@article {3056, title = {Mechanisms for Electron Uptake by Methanosarcina acetivorans during Direct Interspecies Electron Transfer.}, journal = {mBio}, volume = {12}, year = {2021}, month = {2021 Oct 26}, pages = {e0234421}, abstract = {

Direct interspecies electron transfer (DIET) between bacteria and methanogenic archaea appears to be an important syntrophy in both natural and engineered methanogenic environments. However, the electrical connections on the outer surface of methanogens and the subsequent processing of electrons for carbon dioxide reduction to methane are poorly understood. Here, we report that the genetically tractable methanogen Methanosarcina acetivorans can grow via DIET in coculture with Geobacter metallireducens serving as the electron-donating partner. Comparison of gene expression patterns in grown in coculture versus pure-culture growth on acetate revealed that transcripts for the outer-surface multiheme type cytochrome MmcA were higher during DIET-based growth. Deletion of inhibited DIET. The high aromatic amino acid content of archaellins suggests that they might assemble into electrically conductive archaella. A mutant that could not express archaella was deficient in DIET. However, this mutant grew in DIET-based coculture as well as the archaellum-expressing parental strain in the presence of granular activated carbon, which was previously shown to serve as a substitute for electrically conductive pili as a conduit for long-range interspecies electron transfer in other DIET-based cocultures. Transcriptomic data suggesting that the membrane-bound Rnf, Fpo, and HdrED complexes also play a role in DIET were incorporated into a charge-balanced model illustrating how electrons entering the cell through MmcA can yield energy to support growth from carbon dioxide reduction. The results are the first genetics-based functional demonstration of likely outer-surface electrical contacts for DIET in a methanogen. The conversion of organic matter to methane plays an important role in the global carbon cycle and is an effective strategy for converting wastes to a useful biofuel. The reduction of carbon dioxide to methane accounts for approximately a third of the methane produced in anaerobic soils and sediments as well as waste digesters. Potential electron donors for carbon dioxide reduction are H or electrons derived from direct interspecies electron transfer (DIET) between bacteria and methanogens. Elucidating the relative importance of these electron donors has been difficult due to a lack of information on the electrical connections on the outer surfaces of methanogens and how they process the electrons received from DIET. Transcriptomic patterns and gene deletion phenotypes reported here provide insight into how a group of organisms that play an important role in methane production in soils and sediments participate in DIET.

}, keywords = {Archaeal Proteins, Electron Transport, Electrons, Methane, Methanosarcina, Transcriptome}, issn = {2150-7511}, doi = {10.1128/mBio.02344-21}, author = {Holmes, Dawn E and Zhou, Jinjie and Ueki, Toshiyuki and Woodard, Trevor and Lovley, Derek R} } @article {3077, title = {Iron Corrosion via Direct Metal-Microbe Electron Transfer.}, journal = {mBio}, volume = {10}, year = {2019}, month = {2019 May 14}, abstract = {

The concept that anaerobic microorganisms can directly accept electrons from Fe(0) has been controversial because direct metal-microbe electron transfer has previously only been indirectly inferred. Fe(0) oxidation was studied with strain ACL, an autotrophic strain that was previously shown to grow with electrons derived from a graphite cathode as the sole electron donor. Strain ACL grew with Fe(0) as the sole electron donor and fumarate as the electron acceptor. However, it appeared that at least a portion of the electron transfer was via H produced nonenzymatically from the oxidation of Fe(0) to Fe(II). H, which accumulated in abiotic controls, was consumed during the growth of strain ACL, the cells were predominately planktonic, and genes for the uptake hydrogenase were highly expressed. Strain ACL was constructed to prevent growth on H or formate by deleting the genes for the uptake of hydrogenase and formate dehydrogenases from strain ACL. Strain ACL also grew with Fe(0) as the sole electron donor, but H accumulated in the culture, and cells heavily colonized Fe(0) surfaces with no visible planktonic growth. Transcriptomics suggested that the outer surface -type cytochromes OmcS and OmcZ were important during growth of strain ACL on Fe(0). Strain ACL did not grow on Fe(0) if the gene for either of these cytochromes was deleted. The specific attachment of strain ACL to Fe(0), coupled with requirements for known extracellular electrical contacts, suggest that direct metal-microbe electron transfer is the most likely option for Fe(0) serving as an electron donor. The anaerobic corrosion of iron structures is expensive to repair and can be a safety and environmental concern. It has been known for over 100 years that the presence of anaerobic respiratory microorganisms can accelerate iron corrosion. Multiple studies have suggested that there are sulfate reducers, methanogens, and acetogens that can directly accept electrons from Fe(0) to support sulfate or carbon dioxide reduction. However, all of the strains studied can also use H as an electron donor for growth, which is known to be abiotically produced from Fe(0). Furthermore, no proteins definitely shown to function as extracellular electrical contacts with Fe(0) were identified. The studies described here demonstrate that direct electron transfer from Fe(0) can support anaerobic respiration. They also map out a simple genetic approach to the study of iron corrosion mechanisms in other microorganisms. A better understanding of how microorganisms promote iron corrosion is expected to lead to the development of strategies that can help reduce adverse impacts from this process.

