, Hilton Head.

Figure 6. A) Photoimages of a biodegradable MFC in various fabrication stage, left: the 3D printed PLA frame, middle: carbon-veil anode warped over the frame, right: nature rubber cover before brushing on cathode material. B) A single stack with 5 MFCs after the application of cathodes. C) Biodegradation of the egg-based cathode with lanolin layer applied on natural rubber, left: before composting, middle: two months after burial, right: four months after burial. D) Measured voltages of the MFC stacks with or without capacitor bank during charge/discharge test. E) Schematic illustration of the biodegradable paper-polymer battery used for the oxygen-mitigating test. F) Current generated from devices with different oxygen-blocking covers. G) Photoimages of the self-degradation process for PPDD-paper and bare-paper single-layer battery immersed in water. H) SEM images of the degradation process for PPDD-paper and PAA-paper single-layer battery. I) The weight loss of the biobatteries during degradation. A–D) Reproduced with permission.[30] Copyright 2015, Wiley-VCH. F–I) Reproduced with permission.[31] Copyright 2018, Wiley-VCH. four months (Figure 6C), the stacks operated for more than six system with a capacitor bank (0.75 F) for energy storage months with regular urine replenishment. The degradation (Figure 6D). The charge-discharge thresholds were 5 V/8.5 V, appears to accelerate when the fuel feeding was stopped for two and up to 20 J of energy was released during each discharge. weeks during the test. To demonstrate the potential as a power To further miniaturize the device, reduce degradation time, source, the stacks were connected to a power management simplify the operation procedure and test the self-degradation

potential for biobatteries, our group recently developed a paper- major strategies, namely solid-anolyte and cell immobilization polymer green biobattery.[31] Biodegradable polymers poly are being explored to develop the long-lasting biobatteries. (amic) acid (PAA) and poly(pyromellitic dianhydride-p-phe- The use of a solid anolyte, instead of the traditional liquid nylenediamine) (PPDD) were incorporated into the paper to type, allows a lasting and gradual release of nutrients to the improve the device performance and also transiency. Shown in anode. A strong concentration of organics in the anolyte could Figure 6E,F, the use of PAA as the oxygen-blocking layer pro- adversely affect bacterial electricity generation by binding to longed the device operation from 20 min to more than 55 min and blocking the membrane-bound enzymes from electron compared to a Kapton tape layer. Batteries with the PPDD transfer or by facilitating the bacterial cell growth instead of proton exchange membrane generated about 80% of the power electricity generation.[70,249] The initial organic substrate loading from that with Nafion PEM (data not shown) while bearing less and device lifetimes are limited for liquid anolyte MFCs or than 7.7% of the cost (2.2–3.3 µW US$−1 for PAA and PPDD biobatteries. Consequently, solid-anolyte is a straight forward biobattery, and 0.17 µW US$−1 for Nafion ones). After the solution to increase device longevity without the need for anolyte organic substrates in the anolyte were consumed by the inoc- replenishment and human intervention.[93] In 2016, Quaglio ulum Shewanella oneidensis, these on-chip bacteria would assist and co-workers demonstrated an MFC with solid agar anolyte the biodegradation of all the functional parts of the biobattery. (Figure 7A).[93] While a high concentration of sodium acetate, As shown in Figure 6G,H, immersed in water, the PAA and glucose, fructose, peptone, and salts was retained in the agar gel PPDD polymer-paper gradually decomposed over 10 weeks as (Figure 7A inset), the anode was inoculated with enriched bac- the weight loss of the paper was being monitored. The bacteria- teria from seawater in anaerobic conditions. During the 30-day accelerated bioremediation of nickel is shown in Figure 6I, experiment (Figure 7B), the inoculated anode and solid-anolyte demonstrating the advantages of using on-chip bacteria for self- gel was placed in the anodic chamber and immersed in a phos- degradation on biobatteries. phate buffer solution without replenishment or replacement. The combination of biodegradable materials with polymer- The cathodic chamber, however, was filled with potassium fer- based or paper-based platforms exemplifies the versatility of ricyanide in a phosphate buffer solution and replaced two times the biobattery. Although biodegradable biobatteries are in their a week. The MFC was connected to a 1 kΩ load for the first 15 d infancy, compared with other biodegradable energy sources or for stabilization (Figure 7C) with a maximum power density storage devices, biobatteries require less demanding fabrication of 60 mW m−2 observed at day 7 (Figure 7D). For long-term procedures,[241] use less expensive materials,[26] can self-charge operation, the device generated a stable power density around with various organic fuels,[14,242] and have more controllable 45 mW m−2 for an additional 15 d without noticeable degrada- self-degradation with the help of on-board microorganisms.[25] tion of the performance (Figure 7E). The experiment was ter- Researches on the long-term operation, output stability, device minated at day 30; afterward, the remaining energy embedded reliability of the biobattery are in progress. in the solid anolyte was estimated and the author suggested a theoretical device lifetime of 4 months. In another design of the long-lasting biobattery, Tartakovsky 4.3. Long-Lasting Biobatteries and co-workers tested four commonly available biodegradable materials for bacteria electricity generation with a capac- The creation of “smart” objects has attracted considerable itor-based power management circuit for power production interest from academia, industry and the defense sector for maximization.[35] Based on the availability and organic mate- many years.[243] Combined with the advent of the Internet of rial content, humus, sphagnum peat moss, composted cattle Things (IoT), devices capable of autonomous data gathering manure and maple sawdust were compared as potential fuels. (sensing) and transmitting (network connectivity) are per- The substrates were mixed with 10% of sandy loam soil as inoc- vasive today in applications spanning personal health care, ulum source. As shown in Figure 7F, the device employed an air- smart homes, smart cities, smart enterprises, environmental cathode and a self-feeding reservoir was used to provide aqueous monitoring and public services.[244,245] For example, a wrist- environment for the anode. The biobattery was connected to watch with Internet connectivity that provides real-time health a 1 kΩ resistor upon start. The first 50 d experiment showed data for medical care service,[246] or thermally activated remote higher power production from humus MFCs (10.8 mW m−2) forest-fire sensors that could alert the fire service[247] have been and lasting acetate release from sawdust (4.7 mg L−1 at start, put into service. Advanced sensing concepts such as DARPA’s 7.4 mg L−1 by the end). Thus, humus and sawdust were com- Near-Zero Power RF and Sensor Operations (N-ZERO) or bined as the solid anolyte, and further tested for 9 months zero-power self-sustainable wireless sensors were proposed (Figure 7G, inset) with the power management circuit and a 10 to provide persistent monitoring of environmental signals as F capacitor. Three months were needed for off-line statistical radio frequency (RF), chemical presence, acceleration, sounds methods to determine the optimal external resistance value [243,248] or lights are being developed. However, current imple- (Rext) and the boundary of the voltage where the capacitor was mentations are mostly powered by batteries with limited energy charging, Vlow, and discharging, Vhigh. Once those values were budgets, thus, requiring frequent battery replacements or determined, a perturbation-observation algorithm was used charging by human operators, ultimately leading to significant as the Maximum Power Point Tracking (MPPT) method to cost increases for their large-scale deployment.[243] To overcome automatically keep the MFCs operating at the optimal point. those lifetime limitations and achieve true power autonomy, For the first 14 d of autonomous MPPT operation, an average microsized biobatteries are being developed as the power power generation of 3.69 mW m−2 was achieved and the power source for long-lasting, low energy consuming systems. Two output gradually decreased to around 1.9 mW m−2 during the

