Bacterial nanowires

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Geobacter sulfurreducens and its nanowires Proposal of catalyzing bio-voltage memristors.webp
Geobacter sulfurreducens and its nanowires

Bacterial nanowires (also known as microbial nanowires) are electrically conductive appendages produced by a number of bacteria most notably from the Geobacter and Shewanella genera. [1] [2] Conductive nanowires have also been confirmed in the oxygenic cyanobacterium Synechocystis PCC6803 and a thermophilic, methanogenic coculture consisting of Pelotomaculum thermopropionicum and Methanothermobacter thermoautotrophicus . [2] From physiological and functional perspectives, bacterial nanowires are diverse. [3] [4] [5] The precise role microbial nanowires play in their biological systems has not been fully realized, but several proposed functions exist. [3] Outside of a naturally occurring environment, bacterial nanowires have shown potential to be useful in several fields, notably the bioenergy and bioremediation industries. [6] [7]

Contents

Physiology

Geobacter nanowires were originally thought to be modified pili, which are used to establish connections to terminal electron acceptors during some types of anaerobic respiration. Further research has shown that Geobacter nanowires are composed of stacked cytochromes, namely OmcS and OmcZ. Despite being physiologically distinct from pili, bacterial nanowires are often described as pili anyway due to the initial misconception upon their discovery. [5] These stacked cytochrome nanowires form a seamless array of hemes which stabilize the nanowire via pi-stacking and provide a path for electron transport. [8] Species of the genus Geobacter use nanowires to transfer electrons to extracellular electron acceptors (such as Fe(III) oxides). [1] This function was discovered through the examination of mutants, whose nanowires could attach to the iron, but would not reduce it. [1]

Shewanella nanowires are also not technically pili, but extensions of the outer membrane that contain the decaheme outer membrane cytochromes MtrC and OmcA. [4] The reported presence of outer membrane cytochromes, and lack of conductivity in nanowires from the MtrC and OmcA-deficient mutant [9] directly support the proposed multistep hopping mechanism for electron transport through Shewanella nanowires. [10] [11] [12]

Additionally, nanowires can facilitate long-range electron transfer across thick biofilm layers. [6] By connecting to other cells around them, nanowires allow bacteria located in anoxic conditions to still use oxygen as their terminal electron acceptor. For example, organisms in the genus Shewanella have been observed to form electrically conductive nanowires in response to electron-acceptor limitation. [2]

History

The concept of electromicrobiology has been around since the early 1900s when a series of discoveries found cells capable of producing electricity. It was demonstrated for the first time in 1911 by Michael Cressé Potter that cells could convert chemical energy to electrical energy. [3] [13] It wasn't until 1988 that extracellular electron transport (EET) was observed for the first time with the independent discoveries of Geobacter and Shewanella bacteria and their respective nanowires. Since their discoveries, other nanowire containing microbes have been identified, but they remain the most intensively studied. [3] [14] [15] In 1998, EET was observed in a microbial fuel cell setting for the first time using Shewanella bacteria to reduce an Fe(III) electrode. [3] [16] In 2010, bacterial nanowires were shown to have facilitated the flow of electricity into Sporomusa bacteria. This was the first observed instance of EET used to draw electrons from the environment into a cell. [3] [17] Research persists to date to explore the mechanisms, implications, and potential applications of nanowires and the biological systems they are a part of.

Implications and potential applications

Biological implications

Microorganisms have shown to use nanowires to facilitate the use of extracellular metals as terminal electron acceptors in an electron transport chain. The high reduction potential of the metals receiving electrons is capable of driving a considerable ATP production. [18] [3] Aside from that, the extent of the implications brought on by the existence of bacterial nanowires is not fully realized. It has been speculated nanowires may function as conduits for electron transport between different members of a microbial community. This has potential to allow for regulatory feedback or other communication between members of the same or even different microbial species. [17] [18] Some organisms are capable of both expelling and taking in electrons through nanowires. [3] Those species would likely be able to oxidize extracellular metals by using them as an electron or energy source to facilitate energy consuming cellular processes. [18] Microbes also could potentially use nanowires to temporarily store electrons on metals. Building up an electron concentration on a metal anode would create a battery of sorts that the cells could later use to fuel metabolic activity. [18] While these potential implications provide a reasonable hypothesis towards the role of the bacterial nanowire in a biological system, more research is needed to fully understand the extent of how cellular species benefit from nanowire use. [3]

