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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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Three-dimensional structure of AprB from A. fulgidus (A) and selected, homology modeling-based AprB models from Allochromatium vinosum (B) and Pelagibacter ubique (C) (as representatives of SOB from Apr lineage-I), Pyrobaculum calidifontis (D) (as representative of crenarchaeal SRP), Desulfotomaculum reducens (E) (as representative of Gram-positive SRB and LGT-affected deltaproteobacterial SRB), Desulfovibrio vulgaris (F) (as representative of non-LGT-affected deltaproteobacterial SRB), Chlorobaculum tepidum (G) and Thiobacillus denitrificans (H) (as representatives of LGT-affected SOB from Apr lineage-II).Ribbon structure shown from front view (positions of [4Fe-4S] clusters indicated in A. fulgidus AprB). Ribbon structure of A. fulgidus AprB (A) colored by secondary structure elements; ribbon structures of AprB models (B–H) colored by model confidence factor provided by SWISS-MODEL (green, respective region of model and reference structure superpose; red, respective region of model deviates from the reference structure). The missing flexible loop between Cys-B13 and Gly-B19 (enumeration based on A. fulgidus sequence) in models of SOB from Apr lineage-I and Pyrobaculum spp. is marked by red arrows.
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pone-0001514-g003: Three-dimensional structure of AprB from A. fulgidus (A) and selected, homology modeling-based AprB models from Allochromatium vinosum (B) and Pelagibacter ubique (C) (as representatives of SOB from Apr lineage-I), Pyrobaculum calidifontis (D) (as representative of crenarchaeal SRP), Desulfotomaculum reducens (E) (as representative of Gram-positive SRB and LGT-affected deltaproteobacterial SRB), Desulfovibrio vulgaris (F) (as representative of non-LGT-affected deltaproteobacterial SRB), Chlorobaculum tepidum (G) and Thiobacillus denitrificans (H) (as representatives of LGT-affected SOB from Apr lineage-II).Ribbon structure shown from front view (positions of [4Fe-4S] clusters indicated in A. fulgidus AprB). Ribbon structure of A. fulgidus AprB (A) colored by secondary structure elements; ribbon structures of AprB models (B–H) colored by model confidence factor provided by SWISS-MODEL (green, respective region of model and reference structure superpose; red, respective region of model deviates from the reference structure). The missing flexible loop between Cys-B13 and Gly-B19 (enumeration based on A. fulgidus sequence) in models of SOB from Apr lineage-I and Pyrobaculum spp. is marked by red arrows.

Mentions: The three segment-subdivision of the A. fulgidus beta-subunit described by Fritz and coworkers [18], [23] is reflected in all comparative models of the dissimilatory APS reductase irrespective of species metabolism type and phylogenetic affiliation. While the presence and orientation of the secondary structure elements are strictly conserved in the functionally important first and second segment of the models (ferredoxin-like and alpha-subunit interface region), the third, the tail segment, is more variable among the investigated SRP and SOB (see Fig. 3 for AprB models of selected SRP/SOB; all AprB models are presented in supplementary material Table S1 and Figure S1). Significantly higher main chain atom RMS deviations of up to 3.28 Å to the A. fulgidus template were present in this protein region in comparison with the low values of the first segments that ranged between 0.00 and 0.84 Å (see Table 1). The tail region has been proposed to be responsible for the tightening of the subunit interaction and, thus, a stable heterodimer formation by increasing the contact surface between both subunits [18], [23]. The differing presence of secondary structure elements in the tail segments of the models is a result of the high variability in sequence and length. The structural dispersion of the tail regions might reflect the process of speciation by individual structural adaptations at the interacting surface between the beta- and alpha-subunit of each species. Indeed, the tail segment is the only sequence section of the beta-subunit that contains sufficient phylogenetic information to allow inter- and intrafamily differentiation among the SRP and SOB sequences.