Figure 7. A) Synthesized agar solid anolyte (inset) with high embedded energy that immersed into buffer solution with the anode. The 30-d test results of B) mean values of open circuit voltage (Voc) and current density (Jsc); C) maximum power density, D) linear sweep voltammetry (LSV) at day 7, and E) power density and voltages measure with varying external loads from day 15 to day 30. F) Schematic diagram of an MFC utilizing solid natural biodegradable material such as humus or manure. G) Power output of the first 95-d operation with different carbon sources and the inset shows the average power generated each month. A–E) Adapted under the terms of CC BY Creative Commons Attribution 4.0 License.[93] Copyright 2016, the authors. F,G) Reproduced with permission.[35] Copyright 2017, Elsevier. following 6 months, while being stable for the first 3 months. conditions (Figure 8A).[138] As shown in Figure 8B, the HBA Although the solid-anolyte MFCs showed satisfying long-term was prepared by creating a porous poly (vinyl alcohol)/carbon autonomous power generation, the power output is hindered black (CB/PVA) hydrogel cast over a CB coated stainless steel by the inefficacious biocatalytic activities, lack of control over mesh (SSM). Then, inoculum from a mature MFC was elec- anodic environment, and low reproducibility. trochemically propagated into the CB/PVA hydrogel, forming Cell immobilization has played an important role in sus- the HBA anode (denoted as HBA-CB/PVA). As shown in tainable and long-term operation of MFCs and biobatteries. Figure 8C–E, the hydrogel was saturated with immobilized Through controlled adsorbing methods such as covalent bacteria. A CB coated SSM anode without hydrogel was also binding, or entrapping of anodophilic bacteria to the anode, an electrochemically biased for anodic biofilm formation and used artificial “biofilm” could be formed with enhanced tolerance to as control (denoted as CB/SSM). The test was conducted under environmental pressures such as toxicity,[88] high salinity,[250] batch-mode with fresh medium, with continuous nitrogen high organic concentration,[88] dissolved oxygen,[138] and com- or oxygen bubbling in the anode chamber for anaerobic or peting bacteria species.[88] The artificial biofilm increases the aerobic conditions. Whereas the switching from anaerobic to device reproducibility and stability by offering more precise aerobic condition reduced the current generation by the con- control of the anode geometry and microorganism composi- trol MFC, the HBA MFC had negligible changes in current tion, and, therefore, makes biobatteries more mass-fabrication amplitude. Interestingly, the organic substrate consumption friendly.[251] Among all the antagonizing factors that affect elec- rate, or feeding frequency, increased for both MFCs under troactive bacteria, diffused oxygen in the anodic environment aerobic condition, indicating more energy was spent by the has long been a pivotal one because of its acute inactivating bacteria for non-electricity-generation activities. Cyclic voltam- effect on the bioelectrocatalytic activity.[68,252] Chen and co- metry (CV) tests showed even higher bioelectrocatalytic activity workers demonstrated an aerotolerant hydrogel bioanode in the HBA under aerobic conditions (Figure 8F). In another (HBA) that generated similar currents in aerobic or anaerobic example, Teng and co-workers immobilized electroactive

