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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Microbial Biotechnology".

Deadline for manuscript submissions: closed (31 May 2023) | Viewed by 27492

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Dr. Akihiro Okamoto

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Chief Guest Editor

1. National Institute for Materials Science, 1-1 Namiki, Tsukuba, Ibaraki 305-0044, Japan
2. School of Chemical Sciences and Engineering, Hokkaido University, 5 Chome Kita 8 Jonishi, Kita Ward, Sapporo, Hokkaido 060-0808, Japan
Interests: bioelectrochemistry; electrochemical biosensor; microbially influenced iron corrosion; biofilm; outermembrane cytochrome
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Dr. Annette Rowe

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Assistant Professor, Biological Sciences, University of Cincinnati, Cincinnati, OH, USA
Interests: bioelectrochemistry; biocathode; electrosynthesis; synthetic biology; electrochemical cultivation

Special Issue Information

Dear Colleagues,

Since the first reports in 1988, more and more microbes have been suggested or identified to be capable of exchanging electrons with extracellular solids as part of their metabolism, referred to as electrogenic bacteria. While some model-bacteria are extensively investigated as living electrode catalysts to drive various valuable reactions for energy and environmental applications, the importance of electrogenic bacteria for ecophysiology is still poorly understood. Furthermore, some human commensal and pathogenic bacteria have been recently identified as electrochemically active, opening up a new realm of potential importance for these organisms in the human microbiome. However, why or how the lifestyle of pathogens and symbionts uses extracellular electron transport remains unknown. Taken together, we are facing an expanding appreciation for the prevalence of electrogenic bacteria, but understanding their role and significance in many ecosystems remains a challenge. Central to tackling this issue is the cultivation of microbes from their wide-ranging environments, and making a detailed catalog for electrogenic microbes and the habitats where they persist. Ultimately this work can fuel future efforts aimed at understanding the role of microbes in diverse environments.

In this Special Issue of Microorganisms, we look forward to receiving your article or review concerning any aspects related to electrogenic microbe except model microbes, Shewanella and Geobacter, including basic characterization for electrochemical or electrophysiological properties in pure cultures, isolation of electrogenic microbe from any microbiome, and chemical or physical analysis on nano-scale structure with redox properties. We encourage the submission of works on novel or previously uncharacterized strains, but logic quality and data quantity are strictly required. Studies about novel isolation or enrichment methods for electrogenic microbe are also welcome for this Special Issue. Review papers that propose the novel role of electrogenic capability will also be considered.

Dr. Akihiro Okamoto
Chief Guest Editor
Dr. Annette Rowe
Guest Editor

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Keywords

extracellular electron transport
microbial fuel cell
bioanode
extracellular electron uptake
biocathode
microbial electrosynthesis
microbially influenced iron corrosion
pathogen
archaea
extremophile
phototroph

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New Electrogenic Microbes in Microorganisms (2 articles)

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Research

17 pages, 2822 KiB

Open AccessArticle

Exploring Acetogenesis in Firmicutes: From Phylogenetic Analysis to Solid Medium Cultivation with Solid-Phase Electrochemical Isolation Equipments

by Zen-ichiro Kimura, Hiroki Kuriyama and Yuki Iwasaki

Microorganisms 2023, 11(12), 2976; https://doi.org/10.3390/microorganisms11122976 - 13 Dec 2023

Viewed by 1188

Abstract

This study introduces a groundbreaking approach for the exploration and utilization of electrotrophic acetogens, essential for advancing microbial electrosynthesis systems (MES). Our initial focus was the development of Solid-Phase Electrochemical Isolation Equipment (SPECIEs), a novel cultivation method for isolating electrotrophic acetogens directly from environmental samples on a solid medium. SPECIEs uses electrotrophy as a selection pressure, successfully overcoming the traditional cultivation method limitations and enabling the cultivation of diverse microbial communities with enhanced specificity towards acetogens. Following the establishment of SPECIEs, we conducted a genome-based phylogenetic analysis using the Genome Taxonomy Database (GTDB) to identify potential electrotrophic acetogens within the Firmicutes phylum and its related lineages. Subsequently, we validated the electrotrophic capabilities of selected strains under electrode-oxidizing conditions in a liquid medium. This sequential approach, integrating innovative cultivation techniques with detailed phylogenetic analysis, paves the way for further advances in microbial cultivation and the identification of new biocatalysts for sustainable energy applications. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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15 pages, 5622 KiB

Open AccessEditor’s ChoiceArticle

Isolation and Characterisation of Electrogenic Bacteria from Mud Samples

by György Schneider, Dorina Pásztor, Péter Szabó, László Kőrösi, Nandyala Siva Kishan, Penmetsa Appala Rama Krishna Raju and Rajnish Kaur Calay

