Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens

LLOYD, Jon R.; LEANG, Ching; MYERSON, Allison L. HODGES; COPPI, Maddalena V.; CUIFO, Stacey; METHE, Barb; SANDLER, Steven J.; LOVLEY, Derek R.

doi:10.1042/bj20020597

Cited by 373Microbial Fuel Cells and BioremediationMetalloenzymes and iron-sulfur proteinsMicrobial metabolism and enzyme function

Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens

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LLOYD, Jon R., LEANG, Ching, MYERSON, Allison L. HODGES, COPPI, Maddalena V., CUIFO, Stacey, METHE, Barb, SANDLER, Steven J., LOVLEY, Derek R.·2003·Biochemical Journal

DOI 10.1042/bj20020597PMC PMC1223068

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Abstract

A 9.6kDa periplasmic c-type cytochrome, designated PpcA, was purified from the Fe(III)-reducing bacterium Geobacter sulfurreducens and characterized. The purified protein is basic (pI 9.5), contains three haems and has an N-terminal amino acid sequence closely related to those of the previously described trihaem c7 cytochromes of Geobacter metallireducens and Desulfuromonas acetoxidans. The gene encoding PpcA was identified from the G. sulfurreducens genome using the N-terminal sequence, and encodes a protein of 71 amino acids (molecular mass 9.58kDa) with 49% identity to the c7 cytochrome of D. acetoxidans. In order to determine the physiological role of PpcA, a knockout mutant was prepared with a single-step recombination method. Acetate-dependent Fe(III) reduction was significantly inhibited in both growing cultures and cell suspensions of the mutant. When ppcA was expressed in trans, the full capacity for Fe(III) reduction with acetate was restored. The transfer of electrons from acetate to anthraquinone 2,6-disulphonate (AQDS; a humic acid analogue) and to U(VI) was also compromised in the mutant, but acetate-dependent reduction of fumarate was not altered. The rates of reduction of Fe(III), AQDS, U(VI) and fumarate were also the same in the wild type and ppcA mutant when hydrogen was supplied as the electron donor. When taken together with previous studies on other electron transport proteins in G. sulfurreducens, these results suggest that PpcA serves as an intermediary electron carrier from acetate to terminal Fe(III) reductases in the outer membrane, and is also involved in the transfer of electrons from acetate to U(VI) and humics.

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The PpcA protein was able to reduce U(VI) in vitro, while a ppcA deletion mutant supplied with acetate as an electron donor had lower activity against U(VI).
“The protein was able to reduce U(VI) in vitro, while a ppcA deletion mutant supplied with acetate as an electron donor had lower activity against U(VI) [42].”
From Microbial reduction of metals and radionuclides (2003) · cites this paper as [42]
The Physiological role of PpcA section reports that deleting ppcA inhibited U(VI) reduction in cell suspensions when acetate was the electron donor. But the Role of PpcA in the reduction of U(VI) and humics section treats direct U(VI) reduction by PpcA as a possibility, not an established result; our copy does not report an in-vitro demonstration that the purified protein reduces U(VI). Page numbers were not available in the indexed passages. (LLM, conf=0.88)
Experimental — accuracy not yet measured
More recent studies have identified a homologous cytochrome (PpcA), a trihaem periplasmic cytochrome c7 of G. sulfurreducens that may also play a role in U(VI) reduction.
“More recent studies have identi¢ed a homologous cytochrome (PpcA), a trihaem periplasmic cytochrome c 7 of the Fe(III)-reducing bacterium G. sulfurreducens that may also play a role in U(VI) reduction [42].”
From Microbial reduction of metals and radionuclides (2003) · cites this paper as [42]