Figure 8. A) Current generation comparison of the hydrogel bioanode (HBA) and nontreated anode under aerobic and anaerobic conditions. B) Schematic diagram of the HBA fabrication. C–E) SEM images of the HBA. F) CV curves of HBA in anaerobic and aerobic conditions. G) Electricity generation under different acetate levels of MFCs with (i-MFC) and without (c-MFC) agar gel cell immobilization. H) Power density and polarization curves of i-MFC and c-MFC, numerical suffix represent acetate level in g −L 1. I) Anode bacterial community analysis after high-acetate-level exposure of i-MFC and c-MFC. J) Schematic illustration (up) and photoimage (down) of the microliter-scale biobattery using solid-anolyte and cell immobilization techniques. K) Schematic illustration of the microbiobattery operation principle. L) Voltage measurement of the microbiobattery with an external load over 8 d, inset shows measurement of microbiobattery with liquid anolyte. A–F) Reproduced with permission.[138] Copyright 2016, American Chemical Society. G–I) Reproduced with permission.[88] Copyright 2016, Elsevier. J–L) Reproduced with permission.[253] Copyright 2018, PowerMEMS.

Adv. Mater. Technol. 2019, 1900079 1900079 (15 of 26) © 2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.advancedsciencenews.com www.advmattechnol.de anodophiles by directly immersing matured anodes into agar ecosystem in unprecedented variety, fidelity, and quantity.[116,257] phosphate buffer solution at 40 °C before solidification.[88] From a human body perspective, these medical devices The immobilized anodes were assembled into MFCs with could be categorized as invasive (implantable), semi-invasive air-cathodes (denoted as i-MFC) and mature anodes without (ingestible), and noninvasive (wearable). The semi-invasive agar gel were used in control MFCs (c-MFC). With an acetate modalities are gaining research interest as new biomarkers and substrate initial concentration in anolyte ranging from 1 g L−1 therapeutic targets are being discovered in the gastrointestinal (denoted as i-MFC 1, Figure 8G, top) to 10 g L−1 (denoted as (GI) tract. Ingestible devices could feed new data (e.g., tempera- i-MFC 10, Figure 8G, bottom), and all MFCs operating in batch ture, pH, pressure, gas composition, images) into the biosensor mode with 1 kΩ resistive load, the i-MFCs exhibited superior networks and offer new avenues for therapeutic treatment (e.g., resiliency to high organic substrate concentration than did the drug delivery).[116] For example, although certain intestinal control MFCs. The running time for i-MFCs increased linearly gases from bacterial fermentation have long been correlated from 22 to 220 h with acetate loading of 1–10 g L−1, while the with diseases such as irritable bowel syndrome (IBS),[258] the maximum power density decreased from 680 to 370 mW m−2 current analysis methods often rely on the indirect measuring according to the polarization test (Figure 8H). After 1100 h of breath content which could lead to misdiagnosis.[259,260] In (five cycles) operation with 10 g L−1 acetate, anodic bacteria 2018, Gibson and co-workers demonstrated ingestible capsules community composition was examined with DNA analysis for real-time in vivo sensing and profiling CO2, O2 and H2 gases and classification at phylum and genus levels. From Figure 8I, in the human gut (Figure 9A).[261] The capsules successfully more than 90% of the community in i-MFC was composed by detected GI tract gas variations caused by dietary alterations Proteobacteria, Bacteroidetes, and Synergistetes, while the exem- (Figure 9B). Another ingestible device, developed by Lu and plary electroactive anodophiles Geobacter being 61.8% in i-MFC co-workers, confined biosensing bacteria to the capsule with a and only 39.8% in the control MFC. The Shannon diversity semipermeable membrane for in situ biomolecule detection.[262] index showed lower species diversity in i-MFC (2.45 vs 2.69) Showcased in a swine subject, they successfully detected GI indicating a blocking of competitive bacterium (e.g., fermenta- tract bleeding via heme released from lysed red blood cells. tive bacteria) growth in the anode. These devices, by relaying the invaluable information from the Recently, our group developed a long-lasting microliter-scale under-explored gut to researchers, have immense potential for biobattery by combining the cell immobilization technique with augmenting a wide range of practical biomedical applications. solid-anolyte (Figure 8J).