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The Microorganism  SEQ CHAPTER \h \r 1Acidithiobacillus ferrooxidans Can Use Electrical Current as a Direct and Sole Energy Source


Dimitre G. Karamanev


Department of Chemical and Biochemical Engineering, Western University,
London, Ontario N6G 5B9, Canada
Phone: +1 (519) 661 2111, ext. 88230; Fax: +1 (519) 661 3498; e-mail: dkaraman@uwo.ca

Abstract
	It is well known that there are two main groups of living organisms in terms of their energy source: chemotrophs and phototrophs. Recently it has been shown that some living organisms, and in particular, microorganisms, could use electrical current as both a sole energy source and as an electron donor. This, third group of organisms, was named electrotrophs. The experimental results reported here show for the first time that the aerobic microorganism Acidothiobacillus ferrooxidans, can grow in an electrotrophic mode. 

Keywords: Electrotrophy, Acidithiobacillus ferrooxidans, electrical current, electrodes.

Introduction
	All known living organisms such as animals, plants and microorganisms, require energy for their life. The energy is usually supplied by redox reactions, in which an electron acceptor is reduced by consuming electrons, while an electron donor is oxidized, releasing electrons. The process of transfer of electrons, downhill the energy curve, from the electron donor to the electron acceptor, releases energy which is used by the living organisms. The electron donors release electrons due to the energy of either chemical reaction or a photochemical one. Therefore, from the point of view of the nature of the electron donor reaction, all known living organisms are classified into two groups:
chemotrophs. These organisms use either organic or inorganic substances as electron donors, and use their chemical energy as energy source. Humans and animals are typical examples of chemoorganotrophs; some microorganisms such as Acidithiobacillus ferrooxidans are typical chemolithotrophs;
phototrophs. This type of organisms use photochemical reactions as a source of electrons, and their ultimate energy source is light. Typical examples are algae.
	The bacterium A. ferrooxidans has been discovered more than 60 years ago in acid mine drainage ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1126/science.106.2751.253","ISSN":"0036-8075","PMID":"17777068","author":[{"dropping-particle":"","family":"Colmer","given":"A. R.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Hinkle","given":"M. E.","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Science","id":"ITEM-1","issue":"2751","issued":{"date-parts":[["1947","9","19"]]},"page":"253-256","title":"The Role of Microorganisms in Acid Mine Drainage: A Preliminary Report","type":"article-journal","volume":"106"},"uris":["http://www.mendeley.com/documents/?uuid=43a2faf2-c9e6-3e19-9a4b-c7defce6cbdb"]}],"mendeley":{"formattedCitation":"[1]","plainTextFormattedCitation":"[1]","previouslyFormattedCitation":"[1]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[1]. As mentioned above, it is a typical chemolithotroph, obtaining energy from the oxidation of different inorganic electron donors such as sulfides, sulfur, sulfites and ferrous ions ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"author":[{"dropping-particle":"","family":"Nemati","given":"M.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Harrison","given":"S. T L","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Hansford","given":"G. S.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Webb","given":"C.","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biochemical Engineering Journal","id":"ITEM-1","issue":"3","issued":{"date-parts":[["1998"]]},"page":"171-190","publisher":"Elsevier Inc.","title":"Biological oxidation of ferrous sulphate by Thiobacillus ferrooxidans: A review on the kinetic aspects","type":"article-journal","volume":"1"},"uris":["http://www.mendeley.com/documents/?uuid=5c36b1c7-7472-344e-b701-5cc915beb898"]}],"mendeley":{"formattedCitation":"[2]","plainTextFormattedCitation":"[2]","previouslyFormattedCitation":"[2]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[2]ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISSN":"0734-9750","PMID":"14538087","abstract":"Microorganisms are important in metal recovery from ores, particularly sulfide ores. Copper, zinc, gold, etc. can be recovered from sulfide ores by microbial leaching. Mineral solubilization is achieved both by 'direct (contact) leaching' by bacteria and by 'indirect leaching' by ferric iron (Fe(3+)) that is regenerated from ferrous iron (Fe(2+)) by bacterial oxidation. Thiobacillus ferrooxidans is the most studied organism in microbial leaching, but other iron- or sulfide/sulfur-oxidizing bacteria as well as archaea are potential microbial agents for metal leaching at high temperature or low pH environment. Oxidation of iron or sulfur can be selectively controlled leading to solubilization of desired metals leaving undesired metals (e.g., Fe) behind. Microbial contribution is obvious even in electrochemistry of galvanic interactions between minerals.","author":[{"dropping-particle":"","family":"Suzuki","given":"I","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biotechnology advances","id":"ITEM-1","issue":"2","issued":{"date-parts":[["2001","4","1"]]},"page":"119-32","title":"Microbial leaching of metals from sulfide minerals.","type":"article-journal","volume":"19"},"uris":["http://www.mendeley.com/documents/?uuid=582a603e-f669-33a8-b099-8bd8d0151a8c"]}],"mendeley":{"formattedCitation":"[3]","plainTextFormattedCitation":"[3]","previouslyFormattedCitation":"[3]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[3]ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1038/308538a0","ISSN":"0028-0836","abstract":"Isotope composition of sulphate in acid mine drainage as measure of bacterial oxidation","author":[{"dropping-particle":"","family":"Taylor","given":"Bruce E.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Wheeler","given":"Mark C.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Nordstrom","given":"Darrel Kirk","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Nature","id":"ITEM-1","issue":"5959","issued":{"date-parts":[["1984","4","5"]]},"page":"538-541","publisher":"Nature Publishing Group","title":"Isotope composition of sulphate in acid mine drainage as measure of bacterial oxidation","type":"article-journal","volume":"308"},"uris":["http://www.mendeley.com/documents/?uuid=318ee0be-9517-355c-ba4a-a37374e7c50b"]}],"mendeley":{"formattedCitation":"[4]","plainTextFormattedCitation":"[4]","previouslyFormattedCitation":"[4]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[4]. In the latter case, the overall energy-supplying reaction is as follows:
Fe2+  +  �O2  + H+ =  Fe3+  + �H2O	(1)