Bioenergy applications in microbial fuel cells

In microbial fuel cells (MFCs), bacterial nanowires generate electricity via extracellular electron transport to the MFC's anode. [19] Nanowire networks have been shown to enhance the electricity output of MFCs with efficient and long-range conductivity. In particular, bacterial nanowires of Geobacter sulfurreducens possess metallic-like conductivity, producing electricity at levels comparable to those of synthetic metallic nanostructures. [20] When bacterial strains are genetically manipulated to boost nanowire formation, higher electricity yields are generally observed. [21] Coating the nanowires with metal oxides also further promotes electrical conductivity. [22] Additionally, these nanowires can transport electrons up to centimeter-scale distances. [21] Long-range electron transfer via microbial nanowire networks allows viable cells that are not in direct contact with an anode to contribute to electron flow. [6]

To date, the currency produced by bacterial nanowires is very low. Across a biofilm 7 micrometers thick, a current density of around 17 microamperes per square centimeter and a voltage of around 0.5 volts was reported. [23]

Other significant applications

Microbial nanowires of Shewanella and Geobacter have been shown to aid in bioremediation of uranium contaminated groundwater. [24] To demonstrate this, scientists compared and observed the concentration of uranium removed by piliated and nonpiliated strains of Geobacter. Through a series of controlled experiments, they were able to deduce that nanowire present strains were more effective at the mineralization of uranium as compared to nanowire absent mutants. [25]

Further significant application of bacterial nanowires can be seen in the bioelectronics industry. [7] With sustainable resources in mind, scientists have proposed the future use of biofilms of Geobacter as a platform for functional under water transistors and supercapacitors, capable of self-renewing energy. [21]

On 20 April 2020, researchers demonstrated a diffusive memristor fabricated from protein nanowires of the bacterium Geobacter sulfurreducens which functions at substantially lower voltages than the ones previously described and may allow the construction of artificial neurons which function at voltages of biological action potentials. Bacterial nanowires vary from traditionally utilized silicon nanowires by showing an increased degree of biocompatibility. More research is needed, but the memristors may eventually be used to directly process biosensing signals, for neuromorphic computing and/or direct communication with biological neurons. [26] [27]

Related Research Articles

<span class="mw-page-title-main">Biofilm</span> Aggregation of bacteria or cells on a surface

A biofilm comprises any syntrophic consortium of microorganisms in which cells stick to each other and often also to a surface. These adherent cells become embedded within a slimy extracellular matrix that is composed of extracellular polymeric substances (EPSs). The cells within the biofilm produce the EPS components, which are typically a polymeric conglomeration of extracellular polysaccharides, proteins, lipids and DNA. Because they have three-dimensional structure and represent a community lifestyle for microorganisms, they have been metaphorically described as "cities for microbes".

<i>Geobacter</i> Genus of anaerobic bacteria found in soil

Geobacter is a genus of bacteria. Geobacter species are anaerobic respiration bacterial species which have capabilities that make them useful in bioremediation. Geobacter was found to be the first organism with the ability to oxidize organic compounds and metals, including iron, radioactive metals, and petroleum compounds into environmentally benign carbon dioxide while using iron oxide or other available metals as electron acceptors. Geobacter species are also found to be able to respire upon a graphite electrode. They have been found in anaerobic conditions in soils and aquatic sediment.

Microbial fuel cell (MFC) is a type of bioelectrochemical fuel cell system also known as micro fuel cell that generates electric current by diverting electrons produced from the microbial oxidation of reduced compounds on the anode to oxidized compounds such as oxygen on the cathode through an external electrical circuit. MFCs produce electricity by using the electrons derived from biochemical reactions catalyzed by bacteria.Comprehensive Biotechnology MFCs can be grouped into two general categories: mediated and unmediated. The first MFCs, demonstrated in the early 20th century, used a mediator: a chemical that transfers electrons from the bacteria in the cell to the anode. Unmediated MFCs emerged in the 1970s; in this type of MFC the bacteria typically have electrochemically active redox proteins such as cytochromes on their outer membrane that can transfer electrons directly to the anode. In the 21st century MFCs have started to find commercial use in wastewater treatment.