}, keywords = {Anaerobiosis, Corrosion, Cytochromes, Electron Transport, Formate Dehydrogenases, Geobacter, Iron, Oxidation-Reduction, Oxidoreductases, Transcriptome}, issn = {2150-7511}, doi = {10.1128/mBio.00303-19}, author = {Tang, Hai-Yan and Holmes, Dawn E and Ueki, Toshiyuki and Palacios, Paola A and Lovley, Derek R} } @article {3074, title = {A Membrane-Bound Cytochrome Enables To Conserve Energy from Extracellular Electron Transfer.}, journal = {mBio}, volume = {10}, year = {2019}, month = {2019 Aug 20}, abstract = {

Extracellular electron exchange in species and closely related plays an important role in the global carbon cycle and enhances the speed and stability of anaerobic digestion by facilitating efficient syntrophic interactions. Here, we grew with methanol provided as the electron donor and the humic analogue, anthraquione-2,6-disulfonate (AQDS), provided as the electron acceptor when methane production was inhibited with bromoethanesulfonate. AQDS was reduced with simultaneous methane production in the absence of bromoethanesulfonate. Transcriptomics revealed that expression of the gene for the transmembrane, multiheme, -type cytochrome MmcA was higher in AQDS-respiring cells than in cells performing methylotrophic methanogenesis. A strain in which the gene for MmcA was deleted failed to grow via AQDS reduction but grew with the conversion of methanol or acetate to methane, suggesting that MmcA has a specialized role as a conduit for extracellular electron transfer. Enhanced expression of genes for methanol conversion to methyl-coenzyme M and the Rnf complex suggested that methanol is oxidized to carbon dioxide in AQDS-respiring cells through a pathway that is similar to methyl-coenzyme M oxidation in methanogenic cells. However, during AQDS respiration the Rnf complex and reduced methanophenazine probably transfer electrons to MmcA, which functions as the terminal reductase for AQDS reduction. Extracellular electron transfer may enable the survival of methanogens in dynamic environments in which oxidized humic substances and Fe(III) oxides are intermittently available. The availability of tools for genetic manipulation of makes it an excellent model microbe for evaluating -type cytochrome-dependent extracellular electron transfer in The discovery of a methanogen that can conserve energy to support growth solely from the oxidation of organic carbon coupled to the reduction of an extracellular electron acceptor expands the possible environments in which methanogens might thrive. The potential importance of -type cytochromes for extracellular electron transfer to syntrophic bacterial partners and/or Fe(III) minerals in some was previously proposed, but these studies with provide the first genetic evidence for cytochrome-based extracellular electron transfer in The results suggest parallels with Gram-negative bacteria, such as and species, in which multiheme outer-surface -type cytochromes are an essential component for electrical communication with the extracellular environment. offers an unprecedented opportunity to study mechanisms for energy conservation from the anaerobic oxidation of one-carbon organic compounds coupled to extracellular electron transfer in with implications not only for methanogens but possibly also for that anaerobically oxidize methane.

}, keywords = {Acetates, Anthraquinones, Cytochromes, Electron Transport, Electrons, Ferric Compounds, Gene Expression Regulation, Archaeal, Gram-Negative Bacteria, Membranes, Mesna, Methane, Methanol, Methanosarcina, Oxidation-Reduction, Oxidoreductases, Transcriptome}, issn = {2150-7511}, doi = {10.1128/mBio.00789-19}, author = {Holmes, Dawn E and Ueki, Toshiyuki and Tang, Hai-Yan and Zhou, Jinjie and Smith, Jessica A and Chaput, Gina and Lovley, Derek R} }