Skip to main content
SpringerLink
Log in

Evolution: Mitochondrial Ribosomes Across Species

  • Protocol
  • First Online:
The Mitoribosome

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2661))

Abstract

The ribosome is among the most complex and ancient cellular macromolecular assemblies that plays a central role in protein biosynthesis in all living cells. Its function of translation of genetic information encoded in messenger RNA into protein molecules also extends to subcellular compartments in eukaryotic cells such as apicoplasts, chloroplasts, and mitochondria. The origin of mitochondria is primarily attributed to an early endosymbiotic event between an alpha-proteobacterium and a primitive (archaeal) eukaryotic cell. The timeline of mitochondrial acquisition, the nature of the host, and their diversification have been studied in great detail and are continually being revised as more genomic and structural data emerge. Recent advancements in high-resolution cryo-EM structure determination have provided architectural details of mitochondrial ribosomes (mitoribosomes) from various species, revealing unprecedented diversifications among them. These structures provide novel insights into the evolution of mitoribosomal structure and function. Here, we present a brief overview of the existing mitoribosomal structures in the context of the eukaryotic evolution tree showing their diversification from their last common ancestor.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Koonin EV (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol, Nature Publishing Group 1:127–136. https://doi.org/10.1038/nrmicro751

    Article  CAS  Google Scholar 

  2. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 87:4576–4579. https://doi.org/10.1073/pnas.87.12.4576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bernier CR, Petrov AS, Kovacs NA, Penev PI, Williams LD (2018) Translation: the universal structural core of life. Mol Biol Evol 35:2065–2076. https://doi.org/10.1093/molbev/msy101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science, American Association for the Advancement of Science 289:905–920. https://doi.org/10.1126/science.289.5481.905

    Article  CAS  Google Scholar 

  6. Agmon I, Bashan A, Zarivach R, Yonath A (2005) Symmetry at the active site of the ribosome: structural and functional implications. Biol Chem 386:833–844. https://doi.org/10.1515/BC.2005.098

    Article  CAS  PubMed  Google Scholar 

  7. Noller HF (2012) Evolution of protein synthesis from an RNA world. Cold Spring Harb Perspect Biol 4:a003681. https://doi.org/10.1101/cshperspect.a003681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Melnikov S, Ben-Shem A, Garreau de Loubresse N, Jenner L, Yusupova G, Yusupov M (2012) One core, two shells: bacterial and eukaryotic ribosomes. Nat Struct Mol Biol 19:560–567. https://doi.org/10.1038/nsmb.2313

    Article  CAS  PubMed  Google Scholar 

  9. Bowman JC, Petrov AS, Frenkel-Pinter M, Penev PI, Williams LD (2020) Root of the tree: the significance, evolution, and origins of the ribosome. Chem Rev, American Chemical Society 120:4848–4878. https://doi.org/10.1021/acs.chemrev.9b00742

    Article  CAS  Google Scholar 

  10. Gray MW, Burger G, Lang BF (2001) The origin and early evolution of mitochondria. Genome Biol 2:REVIEWS1018. https://doi.org/10.1186/gb-2001-2-6-reviews1018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Martijn J, Vosseberg J, Guy L, Offre P, Ettema TJG (2018) Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature, Nature Publishing Group 557:101–105. https://doi.org/10.1038/s41586-018-0059-5

    Article  CAS  Google Scholar 

  12. Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, van Eijk R, Schleper C, Guy L, Ettema TJG (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature, Nature Publishing Group 521:173–179. https://doi.org/10.1038/nature14447

    Article  CAS  Google Scholar 

  13. Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckström D, Juzokaite L, Vancaester E, Seitz KW, Anantharaman K, Starnawski P, Kjeldsen KU, Stott MB, Nunoura T, Banfield JF, Schramm A, Baker BJ, Spang A, Ettema TJG (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature, Nature Publishing Group 541:353–358. https://doi.org/10.1038/nature21031

    Article  CAS  Google Scholar 

  14. O’Brien TW (2002) Evolution of a protein-rich mitochondrial ribosome: implications for human genetic disease. Gene 286:73–79. https://doi.org/10.1016/s0378-1119(01)00808-3

    Article  PubMed  Google Scholar 

  15. Waltz F, Giegé P (2020) Striking diversity of mitochondria-specific translation processes across eukaryotes. Trends Biochem Sci, Elsevier 45:149–162. https://doi.org/10.1016/j.tibs.2019.10.004