<i>Shewanella</i> Genus of bacteria

Shewanella is the sole genus included in the marine bacteria family Shewanellaceae. Some species within it were formerly classed as Alteromonas. Shewanella consists of facultatively anaerobic Gram-negative rods, most of which are found in extreme aquatic habitats where the temperature is very low and the pressure is very high. Shewanella bacteria are a normal component of the surface flora of fish and are implicated in fish spoilage. Shewanella chilikensis, a species of the genus Shewanella commonly found in the marine sponges of Saint Martin's Island of the Bay of Bengal, Bangladesh.

<span class="mw-page-title-main">Extracellular polymeric substance</span> Gluey polymers secreted by microorganisms to form biofilms

Extracellular polymeric substances (EPSs) are natural polymers of high molecular weight secreted by microorganisms into their environment. EPSs establish the functional and structural integrity of biofilms, and are considered the fundamental component that determines the physicochemical properties of a biofilm. EPS in the matrix of biofilms provides compositional support and protection of microbial communities from the harsh environments. Components of EPS can be of different classes of polysaccharides, lipids, nucleic acids, proteins, lipopolysaccharides, and minerals.

<i>Shewanella oneidensis</i> Species of bacterium

Shewanella oneidensis is a bacterium notable for its ability to reduce metal ions and live in environments with or without oxygen. This proteobacterium was first isolated from Lake Oneida, NY in 1988, hence its name.

A biobattery is an energy storing device that is powered by organic compounds. Although the batteries have never been commercially sold, they are still being tested, and several research teams and engineers are working to further advance the development of these batteries.

<span class="mw-page-title-main">Exoelectrogen</span>

An exoelectrogen normally refers to a microorganism that has the ability to transfer electrons extracellularly. While exoelectrogen is the predominant name, other terms have been used: electrochemically active bacteria, anode respiring bacteria, and electricigens. Electrons exocytosed in this fashion are produced following ATP production using an electron transport chain (ETC) during oxidative phosphorylation. Conventional cellular respiration requires a final electron acceptor to receive these electrons. Cells that use molecular oxygen (O2) as their final electron acceptor are described as using aerobic respiration, while cells that use other soluble compounds as their final electron acceptor are described as using anaerobic respiration. However, the final electron acceptor of an exoelectrogen is found extracellularly and can be a strong oxidizing agent in aqueous solution or a solid conductor/electron acceptor. Two commonly observed acceptors are iron compounds (specifically Fe(III) oxides) and manganese compounds (specifically Mn(III/IV) oxides). As oxygen is a strong oxidizer, cells are able to do this strictly in the absence of oxygen.

A Bioelectrochemical reactor is a type of bioreactor where bioelectrochemical processes are used to degrade/produce organic materials using microorganisms. This bioreactor has two compartments: The anode, where the oxidation reaction takes place; And the cathode, where the reduction occurs. At these sites, electrons are passed to and from microbes to power reduction of protons, breakdown of organic waste, or other desired processes. They are used in microbial electrosynthesis, environmental remediation, and electrochemical energy conversion. Examples of bioelectrochemical reactors include microbial electrolysis cells, microbial fuel cells, enzymatic biofuel cells, electrolysis cells, microbial electrosynthesis cells, and biobatteries.

Geobacter metallireducens is a gram-negative metal-reducing proteobacterium. It is a strict anaerobe that oxidizes several short-chain fatty acids, alcohols, and monoaromatic compounds with Fe(III) as the sole electron acceptor. It can also use uranium for its growth and convert U(VI) to U(IV).

<i>Geobacter sulfurreducens</i> Species of bacterium

Geobacter sulfurreducens is a gram-negative metal and sulphur-reducing proteobacterium. It is rod-shaped, aerotolerant anaerobe, non-fermentative, has flagellum and type four pili, and is closely related to Geobacter metallireducens. Geobacter sulfurreducens is an anaerobic species of bacteria that comes from the family of bacteria called Geobacteraceae. Under the genus of Geobacter, G. sulfurreducens is one out of twenty different species. The Geobacter genus was discovered by Derek R. Lovley in 1987. G. sulfurreducens was first isolated in Norman, Oklahoma, USA from materials found around the surface of a contaminated ditch.

