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Self-recognition mechanism of MamA, a magnetosome-associated TPR-containing protein, promotes complex assembly.

Zeytuni N, Ozyamak E, Ben-Harush K, Davidov G, Levin M, Gat Y, Moyal T, Brik A, Komeili A, Zarivach R
Proc Natl Acad Sci U S A 108 E480-7 (2011)
Related entries: 3as4, 3as8, 3asd, 3asf, 3asg, 3ash

Cited: 55 times
EuropePMC logo PMID: 21784982

Abstract

The magnetosome, a biomineralizing organelle within magnetotactic bacteria, allows their navigation along geomagnetic fields. Magnetosomes are membrane-bound compartments containing magnetic nanoparticles and organized into a chain within the cell, the assembly and biomineralization of magnetosomes are controlled by magnetosome-associated proteins. Here, we describe the crystal structures of the magnetosome-associated protein, MamA, from Magnetospirillum magneticum AMB-1 and Magnetospirillum gryphiswaldense MSR-1. MamA folds as a sequential tetra-trico-peptide repeat (TPR) protein with a unique hook-like shape. Analysis of the MamA structures indicates two distinct domains that can undergo conformational changes. Furthermore, structural analysis of seven crystal forms verified that the core of MamA is not affected by crystallization conditions and identified three protein-protein interaction sites, namely a concave site, a convex site, and a putative TPR repeat. Additionally, relying on transmission electron microscopy and size exclusion chromatography, we show that highly stable complexes form upon MamA homooligomerization. Disruption of the MamA putative TPR motif or N-terminal domain led to protein mislocalization in vivo and prevented MamA oligomerization in vitro. We, therefore, propose that MamA self-assembles through its putative TPR motif and its concave site to create a large homooligomeric scaffold which can interact with other magnetosome-associated proteins via the MamA convex site. We discuss the structural basis for TPR homooligomerization that allows the proper function of a prokaryotic organelle.

Articles - 3as5 mentioned but not cited (3)

  1. Self-recognition mechanism of MamA, a magnetosome-associated TPR-containing protein, promotes complex assembly. Zeytuni N, Ozyamak E, Ben-Harush K, Davidov G, Levin M, Gat Y, Moyal T, Brik A, Komeili A, Zarivach R. Proc Natl Acad Sci U S A 108 E480-7 (2011)
  2. MamA as a Model Protein for Structure-Based Insight into the Evolutionary Origins of Magnetotactic Bacteria. Zeytuni N, Cronin S, Lefèvre CT, Arnoux P, Baran D, Shtein Z, Davidov G, Zarivach R. PLoS One 10 e0130394 (2015)
  3. StaRProtein, a web server for prediction of the stability of repeat proteins. Xu Y, Zhou X, Huang M. PLoS One 10 e0119417 (2015)


Reviews citing this publication (22)

