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Homology modeling of dissimilatory APS reductases (AprBA) of sulfur-oxidizing and sulfate-reducing prokaryotes.

Meyer B, Kuever J - PLoS ONE (2008)

Bottom Line: These structural alterations correlated with the protein phylogeny (three major phylogenetic lineages: (1) SRP including LGT-affected Archaeoglobi and SOB of Apr lineage II, (2) crenarchaeal SRP Caldivirga and Pyrobaculum, and (3) SOB of the distinct Apr lineage I) and the presence of potential APS reductase-interacting redox complexes.The almost identical protein matrices surrounding both [4Fe-4S] clusters, the FAD cofactor, the active site channel and center within the AprB/A models of SRP and SOB point to a highly similar catalytic process of APS reduction/sulfite oxidation independent of the metabolism type the APS reductase is involved in and the species it has been originated from.Based on the comparative models, there are no significant structural differences between dissimilatory APS reductases from SRP and SOB; this might be indicative for a similar catalytic process of APS reduction/sulfite oxidation.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Marine Microbiology, Bremen, Germany.

ABSTRACT

Background: The dissimilatory adenosine-5'-phosphosulfate (APS) reductase (cofactors flavin adenine dinucleotide, FAD, and two [4Fe-4S] centers) catalyzes the transformation of APS to sulfite and AMP in sulfate-reducing prokaryotes (SRP); in sulfur-oxidizing bacteria (SOB) it has been suggested to operate in the reverse direction. Recently, the three-dimensional structure of the Archaeoglobus fulgidus enzyme has been determined in different catalytically relevant states providing insights into its reaction cycle.

Methodology/principal findings: Full-length AprBA sequences from 20 phylogenetically distinct SRP and SOB species were used for homology modeling. In general, the average accuracy of the calculated models was sufficiently good to allow a structural and functional comparison between the beta- and alpha-subunit structures (78.8-99.3% and 89.5-96.8% of the AprB and AprA main chain atoms, respectively, had root mean square deviations below 1 A with respect to the template structures). Besides their overall conformity, the SRP- and SOB-derived models revealed the existence of individual adaptations at the electron-transferring AprB protein surface presumably resulting from docking to different electron donor/acceptor proteins. These structural alterations correlated with the protein phylogeny (three major phylogenetic lineages: (1) SRP including LGT-affected Archaeoglobi and SOB of Apr lineage II, (2) crenarchaeal SRP Caldivirga and Pyrobaculum, and (3) SOB of the distinct Apr lineage I) and the presence of potential APS reductase-interacting redox complexes. The almost identical protein matrices surrounding both [4Fe-4S] clusters, the FAD cofactor, the active site channel and center within the AprB/A models of SRP and SOB point to a highly similar catalytic process of APS reduction/sulfite oxidation independent of the metabolism type the APS reductase is involved in and the species it has been originated from.

Conclusions: Based on the comparative models, there are no significant structural differences between dissimilatory APS reductases from SRP and SOB; this might be indicative for a similar catalytic process of APS reduction/sulfite oxidation.

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AprB protein matrix surrounding the [4Fe-4S] cluster I and II (residues in a distance of less than 5.0 Å are shown) in the three-dimensional structure from A. fulgidus (A) and selected, homology modeling-based models from Allochromatium vinosum (B), Pelagibacter ubique (C), Pyrobaculum calidifontis (D), Desulfotomaculum reducens (E), Desulfovibrio vulgaris (F), Chlorobaculum tepidum (G), and Thiobacillus denitrificans (H).Charged and polar residues are marked (positively charged AA, blue; negatively charged AA, red; polar AA, yellow); tryptophan (Trp-B48/-B43) and cysteine residues are highlighted by violet and green color.
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pone-0001514-g005: AprB protein matrix surrounding the [4Fe-4S] cluster I and II (residues in a distance of less than 5.0 Å are shown) in the three-dimensional structure from A. fulgidus (A) and selected, homology modeling-based models from Allochromatium vinosum (B), Pelagibacter ubique (C), Pyrobaculum calidifontis (D), Desulfotomaculum reducens (E), Desulfovibrio vulgaris (F), Chlorobaculum tepidum (G), and Thiobacillus denitrificans (H).Charged and polar residues are marked (positively charged AA, blue; negatively charged AA, red; polar AA, yellow); tryptophan (Trp-B48/-B43) and cysteine residues are highlighted by violet and green color.

Mentions: The [4Fe-4S] clusters of APS reductases from several sulfate reducing strains have been documented to differ significantly in their reduction potential (approximately −500 mV for cluster II and −60 mV for cluster I) [18], [23], [24]. Based on the X-ray structure of A. fulgidus, the large reduction potential difference of the two clusters was explained by their distinctly different surrounding protein matrix (see Fig. 5 panel A). Generally, local dipole in close proximity to the acid-labile sulfur and cysteinyl sulfur atoms modulate the reduction potential of a [4Fe-4S] cluster: Its reduced state can be stabilized by NH-S hydrogen bonds and backbone amide dipoles that shift the reduction potential of an iron-sulfur center to a more positive value. In the A. fulgidus APS reductase, the number of polar interactions between the sulfur atoms of cluster I compared to cluster II and the backbone amides at a distance of less than 3.5 Å (17 versus 7) is substantially increased and proposed to be responsible for the high reduction potential of cluster I. In contrast, the close proximity of the negatively charged Asp-B11-carboxylate group to an acid-labile sulfur of the cluster II was suggested to stabilize its oxidized state with the result of a low reduction potential [18], [23] (see Fig. 5 panel A; see also supplementary material Figure S2 for details).