Microorganisms 2023, 11(3), 781; https://doi.org/10.3390/microorganisms11030781 - 17 Mar 2023

Cited by 3 | Viewed by 3672

Abstract

To develop efficient microbial fuel cell systems for green energy production using different waste products, establishing characterised bacterial consortia is necessary. In this study, bacteria with electrogenic potentials were isolated from mud samples and examined to determine biofilm-formation capacities and macromolecule degradation. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry identifications have revealed that isolates represented 18 known and 4 unknown genuses. They all had the capacities to reduce the Reactive Black 5 stain in the agar medium, and 48 of them were positive in the wolfram nanorod reduction assay. The isolates formed biofilm to different extents on the surfaces of both adhesive and non-adhesive 96-well polystyrene plates and glass. Scanning electron microscopy images revealed the different adhesion potentials of isolates to the surface of carbon tissue fibres. Eight of them (15%) were able to form massive amounts of biofilm in three days at 23 °C. A total of 70% of the isolates produced proteases, while lipase and amylase production was lower, at 38% and 27% respectively. All of the macromolecule-degrading enzymes were produced by 11 isolates, and two isolates of them had the capacity to form a strong biofilm on the carbon tissue one of the most used anodic materials in MFC systems. This study discusses the potential of the isolates for future MFC development applications. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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14 pages, 3110 KiB

Open AccessArticle

Polyphasic Characterization of Geotalea uranireducens NIT-SL11 Newly Isolated from a Complex of Sewage Sludge and Microbially Reduced Graphene Oxide

by Li Xie, Naoko Yoshida and Lingyu Meng

Microorganisms 2023, 11(2), 349; https://doi.org/10.3390/microorganisms11020349 - 30 Jan 2023

Cited by 3 | Viewed by 1970

Abstract

Graphene oxide (GO), a chemically oxidized sheet of graphite, has been used as a conductive carbon carrier of microbes to boost various bioelectrochemical reactions. However, the types of microbes that can reduce GO have rarely been investigated. In this study, a strain of GO-reducing bacteria, named NIT-SL11, which was obtained from a hydrogel of microbially reduced GO and anaerobic sludge that converts sewage to electricity, was phylogenically identified as a novel strain of Geotalea uraniireducens. Considering the current lack of information on the electrogenic ability of the bacterium and its physicochemical and chemotaxonomic characteristics, the polyphasic characterization of the Geotalea uraniireducens strain NIT-SL11 was performed. NIT-SL11 utilized various organic acids, such as lactate, benzoate, and formate, as electron donors and exhibited respiration using GO, electrodes, fumarate, and malate. The strain contained C16:1ω7c and C16:0 as the major fatty acids and MK-8 and 9 as the major respiratory quinones. The complete genome of NIT-SL11 was 4.7 Mbp in size with a G+C content of 60.9%, and it encoded 80 putative c-type cytochromes and 23 type IV pili-related proteins. The possible extracellular electron transfer (EET) pathways of the strain were the porin–cytochrome (Pcc) EET pathway and type IV pili-based pathway. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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11 pages, 1431 KiB

Open AccessArticle

Enterococcus faecalis NADH Peroxidase-Defective Mutants Stain Falsely in Colony Zymogram Assay for Extracellular Electron Transfer to Ferric Ions

by Lars Hederstedt

Microorganisms 2023, 11(1), 106; https://doi.org/10.3390/microorganisms11010106 - 31 Dec 2022

Cited by 4 | Viewed by 1843

Abstract

Enterococcus faecalis cells can reduce ferric ions and other electron acceptors by extracellular electron transfer (EET). To find mutants with enhanced or defective EET, strain OG1RF with random transposon insertions in the chromosome was screened for ferric reductase activity by colony zymogram staining using the chromogenic ferrous-chelating compound Ferrozine. The screen revealed npr, eetB, and ndh3 mutants. The aberrant ferric reductase phenotype of Npr (NADH peroxidase)-defective mutants was found to be a property of colonies and not apparent with washed cells grown in liquid culture. EetB- and Ndh3-defective mutants, in contrast, consistently showed low ferric reductase activity. It is concluded that colony zymogram staining for ferric reductase activity using Ferrozine can be misleading, especially through false negative results. It is suggested that hydrogen peroxide produced in the colony quenches the zymogram staining. In addition, it is demonstrated that the negative effect of heme on EET to ferric ion in E. faecalis is relieved by cytochrome bd deficiency. The findings can help to identify bacteria with EET ability and contribute to our understanding of EET in Gram-positive bacteria and the physiology of E. faecalis. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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11 pages, 1387 KiB

Open AccessArticle

Electrochemical Enrichment and Isolation of Electrogenic Bacteria from 0.22 µm Filtrate

by Sota Ihara, Satoshi Wakai, Tomoko Maehara and Akihiro Okamoto

Microorganisms 2022, 10(10), 2051; https://doi.org/10.3390/microorganisms10102051 - 18 Oct 2022