Geopsychrobacter electrodiphilus is a species of bacteria, the type species of its genus. It is a psychrotolerant member of its family, capable of attaching to the anodes of sediment fuel cells and harvesting electricity by oxidation of organic compounds to carbon dioxide and transferring the electrons to the anode.

OmcS nanowires are conductive filaments found in some species of bacteria, including Geobacter sulfurreducens, where they catalyze the transfer of electrons. They are multiheme c-Type cytochromes localized outside of the cell of some exoelectrogenic bacterial species, serving as mediator of extracellular electron transfer from cells to Fe(III) oxides and other extracellular electron acceptors.

Dissimilatory metal-reducing microorganisms are a group of microorganisms (both bacteria and archaea) that can perform anaerobic respiration utilizing a metal as terminal electron acceptor rather than molecular oxygen (O2), which is the terminal electron acceptor reduced to water (H2O) in aerobic respiration. The most common metals used for this end are iron [Fe(III)] and manganese [Mn(IV)], which are reduced to Fe(II) and Mn(II) respectively, and most microorganisms that reduce Fe(III) can reduce Mn(IV) as well. But other metals and metalloids are also used as terminal electron acceptors, such as vanadium [V(V)], chromium [Cr(VI)], molybdenum [Mo(VI)], cobalt [Co(III)], palladium [Pd(II)], gold [Au(III)], and mercury [Hg(II)].

<span class="mw-page-title-main">Forest ring</span>

Forest rings are large, circular patterns of low tree density in the boreal forests of northern Canada. These rings can range from 50 metres (160 ft) to nearly 2 kilometres (1.2 mi) in diameter, with rims about 20 metres (66 ft) in thickness. The origin of forest rings is not known, despite several mechanisms for their creation having been proposed. Such hypotheses include radially growing fungus, buried kimberlite pipes, trapped gas pockets, and meteorite impact craters.

Geobacter daltonii is a Gram-negative, Fe(III)- and Uranium(IV)-reducing and non-spore-forming bacterium from the genus of Geobacter. It was isolated from sediments from the Oak Ridge Field Research Center in Oak Ridge, Tennessee in the United States. The specific epithet "daltonii" was refers to Dava Dalton, who performed the initial isolation of the strain, but died shortly thereafter.

Geobacter uraniireducens is a gram-negative, rod-shaped, anaerobic, chemolithotrophic, mesophilic, and motile bacterium from the genus of Geobacter. G. uraniireducens has been found to reduce iron and uranium in sediment and soil. It is being studied for use in bioremediation projects due to its ability to reduce uranium and arsenic.

Electric bacteria are forms of bacteria that directly consume and excrete electrons at different energy potentials without requiring the metabolization of any sugars or other nutrients. This form of life appears to be especially adapted to low-oxygen environments. Most life forms require an oxygen environment in which to release the excess of electrons which are produced in metabolizing sugars. In a low oxygen environment, this pathway for releasing electrons is not available. Instead, electric bacteria "breathe" metals instead of oxygen, which effectively results in both an intake of and excretion of electrical charges.

Gemma Reguera is a Spanish-American microbiologist and professor at Michigan State University. She is the editor-in-chief of the journal Applied and Environmental Microbiology and was elected fellow of the American Academy of Microbiology in 2019. She is the recipient of the 2022 Alice C. Evans Award for Advancement of Women from the American Society for Microbiology. Her lab's research is focused on electrical properties of metal-reducing microorganisms.

Microbial electrochemical technologies (METs) use microorganisms as electrochemical catalyst, merging the microbial metabolism with electrochemical processes for the production of bioelectricity, biofuels, H2 and other valuable chemicals. Microbial fuel cells (MFC) and microbial electrolysis cells (MEC) are prominent examples of METs. While MFC is used to generate electricity from organic matter typically associated with wastewater treatment, MEC use electricity to drive chemical reactions such as the production of H2 or methane. Recently, microbial electrosynthesis cells (MES) have also emerged as a promising MET, where valuable chemicals can be produced in the cathode compartment. Other MET applications include microbial remediation cell, microbial desalination cell, microbial solar cell, microbial chemical cell, etc.,.

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