    Article  CAS  Google Scholar 

  16. Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK (2003) Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115:97–108. https://doi.org/10.1016/s0092-8674(03)00762-1

    Article  CAS  PubMed  Google Scholar 

  17. Frank J, Agrawal RK, Verschoor A (2001) Ribosome structure and shape. In: Encyclopedia of life sciences. John Wiley & Sons, Ltd., London, pp 1–6

    Google Scholar 

  18. Frank J, Zhu J, Penczek P, Li Y, Srivastava S, Verschoor A, Radermacher M, Grassucci R, Lata RK, Agrawal RK (1995) A model of protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature, Nature Publishing Group 376:441–444. https://doi.org/10.1038/376441a0

    Article  CAS  Google Scholar 

  19. Temperley RJ, Wydro M, Lightowlers RN, Chrzanowska-Lightowlers ZM (2010) Human mitochondrial MRNAs--like members of all families, similar but different. Biochim Biophys Acta 1797:1081–1085. https://doi.org/10.1016/j.bbabio.2010.02.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Mears JA, Sharma MR, Gutell RR, McCook AS, Richardson PE, Caulfield TR, Agrawal RK, Harvey SC (2006) A structural model for the large subunit of the mammalian mitochondrial ribosome. J Mol Biol 358:193–212. https://doi.org/10.1016/j.jmb.2006.01.094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Brown A, Amunts A, Bai X, Sugimoto Y, Edwards PC, Murshudov G, Scheres SHW, Ramakrishnan V (2014) Structure of the large ribosomal subunit from human mitochondria. Science, American Association for the Advancement of Science 346:718–722. https://doi.org/10.1126/science.1258026

    Article  CAS  Google Scholar 

  22. Greber BJ, Boehringer D, Leitner A, Bieri P, Voigts-Hoffmann F, Erzberger JP, Leibundgut M, Aebersold R, Ban N (2014) Architecture of the large subunit of the mammalian mitochondrial ribosome. Nature, Nature Publishing Group 505:515–519. https://doi.org/10.1038/nature12890

    Article  CAS  Google Scholar 

  23. Sharma MR, Kaushal PS, Gupta M, Banavali NK, Agrawal RK (2013) Insights into structural basis of mammalian mitochondrial translation. In: Duchêne A-M (ed) Translation in mitochondria and other organelles. Springer, Berlin, Heidelberg, pp 1–28. https://doi.org/10.1007/978-3-642-39426-3_1

    Chapter  Google Scholar 

  24. Amunts A, Brown A, Toots J, Scheres SHW, Ramakrishnan V (2015) The structure of the human mitochondrial ribosome. Science, American Association for the Advancement of Science 348:95–98. https://doi.org/10.1126/science.aaa1193

    Article  CAS  Google Scholar 

  25. Greber BJ, Bieri P, Leibundgut M, Leitner A, Aebersold R, Boehringer D, Ban N (2015) The complete structure of the 55S mammalian mitochondrial ribosome. Science, American Association for the Advancement of Science 348:303–308. https://doi.org/10.1126/science.aaa3872

    Article  CAS  Google Scholar 

  26. Kaushal PS, Sharma MR, Booth TM, Haque EM, Tung C-S, Sanbonmatsu KY, Spremulli LL, Agrawal RK (2014) Cryo-EM structure of the small subunit of the mammalian mitochondrial ribosome. Proc Natl Acad Sci U S A, Proceedings of the National Academy of Sciences 111:7284–7289. https://doi.org/10.1073/pnas.1401657111

    Article  CAS  Google Scholar 

  27. Koripella RK, Sharma MR, Bhargava K, Datta PP, Kaushal PS, Keshavan P, Spremulli LL, Banavali NK, Agrawal RK (2020) Structures of the human mitochondrial ribosome bound to EF-G1 reveal distinct features of mitochondrial translation elongation. Nat Commun, Nature Publishing Group 11:3830. https://doi.org/10.1038/s41467-020-17715-2

    Article  CAS  Google Scholar 

  28. Koripella RK, Sharma MR, Haque ME, Risteff P, Spremulli LL, Agrawal RK (2019) Structure of human mitochondrial translation initiation factor 3 bound to the small ribosomal subunit. iScience 12:76–86. https://doi.org/10.1016/j.isci.2018.12.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Desai N, Brown A, Amunts A, Ramakrishnan V (2017) The structure of the yeast mitochondrial ribosome. Science, American Association for the Advancement of Science 355:528–531. https://doi.org/10.1126/science.aal2415