[253] In-situ immobilized pure culture Nevertheless, there exist unaddressed challenges such as device Shewanella oneidensis MR-1 in agar was cast over the carbon retention, device safety and power supply that often require anode, and a second layer of agar-based solid-anolyte was added contradictory solutions. Device retention within the GI tract, as on top of the hydrogel anode for the continuous releasing of the biggest concern[116,263] for ingestible devices, entails smaller nutrients (Figure 8K). With a 20 µL anodic chamber, the solid- dimension and higher flexibility. The power supply, on the state biobattery autonomously produced a stable current over other hand, requires bigger space for the often-rigid batteries to 7 days with a current density of 6 A m−2 at the end of test ensure sufficient operation time. Despite the advancement in (Figure 8L) while the control biobattery with liquid anolyte battery and energy harvesting techniques, a safe and compact ceased operating after 4 h (Figure 8L, inset). power supply that can provide milliwatt scale power for approx- Additionally, other fabrication techniques such as electro- imately 24 h has yet to be developed. Microbial biobatteries spinning or freeze-drying could fabricate an anode with immo- are the most promising candidates because they could directly bilized or preserved electroactive anodophiles. For example, a use the undigested food in the GI tract as fuels, eliminate the nonwoven fabric anode for flexible applications,[251] or a light- need to carry anolyte, and eventually increase the device pay- weight bio-aerogel anode for long-term storage[254,255] has been load while reducing the device size. On the other hand, the proposed. With the help of cell immobilization, an artificial mostly anaerobic gut environment (Figure 9C) hosts a plethora biofilm capable of enduring harsher conditions could grow of anaerobic bacteria species (Figure 9D) among which are onto the anode in a more controllable and repeatable fashion. weak electroactive anodophiles that could generate electricity Moreover, by combining the long-lasting fuel releasing from for the ingestible devices.[84,264] For instance, as one of the most solid-anolyte, the biobattery has immense potential to power abundant commensal microbes in the GI tract, Faecalibacterium the future applications as autonomous sensors. prausnitzii was found to be able to transfer electrons extracellularly by utilizing shuttling compounds such as flavin or ribo- flavin.[265] The homofermentative Lactococcus lactis are capable [266] 5. Future Applications of using redox compound for anodic electron transfer. As a progenitor of gut-bacterial-electricity-harvesting, in 2012, Liu 5.1. Gut Bacterial Power Generation—Let the Bacteria Find You and co-workers presented a proof-of-concept MFC that was powered by simulated colonic content with fresh fecal inoculum Empowered with data science and equipped with multifunc- (Figure 9E).[267] A maximum power density of 11.73 mW m−2 tional electronic devices, the healthcare industry is undergoing was obtained from the MFC. Notwithstanding the fact that a radical transformation where previously unforeseeable med- this MFC was not designed as an ingestible but as implantable ical practice such as wireless online monitoring of vital signs power supply in the colon, the idea to adopt gut microbiome as through wearable sensors patch,[256] or rapid DNA analysis with an energy source was first proven. As the fields of microbiology, a paper-based device[180] are gradually being realized. Modern electronics, material and biomedical science advance, we envi- medical devices are feeding data to the health technology sion that future biobatteries that are flexible and biocompatible

could be integrated into ingestible devices as the power source. Instead of occupying most of the device space, biobatteries will be wrapped around or coated onto the ingestible device, thereby enabling more avenues for biomedical sensing, diagnosing and therapeutic treatment.

