Invited Talk 21st International Conference on Biological Inorganic Chemistry 2025

Metabolic diversity in the world of biological energy conservation (123546)

Kristian Parey 1 , Laura van Niftrik 2 , Mike Jetten 2 , Andreas Dietl 3 , Boran Kartal 4 , Janet Vonck 5 , Werner Kühlbrand 5 , Volker Zickermann 6 , Thomas Barends 3
  1. University of Osnabrück, Osnabrück, Germany
  2. Radboud University, Nijmegen, the Netherlands
  3. Max Planck Institute for Medical Research, Heidelberg, Germany
  4. Max Planck Institute for Marine Microbiology, Bremen, Germany
  5. Max Planck Institute of Biophysics, Frankfurt am Main, Germany
  6. Goethe University, Frankfurt am Main, Germany

The mitochondrial respiratory chain has been extensively studied and the structures of complexes I–V have been well characterized. Complex I plays a key role in cellular energy metabolism, generating a large proportion of the proton motive force that drives aerobic ATP synthesis (1). The hydrophilic arm of the membrane protein complex transfers electrons from NADH to ubiquinone, providing the energy to drive proton pumping at distant sites in the membrane arm. Despite significant progress, key mechanistic details of the catalytic cycle remained unclear, with conflicting models for the A/D transition still under debate. Over the years, we have addressed these questions by solving several structures to a resolution of 2.1 Å resolution, providing detailed insights into how electrons are transferred from NADH to ubiquinone and the redox potential is coupled to the proton motive force (2).

In contrast, a unique metabolic ability is that of anaerobic ammonium-oxidizing (anammox) bacteria, which are responsible for 50% of all N2 released into the atmosphere by combining ammonium and nitrite (3). To understand how bacteria perform this extraordinary chemistry, we have determined the structures of key enzymes in the process, such as the hydrazine dehydrogenase (HDH), which converts hydrazine to N2 by releasing four low-potential electrons (4). Our structure shows that this 1.7 MDa complex contains an extended system of 192 heme groups that span the entire complex. In addition, anammox bacteria obtain additional reducing equivalents through the oxidation of nitrite to nitrate, catalyzed by a nitrite oxidoreductase (NXR). As with the structure of hydrazine dehydrogenase, our structure of the anammox NXR tubules suggests how electrons are transferred to redox partners (5). Again using this multiscale approach, we are currently working on the complete structure of the surface layer protein (SLP), which form a paracrystalline layer covering the entire cell (6). SLPs are the most abundant macromolecules and play multiple roles including membrane scaffolding and external cell protection. In the context of these bacteria, we believe that SLPs are also involved in nutrient uptake by sequestering ammonium and nitrite ions inside the cell, which are essential for the anammox process.

 

  1. Parey K, Wirth C, Vonck J, Zickermann V (2020) Respiratory complex I - structure, mechanism and evolution. Curr. Opin. Struct. Biol. 63, 1-9
  2. Parey K, Lasham J, Mills DJ, Djurabekova A, Haapanen O, Yoga EG, Xie H, Kühlbrandt W, Sharma V, Vonck J, Zickermann V (2021) High-resolution structure and dynamics of mitochondrial complex I-Insights into the proton pumping mechanism. Sci. Adv. 7, eabj3221
  3. Kartal B, de Almeida NM, Maalcke, WJ, Op den Camp HJ, Jetten MS, Keltjens JT (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol. Rev. 37, 428-461
  4. Akram M, Dietl A, Mersdorf U, Prinz S, Maalcke W, Keltjens J, Ferousi C, de Almeida NM, Reimann J, Kartal B, Jetten MSM, Parey K & Barends TRM (2019) A 192-heme electron transfer network in the hydrazine dehydrogenase complex. Sci. Adv. 5, eaav4310
  5. Chicano TM, Dietrich L, de Almeida NM, Akram M, Hartmann E, Leidreiter F, Leopoldus D, Mueller M, Sánchez R, Nuijten GHL., Reimann J, Seifert KA, Schlichting I, van Niftrik L, Jetten MSM, Dietl A, Kartal B, Parey K & Barends TRM (2021) Structural and functional characterization of the intracellular filament-forming nitrite oxidoreductase multiprotein complex. Nat. Microbiol. 6, 1129-1139
  6. Dallemer D, Nuijten GHL, van Niftrik L, Parey K. Structure of the surface layer protein from anaerobic ammonia-oxidizing bacteria, in preparation