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Electricigens in the Anode of Microbial Fuel Cells: Pure Cultures Versus Mixed Communities

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Electricigens in the Anode of Microbial Fuel Cells: Pure Cultures Versus Mixed Communities Cao et al. Microb Cell Fact (2019) 18:39 https://doi.org/10.1186/s12934-019-1087-z Microbial Cell Factories REVIEW Open Access Electricigens in the anode of microbial fuel cells: pure cultures versus mixed communities Yujin Cao1* , Hui Mu2, Wei Liu1, Rubing Zhang1, Jing Guo1, Mo Xian1* and Huizhou Liu1* Abstract Microbial fuel cell (MFC) is an environmentally friendly technology for electricity harvesting from a variety of sub- strates. Microorganisms used as catalysts in the anodic chamber, which are termed as electricigens, play a major role in the operation of MFCs. This review provides an introduction to the currently identifed electricigens on their taxonomical groups and electricity producing abilities. The mechanism of electron transfer from electricigens to elec- trode is highlighted. The performances of pure culture and mixed communities are compared particularly. It has been proved that the electricity generation capacity and the ability to adapt to the complex environment of MFC systems constructed by pure microbial cultures are less than the systems constructed by miscellaneous consortia. However, pure cultures are useful to clarify the electron transfer mechanism at the microbiological level and further reduce the complexity of mixed communities. Future research trends of electricigens in MFCs should be focused on screening, domestication, modifcation and optimization of multi-strains to improve their electrochemical activities. Although the MFC techniques have been greatly advanced during the past few years, the present state of this technology still requires to be combined with other processes for cost reduction. Keywords: Microbial fuel cell, Electricigens, Pure cultures, Mixed communities Introduction intense study for about 50 years [3]. MFCs are similar Te world’s limited supply of fossil fuels and the impact to any other battery or fuel cell, consisting of two elec- of fossil fuels on climate change require us to develop trodes, an anode and a cathode, which are separated by alternative energy sources. Among the next generation the electrolytes. Te diference is that they use organic energy sources, microbial fuel cell (MFC) is attracting compounds as substrates to generate electricity. On the wide attention due to its intended use to recover energy anode, microorganisms oxidize organic compounds to in the form of electricity. MFCs are fuel cells that convert release electrons and protons. Te electrons produced chemical or solar energy to electrical energy using micro- during oxidation fow to the cathode through external organisms as the catalysts [1]. Unlike other fuel cells, electric circuit to produce current. In the cathode, elec- MFCs do not use precious metal catalysts at the anode tron acceptors react with electrons and protons to pro- [2]. Terefore, MFC technology represents a new and duce reduced compounds. Te reduction of oxygen is the promising approach to generate power in an inexpensive most common cathodic reaction. way. Microorganisms that oxidize organic compounds and Te concept of electric current generation by microor- transfer electrons to the anodes of MFCs are called elec- ganisms has been conceived for more than 100 years and tricigens. Te term ‘electricigen’ is coined to make a clear MFC devices for electricity production have been under distinction in the mechanisms of power generation in MFCs. Electricity generated by electricigens is quite dif- ferent from other microorganisms. In an MFC system, *Correspondence: [email protected]; [email protected]; [email protected] the electricigen used in the anodic chamber is one of the 1 CAS Key Laboratory of Biobased Materials, Qingdao Institute core factors afecting electricity generation performance. of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Here, we summarize recent development and advances Qingdao 266101, China Full list of author information is available at the end of the article of the electricigens in the anode. Te electron transfer © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cao et al. Microb Cell Fact (2019) 18:39 Page 2 of 14 mechanism from the electricigens to the anode is dis- membrane bound cytochromes and allow electricigens cussed in detail. Te performances of pure cultures and to use an electrode which is not in direct cell contact as mixed communities are compared particularly. Future the electron acceptor. Electron transport proteins play an directions of electricigens in MFCs are also proposed. important role in direct electron transfer as they transfer electrons from the cytoplasm to the outer membrane and Mechanisms for electron transfer fnally to the anode. Direct electron transfer is the frst from electricigens to electrodes choice for efcient current generation in MFCs. Te lim- Electron transfer from the respiration chain of electri- itation of direct electron transfer is that the active sites cigens to the electrode is crucial for MFC technology in of electron transport proteins are typically buried within harvesting bioenergy. Te process of electron transfer by the proteins, which results in poor electron transfer rate microorganisms is not a natural phenomenon. Although [5]. Up to now, only several species of electrochemically the mechanism is as yet not completely elucidated, mul- active bacteria such as Shewanella and Geobacter have tiple pathways for the electron transfer from electrici- been identifed to form bacterial nanowires that transfer gens to electrodes have been proposed. Generally, these electrons away from the cell [6, 7]. mechanisms can be divided into two types: direct elec- For indirect electron transfer, electron transfer is tron transfer (direct contact between the cell surface and achieved with the help of low molecule, soluble media- the electrode) and indirect electron transfer (through the tors (Fig. 2) that eliminate the requirement for direct so-called electron mediators) (Fig. 1). contact between the cell and electron acceptor. Te elec- For direct electron transfer, electrons should reach the tron mediators could enter the bacteria cells, extract the outer membrane of the cell and physical contact between electrons from the metabolic reactions of the electrici- the outer membrane and the anode is required. Electrici- gens and supply these electrons to the anode of an MFC gens form bioflms or electrically conductive nanowires [8]. At frst, the presence of electron mediators was con- (pili and fagella) on the anode surface [4]. Electron trans- sidered to be essential for MFC operation [9]. Tey can fer takes place through the outer membrane cytochrome be produced by the electricigens or externally added to and nanowires or trans-membrane electron trans- the anodic chamber. Many species have been identi- port proteins by direct contact without any difusional fed to synthesize self-mediators such as phenazine [10, electron mediators. Te nanowires are connected to 11], pyocyanin [12], and so on. Te potential diference between the mediators and the redox proteins would sig- nifcantly afect the efciency of electron transfer [13]. A number of chemical compounds like anthracenedione, thionine [14], neutral red [15], humic acid [16], ribofa- vin [17] and methylene blue [18] have been investigated to improve the efciency of electron transfer. However, the addition of exogenous mediators is not preferable as they always lead to relatively low current densities as well as being expensive and toxic to the microorganisms, thus causing decline of the performance during long time periods, which makes the technique difcult to com- mercialize. Moreover, the regular addition of exogenous mediators is technologically unfeasible and environmen- tally questionable. Hence, if the microorganism can be efciently used as a catalyst without adding exogenous mediators, it is feasible from a technical point of view that there is no need to gradually add electron mediators as well as being environmentally safe. Pure cultured microorganisms as electricigens in the anode Fig. 1 Proposed electron transfer mechanisms from electricigens As the biocatalyst of MFCs, electricigens are indispen- to the anode. Electrons from electricigens fow to the anode directly sable. Up to now, hundreds of electricigens have been through nanowires or indirectly through an electron mediator. isolated and used in MFCs. Most of these electricigens Medred, reduced electron mediator; Medox, oxidized electron mediator belong to Proteobacteria and Firmicutes. Recent stud- ies showed that the electricigens in MFCs had a diverse Cao et al. Microb Cell Fact (2019) 18:39 Page 3 of 14 Fig. 2 Self-mediators produced by electricigens and exogenous mediators used for indirect electron transfer in MFCs tendency. Microorganisms that have the characteristics density was further improved for both of the archaea and to generate electricity are still waiting to be discovered. In this power output was much higher than Escherichia coli order to further understand the diversity and
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