Cited by 2 | Viewed by 1882

Abstract

Ultramicrobacteria (UMB) that can pass through a 0.22 µm filter are attractive because of their novelty and diversity. However, isolating UMB has been difficult because of their symbiotic or parasitic lifestyles in the environment. Some UMB have extracellular electron transfer (EET)-related genes, suggesting that these symbionts may grow on an electrode surface independently. Here, we attempted to culture from soil samples bacteria that passed through a 0.22 µm filter poised with +0.2 V vs. Ag/AgCl and isolated Cellulomonas sp. strain NTE-D12 from the electrochemical reactor. A phylogenetic analysis of the 16S rRNA showed 97.9% similarity to the closest related species, Cellulomonas algicola, indicating that the strain NTE-D12 is a novel species. Electrochemical and genomic analyses showed that the strain NTE-D12 generated the highest current density compared to that in the three related species, indicating the presence of a unique electron transfer system in the strain. Therefore, the present study provides a new isolation scheme for cultivating and isolating novel UMB potentially with a symbiotic relationship associated with interspecies electron transfer. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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16 pages, 1830 KiB

Open AccessArticle

Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus

by Jorge Vinales, Joshua Sackett, Leah Trutschel, Waleed Amir, Casey Norman, Edmund Leach, Elizabeth Wilbanks and Annette Rowe

Microorganisms 2022, 10(6), 1219; https://doi.org/10.3390/microorganisms10061219 - 14 Jun 2022

Cited by 1 | Viewed by 2728

Abstract

Extracellular electron transfer (EET), the process that allows microbes to exchange electrons in a redox capacity with solid interfaces such as minerals or electrodes, has been predominantly described in microbes that use iron during respiration. In this work, we characterize the physiology, genome, and electrochemical properties of two obligately heterotrophic marine microbes that were previously isolated from marine sediment cathode enrichments. Phylogenetic analysis of isolate 16S rRNA genes showed two strains, SN11 and FeN1, belonging to the genus Idiomarina. Strain SN11 was found to be nearly identical to I. loihiensis L2-TR^T, and strain FeN1 was most closely related to I. maritima 908087^T. Each strain had a relatively small genome (~2.8–2.9 MB). Phenotypic similarities among FeN1, SN11, and the studied strains include being Gram-negative, motile, catalase- and oxidase-positive, and rod-shaped. Physiologically, all strains appeared to exclusively use amino acids as a primary carbon source for growth. This was consistent with genomic observations. Each strain contained 17 to 22 proteins with heme-binding motifs. None of these were predicted to be extracellular, although seven were of unknown localization and lacked functional annotation beyond cytochrome. Despite the lack of homology to known EET pathways, both FeN1 and SN11 were capable of sustained electron uptake over time in an electrochemical system linked to respiration. Given the association of these Idiomarina strains with electro-active biofilms in the environment and their lack of autotrophic capabilities, we predict that EET is used exclusively for respiration in these microbes. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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8 pages, 1800 KiB

Open AccessArticle

Current Production Capability of Drug-Resistant Pathogen Enables Its Rapid Label-Free Detection Applicable to Wastewater-Based Epidemiology

by Waheed Miran, Xizi Long, Wenyuan Huang and Akihiro Okamoto

Microorganisms 2022, 10(2), 472; https://doi.org/10.3390/microorganisms10020472 - 20 Feb 2022

Cited by 4 | Viewed by 2692

Abstract

A rapid and label-free method for the detection of drug-resistant pathogens is in high demand for wastewater-based epidemiology. As recently shown, the extent of electrical current production (I_c) is a useful indicator of a pathogen’s metabolic activity. Therefore, if drug-resistant bacteria have extracellular electron transport (EET) capability, a simple electric sensor may be able to detect not only the growth as a conventional plating technique but also metabolic activity specific for drug-resistant bacteria in the presence of antibiotics. Here, one of the multidrug-resistant pathogens in wastewater, Klebsiella pneumoniae, was shown to generate I_c, and the extent of I_c was unaffected by the microbial growth inhibitor, kanamycin, while the current was markedly decreased in environmental EET bacteria Shewanella oneidensis. Kanamycin differentiated I_c in K. pneumonia and S. oneidensis within 3 h. Furthermore, the detection of K. pneumoniae was successful in the presence of S. oneidensis in the electrochemical cell. These results clarify the advantage of detecting drug-resistant bacteria using whole-cell electrochemistry as a simple and rapid method to detect on-site drug-resistant pathogens in wastewater, compared with conventional colony counting, which takes a few days. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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12 pages, 4873 KiB

