A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA
Summary The multi‐heme, outer membrane c‐type cytochrome (c‐Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In G. sulfurreducens, the omcB gene is part of two tandem...
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| Published in | Environmental microbiology reports Vol. 6; no. 6; pp. 776 - 785 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Blackwell Publishing Ltd
01.12.2014
John Wiley & Sons, Inc Wiley-Blackwell BlackWell Publishing Ltd |
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| Online Access | Get full text |
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| Abstract | Summary
The multi‐heme, outer membrane c‐type cytochrome (c‐Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In G. sulfurreducens, the omcB gene is part of two tandem four‐gene clusters, each is predicted to encode a transcriptional factor (OrfR/OrfS), a porin‐like outer membrane protein (OmbB/OmbC), a periplasmic c‐type cytochrome (OmaB/OmaC) and an outer membrane c‐Cyt (OmcB/OmcC) respectively. Here, we showed that OmbB/OmbC, OmaB/OmaC and OmcB/OmcC of G. sulfurreducens PCA formed the porin‐cytochrome (Pcc) protein complexes, which were involved in transferring electrons across the outer membrane. The isolated Pcc protein complexes reconstituted in proteoliposomes transferred electrons from reduced methyl viologen across the lipid bilayer of liposomes to Fe(III)‐citrate and ferrihydrite. The pcc clusters were found in all eight sequenced Geobacter and 11 other bacterial genomes from six different phyla, demonstrating a widespread distribution of Pcc protein complexes in phylogenetically diverse bacteria. Deletion of ombB‐omaB‐omcB‐orfS‐ombC‐omaC‐omcC gene clusters had no impact on the growth of G. sulfurreducens PCA with fumarate but diminished the ability of G. sulfurreducens PCA to reduce Fe(III)‐citrate and ferrihydrite. Complementation with the ombB‐omaB‐omcB gene cluster restored the ability of G. sulfurreducens PCA to reduce Fe(III)‐citrate and ferrihydrite. |
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| AbstractList | The multi-heme, outer membrane
c
-type cytochrome (
c
-Cyt) OmcB of
G
eobacter sulfurreducens
was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In
G
. sulfurreducens
, the
omcB
gene is part of two tandem four-gene clusters, each is predicted to encode a transcriptional factor (OrfR/OrfS), a porin-like outer membrane protein (OmbB/OmbC), a periplasmic
c-
type cytochrome (OmaB/OmaC) and an outer membrane
c
-Cyt (OmcB/OmcC) respectively. Here, we showed that OmbB/OmbC, OmaB/OmaC and OmcB/OmcC of
G
. sulfurreducens
PCA formed the porin-cytochrome (Pcc) protein complexes, which were involved in transferring electrons across the outer membrane. The isolated Pcc protein complexes reconstituted in proteoliposomes transferred electrons from reduced methyl viologen across the lipid bilayer of liposomes to Fe(III)-citrate and ferrihydrite. The
pcc
clusters were found in all eight sequenced
G
eobacter
and 11 other bacterial genomes from six different phyla, demonstrating a widespread distribution of Pcc protein complexes in phylogenetically diverse bacteria. Deletion of
ombB-omaB-omcB-orfS-ombC-omaC-omcC
gene clusters had no impact on the growth of
G
. sulfurreducens
PCA with fumarate but diminished the ability of
G
. sulfurreducens
PCA to reduce Fe(III)-citrate and ferrihydrite. Complementation with the
ombB-omaB-omcB
gene cluster restored the ability of
G
. sulfurreducens
