The Use of Electroactive Halophilic Bacteria for Improvements and Advancements in Environmental High Saline Biosensing
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biosensors Perspective The Use of Electroactive Halophilic Bacteria for Improvements and Advancements in Environmental High Saline Biosensing Erin M. Gaffney , Olja Simoska and Shelley D. Minteer * Department of Chemistry, University of Utah, Salt Lake City, UT 84112, USA; [email protected] (E.M.G.); [email protected] (O.S.) * Correspondence: [email protected] Abstract: Halophilic bacteria are remarkable organisms that have evolved strategies to survive in high saline concentrations. These bacteria offer many advances for microbial-based biotechnologies and are commonly used for industrial processes such as compatible solute synthesis, biofuel production, and other microbial processes that occur in high saline environments. Using halophilic bacteria in electrochemical systems offers enhanced stability and applications in extreme environments where common electroactive microorganisms would not survive. Incorporating halophilic bacteria into microbial fuel cells has become of particular interest for renewable energy generation and self- powered biosensing since many wastewaters can contain fluctuating and high saline concentrations. In this perspective, we highlight the evolutionary mechanisms of halophilic microorganisms, review their application in microbial electrochemical sensing, and offer future perspectives and directions in using halophilic electroactive microorganisms for high saline biosensing. Keywords: halophilic bacteria; microbial biosensing; microbial electrochemistry Citation: Gaffney, E.M.; Simoska, O.; 1. Introduction Minteer, S.D. The Use of Electroactive Bioelectrochemical systems have become of great interest to the electrochemistry Halophilic Bacteria for Improvements community for exploring avenues of renewable energy generation, biosensing systems, and Advancements in Environmental and bioelectrosynthesis [1–3]. Specifically, microbial electrochemical systems are fit for long- High Saline Biosensing. Biosensors term environmental deployment suitable for wastewater management and monitoring 2021 11 , , 48. https://doi.org/ applications [4–6]. Among the many types of microbial electrochemical systems, the 10.3390/bios11020048 technology used most often for biosensing is the microbial fuel cell since the substrate of the bacterial cells is commonly the driver of the current output. Therefore, the current output Received: 20 January 2021 can be related to the substrate concentration in a variety of wastewaters providing a self- Accepted: 9 February 2021 Published: 12 February 2021 powered sensor [7–10]. The long-term stability stems from the ability of microorganisms to continually reproduce, allowing for a near-infinite bioelectrode where the biocatalysts are Publisher’s Note: MDPI stays neutral being regenerated [11]. The main challenge is identifying microbes capable of extracellular with regard to jurisdictional claims in electron transfer (EET), which allows for interfacing bacterial cells with an electrode surface published maps and institutional affil- capable of producing an electrochemical response (e.g., current) [12–15]. Such bacterial iations. strains can be found by harvesting in environments ripe for the evolution of bacterial strains with EET. These types of environments include areas with a lack of soluble terminal electron acceptors such as oxygen or inorganic salts. These environments create a need for the ability to solubilize insoluble electron donors outside of the cell, such as iron or sulfur oxides and inorganic metals, among other electron donor compounds [12,13]. Pairing Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. the phenomena of EET to an electrode, generalized in Figure1, involves utilizing the This article is an open access article metabolic reaction of a biological substrate to a product with electron transfer steps to distributed under the terms and an electroactive molecule which is either on the cellular surface or can diffuse across the conditions of the Creative Commons cell membrane. The terminal electron transfer step determines the potential of the anode Attribution (CC BY) license (https:// (Eanode in Figure1), and the energetics of the reaction of the substrate to the product creativecommons.org/licenses/by/ determines the potential of the metabolic reaction (EP/S in Figure1), which creates the 4.0/). inherent overpotential (Figure1) in microbial systems. This overpotential will vary in Biosensors 2021, 11, 48. https://doi.org/10.3390/bios11020048 https://www.mdpi.com/journal/biosensors Biosensors 2021, 11, x FOR PEER REVIEW 5 of 5 Biosensors 2021, 11, 48 2 of 13 the inherent overpotential (Figure 1) in microbial systems. This overpotential will vary