Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx
Open accessAbstract
Bacteria that produce Mn oxides are extraordinarily skilled engineers of nanomaterials that contribute significantly to global biogeochemical cycles. Their enzyme-based reaction mechanisms may be genetically tailored for environmental remediation applications or bioenergy production. However, significant challenges exist for structural characterization of the enzymes responsible for biomineralization. The active Mn oxidase in Bacillus sp. PL-12, Mnx, is a complex composed of a multicopper oxidase (MCO), MnxG, and two accessory proteins, MnxE and MnxF. MnxG shares sequence similarity with other, structurally characterized MCOs. MnxE and MnxF have no similarity to any characterized proteins. The ~200 kDa complex has been recalcitrant to crystallization, so its structure is unknown. Here, we show that native mass spectrometry defines the subunit topology and copper binding of Mnx, while high-resolution electron microscopy visualizes the protein and nascent Mn oxide minerals. These data provide critical structural information for understanding Mn biomineralization by such unexplored enzymes.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Heterocomplexes that have multiple subunits with very similar masses are difficult to characterise just from the intact mass, especially when there is high uncertainty in mass measurement.
“Still, heterocomplexes that have multiple subunits with very similar masses are difficult to characterise just from the intact mass, especially when there is high uncertainty in mass measurement.”
From Higher-order structural characterisation of native proteins and complexes by top-down mass spectrometry (2020) · cites this paper as [50]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638 · see citing works
The I-TASSER Suite: protein structure and function prediction
Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015) · Nature Methods · doi:10.1038/nmeth.3213 · Cited by 5,596 · see citing works
Multicopper oxidases and oxygenases
Solomon, E. I., Sundaram, U. M., & Machonkin, T. E. (1996) · Chemical Reviews · doi:10.1021/cr950046o · Cited by 3,664 · see citing works
Fungal laccases – occurrence and properties
Baldrián, P. (2006) · FEMS Microbiology Reviews · doi:10.1111/j.1574-4976.2005.00010.x · Cited by 2,192 · see citing works
ZDOCK server: interactive docking prediction of protein–protein complexes and symmetric multimers
Pierce, B. G., Wiehe, K. J., Hwang, H., Kim, B., Vreven, T., & Weng, Z. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu097 · Cited by 1,767 · see citing works
Imlay, J. A. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3032 · Cited by 1,700 · see citing works
BIOGENIC MANGANESE OXIDES: Properties and Mechanisms of Formation
Tebo, B. M., Bargar, J., Clement, B., Dick, G. J., Murray, K. J., Parker, D. L., Verity, R., & Webb, S. M. (2004) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.32.101802.120213 · Cited by 1,384 · see citing works
Self-citationDirection-Specific Interactions Control Crystal Growth by Oriented Attachment
Li, D., Nielsen, M. H., Lee, J. R. I., Frandsen, C., Banfield, J. F., & Yoreo, J. J. D. (2012) · Science · doi:10.1126/science.1219643 · Cited by 1,119 · see citing works
Xu, D. H., & Zhang, Y. (2012) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.24065 · Cited by 853 · see citing works
Mineralization in ferritin: an efficient means of iron storage
Chasteen, N. D., & Harrison, P. M. (1999) · Journal of Structural Biology · doi:10.1006/jsbi.1999.4118 · Cited by 815 · see citing works
Robinson, D. M., Go, Y. B., Mui, M., Gardner, G., Zhang, Z., Mastrogiovanni, D. D. T., Garfunkel, E. L., Li, J., Greenblatt, M., & Dismukes, G. C. (2013) · Journal of the American Chemical Society · doi:10.1021/ja310286h · Cited by 639 · see citing works
Investigation of intact protein complexes by mass spectrometry
