Title: Direct cathodic electron uptake coupled to sulfate reduction by Desulfovibrio ferrophilus IS5 biofilms
Summary
Direct electron uptake is emerging as a key process for electron transfer in anaerobic microbial communities, both between species and from extracellular sources, such as zero‐valent iron (Fe0) or cathodic surfaces. In this study, we investigated cathodic electron uptake by Fe0‐corrodingDesulfovibrio ferrophilusIS5 and showed that electron uptake is dependent on direct cell contact via a biofilm on the cathode surface rather than through secreted intermediates. Induction of cathodic electron uptake by lactate‐starvedD. ferrophilusIS5 cells resulted in the expression of all components necessary for electron uptake; however, protein synthesis was required for full biofilm formation. Notably, proteinase K treatment uncoupled electron uptake from biofilm formation, likely through proteolytic degradation of proteinaceous components of the electron uptake machinery. We also showed that cathodic electron uptake is dependent on SO42−reduction. The insensitivity of Fe0corrosion to proteinase K treatment suggests that electron uptake from a cathode might involve different mechanism(s) than those involved in Fe0corrosion.
Extracellular electron transfer is a process by which bacterial cells can exchange electrons with a redox-active material located outside of the cell. InShewanella oneidensis, this process is natively used to facilitate respiration using extracellular electron acceptors such as Fe(III) or an anode. Previously, it was demonstrated that this process can be used to drive the microbial electrosynthesis (MES) of 2,3-butanediol (2,3-BDO) inS. oneidensisexogenously expressing butanediol dehydrogenase (BDH). Electrons taken into the cell from a cathode are used to generate NADH, which in turn is used to reduce acetoin to 2,3-BDO via BDH. However, generating NADH via electron uptake from a cathode is energetically unfavorable, so NADH dehydrogenases couple the reaction to proton motive force. We therefore need to maintain the proton gradient across the membrane to sustain NADH production. This work explores accomplishing this task by bidirectional electron transfer, where electrons provided by the cathode go to both NADH formation and oxygen (O2) reduction by oxidases. We show that oxidases use trace dissolved oxygen in a microaerobic bioelectrical chemical system (BES), and the translocation of protons across the membrane during O2reduction supports 2,3-BDO generation. Interestingly, this process is inhibited by high levels of dissolved oxygen in this system. In an aerated BES, O2molecules react with the strong reductant (cathode) to form reactive oxygen species, resulting in cell death.
IMPORTANCE
Microbial electrosynthesis (MES) is increasingly employed for the generation of specialty chemicals, such as biofuels, bioplastics, and cancer therapeutics. For these systems to be viable for industrial scale-up, it is important to understand the energetic requirements of the bacteria to mitigate unnecessary costs. This work demonstrates sustained production of an industrially relevant chemical driven by a cathode. Additionally, it optimizes a previously published system by removing any requirement for phototrophic energy, thereby removing the additional cost of providing a light source. We also demonstrate the severe impact of oxygen intrusion into bioelectrochemical systems, offering insight to future researchers aiming to work in an anaerobic environment. These studies provide insight into both the thermodynamics of electrosynthesis and the importance of the bioelectrochemical systems’ design.
Liu, Xinying; Walker, David J.; Nonnenmann, Stephen S.; Sun, Dezhi; Lovley, Derek R.(
, mBio)
Papoutsakis, Eleftherios T.
(Ed.)
ABSTRACT Geobacter sulfurreducens is a model microbe for elucidating the mechanisms for extracellular electron transfer in several biogeochemical cycles, bioelectrochemical applications, and microbial metal corrosion. Multiple lines of evidence previously suggested that electrically conductive pili (e-pili) are an essential conduit for long-range extracellular electron transport in G. sulfurreducens . However, it has recently been reported that G. sulfurreducens does not express e-pili and that filaments comprised of multi-heme c -type cytochromes are responsible for long-range electron transport. This possibility was directly investigated by examining cells, rather than filament preparations, with atomic force microscopy. Approximately 90% of the filaments emanating from wild-type cells had a diameter (3 nm) and conductance consistent with previous reports of e-pili harvested from G. sulfurreducens or heterologously expressed in Escherichia coli from the G. sulfurreducens pilin gene. The remaining 10% of filaments had a morphology consistent with filaments comprised of the c -type cytochrome OmcS. A strain expressing a modified pilin gene designed to yield poorly conductive pili expressed 90% filaments with a 3-nm diameter, but greatly reduced conductance, further indicating that the 3-nm diameter conductive filaments in the wild-type strain were e-pili. A strain in which genes for five of the most abundant outer-surface c -type cytochromes, including OmcS, were deleted yielded only 3-nm-diameter filaments with the same conductance as in the wild type. These results demonstrate that e-pili are the most abundant conductive filaments expressed by G. sulfurreducens , consistent with previous functional studies demonstrating the need for e-pili for long-range extracellular electron transfer. IMPORTANCE Electroactive microbes have significant environmental impacts, as well as applications in bioenergy and bioremediation. The composition, function, and even existence of electrically conductive pili (e-pili) has been one of the most contentious areas of investigation in electromicrobiology, in part because e-pili offer a mechanism for long-range electron transport that does not involve the metal cofactors common in much of biological electron transport. This study demonstrates that e-pili are abundant filaments emanating from Geobacter sulfurreducens , which serves as a model for long-range extracellular electron transfer in direct interspecies electron transfer, dissimilatory metal reduction, microbe-electrode exchange, and corrosion caused by direct electron uptake from Fe(0). The methods described in this study provide a simple strategy for evaluating the distribution of conductive filaments throughout the microbial world with an approach that avoids artifactual production and/or enrichment of filaments that may not be physiologically relevant.