    Article  CAS  Google Scholar 

  30. Itoh Y, Naschberger A, Mortezaei N, Herrmann JM, Amunts A (2020) Analysis of translating mitoribosome reveals functional characteristics of translation in mitochondria of fungi. Nat Commun, Nature Publishing Group 11:5187. https://doi.org/10.1038/s41467-020-18830-w

    Article  CAS  Google Scholar 

  31. Tobiasson V, Amunts A (2020) Ciliate mitoribosome illuminates evolutionary steps of mitochondrial translation. Wolberger, C., Ed. eLife, eLife Sciences Publications, Ltd 9:e59264. https://doi.org/10.7554/eLife.59264

  32. Ramrath DJF, Niemann M, Leibundgut M, Bieri P, Prange C, Horn EK, Leitner A, Boehringer D, Schneider A, Ban N (2018) Evolutionary shift toward protein-based architecture in trypanosomal mitochondrial ribosomes. Science 362:eaau7735. https://doi.org/10.1126/science.aau7735

    Article  CAS  PubMed  Google Scholar 

  33. Soufari H, Waltz F, Parrot C, Durrieu-Gaillard S, Bochler A, Kuhn L, Sissler M, Hashem Y (2020) Structure of the mature kinetoplastids mitoribosome and insights into its large subunit biogenesis. Proc Natl Acad Sci U S A, Proceedings of the National Academy of Sciences 117:29851–29861. https://doi.org/10.1073/pnas.2011301117

    Article  CAS  Google Scholar 

  34. Waltz F, Nguyen T-T, Arrivé M, Bochler A, Chicher J, Hammann P, Kuhn L, Quadrado M, Mireau H, Hashem Y, Giegé P (2019) Small is big in Arabidopsis mitochondrial ribosome. Nat Plants, Nature Publishing Group 5:106–117. https://doi.org/10.1038/s41477-018-0339-y

    Article  CAS  Google Scholar 

  35. Waltz F, Soufari H, Bochler A, Giegé P, Hashem Y (2020) Cryo-EM structure of the RNA-rich plant mitochondrial ribosome. Nat Plants, Nature Publishing Group 6:377–383. https://doi.org/10.1038/s41477-020-0631-5

    Article  Google Scholar 

  36. Tobiasson V, Berzina I, Amunts A (2022) Structure of a mitochondrial ribosome with fragmented RRNA in complex with membrane-targeting elements. Nat Commun, Nature Publishing Group 13:6132. https://doi.org/10.1038/s41467-022-33582-5

    Article  CAS  Google Scholar 

  37. Waltz F, Salinas-Giegé T, Englmeier R, Meichel H, Soufari H, Kuhn L, Pfeffer S, Förster F, Engel BD, Giegé P, Drouard L, Hashem Y (2021) How to build a ribosome from RNA fragments in Chlamydomonas mitochondria. Nat Commun, Nature Publishing Group 12:7176. https://doi.org/10.1038/s41467-021-27200-z

    Article  CAS  Google Scholar 

  38. Maly P, Brimacombe R (1983) Refined secondary structure models for the 16S and 23S ribosomal RNA of Escherichia coli. Nucleic Acids Res 11:7263–7286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Feagin JE, Harrell MI, Lee JC, Coe KJ, Sands BH, Cannone JJ, Tami G, Schnare MN, Gutell RR (2012) The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum. PLoS One, Public Library of Science 7:e38320. https://doi.org/10.1371/journal.pone.0038320

    Article  Google Scholar 

  40. Rorbach J, Gao F, Powell CA, D’Souza A, Lightowlers RN, Minczuk M, Chrzanowska-Lightowlers ZM (2016) Human mitochondrial ribosomes can switch their structural RNA composition. Proc Natl Acad Sci U S A 113:12198–12201. https://doi.org/10.1073/pnas.1609338113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Christian BE, Spremulli LL (2012) Mechanism of protein biosynthesis in mammalian mitochondria. Biochim Biophys Acta 1819:1035–1054. https://doi.org/10.1016/j.bbagrm.2011.11.009

    Article  CAS  PubMed  Google Scholar 

  42. Yassin AS, Haque ME, Datta PP, Elmore K, Banavali NK, Spremulli LL, Agrawal RK (2011) Insertion domain within mammalian mitochondrial translation initiation factor 2 serves the role of eubacterial initiation factor 1. Proc Natl Acad Sci U S A 108:3918–3923. https://doi.org/10.1073/pnas.1017425108