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Growth of Geobacter sulfurreducens under nutrient‐limiting conditions in continuous culture
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A trans‐outer membrane porin‐cytochrome protein complex for extracellular electron transfer by G eobacter sulfurreducens PCA
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Lack of cytochrome involvement in long-range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens
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Transcriptomic and Genetic Analysis of Direct Interspecies Electron Transfer
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Microbial Community Composition Is Unaffected by Anode Potential
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Linking Spectral and Electrochemical Analysis to Monitor c‐type Cytochrome Redox Status in Living Geobacter sulfurreducens Biofilms
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XAS and XMCD Evidence for Species-Dependent Partitioning of Arsenic During Microbial Reduction of Ferrihydrite to Magnetite
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Performance improvement of microbial fuel cell (MFC) using suitable electrode and Bioengineered organisms: A review
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Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens
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Geobacter sulfurreducens biofilms developed under different growth conditions on glassy carbon electrodes: insights using cyclic voltammetry
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Cytochromes in Extracellular Electron Transfer in Geobacter
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An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
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A New Insight into Potential Regulation on Growth and Power Generation of Geobacter sulfurreducens in Microbial Fuel Cells Based on Energy Viewpoint
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Radiation-resistant extremophiles and their potential in biotechnology and therapeutics
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Role ofGeobacter sulfurreducensOuter Surfacec-Type Cytochromes in Reduction of Soil Humic Acid and Anthraquinone-2,6-Disulfonate
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OmcF, a Putative c -Type Monoheme Outer Membrane Cytochrome Required for the Expression of Other Outer Membrane Cytochromes in Geobacter sulfurreducens
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The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions
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Formation of Nanoscale Elemental Silver Particles via Enzymatic Reduction by Geobacter sulfurreducens
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The Genome Sequence of Geobacter Metallireducens: Features of Metabolism, Physiology and Regulation Common and Dissimilar to Geobacter Sulfurreducens
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Bioremediation: a genuine technology to remediate radionuclides from the environment
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Diving into the redox properties of Geobacter sulfurreducens cytochromes: a model for extracellular electron transfer
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Microtoming coupled to microarray analysis to evaluate the spatial metabolic status of Geobacter sulfurreducens biofilms
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The Genetics of Geochemistry
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The electrifying physiology of Geobacter bacteria, 30 years on
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Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity
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Harnessing the Extracellular Bacterial Production of Nanoscale Cobalt Ferrite with Exploitable Magnetic Properties
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Surface-Enhanced Raman Scattering from Intracellular and Extracellular Bacterial Locations
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Set potential regulation reveals additional oxidation peaks of Geobacter sulfurreducens anodic biofilms
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Biosynthesis of Zinc Substituted Magnetite Nanoparticles with Enhanced Magnetic Properties
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MacA, a Diheme c -Type Cytochrome Involved in Fe(III) Reduction by Geobacter sulfurreducens
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Engineering and kinetic aspects of bacterial uranium reduction for the remediation of uranium contaminated environments
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Biofilm Biology and Engineering of Geobacter and Shewanella spp. for Energy Applications
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Biotechnological Application of Metal-reducing Microorganisms
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Engineering Wired Life: Synthetic Biology for Electroactive Bacteria
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The Low Conductivity of Geobacter uraniireducens Pili Suggests a Diversity of Extracellular Electron Transfer Mechanisms in the Genus Geobacter
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Outer Cell Surface Components Essential for Fe(III) Oxide Reduction by Geobacter metallireducens
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Metabolic versatility of toluene‐degrading, iron‐reducing bacteria in tidal flat sediment, characterized by stable isotope probing‐based metagenomic analysis
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Optimizing Cr(VI) and Tc(VII) Remediation through Nanoscale Biomineral Engineering
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Evidence that OmcB and OmpB ofGeobacter sulfurreducensare outer membrane surface proteins
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A c‐type cytochrome and a transcriptional regulator responsible for enhanced extracellular electron transfer in Geobacter sulfurreducens revealed by adaptive evolution
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Identification of an Uptake Hydrogenase Required for Hydrogen-Dependent Reduction of Fe(III) and Other Electron Acceptors by Geobacter sulfurreducens
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Insights into genes involved in electricity generation in Geobacter sulfurreducens via whole genome microarray analysis of the OmcF-deficient mutant
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A putative multicopper protein secreted by an atypical type II secretion system involved in the reduction of insoluble electron acceptors in Geobacter sulfurreducens
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Comparative metatranscriptomics reveals extracellular electron transfer pathways conferring microbial adaptivity to surface redox potential changes
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Genetic Characterization of a Single Bifunctional Enzyme for Fumarate Reduction and Succinate Oxidation in Geobacter sulfurreducens and Engineering of Fumarate Reduction in Geobacter metallireducens
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Adaptation to Disruption of the Electron Transfer Pathway for Fe(III) Reduction in Geobacter sulfurreducens
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Genes for two multicopper proteins required for Fe(III) oxide reduction in Geobacter sulfurreducens have different expression patterns both in the subsurface and on energy-harvesting electrodes
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Biogenic nano-magnetite and nano-zero valent iron treatment of alkaline Cr(VI) leachate and chromite ore processing residue
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Harnessing the Extracellular Electron Transfer Capability of Geobacter sulfurreducens for Ambient Synthesis of Stable Bifunctional Single‐Atom Electrocatalyst for Water Splitting
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Biotechnological Application of Metal Reducing Microorganisms
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Lack of Specificity in Geobacter Periplasmic Electron Transfer
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Thermodynamic and functional characterization of the periplasmic triheme cytochrome PpcA from Geobacter metallireducens
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Authors: LLOYD, J. R., LEANG, C., MYERSON, A. L. H., COPPI, M. V., CUIFO, S., METHE, B., SANDLER, S. J., & LOVLEY, D. R.
Affiliations: Department of Microbiology, University of Massachusetts, Amherst, MA 01003, U.S.A.
University of Massachusetts Amherst (US)
ORCID: LEANG, Ching
SANDLER, Steven J.
LOVLEY, Derek R.
Venue: Biochemical Journal
Publisher: Portland Press Ltd.
Published: 2003-01-01
Volume: 369
Issue: 1
Pages: 153-161
ISSN: 0264-6021 (ISSN-L)
1470-8728
DOI: 10.1042/bj20020597
PMC: PMC1223068
OpenAlex: W2137755540
Cited by: 373
References: 54
Citations by year: 2026: 6 · 2025: 9 · 2024: 11 · 2023: 20 · 2022: 10 · 2021: 22 · 2020: 15 · 2019: 12 · 2018: 22 · 2017: 15 · 2016: 13 · 2015: 14 · 2014: 20 · 2013: 21 · 2012: 19
FWCI: 19.86
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Biochemical Journal (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
ScholarWorks@UMassAmherst (University of Massachusetts Amherst) (submittedVersion)
Research Explorer (The University of Manchester) (submittedVersion)
Scholarworks (University of Massachusetts Amherst) (submittedVersion)
Funders: National Science Foundation (9727840)
U.S. Department of Energy (DE‐FG02‐, FG0299ER62867)
Topics: Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
Keywords: PpcA, Geobacter sulfurreducens, uranium(VI) reduction, electron transfer, knockout mutants, fumarate reduction
MeSH terms: Amino Acid Sequence, Base Sequence, Cytochrome c Group, DNA, Bacterial, Molecular Sequence Data, Sequence Homology, Amino Acid, Periplasm, Proteobacteria

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Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens

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