1. Structural Biology and Molecular Biophysics

Structural basis of interprotein electron transfer in bacterial sulfite oxidation

  1. Aaron P McGrath
  2. Elise L Laming
  3. G Patricia Casas Garcia
  4. Marc Kvansakul
  5. J Mitchell Guss
  6. Jill Trewhella
  7. Benoit Calmes
  8. Paul V Bernhardt
  9. Graeme R Hanson
  10. Ulrike Kappler
  11. Megan J Maher  Is a corresponding author
  1. University of California, San Diego, United States
  2. The Victor Chang Cardiac Research Institute, Australia
  3. La Trobe University, Australia
  4. University of Sydney, Australia
  5. University of Queensland, Australia
https://doi.org/10.7554/eLife.09066
Share this article
Cite this article
  1. Aaron P McGrath
  2. Elise L Laming
  3. G Patricia Casas Garcia
  4. Marc Kvansakul
  5. J Mitchell Guss
  6. Jill Trewhella
  7. Benoit Calmes
  8. Paul V Bernhardt
  9. Graeme R Hanson
  10. Ulrike Kappler
  11. Megan J Maher
(2015)
Structural basis of interprotein electron transfer in bacterial sulfite oxidation
eLife 4:e09066.
https://doi.org/10.7554/eLife.09066
  2. Download BibTeX
  3. Download .RIS

Abstract

Interprotein electron transfer underpins the essential processes of life and relies on the formation of specific, yet transient protein-protein interactions. In biological systems, the detoxification of sulfite is catalyzed by the sulfite-oxidizing enzymes (SOEs), which interact with an electron acceptor for catalytic turnover. Here, we report the structural and functional analyses of the SOE SorT from Sinorhizobium meliloti and its cognate electron acceptor SorU. Kinetic and thermodynamic analyses of the SorT/SorU interaction showed the complex is dynamic in solution, and that the proteins interact with Kd = 13.5 {plus minus} 0.8 βM. The crystal structures of the oxidized SorT and SorU both in isolation and in complex, reveal the interface to be remarkably electrostatic, with an unusually large number of direct hydrogen bonding interactions. The assembly of the complex is accompanied by an adjustment in the structure of SorU and conformational sampling provides a mechanism for dissociation of the SorT/SorU assembly.

Article and author information

Author details

  1. Aaron P McGrath

    Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Elise L Laming

    The Victor Chang Cardiac Research Institute, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.

  3. G Patricia Casas Garcia

    La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.

  4. Marc Kvansakul

    La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.

  5. J Mitchell Guss

    School of Molecular Bioscience, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.

  6. Jill Trewhella

    School of Molecular Bioscience, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.

  7. Benoit Calmes

    Centre for Metals in Biology, University of Queensland, Brisbane, Australia
    Competing interests
    The authors declare that no competing interests exist.

  8. Paul V Bernhardt

    Centre for Metals in Biology, University of Queensland, Brisbane, Australia
    Competing interests
    The authors declare that no competing interests exist.

  9. Graeme R Hanson

    Centre for Metals in Biology, University of Queensland, Brisbane, Australia
    Competing interests
    The authors declare that no competing interests exist.

  10. Ulrike Kappler

    Centre for Metals in Biology, University of Queensland, Brisbane, Australia
    Competing interests
    The authors declare that no competing interests exist.

  11. Megan J Maher

    School of Molecular Bioscience, University of Sydney, New South Wales, Australia
    For correspondence
    m.maher@latrobe.edu.au
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2015, McGrath et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,347
    views
  • 290
    downloads
  • 20
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Aaron P McGrath
  2. Elise L Laming
  3. G Patricia Casas Garcia
  4. Marc Kvansakul
  5. J Mitchell Guss
  6. Jill Trewhella
  7. Benoit Calmes
  8. Paul V Bernhardt
  9. Graeme R Hanson
  10. Ulrike Kappler
  11. Megan J Maher
(2015)
Structural basis of interprotein electron transfer in bacterial sulfite oxidation
eLife 4:e09066.
https://doi.org/10.7554/eLife.09066

Share this article

https://doi.org/10.7554/eLife.09066

Categories and tags

Further reading

    1. Immunology and Inflammation
    2. Structural Biology and Molecular Biophysics

    Load-based divergence in the dynamic allostery of two TCRs recognizing the same pMHC

    Ana Cristina Chang-Gonzalez, Aoi Akitsu ... Wonmuk Hwang
    Research Advance

    Increasing evidence suggests that mechanical load on the αβ T-cell receptor (TCR) is crucial for recognizing the antigenic peptide-bound major histocompatibility complex (pMHC) molecule. Our recent all-atom molecular dynamics (MD) simulations revealed that the inter-domain motion of the TCR is responsible for the load-induced catch bond behavior of the TCR-pMHC complex and peptide discrimination (Chang-Gonzalez et al., 2024). To further examine the generality of the mechanism, we perform all-atom MD simulations of the B7 TCR under different conditions for comparison with our previous simulations of the A6 TCR. The two TCRs recognize the same pMHC and have similar interfaces with pMHC in crystal structures. We find that the B7 TCR-pMHC interface stabilizes under ∼15 pN load using a conserved dynamic allostery mechanism that involves the asymmetric motion of the TCR chassis. However, despite forming comparable contacts with pMHC as A6 in the crystal structure, B7 has fewer high-occupancy contacts with pMHC and exhibits higher mechanical compliance during the simulation. These results indicate that the dynamic allostery common to the TCRαβ chassis can amplify slight differences in interfacial contacts into distinctive mechanical responses and nuanced biological outcomes.

    1. Immunology and Inflammation
    2. Structural Biology and Molecular Biophysics

    Ab initio prediction of specific phospholipid complexes and membrane association of HIV-1 MPER antibodies by multi-scale simulations

    Colleen A Maillie, Kiana Golden ... Marco Mravic
    Research Article

    A potent class of HIV-1 broadly neutralizing antibodies (bnAbs) targets the envelope glycoprotein’s membrane proximal exposed region (MPER) through a proposed mechanism where hypervariable loops embed into lipid bilayers and engage headgroup moieties alongside the epitope. We address the feasibility and determinant molecular features of this mechanism using multi-scale modeling. All-atom simulations of 4E10, PGZL1, 10E8, and LN01 docked onto HIV-like membranes consistently form phospholipid complexes at key complementarity-determining region loop sites, solidifying that stable and specific lipid interactions anchor bnAbs to membrane surfaces. Ancillary protein-lipid contacts reveal surprising contributions from antibody framework regions. Coarse-grained simulations effectively capture antibodies embedding into membranes. Simulations estimating protein-membrane interaction strength for PGZL1 variants along an inferred maturation pathway show bilayer affinity is evolved and correlates with neutralization potency. The modeling demonstrated here uncovers insights into lipid participation in antibodies’ recognition of membrane proteins and highlights antibody features to prioritize in vaccine design.

    1. Plant Biology
    2. Structural Biology and Molecular Biophysics

    Structure of the Calvin-Benson-Bassham sedoheptulose-1,7-bisphosphatase from the model microalga Chlamydomonas reinhardtii

    Théo Le Moigne, Martina Santoni ... Julien Henri
    Research Article

    The Calvin-Benson-Bassham cycle (CBBC) performs carbon fixation in photosynthetic organisms. Among the eleven enzymes that participate in the pathway, sedoheptulose-1,7-bisphosphatase (SBPase) is expressed in photo-autotrophs and catalyzes the hydrolysis of sedoheptulose-1,7-bisphosphate (SBP) to sedoheptulose-7-phosphate (S7P). SBPase, along with nine other enzymes in the CBBC, contributes to the regeneration of ribulose-1,5-bisphosphate, the carbon-fixing co-substrate used by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). The metabolic role of SBPase is restricted to the CBBC, and a recent study revealed that the three-dimensional structure of SBPase from the moss Physcomitrium patens was found to be similar to that of fructose-1,6-bisphosphatase (FBPase), an enzyme involved in both CBBC and neoglucogenesis. In this study we report the first structure of an SBPase from a chlorophyte, the model unicellular green microalga Chlamydomonas reinhardtii. By combining experimental and computational structural analyses, we describe the topology, conformations, and quaternary structure of Chlamydomonas reinhardtii SBPase (CrSBPase). We identify active site residues and locate sites of redox- and phospho-post-translational modifications that contribute to enzymatic functions. Finally, we observe that CrSBPase adopts distinct oligomeric states that may dynamically contribute to the control of its activity.