Choi, Joonyoung; Park, Jin‐Hong; Kyung, Wonshik; Kim, Younsik; Kim, Mi Kyung; Kwon, Junyoung; Kim, Changyoung; Rhim, Jun‐Won; Park, Se Young; Jo, Younjung(
, Advanced Science)
Abstract
The anomalous Hall conductivity (AHC) in magnetic materials, resulting from inverted band topology, has emerged as a key adjustable function in spin‐torque devices and advanced magnetic sensors. Among systems with near‐half‐metallicity and broken time‐reversal symmetry, cobalt disulfide (CoS2) has proven to be a material capable of significantly enhancing its AHC. In this study, the AHC of CoS2is empirically assessed by manipulating the chemical potential through Fe‐ (hole) and Ni‐ (electron) doping. The primary mechanism underlying the colossal AHC is identified through the application of density functional theory and tight‐binding analyses. The main source of this substantial AHC is traced to four spin‐polarized massive Dirac dispersions in thekz= 0 plane of the Brillouin zone, located slightly below the Fermi level. In Co0.95Fe0.05S2, the AHC, which is directly proportional to the momentum‐space integral of the Berry curvature (BC), reached a record‐breaking value of 2507 Ω−1cm−1. This is because the BCs of the four Dirac dispersions all exhibit the same sign, a consequence of thed‐wave‐like spin‐orbit coupling among spin‐polarizedeg orbitals.
Rhim, Jeemin H.; Zhou, Alice; Amenabar, Maximiliano J.; Boyer, Grayson M.; Elling, Felix J.; Weber, Yuki; Pearson, Ann; Boyd, Eric S.; Leavitt, William D.(
, Applied and Environmental Microbiology)
Spear, John R.
(Ed.)
ABSTRACT
The degree of cyclization, or ring index (RI), in archaeal glycerol dibiphytanyl glycerol tetraether (GDGT) lipids was long thought to reflect homeoviscous adaptation to temperature. However, more recent experiments show that other factors (e.g., pH, growth phase, and energy flux) can also affect membrane composition. The main objective of this study was to investigate the effect of carbon and energy metabolism on membrane cyclization. To do so, we cultivatedAcidianussp. DS80, a metabolically flexible and thermoacidophilic archaeon, on different electron donor, acceptor, and carbon source combinations (S0/Fe3+/CO2, H2/Fe3+/CO2, H2/S0/CO2, or H2/S0/glucose). We show that differences in energy and carbon metabolism can result in over a full unit of change in RI in the thermoacidophileAcidianussp. DS80. The patterns in RI correlated with the normalized electron transfer rate between the electron donor and acceptor and did not always align with thermodynamic predictions of energy yield. In light of this, we discuss other factors that may affect the kinetics of cellular energy metabolism: electron transfer chain (ETC) efficiency, location of ETC reaction components (cytoplasmicvs.extracellular), and the physical state of electron donors and acceptors (gasvs.solid). Furthermore, the assimilation of a more reduced form of carbon during heterotrophy appears to decrease the demand for reducing equivalents during lipid biosynthesis, resulting in lower RI. Together, these results point to the fundamental role of the cellular energy state in dictating GDGT cyclization, with those cells experiencing greater energy limitation synthesizing more cyclized GDGTs.
