Structural investigations of the ferredoxin and terminal oxygenase components of the biphenyl 2,3-dioxygenase from Sphingobium yanoikuyae B1
- Daniel J Ferraro†1,
- Eric N Brown†1,
- Chi-Li Yu2,
- Rebecca E Parales3,
- David T Gibson2 and
- S Ramaswamy1Email author
© Ferraro et al; licensee BioMed Central Ltd. 2007
Received: 11 October 2006
Accepted: 09 March 2007
Published: 09 March 2007
The initial step involved in oxidative hydroxylation of monoaromatic and polyaromatic compounds by the microorganism Sphingobium yanoikuyae strain B1 (B1), previously known as Sphingomonas yanoikuyae strain B1 and Beijerinckia sp. strain B1, is performed by a set of multiple terminal Rieske non-heme iron oxygenases. These enzymes share a single electron donor system consisting of a reductase and a ferredoxin (BPDO-FB1). One of the terminal Rieske oxygenases, biphenyl 2,3-dioxygenase (BPDO-OB1), is responsible for B1's ability to dihydroxylate large aromatic compounds, such as chrysene and benzo[a]pyrene.
In this study, crystal structures of BPDO-OB1 in both native and biphenyl bound forms are described. Sequence and structural comparisons to other Rieske oxygenases show this enzyme to be most similar, with 43.5 % sequence identity, to naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816-4. While structurally similar to naphthalene 1,2-dioxygenase, the active site entrance is significantly larger than the entrance for naphthalene 1,2-dioxygenase. Differences in active site residues also allow the binding of large aromatic substrates. There are no major structural changes observed upon binding of the substrate. BPDO-FB1 has large sequence identity to other bacterial Rieske ferredoxins whose structures are known and demonstrates a high structural homology; however, differences in side chain composition and conformation around the Rieske cluster binding site are noted.
This is the first structure of a Rieske oxygenase that oxidizes substrates with five aromatic rings to be reported. This ability to catalyze the oxidation of larger substrates is a result of both a larger entrance to the active site as well as the ability of the active site to accommodate larger substrates. While the biphenyl ferredoxin is structurally similar to other Rieske ferredoxins, there are distinct changes in the amino acids near the iron-sulfur cluster. Because this ferredoxin is used by multiple oxygenases present in the B1 organism, this ferredoxin-oxygenase system provides the structural platform to dissect the balance between promiscuity and selectivity in protein-protein electron transport systems.
Sphingobium yanoikuyae B1 (B1), previously known as Sphingomonas yanoikuyae B1 and Beijerinckia sp. strain B1 , was isolated by virtue of its ability to use biphenyl as its sole source of carbon and energy for growth . B1 is capable of using naphthalene, phenanthrene, anthracene, toluene, m- and p-xylene as sole sources of carbon and energy . Other compounds are also oxidized by this microorganism and many of these are converted to cis-dihydrodiols. B1 remains one of the only known microbes, along with Mycobacterium vanbaalenii PYR1  and Sphingomonas sp. strain CHY-1 [5–7], able to oxidize large aromatic hydrocarbons such as benzo[a]pyrene, benzo[a]anthracene and chrysene  to cis-dihydrodiols.
In the B1 genome, at least six sets of putative oxygenase genes are present  and are all believed to share a common electron donor system . The genes bphA1A2f, which encode BPDO-OB1, have been sequenced and found to encode a Rieske oxygenase (RO) [11–13] related to naphthalene and biphenyl dioxygenases . BPDO-OB1 is responsible for the oxidation of large aromatic compounds, such as benzo[a]pyrene, by B1. Structural information [15–17] and molecular modeling  have been used to determine features important for substrate specificity in other biphenyl oxidizing oxygenases; however, most of the effort has been targeted at understanding how biphenyl dioxygenases catalyze the degradation of polychlorinated biphenyls (reviewed in [19–22]). Previous structural studies of several ROs provide insight into common features of how the terminal component of the RO systems are organized and how substrate interacts with the enzyme to form the hydroxylated product . To date, structures of enzymes that catalyze cis-dihydroxylation of aromatic substrates with more than three rings have not been reported.
Rieske oxygenase systems have multiple components whose function is to transfer electrons from NAD(P)H to active molecular oxygen and ultimately oxidize aromatic hydrocarbon substrates . A single reductase for the multiple Rieske oxygenases is present in the B1 genome . This reductase passes one electron at a time from NAD(P)H to the Rieske ferredoxin, BPDO-FB1, which in turn passes the electron on to the dioxygenase enzyme . The terminal oxygenase component is responsible for catalyzing the addition of molecular oxygen to the aromatic substrate. This occurs at the mononuclear iron, contained in a large, primarily hydrophobic active site. The residues that form the active site have been shown to control substrate specificity.