PCA to reduce Fe(III)-citrate and ferrihydrite. The multi-heme, outer membrane c-type cytochrome (c-Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In G. sulfurreducens, the omcB gene is part of two tandem four-gene clusters, each is predicted to encode a transcriptional factor (OrfR/OrfS), a porin-like outer membrane protein (OmbB/OmbC), a periplasmic c-type cytochrome (OmaB/OmaC) and an outer membrane c-Cyt (OmcB/OmcC) respectively. Here, we showed that OmbB/OmbC, OmaB/OmaC and OmcB/OmcC of G. sulfurreducens PCA formed the porin-cytochrome (Pcc) protein complexes, which were involved in transferring electrons across the outer membrane. The isolated Pcc protein complexes reconstituted in proteoliposomes transferred electrons from reduced methyl viologen across the lipid bilayer of liposomes to Fe(III)-citrate and ferrihydrite. The pcc clusters were found in all eight sequenced Geobacter and 11 other bacterial genomes from six different phyla, demonstrating a widespread distribution of Pcc protein complexes in phylogenetically diverse bacteria. Deletion of ombB-omaB-omcB-orfS-ombC-omaC-omcC gene clusters had no impact on the growth of G. sulfurreducens PCA with fumarate but diminished the ability of G. sulfurreducens PCA to reduce Fe(III)-citrate and ferrihydrite. Complementation with the ombB-omaB-omcB gene cluster restored the ability of G. sulfurreducens PCA to reduce Fe(III)-citrate and ferrihydrite. Summary The multi‐heme, outer membrane c‐type cytochrome (c‐Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In G. sulfurreducens, the omcB gene is part of two tandem four‐gene clusters, each is predicted to encode a transcriptional factor (OrfR/OrfS), a porin‐like outer membrane protein (OmbB/OmbC), a periplasmic c‐type cytochrome (OmaB/OmaC) and an outer membrane c‐Cyt (OmcB/OmcC) respectively. Here, we showed that OmbB/OmbC, OmaB/OmaC and OmcB/OmcC of G. sulfurreducens PCA formed the porin‐cytochrome (Pcc) protein complexes, which were involved in transferring electrons across the outer membrane. The isolated Pcc protein complexes reconstituted in proteoliposomes transferred electrons from reduced methyl viologen across the lipid bilayer of liposomes to Fe(III)‐citrate and ferrihydrite. The pcc clusters were found in all eight sequenced Geobacter and 11 other bacterial genomes from six different phyla, demonstrating a widespread distribution of Pcc protein complexes in phylogenetically diverse bacteria. Deletion of ombB‐omaB‐omcB‐orfS‐ombC‐omaC‐omcC gene clusters had no impact on the growth of G. sulfurreducens PCA with fumarate but diminished the ability of G. sulfurreducens PCA to reduce Fe(III)‐citrate and ferrihydrite. Complementation with the ombB‐omaB‐omcB gene cluster restored the ability of G. sulfurreducens PCA to reduce Fe(III)‐citrate and ferrihydrite. The multiheme, outer membrane c-type cytochrome (c-Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In G. sulfurreducens, the omcB gene is part of two tandem four-gene clusters, each is predicted to encode a transcriptional factor (OrfR/OrfS), a porin-like outer membrane protein (OmbB/OmbC), a periplasmic c-type cytochrome (OmaB/OmaC), and an outer membrane c-Cyt (OmcB/OmcC), respectively. Here we showed that OmbB/OmbC, OmaB/OmaC and OmcB/OmcC of G. sulfurreducens PCA formed the porin-cytochrome (Pcc) protein complexes, which were involved in transferring electrons across the outer membrane. The isolated Pcc protein complexes reconstituted in proteoliposomes transferred electrons from reduced methyl viologen across the lipid bilayer of liposomes to Fe(III)-citrate and ferrihydrite. The pcc clusters were found in all eight sequenced Geobacter and 11 other bacterial genomes from six different phyla, demonstrating a widespread distribution of Pcc protein complexes in phylogenetically diverse bacteria. Deletion of ombB-omaB-omcB-orfS-ombC-omaC-omcC gene clusters had no impact on the growth of G. sulfurreducens PCA with fumarate, but diminished the ability of G. sulfurreducens PCA to reduce Fe(III)-citrate and ferrihydrite. Finally, complementation with the ombB-omaB-omcB gene cluster restored the ability of G. sulfurreducens PCA to reduce Fe(III)-citrate and ferrihydrite. |
| Author | Shi, Zhi Bond, Daniel R. Liu, Juan Edwards, Marcus J. Wang, Zheming Kennedy, David W. Richardson, David J. Babauta, Jerome T. Clarke, Thomas A. Zachara, John M Rosso, Kevin M. Shi, Liang Beyenal, Haluk Fredrickson, James K. Liu, Yimo Levar, Caleb Butt, Julea N. |