where the ferrous ions are the electron donor, and oxygen is the electron acceptor. Reaction (1) is actually the sum of two half-reactions separated in space: the oxidation of the electron donor:
Fe2+ =  Fe3+  +  e-	(2)
takes place outside of the cell membrane (Figure 1a), while the reduction of the electron acceptor:
�O2  +  H+  +  e-  =  �H2O	(3)
is carried out in the cytoplasmic membrane (Figure 1a). The electrons are transported from the electron donor, through the periplasm, to the electron acceptor via a chain of several redox proteins (Figure 1a). While the exact mechanism of the electron transport in A. ferrooxiadans has not been completely characterized yet, a general scheme was originally proposed by Ingledew ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISSN":"0006-3002","PMID":"6295474","author":[{"dropping-particle":"","family":"Ingledew","given":"W J","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biochimica et biophysica acta","id":"ITEM-1","issue":"2","issued":{"date-parts":[["1982","11","30"]]},"page":"89-117","title":"Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph.","type":"article-journal","volume":"683"},"uris":["http://www.mendeley.com/documents/?uuid=5e520b84-cac8-3501-bbde-7656fbd5d5cc"]}],"mendeley":{"formattedCitation":"[5]","plainTextFormattedCitation":"[5]","previouslyFormattedCitation":"[5]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[5], and later updated by several other authors. Appia-Ayme et al. ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISSN":"0099-2240","PMID":"10543786","abstract":"Despite the importance of Thiobacillus ferrooxidans in bioremediation and bioleaching, little is known about the genes encoding electron transfer proteins implicated in its energetic metabolism. This paper reports the sequences of the four cox genes encoding the subunits of an aa(3)-type cytochrome c oxidase. These genes are in a locus containing four other genes: cyc2, which encodes a high-molecular-weight cytochrome c; cyc1, which encodes a c(4)-type cytochrome (c(552)); open reading frame 1, which encodes a putative periplasmic protein of unknown function; and rus, which encodes rusticyanin. The results of Northern and reverse transcription-PCR analyses indicated that these eight genes are cotranscribed. Two transcriptional start sites were identified for this operon. Upstream from each of the start sites was a sigma70-type promoter recognized in Escherichia coli. While transcription in sulfur-grown T. ferrooxidans cells was detected from the two promoters, transcription in ferrous-iron-grown T. ferrooxidans cells was detected only from the downstream promoter. The cotranscription of seven genes encoding redox proteins suggests that all these proteins are involved in the same electron transfer chain; a model taking into account the biochemistry and the genetic data is discussed.","author":[{"dropping-particle":"","family":"Appia-Ayme","given":"C","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Guiliani","given":"N","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Ratouchniak","given":"J","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Bonnefoy","given":"V","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Applied and environmental microbiology","id":"ITEM-1","issue":"11","issued":{"date-parts":[["1999","11"]]},"page":"4781-7","title":"Characterization of an operon encoding two c-type cytochromes, an aa(3)-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020.","type":"article-journal","volume":"65"},"uris":["http://www.mendeley.com/documents/?uuid=d6d5bf77-808f-376c-a1d4-ffed4b2eee32"]}],"mendeley":{"formattedCitation":"[6]","plainTextFormattedCitation":"[6]","previouslyFormattedCitation":"[6]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[6] proposed the electron transfer pathway showed in Figure 1a. The outer-membrane c-type cytochrome, Cyc2, acquires electrons from ferrous iron oxidation (reaction 2) and transfers them through the chain of other cytochromes and rusticianin to the oxygen reduction site. Regardless of the specific mechanism proposed, it has been established that ferrous iron oxidation takes place outside of the microbial cell ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISSN":"0021-9193","PMID":"11741873","abstract":"A high-molecular-weight c-type cytochrome, Cyc2, and a putative 22-kDa c-type cytochrome were detected in the membrane fraction released during spheroplast formation from Acidithiobacillus ferrooxidans. This fraction was enriched in outer membrane components and devoid of cytoplasmic membrane markers. The genetics, as well as the subcellular localization of Cyc2 at the outer membrane level, therefore make it a prime candidate for the initial electron acceptor in the respiratory pathway between ferrous iron and oxygen.","author":[{"dropping-particle":"","family":"Yarz�bal","given":"Andr�s","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Brasseur","given":"Ga�l","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Ratouchniak","given":"Jeanine","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Lund","given":"Karen","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Lemesle-Meunier","given":"Danielle","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"DeMoss","given":"John A","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Bonnefoy","given":"Violaine","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Journal of bacteriology","id":"ITEM-1","issue":"1","issued":{"date-parts":[["2002","1"]]},"page":"313-7","title":"The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein.","type":"article-journal","volume":"184"},"uris":["http://www.mendeley.com/documents/?uuid=f4cea2dc-31f4-3323-9cea-85526b3ddffe"]}],"mendeley":{"formattedCitation":"[7]","plainTextFormattedCitation":"[7]","previouslyFormattedCitation":"[7]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[7], since the outer-membrane cytochrome is exposed to the external environment (Figure 1a). In addition, it has been shown that the cell-free isolate of A. ferrooxidans cytochromes has an electron affinity in the absence of iron ions ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISSN":"0006-3002","PMID":"6295474","author":[{"dropping-particle":"","family":"Ingledew","given":"W J","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biochimica et biophysica acta","id":"ITEM-1","issue":"2","issued":{"date-parts":[["1982","11","30"]]},"page":"89-117","title":"Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph.","type":"article-journal","volume":"683"},"uris":["http://www.mendeley.com/documents/?uuid=5e520b84-cac8-3501-bbde-7656fbd5d5cc"]}],"mendeley":{"formattedCitation":"[5]","plainTextFormattedCitation":"[5]","previouslyFormattedCitation":"[5]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[5].
	A. ferrooxidans obtains carbon for cell growth from the fixation of carbon dioxide. The energy for carbon dioxide fixation comes from reaction (1). 
	Several researchers studied the coupled electrochemical reduction of Fe3+ with the biological oxidation of Fe2+ ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISSN":"0006-3592","PMID":"10417221","abstract":"In this study, we demonstrated that the period of logarithmic growth for Thiobacillus ferrooxidans could be extended when optimal conditions for cell growth were maintained using potential controlled electrochemical cultivation with sufficient aeration. The optimal pH and Fe(II) concentration for the electrolytic cultivation were determined to be 2.0 and 150 mM, respectively. When the potential was set to 0.0V vs Ag/AgCl, the Pt electrode reduced Fe(III) to Fe(II) with an efficiency of 95%. A porous glass microbubble generator was used to maintain adequate levels of dissolved oxygen, which was the electron acceptor for T. ferrooxidans when the cell density in the medium was high. Under these conditions, cells at an initial density of 10(7) cells/mL grew logarithmically for 4days until the cell density was 4 x 10(9) cells/mL. This corresponded to a period of logarithmic growth that was 3 times longer than was observed in batch cultures without electrolysis. In addition, the final cell density reached 10(10) cells/mL after 6 days of electrochemical cultivation, which was a 50-fold increase over conventional batch culture. Under conditions of increasing cell density, potentiostatic electrolysis made it possible to remove Fe(III), which causes product inhibition, at an increasing rate and to correspondingly increase the production rate of Fe(II), which is the electron donor for T. ferrooxidans. Thus, our cultivation system provides a sufficient supply of electron donor and acceptor for T. ferrooxidans, thereby elongating the period of logarithmic growth and producing very high cell densities.","author":[{"dropping-particle":"","family":"Matsumoto","given":"N","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Nakasono","given":"S","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Ohmura","given":"N","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Saiki","given":"H","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biotechnology and bioengineering","id":"ITEM-1","issue":"6","issued":{"date-parts":[["1999","9","20"]]},"page":"716-21","title":"Extension of logarithmic growth of Thiobacillus ferrooxidans by potential controlled electrochemical reduction of Fe(III).","type":"article-journal","volume":"64"},"uris":["http://www.mendeley.com/documents/?uuid=d3ff4eed-931a-3af6-a3a9-1a95604fff31"]}],"mendeley":{"formattedCitation":"[8]","plainTextFormattedCitation":"[8]","previouslyFormattedCitation":"[8]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[8] in order to regenerate the substrate for the A. ferrooxidans growth (Fe2+) electrochemically. The electrochemical reaction taking place on the surface of the cathode is the reduction of ferric ions:
Fe3+   +  e-  =  Fe2+	(4)
while in the liquid surrounding the cathode, free suspended cells of A. ferrooxidans oxidize the ferrous ions (Reaction 2), which actually is the reversal of the cathode reaction. Thus, electrical energy has been used for the regeneration of microbial substrate (Fe2+) according to Reaction 4, and therefore, the electricity was used indirectly as an energy source for microbial metabolism and growth. However, these microorganisms used directly a chemical electron donor (ferrous ions) for obtaining energy. While this mode of indirect use of electrical current was referred to as �electrotrophy� ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISBN":"9784431785415","abstract":"Bacteria change the surface of the Earth. All kinds of bacteria reside in the biosphere, and although sometimes they may cause damage, they also help in cleaning the surface of the Earth and in the circulation of various substances. Chemolithoautotrophic bacteria in particular have a unique and intimate relationship with inorganic substances and human beings. This book covers in detail advances in the biochemistry and physiology of several chemolithoautotrophic bacteria as well as their relationship to certain environments. Included are recent findings regarding the oxidation mechanisms of amm. General Considerations; Cytochromes; Nitrogen Circulation on Earth and Bacteria; Sulfur Circulation on Earth and Bacteria; Oxidation and Reduction of Iron by Bacteria; Carbon Circulation on Earth and Microorganisms; Organisms Evolutionarily Closest to the Origin of Life.","author":[{"dropping-particle":"","family":"Yamanaka","given":"Tateo.","non-dropping-particle":"","parse-names":false,"suffix":""}],"id":"ITEM-1","issued":{"date-parts":[["2008"]]},"number-of-pages":"157","publisher":"Springer","title":"Chemolithoautotrophic bacteria : biochemistry and environmental biology","type":"book"},"uris":["http://www.mendeley.com/documents/?uuid=6d698f2f-3c87-3385-a70c-0d21053d8d53"]}],"mendeley":{"formattedCitation":"[9]","plainTextFormattedCitation":"[9]","previouslyFormattedCitation":"[9]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[9], the microorganisms used ferrous iron (not electricity) as a direct electron donor. 