IMPORTANCE
Some archaea make unique membrane-spanning lipids with different numbers of five- or six-membered rings in the core structure, which modulate membrane fluidity and permeability. Changes in membrane core lipid composition reflect the fundamental adaptation strategies of archaea in response to stress, but multiple environmental and physiological factors may affect the needs for membrane fluidity and permeability. In this study, we tested howAcidianussp. DS80 changed its core lipid composition when grown with different electron donor/acceptor pairs. We show that changes in energy and carbon metabolisms significantly affected the relative abundance of rings in the core lipids of DS80. These observations highlight the need to better constrain metabolic parameters, in addition to environmental factors, which may influence changes in membrane physiology in Archaea. Such consideration would be particularly important for studying archaeal lipids from habitats that experience frequent environmental fluctuations and/or where metabolically diverse archaea thrive.
Li, Fangzhou; Li, Errui; Samanta, Krishanu; Zheng, Zhaoxi; Wu, Lianqian; Chen, Albert D.; Farha, Omar K.; Staples, Richard J.; Niu, Jia; Schmidt‐Rohr, Klaus; et al(
, Angewandte Chemie)
Abstract
Boron trifluoride (BF3) is a highly corrosive gas widely used in industry. Confining BF3in porous materials ensures safe and convenient handling and prevents its degradation. Hence, it is highly desired to develop porous materials with high adsorption capacity, high stability, and resistance to BF3corrosion. Herein, we designed and synthesized a Lewis basic single‐crystalline hydrogen‐bond crosslinked organic framework (HCOF‐50) for BF3storage and its application in catalysis. Specifically, we introduced self‐complementaryortho‐alkoxy‐benzamide hydrogen‐bonding moieties to direct the formation of highly organized hydrogen‐bonded networks, which were subsequently photo‐crosslinked to generate HCOFs. The HCOF‐50 features Lewis basic thioether linkages and electron‐rich pore surfaces for BF3uptake. As a result, HCOF‐50 shows a record‐high 14.2 mmol/g BF3uptake capacity. The BF3uptake in HCOF‐50 is reversible, leading to the slow release of BF3. We leveraged this property to reduce the undesirable chain transfer and termination in the cationic polymerization of vinyl ethers. Polymers with higher molecular weights and lower polydispersity were generated compared to those synthesized using BF3 ⋅ Et2O. The elucidation of the structure–property relationship, as provided by the single‐crystal X‐ray structures, combined with the high BF3uptake capacity and controlled sorption, highlights the molecular understanding of framework‐guest interactions in addressing contemporary challenges.
McCully, Alexandra L., and Spormann, Alfred M. Direct cathodic electron uptake coupled to sulfate reduction by Desulfovibrio ferrophilus IS5 biofilms. Environmental Microbiology 22.11 Web. doi:10.1111/1462-2920.15235.
McCully, Alexandra L., & Spormann, Alfred M. Direct cathodic electron uptake coupled to sulfate reduction by Desulfovibrio ferrophilus IS5 biofilms. Environmental Microbiology, 22 (11). https://doi.org/10.1111/1462-2920.15235
McCully, Alexandra L., and Spormann, Alfred M.
"Direct cathodic electron uptake coupled to sulfate reduction by Desulfovibrio ferrophilus IS5 biofilms". Environmental Microbiology 22 (11). Country unknown/Code not available: Wiley-Blackwell. https://doi.org/10.1111/1462-2920.15235.https://par.nsf.gov/biblio/10455261.
@article{osti_10455261,
place = {Country unknown/Code not available},
title = {Direct cathodic electron uptake coupled to sulfate reduction by Desulfovibrio ferrophilus IS5 biofilms},
url = {https://par.nsf.gov/biblio/10455261},
DOI = {10.1111/1462-2920.15235},
abstractNote = {Summary Direct electron uptake is emerging as a key process for electron transfer in anaerobic microbial communities, both between species and from extracellular sources, such as zero‐valent iron (Fe0) or cathodic surfaces. In this study, we investigated cathodic electron uptake by Fe0‐corrodingDesulfovibrio ferrophilusIS5 and showed that electron uptake is dependent on direct cell contact via a biofilm on the cathode surface rather than through secreted intermediates. Induction of cathodic electron uptake by lactate‐starvedD. ferrophilusIS5 cells resulted in the expression of all components necessary for electron uptake; however, protein synthesis was required for full biofilm formation. Notably, proteinase K treatment uncoupled electron uptake from biofilm formation, likely through proteolytic degradation of proteinaceous components of the electron uptake machinery. We also showed that cathodic electron uptake is dependent on SO42−reduction. The insensitivity of Fe0corrosion to proteinase K treatment suggests that electron uptake from a cathode might involve different mechanism(s) than those involved in Fe0corrosion.},
journal = {Environmental Microbiology},
volume = {22},
number = {11},
publisher = {Wiley-Blackwell},
author = {McCully, Alexandra L. and Spormann, Alfred M.},
}
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