Open AccessArticle

Novel Methanobacterium Strain Induces Severe Corrosion by Retrieving Electrons from Fe⁰ under a Freshwater Environment

by Shin-ichi Hirano, Sota Ihara, Satoshi Wakai, Yuma Dotsuta, Kyohei Otani, Toru Kitagaki, Fumiyoshi Ueno and Akihiro Okamoto

Microorganisms 2022, 10(2), 270; https://doi.org/10.3390/microorganisms10020270 - 25 Jan 2022

Cited by 12 | Viewed by 3557

Abstract

Methanogens capable of accepting electrons from Fe⁰ cause severe corrosion in anoxic conditions. In previous studies, all iron-corrosive methanogenic isolates were obtained from marine environments. However, the presence of methanogens with corrosion ability using Fe⁰ as an electron donor and their contribution to corrosion in freshwater systems is unknown. Therefore, to understand the role of methanogens in corrosion under anoxic conditions in a freshwater environment, we investigated the corrosion activities of methanogens in samples collected from groundwater and rivers. We enriched microorganisms that can grow with CO₂/NaHCO₃ and Fe⁰ as the sole carbon source and electron donor, respectively, in ground freshwater. Methanobacterium sp. TO1, which induces iron corrosion, was isolated from freshwater. Electrochemical analysis revealed that strain TO1 can uptake electrons from the cathode at lower than −0.61 V vs SHE and has a redox-active component with electrochemical potential different from those of other previously reported methanogens with extracellular electron transfer ability. This study indicated the corrosion risk by methanogens capable of taking up electrons from Fe⁰ in anoxic freshwater environments and the necessity of understanding the corrosion mechanism to contribute to risk diagnosis. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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17 pages, 3707 KiB

Open AccessArticle

Using Oxidative Electrodes to Enrich Novel Members in the Desulfobulbaceae Family from Intertidal Sediments

by Cheng Li, Clare E. Reimers and Yvan Alleau

Microorganisms 2021, 9(11), 2329; https://doi.org/10.3390/microorganisms9112329 - 11 Nov 2021

Cited by 5 | Viewed by 2557

Abstract

Members in the family of Desulfobulbaceae may be influential in various anaerobic microbial communities, including those in anoxic aquatic sediments and water columns, and within wastewater treatment facilities and bioelectrochemical systems (BESs) such as microbial fuel cells (MFCs). However, the diversity and roles of the Desulfobulbaceae in these communities have received little attention, and large portions of this family remain uncultured. Here we expand on findings from an earlier study (Li, Reimers, and Alleau, 2020) to more fully characterize Desulfobulbaceae that became prevalent in biofilms on oxidative electrodes of bioelectrochemical reactors. After incubations, DNA extraction, microbial community analyses, and microscopic examination, we found that a group of uncultured Desulfobulbaceae were greatly enriched on electrode surfaces. These Desulfobulbaceae appeared to form filaments with morphological features ascribed to cable bacteria, but the majority were taxonomically distinct from recognized cable bacteria genera. Thus, the present study provides new information about a group of Desulfobulbaceae that can exhibit filamentous morphologies and respire on the oxidative electrodes. While the phylogeny of cable bacteria is still being defined and updated, further enriching these members can contribute to the overall understanding of cable bacteria and may also lead to identification of successful isolation strategies. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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19 pages, 3480 KiB

Open AccessArticle

Isolation and Polyphasic Characterization of Desulfuromonas versatilis sp. Nov., an Electrogenic Bacteria Capable of Versatile Metabolism Isolated from a Graphene Oxide-Reducing Enrichment Culture

by Li Xie, Naoko Yoshida, Shun’ichi Ishii and Lingyu Meng

Microorganisms 2021, 9(9), 1953; https://doi.org/10.3390/microorganisms9091953 - 14 Sep 2021

Cited by 9 | Viewed by 3146

Abstract

In this study, a novel electrogenic bacterium denoted as strain NIT-T3 of the genus Desulfuromonas was isolated from a graphene-oxide-reducing enrichment culture that was originally obtained from a mixture of seawater and coastal sand. Strain NIT-T3 utilized hydrogen and various organic acids as electron donors and exhibited respiration using electrodes, ferric iron, nitrate, and elemental sulfur. The strain contained C16:1ω7c, C16:0, and C15:0 as major fatty acids and MK-8, 9, and 7 as the major respiratory quinones. Strain NIT-T3 contained four 16S rRNA genes and showed 95.7% similarity to Desulfuromonasmichiganensis BB1^T, the closest relative. The genome was 4.7 Mbp in size and encoded 76 putative c-type cytochromes, which included 6 unique c-type cytochromes (<40% identity) compared to those in the database. Based on the physiological and genetic uniqueness, and wide metabolic capability, strain NIT-T3 is proposed as a type strain of ‘Desulfuromonas versatilis’ sp. nov. Full article

(This article belongs to the Special Issue New Electrogenic Microbes)

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