skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Molecular interactions between Geobacter sulfurreducens triheme cytochromes and the redox active analogue for humic substances

Journal Article · · Biochimica et Biophysica Acta - Bioenergetics
; ; ; ; ;

We report the bacterium Geobacter sulfurreducens can transfer electrons to quinone moieties of humic substances or to anthraquinone-2,6-disulfonate (AQDS), a model for the humic acids. The reduced form of AQDS (AH2QDS) can also be used as energy source by G. sulfurreducens. Such bidirectional utilization of humic substances confers competitive advantages to these bacteria in Fe(III) enriched environments. Previous studies have shown that the triheme cytochrome PpcA from G. sulfurreducens has a bifunctional behavior toward the humic substance analogue. It can reduce AQDS but the protein can also be reduced by AH2QDS. Using stopped-flow kinetic measurements we were able to demonstrate that other periplasmic members of the PpcA-family in G. sulfurreducens (PpcB, PpcD and PpcE) also showed the same behavior. The extent of the electron transfer is thermodynamically controlled favoring the reduction of the cytochromes. NMR spectra recorded for 13C,15N-enriched samples in the presence increasing amounts of AQDS showed perturbations in the chemical shift signals of the cytochromes. The chemical shift perturbations on cytochromes backbone NH and 1H heme methyl signals were used to map their interaction regions with AQDS, showing that each protein forms a low-affinity binding complex through well-defined positive surface regions in the vicinity of heme IV (PpcB, PpcD and PpcE) and I (PpcE). Docking calculations performed using NMR chemical shift perturbations allowed modeling the interactions between AQDS and each cytochrome at a molecular level. In conclusion, the results obtained provided important structural-functional relationships to rationalize the microbial respiration of humic substances in G. sulfurreducens.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; Fundacao para a Ciencia ea Tecnologia of Portugal
Grant/Contract Number:
POCI-01-0145-FEDER-007728; RECI/BBB-BQB/0230/2012; SFRH/BD/89701/2012; UID/Multi/04378/2013; MRF; SFRH/BD/132969/2017; AC02-06CH11357
OSTI ID:
1579374
Alternate ID(s):
OSTI ID: 1465730
Journal Information:
Biochimica et Biophysica Acta - Bioenergetics, Journal Name: Biochimica et Biophysica Acta - Bioenergetics Vol. 1859 Journal Issue: 8; ISSN 0005-2728
Publisher:
ElsevierCopyright Statement
Country of Publication:
Netherlands
Language:
English
Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

References (58)

