Cable bacteria as electronic biological materials: Towards use in biodegradable electronics

Abstract

In modern times, electrical devices have become ingrained with our society. These devices form a major role in communication, leisure and even survival. However, as these devices break and get replaced by newer versions, over 50 million tonnes of electronic waste that is not recycled is generated yearly. Whilst in the long run this will undoubtedly have ecological consequences, in developing countries this already forms a threat to the health of adults and children, even before birth. As the global demand for electronics seems to be ever increasing, it is evident that biodegradable alternatives need to be found. Approximately a decade ago, at the coast of Denmark, long filamentous bacteria were discovered that were found to conduct electricity over centimetre scale distances. The research in this thesis aims to gain more insight into the conductive properties of these bacteria and study the potential of these bacteria to be used as alternatives to the non-biodegradable wires in electronic circuits. The basics of electron transport are well-known for crystalline materials and can be used to create electronic devices, and various models exist for non-crystalline materials (chapter 1.1). Meanwhile, whilst properties such as structure, metabolism and respiration have commonalities in various bacteria (chapter 1.2), some break the mould by bringing electrons out of the cell for their respiration (chapter 1.3). Cable bacteria go one step further by forming chains of tens of thousands of cells that work together to survive (chapter 1.4). These chains transport electrons through wires that are interconnected between the cells. This way, these bacteria thrive in the sediment by stretching out between sulphide in the bottom layers and oxygen at the top. In order to gain more insight into the charge transport properties of cable bacteria, various techniques were employed in this thesis (chapter 2). Through direct conductivity measurements it was found that various electrodes can be used in order to attach the bacteria in a circuit. However, the conductivity of these bacteria decreases under exposure to ambient air and light. Meanwhile, fluorescence microscopy revealed autofluorescence in these bacteria. Nanoscale electronic measurements are used to gain more insights into the connecting structures between the fibres of the bacteria. Finally, using mass spectrometry on different strains of cable bacteria, it was found that nickel and sulphur are common elements in the conductive fibres of these bacteria. How do cable bacteria compare to other biodegradable alternatives for electronics that have been found so far? This search has already found various materials with interesting properties by looking at nature (chapter 3). These materials can be used in the device as either the conductive structure, the substrate or as an encapsulating layer to change the lifetime of the devices. In the world of electromicrobiology, electroactive bacteria such as Geobacter and Shewanella, which produce conductive nanowires, form interesting candidates. Through the study of the proteins and genetic modification, the conductivity of these nanowires can be improved, though the conduction lengths are limited to the micrometre range. Meanwhile, cable bacteria already have conductivities comparable to the previously found biodegradable electronics, with conduction lengths in the range of centimetres. These results may improve even further as more research is done on these bacteria. However, hurdles such as the isolation of the conductive fibres need to be passed before these bacteria can be used in electronics. In order to study the signal transmission properties in cable bacteria, the response to periodic signals was analysed. On the one hand, sinewaves were used for impedance spectroscopy. A new model that considers the microscopic structure of the conductive pathways was proposed that gave a better match to the experimental data than the previous model. On the other hand, square waves were sent through the bacteria in order to simulate a digital signal. Even with the simplified model, the theoretical predictions could be fitted to the experimental data. Based on this data it was concluded that cable bacteria could transmit sinewave and square wave electrical signals in the investigated frequency range up to 500 kHz. This was demonstrated by sending an analog music signal through a cable bacteria filament. From the results obtained in this thesis, it is clear that cable bacteria can be considered as electrical interconnects allowing the transmission of electrical signals in a broad frequency range and therefore have the intrinsic potential to be used as biological electronic components in biohybrid electronics, biodegradable electronics, and other future e-biologics applications. The high conductivity values and good connections cable bacteria form with various electrodes makes it easy to integrate these bacteria in a circuit. However, once integrated, care should be taken to prevent exposure to ambient air or light as these degrade the conductivity of the bacteria. Since these bacteria are capable of transmitting information, maybe one day cable bacteria or other electroactive bacteria could be used to transmit the message that global e-waste is decreasing.