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Previous biochemical studies indicated that the TOM complex functions as a trimer and exists in a dynamic equilibrium with a Tom22\u2010lacking dimer in intact mitochondria. In contrast, recent cryo\u2010electron microscopy (cryo\u2010EM) studies revealed near\u2010atomic structures of the Tom22\u2010containing core dimer. However, the relationship between the core dimer and the functional trimer remains unclear. Here, we analyzed the oligomeric organization and structural properties of purified yeast TOM complexes using high\u2010speed atomic force microscopy (HS\u2010AFM). Purified yeast TOM complexes predominantly adopted a trimeric organization but underwent deformation and dissociation during repeated HS\u2010AFM scanning, leaving dimeric and monomeric particles. Trimeric particles exhibited spherical shapes consistent with previous crosslinking models, whereas dissociated dimers closely resembled TOM core\u2010dimer structures determined by cryo\u2010EM. HS\u2010AFM also revealed the peripheral localization of the Tom20 receptor and enabled direct visualization of substrate\u2013TOM interactions, with TOM association accompanied by reduced substrate mobility. Together, these findings provide quantitative and structural evidence for a predominantly trimeric organization of the purified TOM complex and suggest that the trimer contains a stable core\u2010dimer unit with a more loosely associated third Tom40\u2010containing unit.<\/jats:p>","DOI":"10.1111\/gtc.70154","type":"journal-article","created":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T07:34:43Z","timestamp":1792827283000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Characterization of the Trimeric\n                    <scp>TOM<\/scp>\n                    Complex by\n                    <scp>HS<\/scp>\n                    \u2010\n                    <scp>AFM<\/scp>\n                    Single\u2010Molecule Analysis"],"prefix":"10.1111","volume":"31","author":[{"given":"Nanako","family":"Kobayashi","sequence":"first","affiliation":[{"name":"Department of Clinical Laboratory Science Graduate School of Medical Science, Kanazawa University  Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi N.","family":"Omura","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences Graduate School of Science, the University of Tokyo  Tokyo Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kana","family":"Kuzasa","sequence":"additional","affiliation":[{"name":"Department of Clinical Laboratory Science Graduate School of Medical Science, Kanazawa University  Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenichiro","family":"Imai","sequence":"additional","affiliation":[{"name":"Cellular and Molecular Biotechnology Reserach Institute (CMB), National Institute of Advanced Industrial Science and Technology (AIST)  Tokyo Japan"},{"name":"Integrated Reserach Center for Self\u2010Care Technology (IRC\u2010SRT), National Institute of Advanced Industrial Science and Technology (AIST)  Tokyo Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shiho","family":"Kawai","sequence":"additional","affiliation":[{"name":"Department of Clinical Laboratory Science Graduate School of Medical Science, Kanazawa University  Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hirotatsu","family":"Imai","sequence":"additional","affiliation":[{"name":"Department of Biochemistry Graduate School of Medicine, University of the Ryukyus  Ginowan Japan"},{"name":"WPI\u2010Nano Life Science Institute, Kanazawa University  Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Romain","family":"Amyot","sequence":"additional","affiliation":[{"name":"WPI\u2010Nano Life Science Institute, Kanazawa University  Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3650-3828","authenticated-orcid":false,"given":"Kenichi","family":"Umeda","sequence":"additional","affiliation":[{"name":"WPI\u2010Nano Life Science Institute, Kanazawa University  Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Osamu","family":"Nureki","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences Graduate School of Science, the University of Tokyo  Tokyo Japan"},{"name":"Institute of Science Tokyo, Institute of Integrated Research, Cell Biology Center  Yokohama Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8548-1584","authenticated-orcid":false,"given":"Toshiya","family":"Endo","sequence":"additional","affiliation":[{"name":"Faculty of Life Sciences Kyoto Sangyo University  Kyoto Japan"},{"name":"Institute for Protein Dynamics, Kyoto Sangyo University  Kyoto Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4880-8423","authenticated-orcid":false,"given":"Noriyuki","family":"Kodera","sequence":"additional","affiliation":[{"name":"WPI\u2010Nano Life Science Institute, Kanazawa University  Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8223-7858","authenticated-orcid":false,"given":"Yuhei","family":"Araiso","sequence":"additional","affiliation":[{"name":"Department of Clinical Laboratory Science Graduate School of Medical Science, Kanazawa University  Kanazawa Japan"},{"name":"Environmental Stress Research Center (eSRC), Kanazawa University  Ginowan Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,10,24]]},"reference":[{"issue":"29","key":"e_1_2_11_2_1","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2507279122","article-title":"Structures