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| Notes | istex:E91E84E0F5DF1DE50556363CD819CA2046003658 Pacific Northwest National Laboratory (PNNL) Scientific Focus Area U.S. Department of Energy (DOE) Genome Science Program (GSP) - No. DE-SC0007229 Subsurface Biogeochemical Research program (SBR) Office of Biological and Environmental Research (BER) Fig. S1. The amino acid sequence of OmbB/OmbC. The N-terminus and predicted short solvent-exposed loops are in green, the predicted trans-outer membrane motifs are in red, and predicted long solvent-exposed loops are in blue. The 20 trans-outer membrane motifs are numbered sequentially, and the numbers are displayed in black and above the polypeptide sequence. Fig. S2. Mass spectrometry confirmation of OmbB/OmbC proteins. OmbB/OmbC amino acid sequence with peptides identified by tryptic digest MALDI mass spectrometry are highlighted in red (sequence coverage 22%). Observed peaks and corresponding peptides of OmbB/OmbC are detailed in Table S1. Fig. S3. Verification of gene cluster replacement mutants and related complement strain by heme staining after SDS-PAGE. A. The gene cluster replacement mutants. Lane 1, ΔombB-omaB-omcB; lane 2, ΔombC-omaC-omcC; lane 3, ΔombB-omaB-omcB-orfS-ombC-omaC-omcC. B. Complement strain of ΔombB-omaB-omcB-orfS-ombC-omaC-omcC with ombB-omaB-omcB. G. sulfurreducens PCA cells were used as a positive control. OmaB/OmaC and OmcB/OmcC are indicated. About 104 CFU were loaded in each lane. Fig. S4. Characterization of OmaB/OmaC- or OmcB/OmcC-specific antibodies. A. OmaB/OmaC-specific antibodies. B. OmcB/OmcC-specific antibodies. Migration positions of the proteins standards (kDa) are indicated. Affinity purified OmaBC-specific antibodies were used at 1: 10 000 dilutions; while affinity purified OmcBC-specific antibodies were used at 1: 20 000 dilutions. About 104 CFU were loaded in each lane. Lane 1, G. sulfurreducens PCA; lane 2, ΔombB-omaB-omcB-orfS-ombC-omaC-omcC. Table S1. Identified peptide sequences of OmbB/OmbC by mass spectrometry. Table S2. Identified bacterial Pcc homologuesa. Table S3. Bacterial strains, plasmids, primers and polypeptides used in this study. BER ark:/67375/WNG-9S0X4VLH-9 ArticleID:EMI412204 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 PNNL-SA-104799 USDOE Office of Science (SC), Biological and Environmental Research (BER) AC05-76RL01830; SC0007229 |
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The multi‐heme, outer membrane c‐type cytochrome (c‐Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across... The multi-heme, outer membrane c-type cytochrome (c-Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer... The multi‐heme, outer membrane c‐type cytochrome (c‐Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer... The multiheme, outer membrane c-type cytochrome (c-Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer... The multi-heme, outer membrane c -type cytochrome ( c -Cyt) OmcB of G eobacter sulfurreducens was previously proposed to mediate electron transfer across the... |
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| SubjectTerms | Amino acids Bacteria Bacterial Outer Membrane Proteins - genetics Bacterial Outer Membrane Proteins - metabolism Bacterial Proteins - genetics Bacterial Proteins - metabolism BASIC BIOLOGICAL SCIENCES Brief Reports Citric acid Complementation Cytochrome Cytochromes Cytochromes c - genetics Cytochromes c - metabolism Electron transfer Electron Transport Electrons element cycles and biogeochemical processes Gene clusters Gene deletion Genomes Geobacter - genetics Geobacter - metabolism Geobacter sulfurreducens Gram-negative bacteria Hypotheses Iron Lipid bilayers Lipids Membranes metals Methyl viologen Multigene Family Nanowires OmcB gene Oxidation Oxidation-Reduction Phylogeny Porins - genetics Porins - metabolism Protein Binding Proteins |
| Title | A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA |
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