From iron to bacterial electroconductive filaments: Exploring cytochrome diversity using Geobacter bacteria

Salgueiro, Carlos A.; Morgado, Leonor; Silva, Marta A.; Ferreira, Marisa R.; Fernandes, Tomás M.; Portela, Pilar C.

doi:10.1016/j.ccr.2021.214284

Cited by 28 publications

(14 citation statements)

References 179 publications

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“…The genome of G. sulfurreducens contains genes for over 100 putative c-type cytochromes, with more than 70 of those containing multiple heme-binding motifs (Ding et al 2008). These multiheme cytochromes have been the target of many studies into electron transfer in G. sulfurreducens , but only a few have been definitively linked to a precisely explained function (Salgueiro et al 2022). Even well-characterized cytochromes, such as the periplasmic cytochrome PpcA (Pessanha et al 2006) or the outer membrane complex OmcB (Liu et al 2015), are often known to participate in certain respiratory conditions, but their specific electron donor/acceptor are unknown.…”

Section: Introductionmentioning

confidence: 99%

Cytochrome expression shifts in Geobacter sulfurreducens to maximize energy conservation in response to changes in redox conditions

Howley

Krajmalnik‐Brown

Torres

2022

Preprint

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Previous studies have identified that Geobacter sulfurreducens has three different electron transfer pathways for respiration, and it switches between these pathways to adapt to the redox potential of its electron acceptor. However, only a small fraction of the electron carriers from each pathway have been identified. In this study, we combined electrochemical and gene expression data to identify electron carriers associated with each of the three pathways in the inner membrane, periplasm, outer membrane, and exterior of the cell. We demonstrate that it is not just the electron acceptor redox potential that controls pathway expression in G. sulfurreducens. Our method combining electrochemical modeling and transcriptomics could be adapted to better understand electron transport in other electroactive organisms with complex metabolisms.

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Section: Introductionmentioning

confidence: 99%

Cytochrome expression shifts in Geobacter sulfurreducens to maximize energy conservation in response to changes in redox conditions

Howley

Krajmalnik‐Brown

Torres

2022

Preprint

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“…The mechanism of electron transfer from extracellular cytochrome filaments to the interior of the cells in Geobacter is not well understood. However, a porin:cytochrome c conduit is always expressed under the same conditions as a cytochrome c containing filament in Geobacter (omcS along with extEFG or omcABC under Fe (III) oxide reducing conditions and omcZ along with extABCD during growth on an electrode[53]) and in ANME-SRB consortia (OmcS/OmcX with OetABI or OmcKL). These findings suggest that each cytochrome c filament could act in concert with a porin:cytochrome c conduit ( Figure 2 ) to transfer electrons from the extracellular space to the periplasm.…”

Section: Resultsmentioning

confidence: 99%

Physiological adaptation of sulfate reducing bacteria in syntrophic partnership with anaerobic methanotrophic archaea

Murali

Speth

et al. 2022

Preprint

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Sulfate-coupled anaerobic oxidation of methane (AOM) is performed by multicellular consortia of anaerobic methanotrophic archaea (ANME) in obligate syntrophic partnership with sulfate-reducing bacteria (SRB). Diverse ANME and SRB clades co-associate but the physiological basis for their adaptation and diversification is not well understood. In this work, we explore the metabolic adaptation of four syntrophic SRB clades (HotSeep-1, Seep-SRB2, Seep-SRB1a and Seep-SRB1g) from a phylogenomics perspective, tracing the evolution of conserved proteins in the syntrophic SRB clades, and comparing the genomes of syntrophic SRB to their nearest evolutionary neighbors in the phylum Desulfobacterota. We note several examples of gain, loss or biochemical adaptation of proteins within pathways involved in extracellular electron transfer, electron transport chain, nutrient sharing, biofilm formation and cell adhesion. We demonstrate that the metabolic adaptations in each of these syntrophic clades are unique, suggesting that they have independently evolved, converging to a syntrophic partnership with ANME. Within the clades we also investigated the specialization of different syntrophic SRB species to partnerships with different ANME clades, using metagenomic sequences obtained from ANME and SRB partners in individual consortia after fluorescent-sorting of cell aggregates from anaerobic sediments. In one instance of metabolic adaptation to different partnerships, we show that Seep-SRB1a partners of ANME-2c appear to lack nutritional auxotrophies, while the related Seep-SRB1a partners of a different methanotrophic archaeal lineage, ANME-2a, are missing the cobalamin synthesis pathway, suggesting that the Seep-SRB1a partners of ANME-2a may have a nutritional dependence on its partner. Together, our paired genomic analysis of AOM consortia highlights the specific adaptation and diversification of syntrophic SRB clades linked to their associated ANME lineages.

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“…The evaluation of the electron transfer processes performed by the MC involved in EET pathways requires the production of the proteins in sufficient amounts for their characterization, that typically includes the 3D-structure determination and elucidation of their thermodynamic and kinetics properties [21,22]. Although this is not sufficient to elucidate the role of the protein in the EET process, that commonly requires knock-out approaches and in vivo studies [19], it enables to unravel their electron transfer processes and understand their mode of action.…”

Section: Redox Properties Of MC Involved In Eetmentioning

confidence: 99%

“…MC contain several heme cofactors that are covalently bound to the polypeptide chain. This enables a close proximity of the hemes, necessary to modulate the thermodynamic properties of the redox protein and define its functional role [21,22]. This review will focus on the MC that participate in the EET pathway of electroactive organisms, in particular on those for which a detailed thermodynamic characterization exists.…”

Section: Introductionmentioning

confidence: 99%

Molecular Mechanisms of Microbial Extracellular Electron Transfer: The Importance of Multiheme Cytochromes

Paquete¹,

Morgado²,

Salgueiro³

et al. 2022

Front. Biosci. (Landmark Ed)

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Extracellular electron transfer is a key metabolic process of many organisms that enables them to exchange electrons with extracellular electron donors/acceptors. The discovery of organisms with these abilities and the understanding of their electron transfer processes has become a priority for the scientific and industrial community, given the growing interest on the use of these organisms in sustainable biotechnological processes. For example, in bioelectrochemical systems electrochemical active organisms can exchange electrons with an electrode, allowing the production of energy and added-value compounds, among other processes. In these systems, electrochemical active organisms exchange electrons with an electrode through direct or indirect mechanisms, using, in most cases, multiheme cytochromes. In numerous electroactive organisms, these proteins form a conductive pathway that allows electrons produced from cellular metabolism to be transferred across the cell surface for the reduction of an electrode, or vice-versa. Here, the mechanisms by which the most promising electroactive bacteria perform extracellular electron transfer will be reviewed, emphasizing the proteins involved in these pathways. The ability of some of the organisms to perform bidirectional electron transfer and the pathways used will also be highlighted.

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From iron to bacterial electroconductive filaments: Exploring cytochrome diversity using Geobacter bacteria

Cited by 28 publications

References 179 publications

Cytochrome expression shifts in Geobacter sulfurreducens to maximize energy conservation in response to changes in redox conditions

Cytochrome expression shifts in Geobacter sulfurreducens to maximize energy conservation in response to changes in redox conditions

Physiological adaptation of sulfate reducing bacteria in syntrophic partnership with anaerobic methanotrophic archaea

Molecular Mechanisms of Microbial Extracellular Electron Transfer: The Importance of Multiheme Cytochromes

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