Extracellular electron transfer mechanisms between microorganisms and minerals
TL;DR: The molecular mechanisms that underlie the ability of microorganisms to exchange electrons, such as c-type cytochromes and microbial nanowires, with extracellular minerals and with microorganisms of the same or different species are discussed.
Abstract: Electrons can be transferred from microorganisms to multivalent metal ions that are associated with minerals and vice versa. As the microbial cell envelope is neither physically permeable to minerals nor electrically conductive, microorganisms have evolved strategies to exchange electrons with extracellular minerals. In this Review, we discuss the molecular mechanisms that underlie the ability of microorganisms to exchange electrons, such as c-type cytochromes and microbial nanowires, with extracellular minerals and with microorganisms of the same or different species. Microorganisms that have extracellular electron transfer capability can be used for biotechnological applications, including bioremediation, biomining and the production of biofuels and nanomaterials.
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TL;DR: The finding that DIET can serve as the source of electrons for anaerobic photosynthesis further broadens its potential environmental significance.
Abstract: Direct interspecies electron transfer (DIET) has biogeochemical significance, and practical applications that rely on DIET or DIET-based aspects of microbial physiology are growing. Mechanisms for DIET have primarily been studied in defined cocultures in which Geobacter species are one of the DIET partners. Electrically conductive pili (e-pili) can be an important electrical conduit for DIET. However, there may be instances in which electrical contacts are made between electron transport proteins associated with the outer membranes of the partners. Alternatively, DIET partners can plug into conductive carbon materials, such as granular activated carbon, carbon cloth, and biochar, for long-range electron exchange without the need for e-pili. Magnetite promotes DIET, possibly by acting as a substitute for outer-surface c-type cytochromes. DIET is the primary mode of interspecies electron exchange in some anaerobic digesters converting wastes to methane. Promoting DIET with conductive materials shows promise for stabilizing and accelerating methane production in digesters, permitting higher organic loading rates. Various lines of evidence suggest that DIET is important in terrestrial wetlands, which are an important source of atmospheric methane. DIET may also have a role in anaerobic methane oxidation coupled to sulfate reduction, an important control on methane releases. The finding that DIET can serve as the source of electrons for anaerobic photosynthesis further broadens its potential environmental significance. Microorganisms capable of DIET are good catalysts for several bioelectrochemical technologies and e-pili are a promising renewable source of electronic materials. The study of DIET is in its early stages, and additional investigation is required to better understand the diversity of microorganisms that are capable of DIET, the importance of DIET to carbon and electron flow in anaerobic environments, and the biochemistry and physiology of DIET.
453 citations
08 Mar 2017
TL;DR: In this paper, the authors outline the mechanisms by which electrons are transferred between microorganisms and electrodes, and describe the challenges involved in designing robust and efficient systems, as well as present a review of the current state of the art.
Abstract: Electron transfer between microorganisms and an electrode — even across long distances — enables the former to live by coupling to an electronic circuit. Such a system integrates biological metabolism with artificial electronics; studying these systems adds to our knowledge of charge transport in the chemical species involved, as well as, perhaps most importantly, to our knowledge of charge transport and chemistry at the cell–electrode interfaces. This understanding may lead to microbial electrochemical systems finding widespread application, particularly in the energy sector. Bioelectrochemical systems have already shown promise for electricity generation, as well as for the production of biochemical and chemical feedstocks, and with improvement are likely to give rise to viable applications. Electrodes colonized by microbial electrocatalysts can serve as useful components in the electrosynthesis of valuable chemical products. This Review outlines the mechanisms by which electrons are transferred between microorganisms and electrodes, and describes the challenges involved in designing robust and efficient systems.
368 citations
TL;DR: A greater prevalence of EET-based growth capabilities is suggested and a previously underappreciated relevance for electrogenic bacteria across diverse environments, including host-associated microbial communities and infectious disease is established.