	For the first time the use of electrical current as a direct and sole energy source for living organisms (and more specifically, aerobic microorganisms) was reported a decade ago ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"author":[{"dropping-particle":"","family":"D","given":"Karamanev","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Provisional US Patent","id":"ITEM-1","issued":{"date-parts":[["2003"]]},"title":"Production of Microbial Biomass using Electrical Current","type":"article-journal"},"uris":["http://www.mendeley.com/documents/?uuid=f46c0dba-9adb-4139-97f5-30c4175abf62"]}],"mendeley":{"formattedCitation":"[10]","plainTextFormattedCitation":"[10]","previouslyFormattedCitation":"[10]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[10]ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"author":[{"dropping-particle":"","family":"Karamanev","given":"D","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"World Congress of Industrial Biotechnology","id":"ITEM-1","issued":{"date-parts":[["2006"]]},"title":"Electrotrophs - Microorganisms that Transform Chemical Energy into Electricity","type":"article-journal"},"uris":["http://www.mendeley.com/documents/?uuid=20cad90c-8df6-4aab-8dda-36f88991ceab"]}],"mendeley":{"formattedCitation":"[11]","plainTextFormattedCitation":"[11]","previouslyFormattedCitation":"[11]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[11]. The term �electrotrophy�, and alternatively, �electronotrophy� was proposed in these works to describe the process. Gregory et al. ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1111/j.1462-2920.2004.00593.x","ISSN":"1462-2912","PMID":"15142248","abstract":"It has been demonstrated previously that Geobacter species can transfer electrons directly to electrodes. In order to determine whether electrodes could serve as electron donors for microbial respiration, enrichment cultures were established from a sediment inoculum with a potentiostat-poised graphite electrode as the sole electron donor and nitrate as the electron acceptor. Nitrate was reduced to nitrite with the consumption of electrical current. The stoichiometry of electron and nitrate consumption and nitrite accumulation were consistent with the electrode serving as the sole electron donor for nitrate reduction. Analysis of 16 rRNA gene sequences demonstrated that the electrodes supplied with current were specifically enriched in microorganisms with sequences most closely related to the sequences of known Geobacter species. A pure culture of Geobacter metallireducens was shown to reduce nitrate to nitrite with the electrode as the sole electron donor with the expected stoichiometry of electron consumption. Cells attached to the electrode appeared to be responsible for the nitrate reduction. Attached cells of Geobacter sulfurreducens reduced fumarate to succinate with the electrode as an electron donor. These results demonstrate for the first time that electrodes may serve as a direct electron donor for anaerobic respiration. This finding has implications for the harvesting of electricity from anaerobic sediments and the bioremediation of oxidized contaminants.","author":[{"dropping-particle":"","family":"Gregory","given":"Kelvin B.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Bond","given":"Daniel R.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Lovley","given":"Derek R.","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Environmental Microbiology","id":"ITEM-1","issue":"6","issued":{"date-parts":[["2004","6"]]},"page":"596-604","title":"Graphite electrodes as electron donors for anaerobic respiration","type":"article-journal","volume":"6"},"uris":["http://www.mendeley.com/documents/?uuid=d1e9b1d7-ce8e-335f-9869-a6e2aa6ee0ee"]}],"mendeley":{"formattedCitation":"[12]","plainTextFormattedCitation":"[12]","previouslyFormattedCitation":"[12]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[12] showed �for the first time that electrodes may serve as a direct electron donor for anaerobic respiration�. Later, other anaerobic microorganisms were reported to grow in electrotrophic mode ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1111/j.1758-2229.2010.00211.x","ISSN":"17582229","PMID":"23761228","abstract":"The discovery of electrotrophs, microorganisms that can directly accept electrons from electrodes for the reduction of terminal electron acceptors, has spurred the investigation of a wide range of potential applications. To date, only a handful of pure cultures have been shown to be capable of electrotrophy, but this process has also been inferred in many studies with undefined consortia. Potential electron acceptors include: carbon dioxide, nitrate, metals, chlorinated compounds, organic acids, protons and oxygen. Direct electron transfer from electrodes to cells has many advantages over indirect electrical stimulation of microbial metabolism via electron shuttles or hydrogen production. Supplying electrons with electrodes for the bioremediation of chlorinated compounds, nitrate or toxic metals may be preferable to adding organic electron donors or hydrogen to the subsurface or bioreactors. The most transformative application of electrotrophy may be microbial electrosynthesis in which carbon dioxide and water are converted to multi-carbon organic compounds that are released extracellularly. Coupling photovoltaic technology with microbial electrosynthesis represents a novel photosynthesis strategy that avoids many of the drawbacks of biomass-based strategies for the production of transportation fuels and other organic chemicals. The mechanisms for direct electron transfer from electrodes to microorganisms warrant further investigation in order to optimize envisioned applications.","author":[{"dropping-particle":"","family":"Lovley","given":"Derek R.","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Environmental Microbiology Reports","id":"ITEM-1","issue":"1","issued":{"date-parts":[["2011","2"]]},"page":"27-35","title":"Powering microbes with electricity: direct electron transfer from electrodes to microbes","type":"article-journal","volume":"3"},"uris":["http://www.mendeley.com/documents/?uuid=b8ae5806-dac4-310c-8580-183e56f346cd"]}],"mendeley":{"formattedCitation":"[13]","plainTextFormattedCitation":"[13]","previouslyFormattedCitation":"[13]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[13].