Heck, A. J. R., & van den Heuvel, R. H. H. (2004) · Mass Spectrometry Reviews · doi:10.1002/mas.10081 · Cited by 584 · see citing works
Superoxide Dismutases: Ancient Enzymes and New Insights
Miller, A.-F. (2012) · FEBS Letters · doi:10.1016/j.febslet.2011.10.048 · Cited by 557 · see citing works
Brown, S. D. M., Jório, A., Cório, P., Dresselhaus, M. S., Dresselhaus, G., Saito, R., & Kneipp, K. D. (2001) · Physical review. B, Condensed matter · doi:10.1103/physrevb.63.155414 · Cited by 553 · see citing works
Bacterial enzymes involved in lignin degradation
de Gonzalo, G., Colpa, D. I., Habib, M. H., & Fraaije, M. W. (2016) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2016.08.011 · Cited by 550 · see citing works
Water-oxidation catalysis by manganese in a geochemical-like cycle
Hocking, R. K., Brimblecombe, R., Chang, L.-Y., Singh, A. K., Cheah, M. H., Glover, C. J., Casey, W. H., & Spiccia, L. (2011) · Nature Chemistry · doi:10.1038/nchem.1049 · Cited by 518 · see citing works
Protein Oxidation Implicated as the Primary Determinant of Bacterial Radioresistance
Daly, M. J., Gaidamakova, E. K., Matrosova, V. Y., Vasilenko, A., Zhai, M., Leapman, R. D., Lai, B. C. H., Ravel, B., Li, S.-M. W., Kemner, K., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050092 · Cited by 438 · see citing works
Nature of Activated Manganese Oxide for Oxygen Evolution
Huynh, M., Shi, C., Billinge, S. J. L., & Nocera, D. G. (2015) · Journal of the American Chemical Society · doi:10.1021/jacs.5b06382 · Cited by 437 · see citing works
Protein Complexes in the Gas Phase: Technology for Structural Genomics and Proteomics
Benesch, J. L. P., Ruotolo, B. T., Simmons, D. A., & Robinson, C. V. (2007) · Chemical Reviews · doi:10.1021/cr068289b · Cited by 408 · see citing works
Manganese and Defenses against Oxygen Toxicity in Lactobacillus plantarum
Archibald, F. S., & Fridovich, I. (1981) · Journal of Bacteriology · doi:10.1128/jb.145.1.442-451.1981 · Cited by 373 · see citing works
Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II)
Webb, S. M., Dick, G. J., Bargar, J., & Tebo, B. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409119102 · Cited by 360 · see citing works
Self-citationManganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria
Archibald, F. S., & Fridovich, I. (1981) · Journal of Bacteriology · doi:10.1128/jb.146.3.928-936.1981 · Cited by 319 · see citing works
Function and molecular evolution of multicopper blue proteins
Nakamura, K., & Gō, N. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-5076-x · Cited by 264 · see citing works
Principles of assembly reveal a periodic table of protein complexes
Ahnert, S. E., Marsh, J. A., Hernández, H., Robinson, C. V., & Teichmann, S. A. (2015) · Science · doi:10.1126/science.aaa2245 · Cited by 253 · see citing works
Manganese oxidation by Leptothrix discophora
Boogerd, F. C., & de Vrind, J. P. M. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.2.489-494.1987 · Cited by 251 · see citing works
Learman, D. R., Wankel, S. D., Webb, S. M., Martinez, N., Madden, A. S. E., & Hansel, C. M. (2011) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2011.07.026 · Cited by 243 · see citing works
Manganese-oxidizing photosynthesis before the rise of cyanobacteria
Johnson, J. E., Webb, S. M., Thomas, K., Ono, S., Kirschvink, J. L., & Fischer, W. W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305530110 · Cited by 238 · see citing works
Shall We Dance? How A Multicopper Oxidase Chooses Its Electron Transfer Partner
Quintanar, L., Stoj, C. S., Taylor, A. B., Hart, P. J., Kosman, D. J., & Solomon, E. I. (2007) · Accounts of Chemical Research · doi:10.1021/ar600051a · Cited by 236 · see citing works
Metal Sulfide Cluster Complexes and their Biogeochemical Importance in the Environment
Luther, G. W., & Rickard, D. T. (2005) · Journal of Nanoparticle Research · doi:10.1007/s11051-005-4272-4 · Cited by 223 · see citing works