Reduction of low potential electron acceptors requires the CbcL inner membrane cytochrome of Geobacter sulfurreducens journal February 2016
Computer Review of ChemDraw Ultra 12.0 ChemDraw Ultra 12.0 . CambridgeSoft , 100 Cambridge Park Drive, Cambridge, MA 02140 . www.cambridgesoft.com . See Web site for full pricing information. journal June 2011
Evidence for interaction between the triheme cytochrome PpcA from Geobacter sulfurreducens and anthrahydroquinone-2,6-disulfonate, an analog of the redox active components of humic substances journal June 2014
Molecular interactions between Geobacter sulfurreducens triheme cytochromes and the electron acceptor Fe( iii ) citrate studied by NMR journal January 2017
Overproduction of theBradyrhizobium japonicum c-Type Cytochrome Subunits of thecbb3Oxidase inEscherichia coli journal October 1998
Structural insights into the modulation of the redox properties of two Geobacter sulfurreducens homologous triheme cytochromes journal September 2008
φ Angle Restraints in Protein Backbones from Dipole−Dipole Cross-Correlation between 1 H N − 15 N and 1 H N − 1 H α Vectors journal March 2000
Protective Role of tolC in Efflux of the Electron Shuttle Anthraquinone-2,6-Disulfonate journal March 2002
Diving into the redox properties of Geobacter sulfurreducens cytochromes: a model for extracellular electron transfer journal January 2015
1H, 13C and 15N chemical shift referencing in biomolecular NMR journal September 1995
Humic substances as electron acceptors for microbial respiration journal August 1996
Shewanella oneidensis MR-1 Uses Overlapping Pathways for Iron Reduction at a Distance and by Direct Contact under Conditions Relevant for Biofilms journal August 2005
Dynamics in electron transfer protein complexes: Dynamics in electron transfer protein complexes journal March 2011
Estimation of Uptake of Humic Substances from Different Sources by Escherichia coli Cells under Optimum and Salt Stress Conditions by Use of Tritium-Labeled Humic Materials journal July 2010
Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor journal December 2008
Electricity Production by Geobacter sulfurreducens Attached to Electrodes journal March 2003
The humic acid analogue antraquinone-2,6-disulfonate (AQDS) serves as an electron shuttle in the electricity-driven microbial dechlorination of trichloroethene to cis-dichloroethene journal December 2010
Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens journal February 2011
Outer-membrane cytochrome-independent reduction of extracellular electron acceptors in Shewanella oneidensis journal April 2012
Nomenclature of tetrapyrroles. Recommendations 1986 journal December 1988
Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens journal April 2011
Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity journal July 2010
Structural characterization of a family of cytochromes c7 involved in Fe(III) respiration by Geobacter sulfurreducens journal February 2010
Revealing the structural origin of the redox-Bohr effect: the first solution structure of a cytochrome from Geobacter sulfurreducens journal December 2011
The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions journal July 2006
Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances journal October 2015
Redox properties of standard humic acids journal August 2001
In situ to in silico and back: elucidating the physiology and ecology of Geobacter spp. using genome-scale modelling journal December 2010
Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments journal September 2002
Purification and Characterization of OmcZ, an Outer-Surface, Octaheme c-Type Cytochrome Essential for Optimal Current Production by Geobacter sulfurreducens journal April 2010
Humics as an electron donor for anaerobic respiration journal February 1999
Sequential application of electron donors and humic acids for the anaerobic bioremediation of chlorinated aliphatic hydrocarbons journal December 2011
Microbial Biofilm Voltammetry: Direct Electrochemical Characterization of Catalytic Electrode-Attached Biofilms journal October 2008
Biotransformation products and mineralization potential for hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) in abiotic versus biological degradation pathways with anthraquinone-2,6-disulfonate (AQDS) and Geobacter metallireducens journal February 2008
Remediation and Recovery of Uranium from Contaminated Subsurface Environments with Electrodes journal November 2005
The acceptor specificity of flavins and flavoproteins. I. Techniques for anaerobic spectrophotometry journal March 1971
MtrB Is Required for Proper Incorporation of the Cytochromes OmcA and OmcB into the Outer Membrane of Shewanella putrefaciens MR-1 journal November 2002
Transient protein–protein interactions visualized by solution NMR journal January 2016
Effect of iron(III), humic acids and anthraquinone-2,6-disulfonate on biodegradation of cyclic nitramines by Clostridium sp. EDB2 journal March 2006
Orientation of the axial ligands and magnetic properties of the hemes in the cytochrome c7 family from Geobacter sulfurreducens determined by paramagnetic NMR journal January 2011
Complexes of Photosynthetic Redox Proteins Studied by NMR journal January 2004
Mechanisms for Fe(III) Oxide Reduction in Sedimentary Environments journal March 2002
The HADDOCK2.2 Web Server: User-Friendly Integrative Modeling of Biomolecular Complexes journal February 2016
Insights into genes involved in electricity generation in Geobacter sulfurreducens via whole genome microarray analysis of the OmcF-deficient mutant journal June 2008
An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors journal November 2014
Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction journal October 2006
Humic Substances as a Mediator for Microbially Catalyzed Metal Reduction journal May 1998
Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens journal January 2013
Rational engineering of Geobacter sulfurreducens electron transfer components: a foundation for building improved Geobacter-based bioelectrochemical technologies journal July 2015
Dissimilatory Fe(III) and Mn(IV) Reduction book January 2004
Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens journal January 2003
Isotopic labeling of c-type multiheme cytochromes overexpressed in E. coli journal May 2008
Enhanced anaerobic transformations of carbon tetrachloride by soil organic matter journal December 1999
Linking Spectral and Electrochemical Analysis to Monitor c-type Cytochrome Redox Status in Living Geobacter sulfurreducens Biofilms journal June 2011
The roles of natural organic matter in chemical and microbial reduction of ferric iron journal May 2003
Electrochemical characterization ofGeobacter sulfurreducens cells immobilized on graphite paper electrodes journal January 2008
Role of Geobacter sulfurreducens Outer Surface c-Type Cytochromes in Reduction of Soil Humic Acid and Anthraquinone-2,6-Disulfonate journal February 2010
Combined chemical shift changes and amino acid specific chemical shift mapping of protein–protein interactions journal October 2007

Figures / Tables (15)

Table 1(p. 27)table Table 1
Table 2(p. 28)table Table 2
Table 3(p. 29)table Table 3
Table 4(p. 29)table Table 4
Figure 1(p. 32)figure Figure 1
Figure 2(p. 33)figure Figure 2
Figure 2 (Continued)(p. 34)figure Figure 2 (Continued)
Figure 2 (Continued)(p. 35)figure Figure 2 (Continued)
Figure 3(p. 36)figure Figure 3
Figure 4(p. 37)figure Figure 4
FIGURE 5(p. 38)figure FIGURE 5
FIGURE 6(p. 39)figure FIGURE 6
Supplementary Table(p. 40)figure Supplementary Table
Figure S1(p. 41)figure Figure S1
Figure S2(p. 42)figure Figure S2

Similar Records

Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances
Journal Article · Thu Oct 01 00:00:00 EDT 2015 · Biochimica et Biophysica Acta - Bioenergetics · OSTI ID:1579374
+1 more
Unveiling the Structural Basis That Regulates the Energy Transduction Properties within a Family of Triheme Cytochromes from Geobacter sulfurreducens
Journal Article · Thu Oct 06 00:00:00 EDT 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1579374
+6 more
Unveiling the Structural Basis That Regulates the Energy Transduction Properties within a Family of Triheme Cytochromes from Geobacter sulfurreducens
Journal Article · Tue Sep 27 00:00:00 EDT 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1579374
+6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Geobacter
Humic substances
AQDS
Multiheme cytochromes
NMR
Electron transfer