Here we report the structures of BPDO-FB1 and BPDO-OB1. The structure of BPDO-FB1 shows similarities and important differences compared to other known Rieske dioxygenase ferredoxins. Structures of BPDO-OB1, in both the native form and bound to biphenyl, are presented. These structures demonstrate how BPDO-OB1 binds substrate in the active site. We also discuss the similarities and differences of this terminal oxygenase to other RO terminal oxygenase structures that have been previously determined and how these differences play a role in substrate specificity and regio- and stereoselectivity of product formation.
Results & discussion
Ferredoxin structure determination
Summary of crystallographic data and refinement statistics
Oxygenase (native) (2GBW)
Oxygenase (biphenyl bound) (2GBX)
a = b (Å)
9.49 – 1.90 Å (1.96 – 1.90 Å)
19.80 -1.70 Å (1.76 -1.70 Å)
43.15 – 2.75 (2.85 – 2.75)
93.7 % (65.2 %)
95.3 % (98.1 %)
92.6 % (99.7 %)
RMSD from ideality
Bond lengths (Å)
Bond angles (deg)
Oxygenase structure determination
The asymmetric unit contains the entire BPDO-OB1α3β3 hexamer and residues 6 – 454 of the α subunits and residues 5 – 174 of the β subunits were modeled into the electron density. The structure has been refined to a resolution of 1.7 Å with a final Rfactor of 18.8 % and an Rfree of 22.9 %. The loop region located at the entrance of the α subunit active site is disordered, with higher than average B-factors and low side-chain electron density. This region spanned from residues 220 – 240 with residues 235 – 239 being the most disordered. Corresponding regions in other ROs are also disordered [15, 26–30]. Lsqkab  was used to determine the superposition RMSDs of the three α and β subunits in the asymmetric unit. A few regions in the α subunit, residues 108 – 123 and 411 – 434, and in the β subunit, residues 77 – 85 and 139 – 148, had higher than average RMSDs when compared; however, electron density clearly defined the coordinates of these residues. Crystallographic statistics are reported in Table 1.
Structure of the substrate-free oxygenase enzyme
The α subunit consists of 454 residues, which form two domains. The N-terminal portion consists of a Rieske [2Fe-2S] iron-sulfur cluster domain, defined by residues 40 – 140. The Rieske domain consists of β strands and loops, forming an ISP domain fold . Four residues, two histidines and two cysteins, in the α subunit coordinate the Rieske non-heme iron cluster [2Fe-2S]. His-82 and His-103 coordinate one iron, while Cys-80 and Cys-100 coordinate the other. The C-terminal domain is a mix of helices and strands forming a TBP-like or helix-grip fold and is a member of the Bet v1-like superfamily . The structural conservation suggests that the intraprotein electron transport in BPDO-OB1 is similar to the system described for NDO-O9816-4 and benzoate dioxygenase [32–37].
The β subunit of BPDO-OB1 has a Cystatin-like protein fold and belongs to the protein superfamily of NTF2-like proteins . The function of the β subunits of ROs is not well understood and reports vary as to whether or not mutations in the β subunit of ROs can influence regioselectivity of product formation (reviewed in ). In the case of BPDO-OB1, the β subunit is not directly involved in creating the topology of the active site; however, the mononuclear iron is within 11 Å of the α-β subunit interface. This distance may allow select β-subunit side chains to indirectly affect the topology of the active site by interacting with residues that directly form the active site.