Homology modeling of dissimilatory APS reductases (AprBA) of sulfur-oxidizing and sulfate-reducing prokaryotes.

Meyer B, Kuever J - PLoS ONE (2008)

AprB protein matrix surrounding the [4Fe-4S] cluster I and II (residues in a distance of less than 5.0 Å are shown) in the three-dimensional structure from A. fulgidus (A) and selected, homology modeling-based models from Allochromatium vinosum (B), Pelagibacter ubique (C), Pyrobaculum calidifontis (D), Desulfotomaculum reducens (E), Desulfovibrio vulgaris (F), Chlorobaculum tepidum (G), and Thiobacillus denitrificans (H).Charged and polar residues are marked (positively charged AA, blue; negatively charged AA, red; polar AA, yellow); tryptophan (Trp-B48/-B43) and cysteine residues are highlighted by violet and green color.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2211403&req=5

pone-0001514-g005: AprB protein matrix surrounding the [4Fe-4S] cluster I and II (residues in a distance of less than 5.0 Å are shown) in the three-dimensional structure from A. fulgidus (A) and selected, homology modeling-based models from Allochromatium vinosum (B), Pelagibacter ubique (C), Pyrobaculum calidifontis (D), Desulfotomaculum reducens (E), Desulfovibrio vulgaris (F), Chlorobaculum tepidum (G), and Thiobacillus denitrificans (H).Charged and polar residues are marked (positively charged AA, blue; negatively charged AA, red; polar AA, yellow); tryptophan (Trp-B48/-B43) and cysteine residues are highlighted by violet and green color.
Mentions: The [4Fe-4S] clusters of APS reductases from several sulfate reducing strains have been documented to differ significantly in their reduction potential (approximately −500 mV for cluster II and −60 mV for cluster I) [18], [23], [24]. Based on the X-ray structure of A. fulgidus, the large reduction potential difference of the two clusters was explained by their distinctly different surrounding protein matrix (see Fig. 5 panel A). Generally, local dipole in close proximity to the acid-labile sulfur and cysteinyl sulfur atoms modulate the reduction potential of a [4Fe-4S] cluster: Its reduced state can be stabilized by NH-S hydrogen bonds and backbone amide dipoles that shift the reduction potential of an iron-sulfur center to a more positive value. In the A. fulgidus APS reductase, the number of polar interactions between the sulfur atoms of cluster I compared to cluster II and the backbone amides at a distance of less than 3.5 Å (17 versus 7) is substantially increased and proposed to be responsible for the high reduction potential of cluster I. In contrast, the close proximity of the negatively charged Asp-B11-carboxylate group to an acid-labile sulfur of the cluster II was suggested to stabilize its oxidized state with the result of a low reduction potential [18], [23] (see Fig. 5 panel A; see also supplementary material Figure S2 for details).

Bottom Line: These structural alterations correlated with the protein phylogeny (three major phylogenetic lineages: (1) SRP including LGT-affected Archaeoglobi and SOB of Apr lineage II, (2) crenarchaeal SRP Caldivirga and Pyrobaculum, and (3) SOB of the distinct Apr lineage I) and the presence of potential APS reductase-interacting redox complexes.The almost identical protein matrices surrounding both [4Fe-4S] clusters, the FAD cofactor, the active site channel and center within the AprB/A models of SRP and SOB point to a highly similar catalytic process of APS reduction/sulfite oxidation independent of the metabolism type the APS reductase is involved in and the species it has been originated from.Based on the comparative models, there are no significant structural differences between dissimilatory APS reductases from SRP and SOB; this might be indicative for a similar catalytic process of APS reduction/sulfite oxidation.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Marine Microbiology, Bremen, Germany.

ABSTRACT

Background: The dissimilatory adenosine-5'-phosphosulfate (APS) reductase (cofactors flavin adenine dinucleotide, FAD, and two [4Fe-4S] centers) catalyzes the transformation of APS to sulfite and AMP in sulfate-reducing prokaryotes (SRP); in sulfur-oxidizing bacteria (SOB) it has been suggested to operate in the reverse direction. Recently, the three-dimensional structure of the Archaeoglobus fulgidus enzyme has been determined in different catalytically relevant states providing insights into its reaction cycle.

Methodology/principal findings: Full-length AprBA sequences from 20 phylogenetically distinct SRP and SOB species were used for homology modeling. In general, the average accuracy of the calculated models was sufficiently good to allow a structural and functional comparison between the beta- and alpha-subunit structures (78.8-99.3% and 89.5-96.8% of the AprB and AprA main chain atoms, respectively, had root mean square deviations below 1 A with respect to the template structures). Besides their overall conformity, the SRP- and SOB-derived models revealed the existence of individual adaptations at the electron-transferring AprB protein surface presumably resulting from docking to different electron donor/acceptor proteins. These structural alterations correlated with the protein phylogeny (three major phylogenetic lineages: (1) SRP including LGT-affected Archaeoglobi and SOB of Apr lineage II, (2) crenarchaeal SRP Caldivirga and Pyrobaculum, and (3) SOB of the distinct Apr lineage I) and the presence of potential APS reductase-interacting redox complexes. The almost identical protein matrices surrounding both [4Fe-4S] clusters, the FAD cofactor, the active site channel and center within the AprB/A models of SRP and SOB point to a highly similar catalytic process of APS reduction/sulfite oxidation independent of the metabolism type the APS reductase is involved in and the species it has been originated from.

Conclusions: Based on the comparative models, there are no significant structural differences between dissimilatory APS reductases from SRP and SOB; this might be indicative for a similar catalytic process of APS reduction/sulfite oxidation.

Show MeSH
Related in: MedlinePlus