5.2. Internet of Disposable Things (IoDT)—Undeniably Forgettable

With the exponential growth of the IoT, in which objects are able to communicate over the Internet without human inter- mediation, the number of Internet-connected devices in 2030 is estimated to be 125 billion, or 14 devices per individual worldwide.[268,269] Among this imposing number of apparatus, emerges a new class of the Internet of Disposable Things (IoDT) devices. Defined by the cost, functionality and environmental concerns, these devices are expected to be flexible, biodegradable, and be easily made with inexpensive materials, which are all in accordance with future flexible biobatteries. For instance, although the price index of electronics will keep decreasing, the wide application of IoT devices often requires putting sensors in single-use objects (e.g., baby diapers or packages) that only cost several dollars where the economics will further restrict the budget of these sensors or circuitry to be barely a penny.[268] Researchers and manufacturers are looking at less expensive materials and less stringent fabrication procedures to bring down the costs. For instance, we can simply print paper-based electronics, instead of using cleanrooms.[165] The simple functions of the IoDT devices, often as sensors or inter- mittent transponders, also require little or infrequent power consumption. At the current stage, paper- and textile-based biobatteries have shown an inexpensive and flexible platform for on-demand power generation, while the solid-anolyte and cell immobilization technique paved the way for stable and autonomous electricity production. Some potential challenges with device integration, power capacity, eco-footprint, and most impor- tantly the cytotoxicity from the bacteria used in the biobattery are being addressed. In 2017, Freitag and co-workers used electrospinning method to embed single species electroactive bacterium, Shewanella oneidensis, into a poly(vinyl alcohol) (PVA) hydrogel fiber matrix (Figure 10A, left) which was sub- sequently coated with poly(pxylylene) (PPX) (Figure 10A, right) as a biocomposite nonwoven MFC anode.[251] The PPX coating prevented the bacterial outgrowth (leakage) from the nonwoven

Figure 9. A) 3D rendering and schematic representations of the human intestinal gas sensing capsule. B) Gas profiles measured by the gas sensing capsule from a volunteer switching from low fiber diet to high fiber diet. C) pH and oxygen profile within the gastrointestinal (GI) tract with the approximate gastric transit time as the horizontal axis. D) Environmental factors distribution alone the intestine, from left to right: major metabolites as aryl hydrocarbon receptor (AHR) and short-chain fatty acids (SCFAs), major bacterial community composition, and estimated bacteria concentration. E) Schematic illustration of the implantable MFC in simulated colonic environment. A,B) Reproduced with permission.[261] Copyright 2018, Springer Nature. C) Reproduced with permission.[116] Copyright 2015, Elsevier. D) Reproduced with permission.[264] Copyright 2014, Springer Nature. E) Reproduced with permission.[267] Copyright 2012, Elsevier.

Figure 10. A) SEM image of the PVA hydrogel biocomposite nonwovens before (left) and after (right) the PPX coating. B) Life/Dead stain of nonwovens before (left) and after (right) 7 d culturing in nutrient medium. C) Illustration of using passive components as event-driven RF sensor. A,B) Reproduced with permission.[251] Copyright 2017, Wiley-VCH. C) Reproduced with permission.[248] Copyright 2016, IEEE. electrode, while allowing nutrient exchange between the we believe, the accelerating maturation of the biobattery tech- hydrogel and the aqueous surrounding environment. As shown nologies, combined with the on-going progress of electronics, in Figure 10B, the metabolic activity in the nonwoven electrode will enable versatile new avenues for powering the future increased after 7-day culturing in a nutrient medium (right) IoDT devices. compared to that directly after the spin-coating (left). Although the biocomposite produced a humble maximum power density of 2.5 mW m−2 and bacteria outgrowth was observed in sites 5.3. Hybrid Energy Harvesting—Get the Best of “Two” Worlds where the PPX coating had cracked because of peeling and/or cutting during fabrication, this inspiring method can be further Accompanying the fruition of energy harvesting techniques is improved by adding a conductive polymer to the PVA hydrogel the growing trend of integrating complementary techniques or using more pliable coating materials, ultimately creating for more adaptive and continuous energy conversion.[270] For a flexible, highly reproducible, and fabrication-friendly non- example, Wang and co-workers integrated polymer fiber solar woven anode for biobatteries. Furthermore, the power require- cells and fiber-based triboelectric nanogenerators into a smart ment of the future sensors will keep reducing thanks to the textile for simultaneous harvesting ambient light and mechan- advancing electronic technologies. As demonstrated by Gordon ical energy.[271] Lennon and co-workers fabricated an anodic and co-workers, many low-power passive components such as amorphous molybdenum oxide (a-MoOx) pseudocapacitive micro-electro-mechanical systems (MEMS) transformers, fil- electrode on the backside of the aluminum current collector of ters, and switches for signal amplification, rectification and an industrially produced crystalline silicon (c-Si) photovoltaic threshold detection[248] can be used. Moreover, it is possible to panel, creating an energy harvesting-storage solar cell with on- generate a trigger signal upon certain wake-up events while the board output smoothing capability.[272] Similar trends were also rest of the circuit is in a quiescent state (Figure 10C). Therefore, observed with bio-electrochemical energy harvesting. As one