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kummer E, Leibundgut M, Rackham O, Lee RG, Boehringer D, Filipovska A, Ban N (2018) Unique features of mammalian mitochondrial translation initiation revealed by cryo-EM. Nature 560:263–267. https://doi.org/10.1038/s41586-018-0373-y

    Article  CAS  PubMed  Google Scholar 

  44. Khawaja A, Itoh Y, Remes C, Spåhr H, Yukhnovets O, Höfig H, Amunts A, Rorbach J (2020) Distinct pre-initiation steps in human mitochondrial translation. Nat Commun 11:2932. https://doi.org/10.1038/s41467-020-16503-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Kummer E, Ban N (2020) Structural insights into mammalian mitochondrial translation elongation catalyzed by MtEFG1. EMBO J 39:e104820. https://doi.org/10.15252/embj.2020104820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Desai N, Yang H, Chandrasekaran V, Kazi R, Minczuk M, Ramakrishnan V (2020) Elongational stalling activates mitoribosome-associated quality control. Science 370:1105–1110. https://doi.org/10.1126/science.abc7782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kummer E, Schubert KN, Schoenhut T, Scaiola A, Ban N (2021) Structural basis of translation termination, rescue, and recycling in mammalian mitochondria. Mol Cell 81:2566–2582.e6. https://doi.org/10.1016/j.molcel.2021.03.042

    Article  CAS  PubMed  Google Scholar 

  48. Koripella RK, Sharma MR, Risteff P, Keshavan P, Agrawal RK (2019) Structural insights into unique features of the human mitochondrial ribosome recycling. Proc Natl Acad Sci U S A 116:8283–8288. https://doi.org/10.1073/pnas.1815675116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Koripella RK, Deep A, Agrawal EK, Keshavan P, Banavali NK, Agrawal RK (2021) Distinct mechanisms of the human mitoribosome recycling and antibiotic resistance. Nat Commun 12:3607. https://doi.org/10.1038/s41467-021-23726-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Aibara S, Singh V, Modelska A, Amunts A (2020) Structural basis of mitochondrial translation. eLife 9:e58362. https://doi.org/10.7554/eLife.58362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Watanabe K (2010) Unique features of animal mitochondrial translation systems. The non-universal genetic code, unusual features of the translational apparatus and their relevance to human mitochondrial diseases. Proc Jpn Acad Ser B Phys Biol Sci 86:11–39. https://doi.org/10.2183/pjab.86.11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Itoh Y, Khawaja A, Laptev I, Cipullo M, Atanassov I, Sergiev P, Rorbach J, Amunts A (2022) Mechanism of mitoribosomal small subunit biogenesis and preinitiation. Nature, Nature Publishing Group 606:603–608. https://doi.org/10.1038/s41586-022-04795-x

    Article  CAS  Google Scholar 

  53. Amunts A, Brown A, Bai X, Llácer JL, Hussain T, Emsley P, Long F, Murshudov G, Scheres SHW, Ramakrishnan V (2014) Structure of the yeast mitochondrial large ribosomal subunit. Science, American Association for the Advancement of Science 343:1485–1489. https://doi.org/10.1126/science.1249410

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the National Institutes of Health grant R01 GM61576 (to R.K.A.). R.K.A. also acknowledges the financial support to his lab through following NIH grants: R01 GM139277, R01 AI132422, and R01 AI155473. The authors thank Dr. Nilesh Banavali for critical reading of the manuscript.

Author information

Authors and Affiliations

  1. Division of Translational Medicine, Wadsworth Center, New York State Department of Health Empire State Plaza, Albany, NY, USA

    Rajendra K. Agrawal & Soneya Majumdar

  2. Department of Biomedical Sciences, University at Albany, SUNY, Rensselaer, NY, USA

    Rajendra K. Agrawal

Authors
  1. Rajendra K. Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Soneya Majumdar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rajendra K. Agrawal .

Editor information

Editors and Affiliations

  1. Miller School of Medicine, University of Miami, Miami, FL, USA

    Antoni Barrientos

  2. Miller School of Medicine, University of Miami, Miami, FL, USA

    Flavia Fontanesi

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Agrawal, R.K., Majumdar, S. (2023). Evolution: Mitochondrial Ribosomes Across Species. In: Barrientos, A., Fontanesi, F. (eds) The Mitoribosome. Methods in Molecular Biology, vol 2661. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3171-3_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-3171-3_2

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-3170-6

  • Online ISBN: 978-1-0716-3171-3

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation