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Structural basis of respiratory complexes adaptation to cold temperatures

Young-Cheul Shin, Pedro Latorre-Muro, Amina Djurabekova, Oleksii Zdorevskyi, Christopher F. Bennett, Nils Burger, Kangkang Song, Chen Xu, Vivek Sharma, Maofu Liao, Pere Puigserver

Posted on: 10 April 2024

Preprint posted on 17 January 2024

Discover how organisms adapt to cold weather! Shin and Latorre-Muro et al. unveil a mitochondrial response to low temperatures in their comprehensive study of respiration and heat generation.

Selected by Pamela Ornelas

Categories: biochemistry, biophysics, cell biology

Background

When exposed to cold environments, mammals activate brown adipocyte cells (BAs) to generate heat and regulate body temperature (1). BAs, dense with mitochondrial cristae, undergo deep protein and lipid remodeling to sustain heightened oxidation rates of glucose and fatty acids in response to low temperatures (2). This adaptation mechanism relies on the electron transport chain (ETC) within mitochondria, which generates a proton motive force that can be used to release energy in the form of heat (3,4). However, the structural basis of cold-induced effects on respiratory complexes is not well understood.

In their preprint, Shin, Latorre-Muro, and colleagues combined thermoregulatory physiology and cryo-electron microscopy (cryoEM) to investigate respiratory supercomplexes exposed to different temperatures. They identified a cold-induced conformation within the CI:III2 supercomplex, elucidating the unique lipid-protein arrangements that stabilize it.

Key findings

Exposure to cold temperatures

Shin, Latorre-Muro, and colleagues compared brown adipose tissue samples from wild-type and model mice exposed to varying temperatures over 8 days. After mitochondrial solubilization, respiratory supercomplexes were purified through size exclusion chromatography, with subsequent activity determination. Peak fractions were analyzed through single particle cryoEM, resulting in high-resolution maps of the CI:III2 supercomplex across different temperatures. This revealed a conformational change of the respiratory complex as a cold adaptation response.

Respiratory complex remodeling

The study resolved two conformations of the CI:III2 supercomplex. Thermoneutral mouse samples presented only a canonical (type 1) conformation, while a structurally different second conformation (type 2) was also observed in samples of cold-acclimated mice. This suggests that in response to cold temperatures, type 1 respiratory complexes transit to the type 2 conformation. The difference between these conformations lies in the 25˚ rearrangement of the CIII2 axis, perpendicular to the CI membrane domain, resulting in an open angle between the longitudinal CI membrane domain and the CIII2 transversal axes.

Lipids play an important role

Given that lipid remodeling in mitochondrial membranes increases ETC activity (5), Shin, Latorre-Muro, and colleagues conducted lipidomics analyses on isolated mitochondria. They found a distinct enrichment in unsaturated phosphatidylethanolamine (PE) and phosphatidylcholine (PC) in tissues exposed to cold and neutral temperatures. Molecular dynamics simulations revealed increased lipid density at the CI/CIII2 interface in the type 2 supercomplex compared to type 1. On this basis, the conformational transition from type 1 to type 2 under cold conditions is proposed to occur by lipid remodeling (PC/PE), increasing membrane flexibility and allowing the accommodation of type 2 complexes to straightened cristae. This results in a lower energy barrier compared to thermoneutral conditions.

In summary, mammalian survival in cold temperatures involves remodeling of brown fat mitochondrial proteins. The authors propose that upon rotation of CIII2, type 2 assemblies become highly active and increase respiration, supporting heat production and maintaining body temperature.

Why is this important?

This preprint provides a great insight into the dynamics of respiratory adaptation under low temperatures. The work presented by Shin, Latorre-Muro, and their colleagues is comprehensive, as they study adipose tissue under different genetic and environmental conditions using cryo-EM, molecular dynamic simulations, and biochemical analyses. This research offers a fresh perspective on cellular temperature regulation and metabolic response to external factors.

I was particularly interested in this work for personal reasons. Every winter, my structural biology friends and I challenge ourselves to swim a nearby lake on Sunday mornings. Our short submersions in near 0˚ C water often prompt discussions about our body’s amazing capacity to adapt to the cold and have sparked our curiosity about metabolism in extreme weather conditions.

 

Questions to the authors

    1. Do you expect an increase in mitochondrial protein and lipid import under cold-induced stress to make up for the cristae rearrangement? Are there specific regulatory factors involved in this process?
    2. Based on your molecular dynamics simulations, can you predict the speed of the conformational change between type 1 and 2 assemblies?
    3. Would you expect similar reorganization in other respiratory supercomplexes to maximize electron transfer?
    4. Are there shared mechanisms used by prokaryotes to maintain energy production under cold temperatures?