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

Meyer B, Kuever J - PLoS ONE (2008)

Three-dimensional structure of AprB from A. fulgidus (A) and selected, homology modeling-based AprB models from Allochromatium vinosum (B) and Pelagibacter ubique (C) (as representatives of SOB from Apr lineage-I), Pyrobaculum calidifontis (D) (as representative of crenarchaeal SRP), Desulfotomaculum reducens (E) (as representative of Gram-positive SRB and LGT-affected deltaproteobacterial SRB), Desulfovibrio vulgaris (F) (as representative of non-LGT-affected deltaproteobacterial SRB), Chlorobaculum tepidum (G) and Thiobacillus denitrificans (H) (as representatives of LGT-affected SOB from Apr lineage-II).Ribbon structure shown from front view (positions of [4Fe-4S] clusters indicated in A. fulgidus AprB). Ribbon structure of A. fulgidus AprB (A) colored by secondary structure elements; ribbon structures of AprB models (B–H) colored by model confidence factor provided by SWISS-MODEL (green, respective region of model and reference structure superpose; red, respective region of model deviates from the reference structure). The missing flexible loop between Cys-B13 and Gly-B19 (enumeration based on A. fulgidus sequence) in models of SOB from Apr lineage-I and Pyrobaculum spp. is marked by red arrows.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2211403&req=5

pone-0001514-g003: Three-dimensional structure of AprB from A. fulgidus (A) and selected, homology modeling-based AprB models from Allochromatium vinosum (B) and Pelagibacter ubique (C) (as representatives of SOB from Apr lineage-I), Pyrobaculum calidifontis (D) (as representative of crenarchaeal SRP), Desulfotomaculum reducens (E) (as representative of Gram-positive SRB and LGT-affected deltaproteobacterial SRB), Desulfovibrio vulgaris (F) (as representative of non-LGT-affected deltaproteobacterial SRB), Chlorobaculum tepidum (G) and Thiobacillus denitrificans (H) (as representatives of LGT-affected SOB from Apr lineage-II).Ribbon structure shown from front view (positions of [4Fe-4S] clusters indicated in A. fulgidus AprB). Ribbon structure of A. fulgidus AprB (A) colored by secondary structure elements; ribbon structures of AprB models (B–H) colored by model confidence factor provided by SWISS-MODEL (green, respective region of model and reference structure superpose; red, respective region of model deviates from the reference structure). The missing flexible loop between Cys-B13 and Gly-B19 (enumeration based on A. fulgidus sequence) in models of SOB from Apr lineage-I and Pyrobaculum spp. is marked by red arrows.
Mentions: The three segment-subdivision of the A. fulgidus beta-subunit described by Fritz and coworkers [18], [23] is reflected in all comparative models of the dissimilatory APS reductase irrespective of species metabolism type and phylogenetic affiliation. While the presence and orientation of the secondary structure elements are strictly conserved in the functionally important first and second segment of the models (ferredoxin-like and alpha-subunit interface region), the third, the tail segment, is more variable among the investigated SRP and SOB (see Fig. 3 for AprB models of selected SRP/SOB; all AprB models are presented in supplementary material Table S1 and Figure S1). Significantly higher main chain atom RMS deviations of up to 3.28 Å to the A. fulgidus template were present in this protein region in comparison with the low values of the first segments that ranged between 0.00 and 0.84 Å (see Table 1). The tail region has been proposed to be responsible for the tightening of the subunit interaction and, thus, a stable heterodimer formation by increasing the contact surface between both subunits [18], [23]. The differing presence of secondary structure elements in the tail segments of the models is a result of the high variability in sequence and length. The structural dispersion of the tail regions might reflect the process of speciation by individual structural adaptations at the interacting surface between the beta- and alpha-subunit of each species. Indeed, the tail segment is the only sequence section of the beta-subunit that contains sufficient phylogenetic information to allow inter- and intrafamily differentiation among the SRP and SOB sequences.

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