  1. Structural and functional discussion of the tetra-trico-peptide repeat, a protein interaction module. Zeytuni N, Zarivach R. Structure 20 397-405 (2012)
  2. Magnetosome biogenesis in magnetotactic bacteria. Uebe R, Schüler D. Nat Rev Microbiol 14 621-637 (2016)
  3. Ecology, diversity, and evolution of magnetotactic bacteria. Lefèvre CT, Bazylinski DA. Microbiol Mol Biol Rev 77 497-526 (2013)
  4. Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria. Komeili A. FEMS Microbiol Rev 36 232-255 (2012)
  5. Tetratricopeptide repeat motifs in the world of bacterial pathogens: role in virulence mechanisms. Cerveny L, Straskova A, Dankova V, Hartlova A, Ceckova M, Staud F, Stulik J. Infect Immun 81 629-635 (2013)
  6. Natural inorganic nanoparticles--formation, fate, and toxicity in the environment. Sharma VK, Filip J, Zboril R, Varma RS. Chem Soc Rev 44 8410-8423 (2015)
  7. Biomineralization-inspired synthesis of functional organic/inorganic hybrid materials: organic molecular control of self-organization of hybrids. Arakaki A, Shimizu K, Oda M, Sakamoto T, Nishimura T, Kato T. Org Biomol Chem 13 974-989 (2015)
  8. From bacteria to mollusks: the principles underlying the biomineralization of iron oxide materials. Faivre D, Godec TU. Angew Chem Int Ed Engl 54 4728-4747 (2015)
  9. Magnetotactic bacteria as potential sources of bioproducts. Araujo AC, Abreu F, Silva KT, Bazylinski DA, Lins U. Mar Drugs 13 389-430 (2015)
  10. Evolution of the bacterial organelle responsible for magnetotaxis. Lefèvre CT, Wu LF. Trends Microbiol 21 534-543 (2013)
  11. Organelle Formation in Bacteria and Archaea. Grant CR, Wan J, Komeili A. Annu Rev Cell Dev Biol 34 217-238 (2018)
  12. Biogenesis and subcellular organization of the magnetosome organelles of magnetotactic bacteria. Greene SE, Komeili A. Curr Opin Cell Biol 24 490-495 (2012)
  13. From invagination to navigation: The story of magnetosome-associated proteins in magnetotactic bacteria. Barber-Zucker S, Keren-Khadmy N, Zarivach R. Protein Sci 25 338-351 (2016)
  14. Physiological origin of biogenic magnetic nanoparticles in health and disease: from bacteria to humans. Gorobets O, Gorobets S, Koralewski M. Int J Nanomedicine 12 4371-4395 (2017)
  15. The Potential of Intrinsically Magnetic Mesenchymal Stem Cells for Tissue Engineering. Kerans FFA, Lungaro L, Azfer A, Salter DM. Int J Mol Sci 19 E3159 (2018)
  16. Bioinspired Magnetic Nanochains for Medicine. Kralj S, Marchesan S. Pharmaceutics 13 1262 (2021)
  17. TTC3-Mediated Protein Quality Control, A Potential Mechanism for Cognitive Impairment. Zhou X, Chen X, Hong T, Zhang M, Cai Y, Cui L. Cell Mol Neurobiol 42 1659-1669 (2022)
  18. Current view of iron biomineralization in magnetotactic bacteria. Ben-Shimon S, Stein D, Zarivach R. J Struct Biol X 5 100052 (2021)
  19. Intrinsically Magnetic Cells: A Review on Their Natural Occurrence and Synthetic Generation. Pekarsky A, Spadiut O. Front Bioeng Biotechnol 8 573183 (2020)
  20. Translating the Arabidopsis thaliana Peroxisome Proteome Insights to Solanum lycopersicum: Consensus Versus Diversity. Tarafdar S, Chowdhary G. Front Cell Dev Biol 10 909604 (2022)
  21. Biosensors and Drug Delivery in Oncotheranostics Using Inorganic Synthetic and Biogenic Magnetic Nanoparticles. Zimina TM, Sitkov NO, Gareev KG, Fedorov V, Grouzdev D, Koziaeva V, Gao H, Combs SE, Shevtsov M. Biosensors (Basel) 12 789 (2022)
  22. Hypomagnetic Conditions and Their Biological Action (Review). Sarimov RM, Serov DA, Gudkov SV. Biology (Basel) 12 1513 (2023)