Abstract: Extracellular electron transfer (EET) describes microbial bioelectrochemical processes in which electrons are transferred from the cytosol to the exterior of the cell1. Mineral-respiring bacteria use elaborate haem-based electron transfer mechanisms2-4 but the existence and mechanistic basis of other EETs remain largely unknown. Here we show that the food-borne pathogen Listeria monocytogenes uses a distinctive flavin-based EET mechanism to deliver electrons to iron or an electrode. By performing a forward genetic screen to identify L. monocytogenes mutants with diminished extracellular ferric iron reductase activity, we identified an eight-gene locus that is responsible for EET. This locus encodes a specialized NADH dehydrogenase that segregates EET from aerobic respiration by channelling electrons to a discrete membrane-localized quinone pool. Other proteins facilitate the assembly of an abundant extracellular flavoprotein that, in conjunction with free-molecule flavin shuttles, mediates electron transfer to extracellular acceptors. This system thus establishes a simple electron conduit that is compatible with the single-membrane structure of the Gram-positive cell. Activation of EET supports growth on non-fermentable carbon sources, and an EET mutant exhibited a competitive defect within the mouse gastrointestinal tract. Orthologues of the genes responsible for EET are present in hundreds of species across the Firmicutes phylum, including multiple pathogens and commensal members of the intestinal microbiota, and correlate with EET activity in assayed strains. These findings suggest a greater prevalence of EET-based growth capabilities and establish a previously underappreciated relevance for electrogenic bacteria across diverse environments, including host-associated microbial communities and infectious disease.
352 citations
TL;DR: Application aspects and mechanisms of action of heavy metal tolerant-plant growth promoting (HMT-PGP) microbes in ensuring plant survival and growth in contaminated soils are discussed and can be of immense use/importance in reclaiming the HM contaminated soils, thus increasing the quality and yield of such soils.
Abstract: Increasing concentration of heavy metals (HM) due to various anthropogenic activities is a serious problem. Plants are very much affected by HM pollution particularly in contaminated soils. Survival of plants becomes tough and its overall health under HM stress is impaired. Remediation of HM in contaminated soil is done by physical and chemical processes which are costly, time-consuming and non-sustainable. Metal-microbe interaction is an emerging but under-utilized technology that can be exploited to reduce HM stress in plants. Several rhizosphere microorganisms are known to play essential role in the management of HM stresses in plants. They can accumulate, transform or detoxify HM. In general, the benefit from these microbes can have a vast impact on plant’s health. Plant‐microbe associations targeting HM stress may provide another dimension to existing phytoremediation and rhizoremediation uses. In this review, applied aspects and mechanisms of action of heavy metal tolerant (HMT) plant growth promoting (PGP) microbes in ensuring plant survival and growth in contaminated soils is discussed. The use of HMT-PGP microbes and their interaction with plants in remediation of contaminated soil can be the approach for the future. This low input and sustainable biotechnology can be of immense use/importance in reclaiming the HM contaminated soils, thus increasing the quality and yield of such soils.
338 citations
TL;DR: The aim is to present a detailed overview of the key aspects related to these mineral phases which can be used as an important resource for researchers working in a diverse range of fields dealing with mixed-valent iron minerals.
Abstract: Mixed-valent iron [Fe(II)-Fe(III)] minerals such as magnetite and green rust have received a significant amount of attention over recent decades, especially in the environmental sciences. These mineral phases are intrinsic and essential parts of biogeochemical cycling of metals and organic carbon and play an important role regarding the mobility, toxicity, and redox transformation of organic and inorganic pollutants. The formation pathways, mineral properties, and applications of magnetite and green rust are currently active areas of research in geochemistry, environmental mineralogy, geomicrobiology, material sciences, environmental engineering, and environmental remediation. These aspects ultimately dictate the reactivity of magnetite and green rust in the environment, which has important consequences for the application of these mineral phases, for example in remediation strategies. In this review we discuss the properties, occurrence, formation by biotic as well as abiotic pathways, characterization t...