Figure 11. A) Conceptual illustration of synergistic interaction between photosynthetic and heterotrophic bacteria in the hybrid biosolar cell. B) Current density measured from the hybrid biosolar cell. C) Current density measured from the control solar cell with only photosynthetic bacteria. D) Conceptual illustration of the site-specific binding of microorganism to electrode surface. E) Power density of MFCs with electrodes bound to E. coli surface displayed ADHII on sites a) V66, b) P182, c) D314, d) nonspecifical binding location, and e) purified ADHII nonspecifically attached to electrode, f) E. coli with surface displayed ADHII but not attached to the electrode, (g) wild type E. coli. F) Power density of an MFC with anode attached to E. coli on ADHII sites V66 measured at the end of day: a) 1, b) 2, c) 4, d) 6, and e) 7. A–C) Reproduced with permission.[273] Copyright 2017, Elsevier. D–F) Reproduced with permission.[281] Copyright 2013, American Chemical Society.

of our recent works, heterotrophic and photosynthetic bacteria the inactivated catalyst by the living microorganisms.[280] In were integrated in the anode chamber to create a solar-driven 2012, Alfonta and co-workers investigated the longevity and self-sustaining MFC for continuous bioelectricity generation site-specific attachment of a bacteria-enzyme biohybrid in (Figure 11A).[273] The syntrophic interactions between hetero- MFCs.[281] Living Escherichia coli with surface-displayed alcohol trophic anodophiles and phototrophs, namely, in situ organic dehydrogenase II (ADHII) were covalently linked to gold elec- substrates regeneration by the photosynthetic Synechocystis trode with defined enzyme orientation (Figure 11D). Three for the heterotrophic Shewanella oneidensis, and the carbon enzyme sites (V66, P182, D314) were individually incorporated dioxide production by heterotrophs for phototrophs, created a with unnatural amino acid (UAA) para-azido-L-phenylalanine self-supporting reciprocal cycle. The co-culture MFC generated (Az-Phe) to conjugate the enzyme to the gold electrode (via 70 times more current than that of a device with only photo- copper (I) catalyzed azide-alkyne cycloaddition). While the V66 trophs (Figure 11B,C). While the symbioses provide a way to and P182 sites in close proximity to the catalytic center, the integrate solar energy harvesting with bioelectricity generation, distant D314 was chosen as negative control site. As shown in another prominent development is to integrate enzymes with Figure 11E, maximum power density of 13.5 and 12.6 µW cm−2 microorganisms such that the enzymes can be self-regenerated were obtained from electrodes conjugated by V66 and P182 by the microbial metabolisms, ultimately creating a highly effi- locations, the control electrode (D314) exhibited low power den- cient and long-lasting bioelectrochemical hybrid system.[274,275] sity similar to that of electrode with nonspecifically attached While the EFCs are limited by the relatively short life-time of enzyme (WT ADHII). An MFC inoculated with E. coli wired to the catalyst and anisotropic electron transport between the the electrode by the V66 site was operated over a week, whereas catalytic center and the electrode,[276,277] the MFCs, on the other the power density increased to 45 µW cm−2 at the end of 7th hand, are hindered by the low volumetric catalytic activities day due to the increased bacteria population and secreted redox due to the complex cell structure[278] and slow mass transfer rate active molecules (Figure 11F). impeded by the cell membrane.[279] One solution to overcome From the device perspective, one noteworthy progress is these drawbacks is using genetically engineered microorgan- the integration of bio-electrocatalytic and charge-storage fea- isms that display the designed enzymes on the cell surface, tures. One approach is to increase the double-layer capaci- creating a biohybrid that could circumvent the cell membrane tance of the anode in the MFC. For instance, high specific transfer-related hindrance while allowing the renewing of area materials as activated carbon or carbon-nanotubes were

Adv. Mater. Technol. 2019, 1900079 1900079 (19 of 26) © 2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.advancedsciencenews.com www.advmattechnol.de coated over the conventional brush anode to increase the of electrode configuration on charge transfer/storage perfor- double-layer capacitance with reduced anodic charge transfer mance, Atanassov and co-workers constructed MFCs with dif- resistance.[282] Flexible supercapacitive film electrodes were ferent anodic and cathodic dimensions (Figure 12A).[284] Three also fabricated by depositing nanostructured carbon (NS-c) anode configurations with 1, 2, and 3 brushes (with projected onto Mylar polymer films.[283] To further determine the effect surface areas of 9, 18, and 27 cm2, denoted as 1 BR, 2 BR,

Figure 12. A) Photoimage of the supercapacitive MFC. B) Power output measured from supercapacitive MFCs with different anode configuration. C) Power output measured from supercapacitive MFCs with different cathode configuration. D) Schematic illustration of the electron transfer from cytochromes to the anode under different operating conditions with hypothetically anode potential limitations. E) Output voltage measurement under transient and steady-state operating mode from MFCs with the same configuration. F) Schematic illustration of the electron transfer pathway in an MFC with polyhydroquinone (PHQ) modified anode. G) CV curves measured from graphite felt (GF), acid-cleaned graphite felt (AGF), PHQ-modified graphite felt (PHQ-GF), and PHQ-modified acid-cleaned graphite felt (PHQ-AGF) anodes. H) Faradaic peak currents over scan rate extracted from CVs of the PHQ-AGF anodes. I) Nyquist plots of the inoculated anode with different polymer modifications. J) Polarization curve and power density of MFCs with different anode polymer modifications. A–C) Adapted under the terms of CC BY Creative Commons Attribution 4.0 License.[284] Copyright 2016, the authors. D, E) Reproduced with permission.[290] Copyright 2017, Elsevier. F–J) Adapted under the terms of CC BY Creative Commons Attribution 4.0 License.[292] Copyright 2017, the authors.

and 3 BR) and three air-cathodes areas of 2.54 cm2 (single felt (GF) without acid washing were used as control. CV curves cathode), 3.67 cm2 (two cathodes, one of 2.54 cm2 and one of showed substantial capacitance increase with the character- 1.13 cm2), and 5.09 cm2 (two cathodes of 2.54 cm2) were used istic pseudocapacitance reversible redox peaks of the polymer for comparison. When the same cathode area (5.09 cm2) was coated electrodes (PHQ-GF, PHQ-AGF) compared with the used with different number of anode brushes (1, 2, and 3), the untreated ones (GF, AGF) (Figure 12G). A further investiga- anodic and cell capacitance (derived from the measured voltage tion into the linear dependency of the Faradaic peak currents profiles) varied from 50 mF, to 121 mF, 194 mF and 30 mF, on scan rate confirmed the surface-immobilized redox couple to 50 mF, 63 mF respectively. While the internal resistance of as the source of the pseudocapacitive charging and discharging the MFC varied from 30.5 Ω to 29.5 Ω and 26.8 Ω. The com- (Figure 12H). Electrochemical impedance spectra (EIS) curves bined effect on output power density is shown in Figure 12B. of inoculated anodes revealed much smaller charge transfer Similarly, when the same number of anode brushes (1 BR) was resistance on the PHQ treated anodes, while no significant used with different cathode areas, the resulted cathode and change was observed for ohmic resistance (Figure 12I). As can cell capacitances were 51.2 mF, 61.5 mF, 73.2 mF and 24 mF, be expected, MFCs used the pseudocapacitive anodes with their 26.5 mF, 30 mF, respectively. While the effects of cathode EET promoting polymer interface exhibited enhanced anodic geometry on cell capacitance was less distinct, the internal performance and, hence, power output (Figure 12J). resistance decreased from 58.6 Ω to 38.1 Ω and 30.5 Ω with enlarged cathode areas, leading to a substantial increase in power density (Figure 12C). As implied by these experimental 6. Conclusions data, the balance between anodic and cathodic geometries is critical for the whole cell performance. While the increase of Here, we provided a summary of the progress toward devel- anodic capacitance can improve the power output, a cathode oping single-use disposable biobatteries derived from the MFC. with comparable area and performance to reduce the cathode Although early promise has been realized, the electroactive loss and the MFC internal resistance is of equal importance. microbes have not yet substantially met the expectations of Another method to create supercapacitive MFCs uses a micro- revolutionizing renewable energy generation. While the MFC bial Faraday process to enhance the pseudocapacitive effect on technology is impeded by the low power density, nonlinear electrodes, either by operating the MFC in transient-state regu- output power increases with device scaling up, and great lation (TSR) mode to engage the extracytoplasmic cytochromes operation and maintenance costs in large-scale operation, the as the pseudocapacitive molecules or by introducing artificial realization of a small, autonomous, and disposable battery-type pseudocapacitive materials such as manganese dioxide (MnO2). MFC for low-power-consuming applications is a novel, yet rea- Although it has long been observed that periodically connecting sonable approach. Distinguished by the remission of reagent and disconnecting the MFC to an external load (a.k.a. transient- replenishment, the biobattery is a self-contained system with state regulation mode, TSR or supercapacitive mode) would preloaded biocatalyst and fuels. Nevertheless, it is important to enhance the average power generation,[285] various studies underline that a biobattery shares the same fundamental opera- showed that extracytoplasmic cytochromes could act as pseudo- tion principles with an MFC, thus should be considered as a capacitive material by storing electrons when external electron subsite of the broader MFC family. acceptors are not available (e.g., open circuit).[286–289] The exact Many pioneering works were highlighted as the answers to mechanism behind these microbial Faraday processes and the the question, “Then, should it be a science fiction to translate the optimum practice to maximize power generation demand fur- MFC technology to practical real-world applications?” For instance, ther investigation.[290,291] On one hand, as suggested by Huang since low-power applications such as wearable sensors or smart and co-workers, the varying anode potential during TSR mode packages for IoTs dictate flexibility, flexible biobatteries were might allow different cytochromes or redox species to transfer developed for these applications. Carbon-based materials such as electrons to the anode (Figure 12D, right), while a constant carbon fiber and carbon nanotubes have been widely used as flex- anode potential during continuous mode would only har- ible anodes with high specific surface area, conductivity, chem- vest limited electrons from certain cytochromes (Figure 12D, ical stability, biocompatibility, and versatile surface-modifiability. left).[290] As part of their study, transient operation conditions Novel cable-type or fiber-type designs were presented with small such as switching frequency, duty cycle, and external load were device footprints, high flexibility, and impressive power output. first optimized. Then, the outputs were compared between Nevertheless, their high fabrication cost remains challenging MFCs under optimized TSR mode and steady-state mode. for disposable uses. The paper-based biobatteries provide an During a single batch period, the MFCs operated in TSR mode inexpensive and compact platform for green bioelectricity consistently outperformed steady-state mode ones and gener- generation. When combined with preloaded lyophilized bacteria, ated an average 15.7% higher current and 32.7% greater power paper-based biobatteries can be stored for on-site and on-demand during the entire 11 h test (Figure 12E). On the other hand, activation. However, the inelastic paper substrate undermines electro-active species with fast redox reactions were applied their usage in applications that entail constant bending, twisting to the anode to enhance this pseudocapacitance effect. As or stretching. Textile biobatteries present added advantages of demonstrated by Feng and co-workers, a solid redox-active enhanced mechanical strength, fabrication versatility and wear- polyhydroquinone (PHQ) film was coated over an acid-washed ability that allows easy integration with other wearable electronic graphite felt (AGF) anode, bridging between the biofilm and applications. Among these batteries, yarn-based biobatteries are the electrode by the fast redox transformation between polyhy- particularly promising as they can be easily woven or knitted droquinone and polybenzoquinone (Figure 12F).[292] Graphite into smart fabric and textiles. Recently developed biodegradable