Durão, P., Chen, Z., Fernandes, A. T., Hildebrandt, P., Murgida, D. H., Todorović, S., Pereira, M. M., Melo, E. P., & Martins, L. O. (2007) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-007-0312-0 · Cited by 209 · see citing works
Enzymatic Manganese(II) Oxidation by Metabolically Dormant Spores of Diverse Bacillus Species
Francis, C. A., & Tebo, B. M. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.2.874-880.2002 · Cited by 201 · see citing works
Self-citationMn(II,III) oxidation and MnO 2 mineralization by an expressed bacterial multicopper oxidase
Butterfield, C. N., Soldatova, A. V., Lee, S., Spiro, T. G., & Tebo, B. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303677110 · Cited by 187 · see citing works
Self-citationManganous Phosphate Acts as a Superoxide Dismutase
Barnese, K., Gralla, E. B., Cabelli, D. E., & Valentine, J. S. (2008) · Journal of the American Chemical Society · doi:10.1021/ja710162n · Cited by 183 · see citing works
Towards a mechanistic understanding of carbon stabilization in manganese oxides
Johnson, K. L., Purvis, G., López‐Capél, E., Peacock, C. L., Gray, N., Wagner, T., März, C., Bowen, L., Ojeda, J. J., Finlay, N., et al. (2015) · Nature Communications · doi:10.1038/ncomms8628 · Cited by 174 · see citing works
Manganese binding and oxidation by spores of a marine bacillus
Rosson, R. A., & Nealson, K. H. (1982) · Journal of Bacteriology · doi:10.1128/jb.151.2.1027-1034.1982 · Cited by 172 · see citing works
Kosman, D. J. (2009) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-009-0590-9 · Cited by 170 · see citing works
Dick, G. J., Torpey, J. W., Beveridge, T. J., & Tebo, B. M. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01240-07 · Cited by 168 · see citing works
Self-citationvan Waasbergen, L. G., Hildebrand, M., & Tebo, B. M. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.12.3517-3530.1996 · Cited by 165 · see citing works
Self-citationNon-heme manganese catalase – The ‘other’ catalase
Whittaker, J. W. (2011) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2011.12.008 · Cited by 158 · see citing works
Andeer, P. F., Learman, D. R., McIlvin, M. R., Dunn, J. A., & Hansel, C. M. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.12893 · Cited by 152 · see citing works
Anderson, C. R., Johnson, H. A., Caputo, N., Davis, R. E., Torpey, J., & Tebo, B. M. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02890-08 · Cited by 148 · see citing works
Self-citationOkazaki, M., Sugita, T., Shimizu, M., Ohode, Y., Iwamoto, K., Jong, E. W. D. V., de Vrind, J. P. M., & Corstjens, P. L. A. M. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.12.4793-4799.1997 · Cited by 144 · see citing works
NMR reveals pathway for ferric mineral precursors to the central cavity of ferritin
Turano, P., Lalli, D., Felli, I. C., Theil, E. C., & Bertini, I. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908082106 · Cited by 142 · see citing works
Computational identification of self‐inhibitory peptides from envelope proteins
Xu, Y., Rahman, N. A., Othman, R., Hu, P., & Huang, M. (2012) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.24105 · Cited by 138 · see citing works
Surface Induced Dissociation: Dissecting Noncovalent Protein Complexes in the Gas phase
Zhou, M., & Wysocki, V. H. (2014) · Accounts of Chemical Research · doi:10.1021/ar400223t · Cited by 136 · see citing works
Self-citationThe catalytic center of ferritin regulates iron storage via Fe(II)-Fe(III) displacement
Ebrahimi, K. H., Bill, E., Hagedoorn, P., & Hagen, W. R. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.1071 · Cited by 124 · see citing works
CotA, a Multicopper Oxidase from Bacillus pumilus WH4, Exhibits Manganese-Oxidase Activity
Su, J., Bao, P., Bai, T., Deng, L., Wu, H., Liu, F., & He, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060573 · Cited by 109 · see citing works
Manganese(II)-Oxidizing Bacillus Spores in Guaymas Basin Hydrothermal Sediments and Plumes
Dick, G. J., Lee, Y. E., & Tebo, B. M. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.5.3184-3190.2006 · Cited by 108 · see citing works
Self-citationTao, Z., Li, X., Han, Z., & Gong, L. (2015) · Journal of the American Chemical Society · doi:10.1021/jacs.5b00507 · Cited by 105 · see citing works
Constraints on superoxide mediated formation of manganese oxides
Learman, D. R., Voelker, B. M., Madden, A. S. E., & Hansel, C. M. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00262 · Cited by 104 · see citing works
Francis, C. A., Casciotti, K. L., & Tebo, B. M. (2002) · Archives of Microbiology · doi:10.1007/s00203-002-0472-9 · Cited by 101 · see citing works
Self-citationLarsen, E. I., Sly, L. I., & McEwan, A. G. (1999) · Archives of Microbiology · doi:10.1007/s002030050708 · Cited by 94 · see citing works
Identification of a Third Mn(II) Oxidase Enzyme in Pseudomonas putida GB-1
Geszvain, K., Smesrud, L., & Tebo, B. M. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.00046-16 · Cited by 89 · see citing works
Self-citationQuintyn, R. S., Yan, J. R., & Wysocki, V. H. (2015) · Chemistry & Biology · doi:10.1016/j.chembiol.2015.03.019 · Cited by 75 · see citing works
Self-citationManganese (Mn) Oxidation Increases Intracellular Mn in Pseudomonas putida GB-1
Banh, A. Q., Chavez, V., Doi, J., Nguyen, A., Hernandez, S., Ha, V. H., Jimenez, P., Espinoza, F., & Johnson, H. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077835 · Cited by 75 · see citing works
Nonspecific aggregation in native electrokinetic nanoelectrospray ionization
Davidson, K. L., Oberreit, D. R., Hogan, C. J., & Bush, M. F. (2016) · International Journal of Mass Spectrometry · doi:10.1016/j.ijms.2016.09.013 · Cited by 75 · see citing works
Popa, V., Trecroce, D. A., McAllister, R. G., & Konermann, L. (2016) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.6b03035 · Cited by 73 · see citing works
Soldatova, A. V., Butterfield, C. N., Oyerinde, O. F., Tebo, B. M., & Spiro, T. G. (2012) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-012-0928-6 · Cited by 72 · see citing works
Self-citationParker, D. L., Morita, T., Mozafarzadeh, M. L., Verity, R., McCarthy, J. K., & Tebo, B. M. (2007) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2007.03.042 · Cited by 68 · see citing works
Self-citationNakama, K., Medina, M., Lien, A., Ruggieri, J., Collins, K., & Johnson, H. A. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.01873-14 · Cited by 49 · see citing works
Brown, M. A., Stenberg, L. M., & Mauk, A. G. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)02652-2 · Cited by 30 · see citing works
Tao, L., Stich, T. A., Butterfield, C. N., Romano, C. A., Spiro, T. G., Tebo, B. M., Casey, W. H., & Britt, R. D. (2015) · Journal of the American Chemical Society · doi:10.1021/jacs.5b04331 · Cited by 29 · see citing works
Self-citationMulticopper manganese oxidase accessory proteins bind Cu and heme
Butterfield, C. N., Tao, L., Chacón, K. N., Spiro, T. G., Blackburn, N. J., Casey, W. H., Britt, R. D., & Tebo, B. M. (2015) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2015.08.012 · Cited by 26 · see citing works
Self-citationButterfield, C. N., & Tebo, B. M. (2017) · Metallomics · doi:10.1039/c6mt00239k · Cited by 26 · see citing works
Self-citationQuintyn, R. S., Zhou, M., Dagan, S., Finke, J. M., & Wysocki, V. H. (2013) · International Journal for Ion Mobility Spectrometry · doi:10.1007/s12127-013-0126-4 · Cited by 12 · see citing works
Self-citationPhylogenetic Analysis of Six-Domain Multi-Copper Blue Proteins
Vasin, A. V., Klotchenko, S. A., & Puchkova, L. V. (2013) · PLoS Currents · doi:10.1371/currents.tol.574bcb0f133fe52835911abc4e296141 · Cited by 12 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Zhou M., et al. Unveiling the heterogeneity of an uncharacterized manganese oxidizing multicopper oxidase using high resolution native mass spectrometry and surface induced dissociation. Proc. 64th Am. Soc. Mass Spectrom. Conf. 279055 (2016).
Cited by
Sorted by citations
Zhou, H., & Fu, C. (2020) · Reviews in Environmental Science and Bio/Technology · doi:10.1007/s11157-020-09541-1 · Cited by 163 · see citing works
Protein–Small Molecule Interactions in Native Mass Spectrometry
Bennett, J. L., Nguyen, G. T. H., & Donald, W. A. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00293 · Cited by 159 · see citing works
Liu, J., Chen, Q., Yang, Y., Wei, H., Laipan, M., Zhu, R., He, H., & Hochella, M. F. (2022) · Earth-Science Reviews · doi:10.1016/j.earscirev.2022.104105 · Cited by 149 · see citing works
Zhou, M., Lantz, C., Brown, K. A., Ge, Y., Paša-Tolić, L., Loo, J. A., & Lermyte, F. (2020) · Chemical Science · doi:10.1039/d0sc04392c · Cited by 146 · see citing works
Self-citationSoldatova, A. V., Balakrishnan, G., Oyerinde, O. F., Romano, C. A., Tebo, B. M., & Spiro, T. G. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.8b05806 · Cited by 131 · see citing works
Self-citationStiving, A. Q., VanAernum, Z. L., Büsch, F., Harvey, S. R., Sarni, S. H., & Wysocki, V. H. (2018) · Analytical Chemistry · doi:10.1021/acs.analchem.8b05071 · Cited by 107 · see citing works
Self-citationNewsome, L., & Falagán, C. (2021) · GeoHealth · doi:10.1029/2020gh000380 · Cited by 105 · see citing works
Metal oxide nanoparticles in biomedical applications
Murthy, S., Effiong, P. E., & Fei, C. C. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-817505-7.00011-7 · Cited by 86 · see citing works
Surface-induced Dissociation Mass Spectrometry as a Structural Biology Tool
Snyder, D. T., Harvey, S. R., & Wysocki, V. H. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00309 · Cited by 86 · see citing works
Self-citationHe, Z., Zhang, Q., Wei, Z., Wang, S., & Pan, X. (2019) · Water Research · doi:10.1016/j.watres.2019.03.064 · Cited by 81 · see citing works
Relative interfacial cleavage energetics of protein complexes revealed by surface collisions
Harvey, S. R., Seffernick, J. T., Quintyn, R. S., Song, Y., Ju, Y., Yan, J. R., Sahasrabuddhe, A., Norris, A. S., Zhou, M., Behrman, E. J., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1817632116 · Cited by 79 · see citing works
Self-citationRedox Cycling Driven Transformation of Layered Manganese Oxides to Tunnel Structures
Jung, H., Taillefert, M., Sun, J., Wang, Q., Borkiewicz, O. J., Liu, P., Yang, L., Chen, S., Chen, H., & Tang, Y. (2020) · Journal of the American Chemical Society · doi:10.1021/jacs.9b12266 · Cited by 78 · see citing works
VanAernum, Z. L., Gilbert, J. D., Belov, M. E., Makarov, A., Horning, S. R., & Wysocki, V. H. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.8b05605 · Cited by 80 · see citing works
Self-citationJones, M. R., Luther, G. W., Mucci, A. O., & Tebo, B. M. (2019) · Talanta · doi:10.1016/j.talanta.2019.03.026 · Cited by 64 · see citing works
Self-citationConfirmation of intersubunit connectivity and topology of designed protein complexes by native MS