284 citations
References
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TL;DR: This is the first demonstration that microorganisms can completely oxidize organic compounds with Fe(III) or Mn(IV) as the sole electron acceptor and that oxidation of organic matter coupled to dissimilatory Fe( III), Mn( IV), or Mn (IV) reduction can yield energy for microbial growth.
Abstract: A dissimilatory Fe(III)- and Mn(IV)-reducing microorganism was isolated from freshwater sediments of the Potomac River, Maryland. The isolate, designated GS-15, grew in defined anaerobic medium with acetate as the sole electron donor and Fe(III), Mn(IV), or nitrate as the sole electron acceptor. GS-15 oxidized acetate to carbon dioxide with the concomitant reduction of amorphic Fe(III) oxide to magnetite (Fe(3)O(4)). When Fe(III) citrate replaced amorphic Fe(III) oxide as the electron acceptor, GS-15 grew faster and reduced all of the added Fe(III) to Fe(II). GS-15 reduced a natural amorphic Fe(III) oxide but did not significantly reduce highly crystalline Fe(III) forms. Fe(III) was reduced optimally at pH 6.7 to 7 and at 30 to 35 degrees C. Ethanol, butyrate, and propionate could also serve as electron donors for Fe(III) reduction. A variety of other organic compounds and hydrogen could not. MnO(2) was completely reduced to Mn(II), which precipitated as rhodochrosite (MnCO(3)). Nitrate was reduced to ammonia. Oxygen could not serve as an electron acceptor, and it inhibited growth with the other electron acceptors. This is the first demonstration that microorganisms can completely oxidize organic compounds with Fe(III) or Mn(IV) as the sole electron acceptor and that oxidation of organic matter coupled to dissimilatory Fe(III) or Mn(IV) reduction can yield energy for microbial growth. GS-15 provides a model for how enzymatically catalyzed reactions can be quantitatively significant mechanisms for the reduction of iron and manganese in anaerobic environments.
2,233 citations
TL;DR: Results indicate that the pili of G. sulfurreducens might serve as biological nanowires, transferring electrons from the cell surface to the surface of Fe(iii) oxides, indicating possibilities for other unique cell-surface and cell–cell interactions, and for bioengineering of novel conductive materials.
Abstract: Microbes that can transfer electrons to extracellular electron acceptors, such as Fe(iii) oxides, are important in organic matter degradation and nutrient cycling in soils and sediments. Previous investigations on electron transfer to Fe(iii) have focused on the role of outer-membrane c-type cytochromes. However, some Fe(iii) reducers lack c-cytochromes. Geobacter species, which are the predominant Fe(iii) reducers in many environments, must directly contact Fe(iii) oxides to reduce them, and produce monolateral pili that were proposed, on the basis of the role of pili in other organisms, to aid in establishing contact with the Fe(iii) oxides. Here we report that a pilus-deficient mutant of Geobacter sulfurreducens could not reduce Fe(iii) oxides but could attach to them. Conducting-probe atomic force microscopy revealed that the pili were highly conductive. These results indicate that the pili of G. sulfurreducens might serve as biological nanowires, transferring electrons from the cell surface to the surface of Fe(iii) oxides. Electron transfer through pili indicates possibilities for other unique cell-surface and cell-cell interactions, and for bioengineering of novel conductive materials.
2,225 citations
TL;DR: The results suggest that the effectiveness of microbial fuel cells can be increased with organisms such as G. sulfurreducens that can attach to electrodes and remain viable for long periods of time while completely oxidizing organic substrates with quantitative transfer of electrons to an electrode.