Adv. Mater. Technol. 2019, 1900079 1900079 (21 of 26) © 2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.advancedsciencenews.com www.advmattechnol.de biobatteries open up new avenues for energizing transient elec- medical devices, biobatteries can be a promising choice of tronics. The on-board inoculum offers distinct advantages for power sources. However, there exist unaddressed needs to controlled self-disintegration owing to its ability to accelerate increase output power density, improve device reproducibility biodegradation after the anodic nutrient consumption. The main for large-scale fabrication, segregate inoculum from users, pro- drawbacks for biodegradable biobatteries are the low power long the battery storage and operation time, and further reduce density and long biodegradation time. Two major approaches device cost. While these challenges are nontrivial, based on to design biobatteries for long-lasting, low-energy consuming existing results, we are optimistic that biobatteries will be trans- systems were discussed. On one hand, the self-sufficing solid- ferred to practical real-world applications as a game-changing anolyte allows a gradual and lasting release of highly concen- technology. trated nutrients that would other wisely be detrimental to the biocatalytic activities and bio-electricity generation. On the other hand, cell immobilization techniques provide controllable and Acknowledgements reproducible fabrication of artificial biofilms with remarkable This work was supported by the Office of Naval Research (#N00014- tolerance to stresses such as toxins, dissolved oxygen, high con- 81-1-2422), the National Science Foundation (ECCS #1703394 & IOS centrations of salt and nutrients, and rival microorganism, which #1543944), Integrated Electronics Engineering Center (IEEC), and the ultimately prolongs the battery longevity. Combining these two SUNY Binghamton Research Foundation (SE-TAE). parallel research paths, the long-lasting biobatteries are expected to be an enduring microsized power source facilitating future sensor networks with true power autonomy. Conflict of Interest Further progress in this field will rely on the foundations of the abovementioned works, yet, new focal points are being dis- The authors declare no conflict of interest. covered as our understanding expands. The human GI tract, as the host of an increasing number of biomarker and therapeutic targets, harbors abundant weak electricigens in its mostly Keywords anaerobic environment. By using the gut bacteria as a biocat- biobatteries, electric bacteria, microbial fuel cells, on-demand power alyst and undigested food as fuels for electricity generation, generation, single-use applications small form-factor biobatteries are anticipated to continuously power devices such as ingestible sensors or smart drug delivery Received: January 23, 2019 pills. While early promises had been realized by the founda- Revised: February 18, 2019 tional works, it is our outlook that the next generation biobat- Published online: teries will benefit from the integration of current technology advances. For example, as in case of smart packages or tracking labels for disposable IoTs, future biodegradable biobatteries [1] M. Urdea, L. A. Penny, S. S. Olmsted, M. Y. Giovanni, P. 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