 

References:

    1. Cannon, J. Nedergaard, Brown adipose tissue: function and physiological significance. Physiol Rev 84, 277–359 (2004).
    2. Orava, P. Nuutila, M. E. Lidell, V. Oikonen, T. Noponen, T. Viljanen, M. Scheinin, M. Taittonen, T. Niemi, S. Enerbäck, K. A. Virtanen, Different Metabolic Responses of Human Brown Adipose Tissue to Activation by Cold and Insulin. Cell Metab 14, 272–279 (2011).
    3. Enerbäck, A. Jacobsson, E. M. Simpson, C. Guerra, H. Yamashita, M.-E. Harper, L. P. Kozak, Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387, 90–94 (1997).
    4. Kazak, B. M. Spiegelman, Mechanism of futile creatine cycling in thermogenesis. Am J Physiol Endocrinol Metab 319, E947–E949 (2020).
    5. G. Sustarsic, T. Ma, M. D. Lynes, M. Larsen, I. Karavaeva, J. F. Havelund, C. H. Nielsen, M. P. Jedrychowski, M. Moreno-Torres, M. Lundh, K. Plucinska, N. Z. Jespersen, T. J. Grevengoed, B. Kramar, J. Peics, J. B. Hansen, F. Shamsi, I. Forss, D. Neess, S. Keipert, J. Wang, K. Stohlmann, I. Brandslund, C. Christensen, M. E. Jørgensen, A. Linneberg, O. Pedersen, M. A. Kiebish, K. Qvortrup, X. Han, B. K. Pedersen, M. Jastroch, S. Mandrup, A. Kjær, S. P. Gygi, T. Hansen, M. P. Gillum, N. Grarup, B. Emanuelli, S. Nielsen, C. Scheele, Y. H. Tseng, N. J. Færgeman, Z. Gerhart-Hines, Cardiolipin Synthesis in Brown and Beige Fat Mitochondria Is Essential for Systemic Energy Homeostasis. Cell Metab 28, 159-174.e11 (2018).

Tags: cryoem, mitochondria, respiration, respiratory complex

doi: https://doi.org/10.1242/prelights.37071

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Author's response

The author team shared

  1. Do you expect an increase in mitochondrial protein and lipid import under cold-induced stress to make up for the cristae rearrangement? Are there specific regulatory factors involved in this process?

R: There is a growing interest in the understanding of organelle remodeling in response to environmental factors. We have previously reported that, during cold acclimation, the activity of mitochondrial import machineries, and more specifically, the receptor TOM70, regulates the mitochondrial protein import of at least the cristae component MIC19(1). These results show how cristae remodeling impacts the capability of brown adipocytes to adapt to cold environments. This process is regulated by the PERK branch of the Integrated Stress Response (ISR) through a non-canonical pathway and indicates that protein remodeling is necessary for successful cold acclimation. In addition, we have seen that MIC19 overexpression in livers can protect against diet-induced obesity, further supporting the connection between mitochondria cristae and metabolic adaptation(2). Based on these findings, it seems feasible that protein and lipid remodeling converge together.  Previous literature and our results suggest that lipid remodeling during cold acclimation enriches the presence of unsaturated PC and PE species(3), which aid the stabilization of respiratory supercomplexes(4). Yet, further research is necessary to investigate how these lipids are generated and delivered to mitochondria.

 

  1. Based on your molecular dynamics simulations, can you predict the speed of the conformational change between type 1 and 2 assemblies?

R: This is a very good question, and we would indeed like to know about the energy barriers that separate the two states. This may tell us about the rates of conversion between two states. However, this is a complex process, and this scenario involves many players – protein and lipid dynamics, lipid composition, and several other factors involving mitochondrial membrane. Treating such aspects in a coupled fashion through modeling and simulation methods alone is a current challenge.

 

  1. Would you expect similar reorganization in other respiratory supercomplexes to maximize electron transfer?

R: The initial description of type 2 complexes is from 2016 using samples from ovine hearts(5). A second paper in 2022 described a rotation of CIII2:IV relative to CI in swine hearts(6). Yet, EM maps were obtained at 8-10Å, likely due to the low stoichiometry of these particles. These works indicate that in tissues other than brown adipose tissue, type 2 complexes exist. Our work addresses the question of the existence of these rotated complexes by employing mouse models under very controlled environmental conditions, thermoneutrality and cold-acclimation. These conditions represent the minimum and maximum metabolic level of activity in brown adipocytes, respectively. By clearly segregating the metabolic state, we were able to maximize the number of particles with a rotated conformation in our samples and obtain high-resolution maps. The structural information allowed us to calculate the behavior of these assemblies by molecular dynamics simulations that suggest, along with the biochemical data, that type 2 complexes maintain the system in a high-energy state. Therefore, the rearrangement of respiratory complexes from type 1 to highly active type 2 is a general process that can reign across tissues in response to environmental cues to satisfy cellular energetic demands.

 

  1. Are there shared mechanisms used by prokaryotes to maintain energy production under cold temperatures?

R: That is a very interesting question. Prokaryotes slow down their metabolism under cold conditions. Some bacteria show optimal growth rates at 10-20°C instead of the standard 37°C. However, during recent years, several works have observed correlation between cristae morphology and respiratory complex structure across kingdoms(7–10). This implies that the different forms of life adapt their respiratory machineries to satisfy their energetic needs in response to environmental cues.

 

  1. P. Latorre-Muro, K. E. O’Malley, C. F. Bennett, E. A. Perry, E. Balsa, C. D. J. Tavares, M. Jedrychowski, S. P. Gygi, P. Puigserver, A cold-stress-inducible PERK/OGT axis controls TOM70-assisted mitochondrial protein import and cristae formation. Cell Metab 33, 598-614.e7 (2021).
  2. J. H. Sohn, B. Mutlu, P. Latorre-Muro, J. Liang, C. F. Bennett, K. Sharabi, N. Kantorovich, M. Jedrychowski, S. P. Gygi, A. S. Banks, P. Puigserver, Liver mitochondrial cristae organizing protein MIC19 promotes energy expenditure and pedestrian locomotion by altering nucleotide metabolism. Cell Metab 35, 1356–1372 (2023).
  3. E. G. Sustarsic, T. Ma, M. D. Lynes, M. Larsen, I. Karavaeva, J. F. Havelund, C. H. Nielsen, M. P. Jedrychowski, M. Moreno-Torres, M. Lundh, K. Plucinska, N. Z. Jespersen, T. J. Grevengoed, B. Kramar, J. Peics, J. B. Hansen, F. Shamsi, I. Forss, D. Neess, S. Keipert, J. Wang, K. Stohlmann, I. Brandslund, C. Christensen, M. E. Jørgensen, A. Linneberg, O. Pedersen, M. A. Kiebish, K. Qvortrup, X. Han, B. K. Pedersen, M. Jastroch, S. Mandrup, A. Kjær, S. P. Gygi, T. Hansen, M. P. Gillum, N. Grarup, B. Emanuelli, S. Nielsen, C. Scheele, Y. H. Tseng, N. J. Færgeman, Z. Gerhart-Hines, Cardiolipin Synthesis in Brown and Beige Fat Mitochondria Is Essential for Systemic Energy Homeostasis. Cell Metab 28, 159-174.e11 (2018).
  4. C. F. Bennett, K. E. O’Malley, E. A. Perry, E. Balsa, P. Latorre-Muro, C. L. Riley, C. Luo, M. Jedrychowski, S. P. Gygi, P. Puigserver, Peroxisomal-derived ether phospholipids link nucleotides to respirasome assembly. Nat Chem Biol 17, 703–710 (2021).
  5. J. S. Sousa, D. J. Mills, J. Vonck, W. Kühlbrandt, Functional asymmetry and electron flow in the bovine respirasome. Elife 5, e21290 (2016).
  6. T. J. Jeon, S.-G. Lee, S. H. Yoo, M. Kim, D. Song, J. Ryu, H. Park, D.-S. Kim, J. Hyun, H. M. Kim, S. E. Ryu, A Dynamic Substrate Pool Revealed by cryo-EM of a Lipid-Preserved Respiratory Supercomplex. Antioxid Redox Signal 36, 1101–1118 (2022).
  7. L. Zhou, M. Maldonado, A. Padavannil, F. Guo, J. A. Letts, Structures of Tetrahymena’s respiratory chain reveal the diversity of eukaryotic core metabolism. Science 376, 831–839 (2022).
  8. N. Klusch, M. Dreimann, J. Senkler, N. Rugen, W. Kühlbrandt, H.-P. Braun, Cryo-EM structure of the respiratory I + III2 supercomplex from Arabidopsis thaliana at 2 Å resolution. Nat Plants 9, 142–156 (2022).
  9. M. Maldonado, Z. Fan, K. M. Abe, J. A. Letts, Plant-specific features of respiratory supercomplex I + III2 from Vigna radiata. Nat Plants 9, 157–168 (2022).
  10. A. Mühleip, R. K. Flygaard, R. Baradaran, O. Haapanen, T. Gruhl, V. Tobiasson, A. Maréchal, V. Sharma, A. Amunts, Structural basis of mitochondrial membrane bending by the I–II–III2–IV2 supercomplex. Nature 615, 934–938 (2023).

 

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