Abstract: Previous studies have suggested that members of the Geobacteraceae can use electrodes as electron acceptors for anaerobic respiration. In order to better understand this electron transfer process for energy production, Geobacter sulfurreducens was inoculated into chambers in which a graphite electrode served as the sole electron acceptor and acetate or hydrogen was the electron donor. The electron-accepting electrodes were maintained at oxidizing potentials by connecting them to similar electrodes in oxygenated medium (fuel cells) or to potentiostats that poised electrodes at +0.2 V versus an Ag/AgCl reference electrode (poised potential). When a small inoculum of G. sulfurreducens was introduced into electrode-containing chambers, electrical current production was dependent upon oxidation of acetate to carbon dioxide and increased exponentially, indicating for the first time that electrode reduction supported the growth of this organism. When the medium was replaced with an anaerobic buffer lacking nutrients required for growth, acetate-dependent electrical current production was unaffected and cells attached to these electrodes continued to generate electrical current for weeks. This represents the first report of microbial electricity production solely by cells attached to an electrode. Electrode-attached cells completely oxidized acetate to levels below detection (<10 micro M), and hydrogen was metabolized to a threshold of 3 Pa. The rates of electron transfer to electrodes (0.21 to 1.2 micro mol of electrons/mg of protein/min) were similar to those observed for respiration with Fe(III) citrate as the electron acceptor (E(o)' =+0.37 V). The production of current in microbial fuel cell (65 mA/m(2) of electrode surface) or poised-potential (163 to 1,143 mA/m(2)) mode was greater than what has been reported for other microbial systems, even those that employed higher cell densities and electron-shuttling compounds. Since acetate was completely oxidized, the efficiency of conversion of organic electron donor to electricity was significantly higher than in previously described microbial fuel cells. These results suggest that the effectiveness of microbial fuel cells can be increased with organisms such as G. sulfurreducens that can attach to electrodes and remain viable for long periods of time while completely oxidizing organic substrates with quantitative transfer of electrons to an electrode.
2,133 citations
TL;DR: Nanowires produced by the oxygenic phototrophic cyanobacterium Synechocystis PCC6803 and the thermophilic, fermentative bacterium Pelotomaculum thermopropionicum reveal that electrically conductive appendages are not exclusive to dissimilatory metal-reducing bacteria and may, in fact, represent a common bacterial strategy for efficient electron transfer and energy distribution.
Abstract: Shewanella oneidensis MR-1 produced electrically conductive pilus-like appendages called bacterial nanowires in direct response to electron-acceptor limitation. Mutants deficient in genes for c-type decaheme cytochromes MtrC and OmcA, and those that lacked a functional Type II secretion pathway displayed nanowires that were poorly conductive. These mutants were also deficient in their ability to reduce hydrous ferric oxide and in their ability to generate current in a microbial fuel cell. Nanowires produced by the oxygenic phototrophic cyanobacterium Synechocystis PCC6803 and the thermophilic, fermentative bacterium Pelotomaculum thermopropionicum reveal that electrically conductive appendages are not exclusive to dissimilatory metal-reducing bacteria and may, in fact, represent a common bacterial strategy for efficient electron transfer and energy distribution.
1,666 citations
TL;DR: In this article, it was shown that some microorganisms found in soils and sediments are able to use humic substances as an electron acceptor for the anaerobic oxidation of organic compounds and hydrogen.
Abstract: HUMIC substances are heterogeneous high-molecular-weight organic materials which are ubiquitous in terrestrial and aquatic environments. They are resistant to microbial degradation1 and thus are not generally considered to be dynamically involved in microbial metabolism, especially in anoxic habitats. However, we show here that some microorganisms found in soils and sediments are able to use humic substances as an electron acceptor for the anaerobic oxidation of organic compounds and hydrogen. This electron transport yields energy to support growth. Microbial humic reduction also enhances the capacity for microorganisms to reduce other, less accessible electron acceptors, such as insoluble Fe(III) oxides, because humic substances can shuttle electrons between the humic-reducing microorganisms and the Fe(III) oxide. The finding that microorganisms can donate electrons to humic acids has important implications for the mechanisms by which microorganisms oxidize both natural and contaminant organics in anaerobic soils and sediments, and suggests a biological source of electrons for humics-mediated reduction of contaminant metals and organics.
1,651 citations