Sahasrabuddhe, A., Hsia, Y., Büsch, F., Sheffler, W., King, N. P., Baker, D. A., & Wysocki, V. H. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713646115 · Cited by 60 · see citing works
Self-citationLiu, R., Xia, S., & Li, H. (2022) · Mass Spectrometry Reviews · doi:10.1002/mas.21793 · Cited by 59 · see citing works
Hu, X., Yang, B., Zhang, W., Qin, C., Sheng, X., Oleszczuk, P., & Gao, Y. (2019) · Environmental Science Nano · doi:10.1039/c8en01447g · Cited by 57 · see citing works
Marine microbial Mn(II) oxidation mediates Cr(III) oxidation and isotope fractionation
Miletto, M., Wang, X., Planavsky, N. J., Luther, G. W., Lyons, T. W., & Tebo, B. M. (2021) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2021.01.008 · Cited by 50 · see citing works
Self-citationIron and manganese removal from groundwater using limestone filter with iron-oxidized bacteria
Aziz, H. B. A., Tajarudin, H. A., Wei, T. H. L., & Alazaiza, M. Y. D. (2020) · International Journal of Environmental Science and Technology · doi:10.1007/s13762-020-02681-5 · Cited by 49 · see citing works
Jia, L., Zhou, Q. F., Li, Y., & Wu, W. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.139219 · Cited by 46 · see citing works
Liu, J., Feng, L., & Wu, Y. (2021) · Nanoscale · doi:10.1039/d1nr02400k · Cited by 46 · see citing works
Wang, X., Jones, M. R., Pan, Z., Lu, X., Deng, Y., Zhu, M., & Wang, Z. (2024) · Water Research · doi:10.1016/j.watres.2024.122198 · Cited by 41 · see citing works
Gonçalves, J. P. Z., Seraglio, J., Macuvele, D. L. P., Padoin, N., Soares, C., & Riella, H. G. (2021) · Colloids and Surfaces A Physicochemical and Engineering Aspects · doi:10.1016/j.colsurfa.2021.128180 · Cited by 38 · see citing works
Huang, Y., Huangfu, X., Ma, C., & Liu, Z. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.138594 · Cited by 37 · see citing works
Metal oxyanion removal from wastewater using manganese-oxidizing aerobic granular sludge
He, Z., Wei, Z., Zhang, Q., Zou, J., & Pan, X. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.124353 · Cited by 35 · see citing works
Wang, H., Lv, Z., Song, Y., Wang, Y., Zhang, D., Sun, Y., Tsang, Y. F., & Pan, X. (2019) · Process Safety and Environmental Protection · doi:10.1016/j.psep.2019.02.022 · Cited by 34 · see citing works
Self-citationCorbera-Rubio, F., Laureni, M., Koudijs, N., Müller, S., van Alen, T. A., Schoonenberg, F., Lücker, S., Pabst, M., van Loosdrecht, M. C. M., & van Halem, D. (2023) · Water Research · doi:10.1016/j.watres.2023.119805 · Cited by 33 · see citing works
Abuzeid, H. M., Hashem, A. M., Kaus, M., Knapp, M., Indris, S., Ehrenberg, H., Mauger, A., & Julien, C. M. (2018) · Journal of Alloys and Compounds · doi:10.1016/j.jallcom.2018.02.260 · Cited by 32 · see citing works
Protein Structure Prediction with Mass Spectrometry Data
Biehn, S. E., & Lindert, S. (2021) · Annual Review of Physical Chemistry · doi:10.1146/annurev-physchem-082720-123928 · Cited by 31 · see citing works
Dissecting the structural heterogeneity of proteins by native mass spectrometry
Reid, D. J., Thibert, S. M., & Zhou, M.-W. (2023) · Protein Science · doi:10.1002/pro.4612 · Cited by 23 · see citing works
Self-citationZhou, M., Yan, J. R., Romano, C. A., Tebo, B. M., Wysocki, V. H., & Paša‐Tolić, L. (2018) · Journal of the American Society for Mass Spectrometry · doi:10.1007/s13361-017-1882-x · Cited by 27 · see citing works
Self-citationOrganic buffers act as reductants of abiotic and biogenic manganese oxides
Hausladen, D. M., & Peña, J. (2023) · Scientific Reports · doi:10.1038/s41598-023-32691-5 · Cited by 26 · see citing works
He, Z., Zhang, Q., Wei, Z., Zhu, Y., & Pan, X. (2019) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2019.134510 · Cited by 25 · see citing works
Algae promotes the biogenic oxidation of Mn(II) by accelerated extracellular superoxide production
Qi, J., Wang, X., Lin, Z., Zhao, J., Hu, C., & Qu, J. (2024) · Water Research · doi:10.1016/j.watres.2024.122063 · Cited by 22 · see citing works
Jiang, X., Gong, J., Ren, J., Liu, Q., Zhang, J., & Chou, Y. (2020) · Sedimentary Geology · doi:10.1016/j.sedgeo.2019.105588 · Cited by 22 · see citing works
Yao, M.-C., Huang, Q., Xie, H.-X., Zhang, X., & Sheng, G. (2025) · Environmental Science & Technology · doi:10.1021/acs.est.5c09864 · Cited by 21 · see citing works
Selective Hydrogenation of Acetylene over Pd-Mn/Al2O3 Catalysts
Melnikov, D. P., Stytsenko, V. D., Savel’eva, E. V., Kotelev, M. S., Lyubimenko, V. A., Ivanov, E. V., Glotov, A. P., & Vinokurov, V. A. (2020) · Catalysts · doi:10.3390/catal10060624 · Cited by 21 · see citing works
Natural attenuation of lead by microbial manganese oxides in a karst aquifer
Newsome, L., Bacon, C. G. D., Song, H., Luo, Y., Sherman, D. Μ., & Lloyd, J. R. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.142312 · Cited by 19 · see citing works
Gehin, G., Carraro, N., Gurfield, K., van der Meer, J. R., & Peña, J. (2025) · Environmental Science & Technology · doi:10.1021/acs.est.5c00255 · Cited by 17 · see citing works
Jones, M. R., Oldham, V. E., Luther, G. W., Mucci, A. O., & Tebo, B. M. (2018) · Marine Chemistry · doi:10.1016/j.marchem.2018.11.005 · Cited by 17 · see citing works
Self-citationWu, J., Kang, F., Wang, Z., Song, L., Guan, X., & Zhou, H. (2022) · International Microbiology · doi:10.1007/s10123-022-00254-9 · Cited by 16 · see citing works
Catalase-peroxidase StKatG is a bacterial manganese oxidase from endophytic Salinicola tamaricis
Zhao, G., Wang, W., Zheng, L., Chen, L., Duan, G., Chang, R., Chen, Z., Zhang, S., Dai, M., & Yang, G. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.10.123 · Cited by 16 · see citing works
Manganese Oxide Nanoclusters for Skin Photoprotection.