Structure of the biphenyl bound oxygenase enzyme
Comparison of BPDO-FB1 to other Rieske oxygenase ferredoxins
Sequence and structural statistics for various Rieske oxygenases compared to biphenyl 2,3-dioxygenase
Ferredoxin (PDB ID)
Terminal oxygenase α Subunit (PDB ID)
Terminal oxygenase β Subunit (PDB ID)
Structurally analogous residues near the iron-sulfur cluster in various Rieske dioxygenase ferredoxins
Rieske cluster coordinating residues
Outer shell residues
Comparison of BPDO-OB1 to other Rieske oxygenases
The BPDO-ORHA1 (PDB entry 1ULI) active site has a significantly smaller volume, ~27 Å3, than BPDO-OB1, ~43 Å3. This is due to bulkier side-chains in BPDO-ORHA1 and variability in the loop positions at the active site entrance. Comparing the ligand bound structures, biphenyl carbons 2 and 3 are closer to the mononuclear iron in BPDO-ORHA1, 4.3 and 4.6 Å respectively, as compared to BPDO-OB1 which has an average distance of approximately 5.0 Å for both the 2 and 3 carbons in the three subunits. However, in both BPDO-ORHA1 and BPDO-OB1, the distances between the biphenyl and the iron-bound water are similar. The closer position in BPDO-ORHA1 is mediated by an interaction with Met-222, which is not present in BPDO-OB1. The glycine (Gly-205) present in the structurally analogous position leaves room for the ligand to move slightly further from the iron. The lack of large side-chain rearrangement upon substrate binding is similar to results seen in NDO-O9816-4 [27, 40] and BPDO-ORHA1 . The loop covering the active site entrance of BPDO-OB1 shifts upon binding of biphenyl. While large changes in this loop are not seen in the structures of NDO-O9816-4, this loop is believed to be flexible in NDO-O9816-4[27, 40]. BPDO-ORHA1 does show significant movement of residues 271 – 276 shifting 1 – 2 Å toward the active site, with the side-chain Leu-274 forming van der Waals interactions with the ligand . Loops covering the active site in the α3 Rieske monooxygenase 2-oxoquinoline 8-monooxygenase also demonstrate changes upon substrate binding . This loop motion observed in the BPDO-OB1 and other RO structures allows the active site to "breathe" to accommodate ligands and may be one of the key features that allows this class of enzymes to perform catalysis on diverse sets of substrates with respect to overall size and shape.
Role of oxygenase active site entrance
Crystal structures of BPDO-FB1 and BPDO-OB1 from Sphingobium yanoikuyae strain B1 are presented and demonstrate strong structural conservation with other RO ferredoxin and oxygenase components. The structures reported here provide a rational basis for the ability of BPDO-OB1 to catalyze large aromatic substrates. It also provides a framework to interpret the product regioselectivity of BPDO-OB1 and the differences in product regioselectivity compared to other ROs. While the Rieske ferredoxin structure is very similar to other Rieske ferredoxins, the differences in amino acid composition near the cluster in BPDO-FB1 provide a unique opportunity among the Rieske oxygenase ferredoxins to examine the effect of cluster environment and hydrogen bonding on reduction potential.
Protein expression, purification and crystallization
BPDO-OB1, bphA1fA2f [11, 14] and BPDO-FB1, bphA4 , were each cloned from B1 into the protein expression vectors pET101D (Invitrogen, Carlsbad, CA) and pT7-7, respectively, and expressed as described in Yu et al. . Crystallization of the ferredoxin protein was performed using 33 mg/mL of BPDO-FB1 protein in a 50 mM phosphate buffer, pH 6.8, with 0.1 M citric acid and 1.6 M ammonium sulfate as precipitants. Crystallization of the oxygenase protein was performed using purified BPDO-OB1 protein at 20 mg/ml in a 20 mM potassium phosphate buffer, pH 6.8 . Mineral oil was used as a cryoprotectant for the crystals.
Oxygenase crystals were also used for soaking experiments in an attempt to generate the BPDO-OB1 protein-biphenyl complex. Soaking experiments were based on similar experiments previously done with NDO-O9816-4 to generate crystals of ligand-bound enzyme [27, 38, 40]. Crystals were moved to fresh drops containing reservoir buffer. Ethanol saturated with biphenyl was added to these drops. The crystals tolerated up to 5% ethanol in the drop. Crystals were allowed to soak for 3–5 days, then were removed from the drop and flash-cooled to 100 K. Mineral oil was used as a cryoprotectant.
Data collection, processing, structure solution and refinement
X-ray diffraction data for BPDO-FB1 were collected on beamline X6A at Brookhaven National Laboratory and data for BPDO-OB1 were collected on the IMCA-CAT beamline 17-ID at the Advanced Photon Source in Argonne National Laboratory. Crystallographic statistics are presented in Table 1. d*TREK  was used to process the data for BPDO-FB1 to a resolution of 1.60Å. Analyzing systematic absences, the space group was determined to be either P6122 or P6522. Molecular replacement using AMoRe  and a polyalanine model based on BPDO-FLB400 (PDB entry 1FQT) produced a solution in space group P6522. Model building using O  and Coot , density modification using DM, and refinement using Refmac5  from the CCP4-4.0 program suite were assisted by non-crystallographic symmetry between the two monomers in the asymmetric unit. These NCS restraints were loosened as refinement progressed. Cycles of Refmac5 with ARP/wARP [58, 59] or the Coot find waters routines were used to identify solvent atoms. Asp-96 in chain B was modeled as having two side chain conformations. A single round of TLS optimization was used at the end of refinement with each protein monomer acting as a TLS group.
Data collected from native BPDO-OB1 crystals was processed using d*TREK  to a resolution of 1.70 Å. Analysis of systematic absences suggested that the space group was P3x21. Molecular replacement was performed using a polyalanine model based on NDO-O9816-4(PDB entry 1NDO) . Molecular replacement using AMoRe  gave a clear solution in the space group P3121. Initial refinement of the polyalanine model with the program Refmac5  of the CCP4-5.0.2  suite of programs yielded good starting electron densities. The molecular visualization program O  was used for model building. After the bulk of the structure was modeled, refinement was continued with Refmac5 without NCS restraints. Solvent molecules were found using the program Arp/Warp [58, 59] and multiple side-chain conformations were modeled using the molecular visualization programs XtalView  and Coot . The calculated solvent content was 50 % . The asymmetric unit contains a complete α3β3 protein.
Data from biphenyl soaked oxygenase crystals were processed using d*TREK to a resolution of 2.8 Å. The native BPDO-OB1 structure, with solvent molecules removed, was used as a starting point for the refinement of the ligand bound structure. An energy-minimized structure of the small molecule biphenyl was constructed using the program SYBYL 7.1 . This model was used to create a refinement dictionary for Refmac5 using the ligand sketcher program in CCP4-5.0.2. After initial refinement of the protein model, the biphenyl ligand was modeled into the active site of the enzyme where electron density maps showed un-modeled density in both 2Fo-Fc and Fo-Fc maps. The torsion angle between the two rings of biphenyl was allowed to rotate during refinement and solvent molecules were modeled as appropriate.
Sequence and structural alignments
TCoffee  was used to produce a structure-based sequence alignment of the four known RO ferredoxin structures and 19 other RO ferredoxin sequences. Structural alignment of native BPDO-OB1 with structures of other RO oxygenases was performed using the program Indonesia . Structural alignments in Indonesia were done pairwise using the Levitt and Gerstein method with a cut-off value of 3.5 Å. Sequence alignment and comparison was done using full sequences for each of the proteins without structural information. Protein-protein sequence alignments were performed using blastp on the NCBI blast server . All figures showing structures were created using PyMOL 0.98 . Figure 6 was produced using a modified version of LigPlot .
- BPDO-OB1 – Biphenyl 2:
3-dioxygenase from Sphingobium yanoikuyae strain B1
- BPDO-FB1 – Biphenyl 2:
3-dioxygenase ferredoxin from Sphingobium yanoikuyae strain B1
- BPDO-ORHA1 – Biphenyl 2:
3-dioxygenase from Rhodococcus sp. strain RHA1
- NDO-F9816-4 – Naphthalene 1:
2-dioxygenase ferredoxin from Pseudomonas sp. strain NCIB 9816-4
- NDO-O9816-4 – Naphthalene 1:
2-dioxygenase from Pseudomonas sp. strain NCIB 9816-4
Sphingobium yanoikuyae strain B1
We thank Jon Mowers, Adam Okerlund, Nathan Coussens and Heather Hanson for critical reading of this manuscript and assistance with various experiments performed in this manuscript. We also thank Gerben Zylstra for providing clones of the B1bphA1A2f genes. Use of the IMCA-CAT beamline 17-ID at the Advanced Photon Source was supported by the companies of the Industrial Macromolecular Crystallography Association through a contract with the Center for Advanced Radiation Sources at the University of Chicago. Use of the Advanced Photon Source was supported by the U. S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. W-31-109-Eng-38. We would like to thank Lisa Keefe, Kevin Battaile and Irina Koshelev for help with data collection at the IMCA-CAT facility. Research carried out at X6A beam line, National Synchrotron Light Source, Brookhaven National Laboratory, is supported by the U.S. Department of Energy under contract # DE-AC02-98CH10886. X6A is funded by NIH/NIGMS under agreement Y1 GM-0080-03. We thank Vivian Stojanoff for help with data collection at X6A. D.F. and E.B. are U. of I. MSTP trainees and would like to acknowledge financial support through a fellowship from the U. of I. Center for Biocatalysis and Bioprocessing. D.F. would like to acknowledge a thesis-parts award by the Department of Energy Division of Student Programs for work at the Advanced Photon Source in Argonne National Laboratory. C.-L.Y would like to acknowledge financial support by National Science Foundation Engineering Research Centers Program grant # EEC-0310689. S.R. would like to acknowledge financial support from USPHS Grant # GM62904.
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