of Chaetomium thermophilum TOM Complexes With Bound Preproteins","volume":"122","author":"Agip A. A.","year":"2025","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"11","key":"e_1_2_11_3_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1008444","article-title":"BioAFMviewer: An Interactive Interface for Simulated AFM Scanning of Biomolecular Structures and Dynamics","volume":"16","author":"Amyot R.","year":"2020","journal-title":"PLoS Computational Biology"},{"issue":"1","key":"e_1_2_11_4_1","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1146\/annurev-biophys-030722-113353","article-title":"High\u2010Speed Atomic Force Microscopy for Filming Protein Molecules in Dynamic Action","volume":"53","author":"Ando T.","year":"2024","journal-title":"Annual Review of Biophysics"},{"issue":"22","key":"e_1_2_11_5_1","doi-asserted-by":"crossref","first-page":"12468","DOI":"10.1073\/pnas.211400898","article-title":"A High\u2010Speed Atomic Force Microscope for Studying Biological Macromolecules","volume":"98","author":"Ando T.","year":"2001","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"e_1_2_11_6_1","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.progsurf.2008.09.001","article-title":"High\u2010Speed Atomic Force Microscopy for Nano\u2010Visualization of Dynamic Biomolecular Processes","volume":"83","author":"Ando T.","year":"2008","journal-title":"Progress in Surface Science"},{"issue":"18","key":"e_1_2_11_7_1","doi-asserted-by":"crossref","first-page":"5300","DOI":"10.1111\/febs.15661","article-title":"Structural Snapshot of the Mitochondrial Protein Import Gate","volume":"288","author":"Araiso Y.","year":"2020","journal-title":"FEBS Journal"},{"key":"e_1_2_11_8_1","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1146\/annurev-biochem-032620-104527","article-title":"Role of the TOM Complex in Protein Import Into Mitochondria: Structural Views","volume":"91","author":"Araiso Y.","year":"2022","journal-title":"Annual Review of Biochemistry"},{"issue":"7782","key":"e_1_2_11_9_1","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1038\/s41586-019-1680-7","article-title":"Structure of the Mitochondrial Import Gate Reveals Distinct Preprotein Paths","volume":"575","author":"Araiso Y.","year":"2019","journal-title":"Nature"},{"issue":"6302","key":"e_1_2_11_10_1","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1038\/348605a0","article-title":"A Yeast Mitochondrial Outer Membrane Protein Essential for Protein Import and Cell Viability","volume":"348","author":"Baker K. 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Molecular Cell Biology"},{"issue":"3","key":"e_1_2_11_29_1","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/nmeth.4169","article-title":"cryoSPARC: Algorithms for Rapid Unsupervised Cryo\u2010EM Structure Determination","volume":"14","author":"Punjani A.","year":"2017","journal-title":"Nature Methods"},{"key":"e_1_2_11_30_1","doi-asserted-by":"crossref","first-page":"1214","DOI":"10.1038\/s41592-020-00990-8","article-title":"Non\u2010Uniform Refinement: Adaptive Regularization Improves Single\u2010Particle Cryo\u2010EM Reconstruction","volume":"17","author":"Punjani A.","year":"2020","journal-title":"Nature Methods"},{"issue":"4","key":"e_1_2_11_31_1","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1016\/j.jmb.2003.07.013","article-title":"Optimal Determination of Particle Orientation, Absolute Hand, and Contrast Loss in Single\u2010Particle Electron Cryomicroscopy","volume":"333","author":"Rosenthal P. 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Sciences"},{"key":"e_1_2_11_35_1","doi-asserted-by":"crossref","DOI":"10.1093\/pnasnexus\/pgae269","article-title":"Structure of the Intact Tom20 Receptor in the Human Translocase of the Outer Membrane Complex","volume":"3","author":"Su F.","year":"2024","journal-title":"PNAS Nexus"},{"key":"e_1_2_11_36_1","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2200158119","article-title":"Structural Basis of Tom20 and Tom22 Cytosolic Domains as the Human TOM Complex Receptors","volume":"119","author":"Su J.","year":"2022","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"12","key":"e_1_2_11_37_1","doi-asserted-by":"crossref","first-page":"1158","DOI":"10.1038\/s41594-019-0339-2","article-title":"Cryo\u2010EM Structure of the Mitochondrial Protein\u2010Import Channel TOM Complex at Near\u2010Atomic Resolution","volume":"26","author":"Tucker K.","year":"2019","journal-title":"Nature Structural & Molecular 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D.","year":"1989","journal-title":"Nature"},{"key":"e_1_2_11_41_1","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/s41421-020-00198-2","article-title":"Atomic Structure of Human TOM Core Complex","volume":"6","author":"Wang W.","year":"2020","journal-title":"Cell Discovery"},{"issue":"7","key":"e_1_2_11_42_1","doi-asserted-by":"crossref","first-page":"3799","DOI":"10.1074\/jbc.M708339200","article-title":"Tom20 and Tom22 Share the Common Signal Recognition Pathway in Mitochondrial Protein Import","volume":"283","author":"Yamano K.","year":"2008","journal-title":"Journal of Biological Chemistry"}],"container-title":["Genes to 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