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  1. Comparative genomic analysis of magnetotactic bacteria from the Deltaproteobacteria provides new insights into magnetite and greigite magnetosome genes required for magnetotaxis. Lefèvre CT, Trubitsyn D, Abreu F, Kolinko S, Jogler C, de Almeida LG, de Vasconcelos AT, Kube M, Reinhardt R, Lins U, Pignol D, Schüler D, Bazylinski DA, Ginet N. Environ Microbiol 15 2712-2735 (2013)
  2. Genetic dissection of the mamAB and mms6 operons reveals a gene set essential for magnetosome biogenesis in Magnetospirillum gryphiswaldense. Lohße A, Borg S, Raschdorf O, Kolinko I, Tompa E, Pósfai M, Faivre D, Baumgartner J, Schüler D. J Bacteriol 196 2658-2669 (2014)
  3. Structure prediction of magnetosome-associated proteins. Nudelman H, Zarivach R. Front Microbiol 5 9 (2014)
  4. Spatio-temporal assembly of functional mineral scaffolds within microbial biofilms. Oppenheimer-Shaanan Y, Sibony-Nevo O, Bloom-Ackermann Z, Suissa R, Steinberg N, Kartvelishvily E, Brumfeld V, Kolodkin-Gal I. NPJ Biofilms Microbiomes 2 15031 (2016)
  5. A tailored galK counterselection system for efficient markerless gene deletion and chromosomal tagging in Magnetospirillum gryphiswaldense. Raschdorf O, Plitzko JM, Schüler D, Müller FD. Appl Environ Microbiol 80 4323-4330 (2014)
  6. Cation diffusion facilitators transport initiation and regulation is mediated by cation induced conformational changes of the cytoplasmic domain. Zeytuni N, Uebe R, Maes M, Davidov G, Baram M, Raschdorf O, Nadav-Tsubery M, Kolusheva S, Bitton R, Goobes G, Friedler A, Miller Y, Schüler D, Zarivach R. PLoS One 9 e92141 (2014)
  7. Hybrid Sterility in Rice (Oryza sativa L.) Involves the Tetratricopeptide Repeat Domain Containing Protein. Yu Y, Zhao Z, Shi Y, Tian H, Liu L, Bian X, Xu Y, Zheng X, Gan L, Shen Y, Wang C, Yu X, Wang C, Zhang X, Guo X, Wang J, Ikehashi H, Jiang L, Wan J. Genetics 203 1439-1451 (2016)
  8. Magnetospira thiophila gen. nov., sp. nov., a marine magnetotactic bacterium that represents a novel lineage within the Rhodospirillaceae (Alphaproteobacteria). Williams TJ, Lefèvre CT, Zhao W, Beveridge TJ, Bazylinski DA. Int J Syst Evol Microbiol 62 2443-2450 (2012)
  9. Expanding magnetic organelle biogenesis in the domain Bacteria. Lin W, Zhang W, Paterson GA, Zhu Q, Zhao X, Knight R, Bazylinski DA, Roberts AP, Pan Y. Microbiome 8 152 (2020)
  10. Overproduction of Magnetosomes by Genomic Amplification of Biosynthesis-Related Gene Clusters in a Magnetotactic Bacterium. Lohße A, Kolinko I, Raschdorf O, Uebe R, Borg S, Brachmann A, Plitzko JM, Müller R, Zhang Y, Schüler D. Appl Environ Microbiol 82 3032-3041 (2016)
  11. Control of magnetite nanocrystal morphology in magnetotactic bacteria by regulation of mms7 gene expression. Yamagishi A, Tanaka M, Lenders JJ, Thiesbrummel J, Sommerdijk NA, Matsunaga T, Arakaki A. Sci Rep 6 29785 (2016)
  12. Bacterial magnetosome biomineralization--a novel platform to study molecular mechanisms of human CDF-related Type-II diabetes. Zeytuni N, Uebe R, Maes M, Davidov G, Baram M, Raschdorf O, Friedler A, Miller Y, Schüler D, Zarivach R. PLoS One 9 e97154 (2014)
  13. Crystal structure of c5321: a protective antigen present in uropathogenic Escherichia coli strains displaying an SLR fold. Urosev D, Ferrer-Navarro M, Pastorello I, Cartocci E, Costenaro L, Zhulenkovs D, Maréchal JD, Leonchiks A, Reverter D, Serino L, Soriani M, Daura X. BMC Struct Biol 13 19 (2013)
  14. Human apo-SRP72 and SRP68/72 complex structures reveal the molecular basis of protein translocation. Gao Y, Zhang Q, Lang Y, Liu Y, Dong X, Chen Z, Tian W, Tang J, Wu W, Tong Y, Chen Z. J Mol Cell Biol 9 220-230 (2017)