in the electroactive species used in the microbial electrochemical system and the electron transferthe electroactive mechanisms species at play, used which in the can microbial be extremely electrochemical complicated system [16]. and Many the electron approaches aretransfer focused mechanisms on studying at play,these which phenomena, can be extremely including complicated bioinformatics [16]. Many and approaches computational modelingare focused [17,18]. on studying these phenomena, including bioinformatics and computational modeling [17,18]. Figure 1. Pairing the microbial metabolism to an electrode surface (here, anode). Made with FigureBioRender.com. 1. Pairing the As microbial bacterial cells metabolism catalyze anto intracellularan electrode redox surface reaction, (here, generically anode). Made represented with Bio- Render.com.as substrate As to bacterial product, cells electrons catalyze flow an to intrac an eventualellular terminalredox reaction, electron ge acceptornerically such represented as redox- as substrateactive proteinto product, on the electrons cell surface flow or to a an biomolecule eventual terminal (Xox going electron to Xred )acceptor which is such then re-oxidizedas redox-active at the electrode surface. Therefore, the potential of the anode (E ) will be determined by the protein on the cell surface or a biomolecule (Xox going to Xred) whichanode is then re-oxidized at the elec- η trodeelectrochemical surface. Therefore, potential the of thepotential terminal of electronthe anode transfer (Eanode reaction) will be (EXox/Xred determined). The by overpotential the electrochemi- ( ) cal potentialwill be determined of the terminal by the differenceelectron transfer between reaction the electrochemical (EXox/Xred). The potential overpotential of the metabolic (η) will redox be deter- minedreaction by the initiating difference electron between transfer the (E P/Selectrochemi) and the electrochemicalcal potential potentialof the metabolic of the reaction redox occurring reaction initiatingat the anodeelectron surface. transfer (EP/S) and the electrochemical potential of the reaction occurring at the anode surface. Many bacterial strains have been characterized and isolated for EET, with a few model organisms that have been intensely studied, including Geobacter sulfurreducens and ShewanellaMany bacterial oneidensis strains[19–22]. have Even withbeen the characterized advances of characterizing and isolated many for strains EET, capablewith a few modelof this organisms feat, few organisms that have have been been intensely identified studied, which areincluding extremophilic Geobacter and havesulfurreducens the ability and Shewanellato perform oneidensis EET [23 ].[19–22]. Such organisms Even with are the of greatadvances interest of forcharacterizing environmental many applications strains capa- ble ofof microbialthis feat, few electrochemical organisms systemshave been due identified to the creation which of are robust extremophilic bioanodes and capable have the abilityof survival to perform and performanceEET [23]. Such in aorganisms dynamic rangeare of of great environments interest for [23 environmental,24]. Specifically, appli- cationschemical of microbial environments electrochemical of high saline aresystems of interest due for to thethe development creation of ofrobust water bioanodes treatment ca- pableand of biosensing survival forand contaminants, performance since in a thesedyna watersmic range account of environments for 5% of the total [23,24]. world’s Specifi- liquids and result from a variety of industrial processes [25]. This perspective will discuss cally, chemical environments of high saline are of interest for the development of water the phenomena of halotolerance and the environments which are of particular interest treatmentin incorporating and biosensing halotolerant for contaminants, bacteria in microbial since these electrochemical waters account biosensors. for 5% Futureof the total world’sdirections liquids and and opportunities result from offered a variety by the of studyindustrial will also processes be discussed, [25]. This mainly perspective focusing will discusson the the applications phenomena and of engineering halotolerance of electroactive and the environments halophilic bacterial which driven are microbial of particular interestelectrochemical in incorporating biosensors. halotolerant bacteria in microbial electrochemical biosensors. Fu- ture directions and opportunities offered by the study will also be discussed, mainly fo- cusing on the applications and engineering of electroactive halophilic bacterial driven mi- crobial electrochemical biosensors. Biosensors 2021, 11, x FOR PEER REVIEW 5 of 5 Biosensors 2021, 11, 48 3 of 13 2. Electrifying Halophilic Bacteria Halotolerant strains2. Electrifying are extremely Halophilic