	Since the electron generation reaction by the electron donor in A. ferrooxidans (2) is carried out at the outer cell surface, and since the redox proteins responsible for ferrous iron oxidation have electron affinity even in the absence of iron, the main question behind this work was: is it possible to supply the outer membrane redox proteins of the microbial cell with electrons from an electrode (replacing Reaction 2), which physically contacts the microorganism, according to Figure 1b? In order to answer this question, an electrobiochemical experimental setup was designed (Figure 2).

Materials and Methods
	The experimental setup used in this work is shown in Figure 2. Its main part was an electrobiochemical cell, in which microbial cells of A. ferrooxidans were immobilized on the surface of the cathode. The cell had a cylindrical shape. The cathodic compartment was 2.7 cm in diameter and 2 cm deep, while the anodic compartment was 2.7 cm in diameter and 7 mm deep. The cathode was made of carbon felt, containing 0.5 g SiO2 powder, used to improve the immobilization of A. ferrooxidans cells. The current collector was a graphite rod, so that microorganisms and the catholyte contacted only carbon as an electrically-conductive material. The cathode potential was measured by using a reference Ag/AgCl electrode, submerged in the catholyte, and was controlled, when required, by varying the voltage of the power supply (Figure 2). 
	The catholyte, which contained the microbial nutrients, was an aqueous solution of 9K salts of Silverman and Lundgren ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISSN":"0021-9193","PMID":"13654231","author":[{"dropping-particle":"","family":"Silverman","given":"M P","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Lundgren","given":"D G","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Journal of bacteriology","id":"ITEM-1","issue":"5","issued":{"date-parts":[["1959","5"]]},"page":"642-7","title":"Studies on the chemoautotrophic iron bacterium Ferrobacillus ferrooxidans. I. An improved medium and a harvesting procedure for securing high cell yields.","type":"article-journal","volume":"77"},"uris":["http://www.mendeley.com/documents/?uuid=43816851-35c3-3132-b261-7bcb9a97f64f"]}],"mendeley":{"formattedCitation":"[14]","plainTextFormattedCitation":"[14]","previouslyFormattedCitation":"[14]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[14]. During the electrotrophic experiments, the liquid phase surrounding the microbial cells contained no chemical or photochemical electron donors. Therefore, the cathode itself was the only source of electrons to microorganisms, delivered by electrical current. The electron acceptor for the microbial cells was molecular oxygen, dissolved in the liquid; it was reduced according to reaction (3). The anode material was platinum wire, and the anolyte was 0.2 M aqueous solution of sulfuric acid. The cathodic space was separated from the anodic one by means of Nafion proton-exchange membrane (DuPont, USA). The microbial culture of A. ferrooxidans, JCM3863, was obtained from the Japan Collection of Microorganisms.

Results and Discussion
	The microbial culture was initially grown in a shake flask in an aqueous solution, containing 9 g/L Fe2+ in the form of sulfate, as well as a nutrient salts composition, according to the 9K medium. The pH of the medium was 2.2, obtained by adding sulphuric acid. Once 99% of ferrous iron was oxidized, liquid was pumped from the shake flask into the cathode space of the electrobiochemical cell and returned back to the shake flask by means of continuously operating peristaltic pump (Figure 2). At this stage, the flask was aerated by air bubbling instead of shaking. The cathode potential was kept at 640 mV (versus standard hydrogen electrode) by varying the voltage of the external power source. All potentials reported in this work are given versus a standard hydrogen electrode. The initial value of the electrical current flowing through the cell was 103 mA, which was slowly decreasing until a steady-state condition, characterized by the equality between the rate of electrochemical reduction of ferric ions and biological oxidation of ferrous ions, was reached. The steady-state current was 45 mA. The microbial growth on the cathode surface was encouraged by the fact that the concentration of substrate (Fe2+) in the vicinity of the cathode surface was higher than anywhere else in the recirculation system, due to the electrochemical reduction of Fe3+ (reaction 4) on the cathode. The iron ions, present in the system, did not allow to study the possibility for electrotrophic growth of A. ferrooxidans, because iron acted as an intermediate electron carrier between the cathode and microbial cells. Therefore, our next goal was to remove the iron ions from the system in order to check the possibility of growing A. ferrooxidans directly on electrical current. Once a stable electrical current of 45 mA was obtained, the catholyte, containing iron ions, was replaced with a 9K solution, containing no iron ions. The system contained some residual iron in the form of both soluble and insoluble compounds. The latter was represented by jarosite ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1016/J.MINENG.2005.10.024","ISSN":"0892-6875","abstract":"Jarosite precipitation is a very important phenomenon that is observed in many bacterial cultures. In many applications involving Acidithiobacillus ferrooxidans, like coal desulphurization and bioleaching, it is crucial to minimize jarosite formation in order to increase efficiency. The formation of jarosite during the oxidation of ferrous iron by free suspended cells of A. ferrooxidans was studied. The process was studied as a function of time, pH and temperature. The main parameter affecting the jarosite formation was pH. Several experiments yielded results showing oxidation rates as high as 0.181�0.194g/Lh, with low jarosite precipitation of 0.0125�0.0209g at conditions of pH 1.6�1.7 with an operating temperature of 35�C.","author":[{"dropping-particle":"","family":"Daoud","given":"J.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Karamanev","given":"D.","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Minerals Engineering","id":"ITEM-1","issue":"9","issued":{"date-parts":[["2006","7","1"]]},"page":"960-967","publisher":"Pergamon","title":"Formation of jarosite during Fe2+ oxidation by Acidithiobacillus ferrooxidans","type":"article-journal","volume":"19"},"uris":["http://www.mendeley.com/documents/?uuid=9865c58f-4bda-30c9-8d26-2f14aa74eb1b"]}],"mendeley":{"formattedCitation":"[15]","plainTextFormattedCitation":"[15]","previouslyFormattedCitation":"[15]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[15] formed on the surface of the cathode. The slow dissolution of jarosite caused an increase in the iron concentration in the catholyte in time. In order to remove this residual iron, the catholyte was replaced by iron-free 9K solution 7 times. The concentration of iron ions in the catholyte was measured by the sulfosalycillic acid method ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1016/S0892-6875(02)00026-2","ISSN":"08926875","author":[{"dropping-particle":"","family":"Karamanev","given":"D.G.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Nikolov","given":"L.N.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Mamatarkova","given":"V.","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Minerals Engineering","id":"ITEM-1","issue":"5","issued":{"date-parts":[["2002","5"]]},"page":"341-346","title":"Rapid simultaneous quantitative determination of ferric and ferrous ions in drainage waters and similar solutions","type":"article-journal","volume":"15"},"uris":["http://www.mendeley.com/documents/?uuid=cb748b54-7535-3f8b-917c-bbf8fc8ff9f2"]}],"mendeley":{"formattedCitation":"[16]","plainTextFormattedCitation":"[16]","previouslyFormattedCitation":"[16]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[16].  In all the experiments described above, the liquid was recirculated between the cathode space and the aerated flask. In order to ensure complete removal of iron from the system, the iron-free 9K solution was next introduced to the cathode in a flow-through mode (retention time of 4.3 min) for a period of six days. At that point, the total iron ions concentration in the liquid effluent of the cathode fell below the detection level (approx. 50 �g/L) of the analytical method used, and no iron was detected in the liquid until the end of the experiments. 
	The effect of the cathode overpotential on the current was studied (Figure 3). It can be seen that the curve is linear in a semi-logarithmic plot, and therefore, it follows the Tafel equation. In a separate, sterile experiment, no electrical current was detected within the same range of overpotential values, and therefore, there was no electrochemical reduction of oxygen on the cathode. In the biological experiment, the open-circuit potential of the cathode was found to be 606 mV. It is interesting to note that this overpotential is quite close to the formal potential of the Fe3+/Fe2+ electrochemical couple in 9K solution (676 mV) ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1016/J.BEJ.2010.03.004","ISSN":"1369-703X","abstract":"A study of the kinetics of ferrous iron oxidation by a free suspended culture of the bacterium Leptospirillum ferriphilum in batch regime at moderate to high iron concentrations was conducted. A circulating bed airlift bioreactor was used in order to obtain reliable biokinetic data, unaffected by biofilm growth. The two major factors in consideration were the effects of the pH and the total iron concentration in the range of 5�40g/L. The optimal pH was found between 1.05 and 1.80. In this range a strictly growth associated biooxidation with constant yield coefficient was proven, while at suboptimal pH values non-growth associated iron biooxidation was shown at pH as low as 0.4. This effect was taken into consideration for the derivation of a Monod-type kinetic model, derived on first principles from the electrochemical-enzymatic model for ferrous iron biooxidation. Our model shows a linear dependence between the apparent half-saturation constant (Kapp) and the total iron concentration in studied range of iron concentration.","author":[{"dropping-particle":"","family":"Penev","given":"Kalin","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Karamanev","given":"Dimitre","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biochemical Engineering Journal","id":"ITEM-1","issue":"1-2","issued":{"date-parts":[["2010","6","15"]]},"page":"54-62","publisher":"Elsevier","title":"Batch kinetics of ferrous iron oxidation by Leptospirillum ferriphilum at moderate to high total iron concentration","type":"article-journal","volume":"50"},"uris":["http://www.mendeley.com/documents/?uuid=590443b3-085b-3133-8b5b-e67115b4f16d"]}],"mendeley":{"formattedCitation":"[17]","plainTextFormattedCitation":"[17]","previouslyFormattedCitation":"[17]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[17] which is the usual substrate for A. ferrooxidans. The oxygen consumption in the cathodic space was studied in continuous regime, when the liquid flowed through the cathodic space with different flow rates without recycle. The oxygen consumption rate in the cathodic space was relatively constant with an average value of 7.0 �g/min. The theoretical oxygen consumption rate, calculated from the current of the cell using the Faraday�s law, was 2.9 �g/min, or 41% of the actual value. The difference between the two values (59%) can be explained by the oxygen use for biomass formation. This value is somehow higher than that reported for A. ferrooxidans growing on ferrous iron, where between 3% and 30% of oxygen consumed is used for biomass formation ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"author":[{"dropping-particle":"","family":"Nemati","given":"M.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Harrison","given":"S. T L","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Hansford","given":"G. S.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Webb","given":"C.","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biochemical Engineering Journal","id":"ITEM-1","issue":"3","issued":{"date-parts":[["1998"]]},"page":"171-190","publisher":"Elsevier Inc.","title":"Biological oxidation of ferrous sulphate by Thiobacillus ferrooxidans: A review on the kinetic aspects","type":"article-journal","volume":"1"},"uris":["http://www.mendeley.com/documents/?uuid=5c36b1c7-7472-344e-b701-5cc915beb898"]}],"mendeley":{"formattedCitation":"[2]","plainTextFormattedCitation":"[2]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[2]. 
	The oxygen consumption by microorganisms was also measured in batch regime (Figure 4). At oxygen concentrations higher than 2.6 mg/L, the oxygen consumption rate was approximately constant at 8.6 �g/min and the electrical current remained constant. At lower oxygen concentrations, the oxygen consumption rate and the current decreased proportionally to each other. The decrease in the oxygen consumption rate at low oxygen concentrations can be explained by the Monod-type relationship between these two parameters. 
	In order to make sure that the inorganic salts in the 9K medium are not electron donors for the microorganisms, the cathodic space was next fed with water containing only sulfuric acid (for pH control at 2.8). The liquid was recirculated between the cathodic space and the aerated vessel. Immediately after the replacement of the salts medium with H2SO4 solution, the current dropped from 0.74 mA to 0.28 mA, but within the next 30 hours it rose back to 0.72 mA, and remained at that value for the length of the experiment (four days). 
	The viability of microorganisms in the cathodic space was determined by both microscopic observation using a phase-contrast microscopy, and by determination of the ferrous iron oxidation activity. This study was performed after 10 days of electrotrophic growth (i.e. in the absence of chemical electron donors such as dissolved iron in the catholyte). The microscopic study of a sample of the cathode (carbon fibre) showed a large amount of viable microbial cells having the shape and size of A. ferrooxidans. Most of the cells were attached to the carbon fibre surface. In order to check the iron oxidation activity of the microbial cells, immobilized on the cathode surface, a catholyte containing 1.2 g /L ferrous ions and nutrient salts (9K) was used. The power supply was detached from the electrobiochemical cell. After a lag period of 30 minutes, the ferrous iron was oxidized with a rate of 650 mg/L.h. This is a typical value for the iron oxidation by immobilized A. ferrooxidans ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1002/bit.260310403","ISSN":"10970290","abstract":"The influence of temperature, pH, and substrate and product concentrations on the oxidation rate of ferrous iron by biofilm of Thiobacillus ferrooxidans was determined. The experiments were performed in an inverse fluidized bed biofilm reactor in which the biofilm thickness was kept constant at 80 �m. Oxygen concentration and diffusion through the biofilm did not limit the oxidation rate. The oxidation rate was almost unaffected by temperature between 13 and 38�C, pH between 1.3 and 2.2, ferric iron concentration up to 14 g/L, or ferrous iron concentration from 4 to 13 g/L. The kinetics of the process was described by the Monod equation with respect to the mass of the biofilm and with ferrous ions as the limiting substrate. Copyright � 1988 John Wiley  &  Sons, Inc.","author":[{"dropping-particle":"","family":"Karamanev","given":"D.G.","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Nikolov","given":"L.N.","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biotechnology and Bioengineering","id":"ITEM-1","issue":"4","issued":{"date-parts":[["1988"]]},"title":"Influence of some physicochemical parameters on bacterial activity of biofilm: Ferrous iron oxidation by Thiobacillus ferrooxidans","type":"article-journal","volume":"31"},"uris":["http://www.mendeley.com/documents/?uuid=d07f734d-98f4-3cb6-a5a5-2b7421bbacb9"]}],"mendeley":{"formattedCitation":"[18]","plainTextFormattedCitation":"[18]","previouslyFormattedCitation":"[18]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[18]. 