  15. Structural basis for isoform-specific kinesin-1 recognition of Y-acidic cargo adaptors. Pernigo S, Chegkazi MS, Yip YY, Treacy C, Glorani G, Hansen K, Politis A, Bui S, Dodding MP, Steiner RA. Elife 7 e38362 (2018)
  16. Structure and Interactions of the TPR Domain of Sgt2 with Yeast Chaperones and Ybr137wp. Krysztofinska EM, Evans NJ, Thapaliya A, Murray JW, Morgan RML, Martinez-Lumbreras S, Isaacson RL. Front Mol Biosci 4 68 (2017)
  17. Comparative Subcellular Localization Analysis of Magnetosome Proteins Reveals a Unique Localization Behavior of Mms6 Protein onto Magnetite Crystals. Arakaki A, Kikuchi D, Tanaka M, Yamagishi A, Yoda T, Matsunaga T. J Bacteriol 198 2794-2802 (2016)
  18. A protein-protein interaction in magnetosomes: TPR protein MamA interacts with an Mms6 protein. Nguyen HV, Suzuki E, Oestreicher Z, Minamide H, Endoh H, Fukumori Y, Taoka A. Biochem Biophys Rep 7 39-44 (2016)
  19. Exploring ligand recognition, selectivity and dynamics of TPR domains of chloroplast Toc64 and mitochondria Om64 from Arabidopsis thaliana. Panigrahi R, Whelan J, Vrielink A. J Mol Recognit 27 402-414 (2014)
  20. Screening for the interacting partners of the proteins MamK & MamJ by two-hybrid genomic DNA library of Magnetospirillum magneticum AMB-1. Pan W, Xie C, Lv J. Curr Microbiol 64 515-523 (2012)
  21. Ligand recognition by the TPR domain of the import factor Toc64 from Arabidopsis thaliana. Panigrahi R, Adina-Zada A, Whelan J, Vrielink A. PLoS One 8 e83461 (2013)
  22. Core Amino Acid Residues in the Morphology-Regulating Protein, Mms6, for Intracellular Magnetite Biomineralization. Yamagishi A, Narumiya K, Tanaka M, Matsunaga T, Arakaki A. Sci Rep 6 35670 (2016)
  23. Genes encoding Cher-TPR fusion proteins are predominantly found in gene clusters encoding chemosensory pathways with alternative cellular functions. Muñoz-Martínez F, García-Fontana C, Rico-Jiménez M, Alfonso C, Krell T. PLoS One 7 e45810 (2012)
  24. Ssn6-Tup1 global transcriptional co-repressor: Role of the N-terminal glutamine-rich region of Ssn6. Tartas A, Zarkadas C, Palaiomylitou M, Gounalaki N, Tzamarias D, Vlassi M. PLoS One 12 e0186363 (2017)
  25. Structure and evolution of the magnetochrome domains: no longer alone. Arnoux P, Siponen MI, Lefèvre CT, Ginet N, Pignol D. Front Microbiol 5 117 (2014)
  26. Crystal structures of the amino-terminal domain of LpoA from Escherichia coli and Haemophilus influenzae. Kelley A, Vijayalakshmi J, Saper MA. Acta Crystallogr F Struct Biol Commun 75 368-376 (2019)
  27. Novel Protein Mg2046 Regulates Magnetosome Synthesis in Magnetospirillum gryphiswaldense MSR-1 by Modulating a Proper Redox Status. Wang X, Zheng H, Wang Q, Jiang W, Wen Y, Tian J, Sun J, Li Y, Li J. Front Microbiol 10 1478 (2019)
  28. Crystal structure of the magnetobacterial protein MtxA C-terminal domain reveals a new sequence-structure relationship. Davidov G, Müller FD, Baumgartner J, Bitton R, Faivre D, Schüler D, Zarivach R. Front Mol Biosci 2 25 (2015)
  29. Structural characterization of the Sel1-like repeat protein LceB from Legionella pneumophila. Penner TV, Lorente Cobo N, Patel DT, Patel DH, Savchenko A, Brassinga AKC, Prehna G. Protein Sci 33 e4889 (2024)
  30. The Disruption of an OxyR-Like Protein Impairs Intracellular Magnetite Biomineralization in Magnetospirillum gryphiswaldense MSR-1. Zhang Y, Wen T, Guo F, Geng Y, Liu J, Peng T, Guan G, Tian J, Li Y, Li J, Ju J, Jiang W. Front Microbiol 8 208 (2017)


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