	Electrotrophy can potentially have significant practical importance. Some potential applications of electrotrophs can include:
	production of biomass (single-cell protein) using electricity as a substrate (Karamanev, 2003). It has already been shown that A. ferrooxidans contains 44% protein, 26% lipids and 15% carbohydrates ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"DOI":"10.1038/281555a0","ISSN":"0028-0836","abstract":"Solar bacterial biomass bypasses efficiency limits of photosynthesis","author":[{"dropping-particle":"","family":"Tributsch","given":"Helmut","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Nature","id":"ITEM-1","issue":"5732","issued":{"date-parts":[["1979","10","18"]]},"page":"555-556","publisher":"Nature Publishing Group","title":"Solar bacterial biomass bypasses efficiency limits of photosynthesis","type":"article-journal","volume":"281"},"uris":["http://www.mendeley.com/documents/?uuid=9806449b-5e42-359b-886e-47188b90e36d"]}],"mendeley":{"formattedCitation":"[19]","plainTextFormattedCitation":"[19]","previouslyFormattedCitation":"[19]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[19]. The single-cell protein produced by electrotrophy is expected to be free from residual toxic substrates (such as methanol in some of the conventional processes) and pathogenic microorganisms ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"ISSN":"0734-9750","PMID":"14538097","abstract":"The alarming rate of population growth has increased the demand for food production in third-world countries leading to a yawning gap in demand and supply. This has led to an increase in the number of hungry and chronically malnourished people. This situation has created a demand for the formulation of innovative and alternative proteinaceous food sources. Single cell protein (SCP) production is a major step in this direction. SCP is the protein extracted from cultivated microbial biomass. It can be used for protein supplementation of a staple diet by replacing costly conventional sources like soymeal and fishmeal to alleviate the problem of protein scarcity. Moreover, bioconversion of agricultural and industrial wastes to protein-rich food and fodder stocks has an additional benefit of making the final product cheaper. This would also offset the negative cost value of wastes used as substrate to yield SCP. Further, it would make food production less dependent upon land and relieve the pressure on agriculture. This article reviews diversified aspects of SCP as an alternative protein-supplementing source. Various potential strains and substrates that could be utilized for SCP production are described. Nutritive value and removal of nucleic acids and toxins from SCP as a protein-supplementing source are discussed. New processes need to be exploited to improve yield. In that direction the solid state fermentation (SSF) method and its advantages for SCP production are highlighted.","author":[{"dropping-particle":"","family":"Anupama","given":"","non-dropping-particle":"","parse-names":false,"suffix":""},{"dropping-particle":"","family":"Ravindra","given":"P","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Biotechnology advances","id":"ITEM-1","issue":"6","issued":{"date-parts":[["2000","10"]]},"page":"459-79","title":"Value-added food: single cell protein.","type":"article-journal","volume":"18"},"uris":["http://www.mendeley.com/documents/?uuid=286b5229-de0b-3a7f-92cd-1de0fd1f0947"]}],"mendeley":{"formattedCitation":"[20]","plainTextFormattedCitation":"[20]","previouslyFormattedCitation":"[20]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[20], since the latter are not expected to grow under electrotrophic conditions. It should be noted that in the case of electrotrophic single-cell protein production, carbon dioxide is used as a carbon source, and therefore, the production of biomass is coupled with the consumption of CO2 from atmosphere;
	production of energy in biofuel cells ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"author":[{"dropping-particle":"","family":"Karamanev","given":"D","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"World Congress of Industrial Biotechnology","id":"ITEM-1","issued":{"date-parts":[["2006"]]},"title":"Electrotrophs - Microorganisms that Transform Chemical Energy into Electricity","type":"article-journal"},"uris":["http://www.mendeley.com/documents/?uuid=20cad90c-8df6-4aab-8dda-36f88991ceab"]}],"mendeley":{"formattedCitation":"[11]","plainTextFormattedCitation":"[11]","previouslyFormattedCitation":"[11]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[11]. The electrotrophic microorganisms can replace platinum and other highly expensive cathode catalysts in fuel cells;
	microbial electronics. Some of the electrical features of electrotrophs, such as one-way electron  transport,  could be used in electronic devices.
	Since A. ferrooxidans, as a chemolithotroph, is considered to be one of the simplest forms of life, according to some theories of the origin of life, it played a significant role in the life�s early evolution ADDIN CSL_CITATION {"citationItems":[{"id":"ITEM-1","itemData":{"author":[{"dropping-particle":"","family":"M. J. RUSSELL","given":"A. J. HALL","non-dropping-particle":"","parse-names":false,"suffix":""}],"container-title":"Journal of the Geological Society, London","id":"ITEM-1","issued":{"date-parts":[["1997"]]},"page":"377-402","title":"The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front","type":"article-journal","volume":"154"},"uris":["http://www.mendeley.com/documents/?uuid=dfa60354-0188-4374-8e3b-439cae5dad81"]}],"mendeley":{"formattedCitation":"[21]","plainTextFormattedCitation":"[21]","previouslyFormattedCitation":"[21]"},"properties":{"noteIndex":0},"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citation.json"}[21]. Now, with the discovery of electrotrophy, even a simpler life form than lithotrophs has been found. Thus, electrotrophy potentially could find its place in life evolution theories.
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Acknowledgement

This work was supported financially by the Natural Sciences and Engineering Research Council of Canada.

Figure Legends

Figure 1. Scheme of the electron transfer in A. ferrooxidans: a) using ferrous iron as an electron donor; b) using electrical current as an electron donor.

Figure 2. Scheme of the experimental setup.

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