Xiong, L., Zhao, M.-Y., Fan, Y., Wang, S.-F., Yang, Y., Li, X.-M., Zhao, D.-Y., & Zhang, F. (2019) · ACS Applied Bio Materials · doi:10.1021/acsabm.9b00528 · Cited by 13 · see citing works
Tao, L., Stich, T. A., Soldatova, A. V., Tebo, B. M., Spiro, T. G., Casey, W. H., & Britt, R. D. (2018) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-018-1587-z · Cited by 15 · see citing works
Self-citationTojo, F., 北山, 阿., Miyata, N., Okano, K., Fukushima, J., Suzuki, R., & Tani, Y. (2020) · Catalysts · doi:10.3390/catal10060686 · Cited by 14 · see citing works
Wang, R., Hu, H., Shi, D., Liang, J., & Shao, S. (2023) · Separation and Purification Technology · doi:10.1016/j.seppur.2023.125214 · Cited by 14 · see citing works
Novel manganese cycling at very low ionic strengths in the Columbia River Estuary
Jones, M. R., & Tebo, B. M. (2021) · Water Research · doi:10.1016/j.watres.2021.117801 · Cited by 14 · see citing works
Self-citationMiyata, N., Suganuma, R., Sunouchi, K., Okano, K., Fuchida, S., Watanabe, M., Fujibayashi, M., Sato, Y., & Tokoro, C. (2023) · Biochemical Engineering Journal · doi:10.1016/j.bej.2023.109187 · Cited by 13 · see citing works
Keffer, J. L., Zhou, N., Rushworth, D. D., Yu, Y., & Chan, C. S. (2025) · Applied and Environmental Microbiology · doi:10.1128/aem.01865-24 · Cited by 13 · see citing works
Gehin, G., Carraro, N., van der Meer, J. R., & Peña, J. (2025) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00670-5 · Cited by 13 · see citing works
Ji, R., Ge, W., Wang, H., Zhao, Y., & Feng, H. (2019) · Gene · doi:10.1016/j.gene.2019.02.031 · Cited by 13 · see citing works
Yu, L., Li, Y., & Ruan, Y. (2021) · Environmental Science & Technology · doi:10.1021/acs.est.0c07733 · Cited by 11 · see citing works
Liu, J., Gu, T., Li, L., & Li, L. (2021) · Nanomaterials · doi:10.3390/nano11020361 · Cited by 12 · see citing works
Synthesis and Antibacterial Properties of Manganese Dioxide Nanostructures: A Review
Velho-Pereira, S., & Parmekar, M. V. (2024) · ChemistrySelect · doi:10.1002/slct.202402247 · Cited by 11 · see citing works
Tang, W., Haoxiang, L., & Zeng, X. (2021) · Chemosphere · doi:10.1016/j.chemosphere.2021.130807 · Cited by 11 · see citing works
Metallo-inhibition of Mnx, a bacterial manganese multicopper oxidase complex
Soldatova, A. V., Fu, W., Romano, C. A., Tao, L., Casey, W. H., Britt, R. D., Tebo, B. M., & Spiro, T. G. (2021) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2021.111547 · Cited by 11 · see citing works
Self-citationNovikova, I. V., Soldatova, A. V., Moser, T. H., Thibert, S. M., Romano, C. A., Zhou, M., Tebo, B. M., Evans, J. E., & Spiro, T. G. (2024) · Journal of the American Chemical Society · doi:10.1021/jacs.3c06537 · Cited by 10 · see citing works
Self-citationChallenges of Measuring Soluble Mn(III) Species in Natural Samples
Kim, B., Lingappa, U. F., Magyar, J. S., Monteverde, D. R., Valentine, J. S., Cho, J., & Fischer, W. W. (2022) · Molecules · doi:10.3390/molecules27051661 · Cited by 10 · see citing works
Manganese Cycling in the Oceans
Tebo, B. M., & Luther, G. W. (2019) · Encyclopedia of Water · doi:10.1002/9781119300762.wsts0065 · Cited by 10 · see citing works
Self-citationFarda, B., Vaccarelli, I., Ercole, C., Djebaili, R., Gallo, M. D., & Pellegrini, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-24159-9 · Cited by 9 · see citing works
Zhang, A., Hou, Y., Hou, S., Wang, Y., & Wang, Q. (2025) · Chemical Engineering Journal · doi:10.1016/j.cej.2025.160579 · Cited by 8 · see citing works
Liu, F. C., Cropley, T. C., & Bleiholder, C. (2023) · Journal of the American Society for Mass Spectrometry · doi:10.1021/jasms.3c00191 · Cited by 8 · see citing works
Tandem surface-induced dissociation of protein complexes on an ultrahigh resolution platform
Snyder, D. T., Lin, Y.-F., Somogyi, Á., & Wysocki, V. H. (2021) · International Journal of Mass Spectrometry · doi:10.1016/j.ijms.2020.116503 · Cited by 9 · see citing works
Self-citationMorales, E., Formanski, L. N., Shaner, S. E., & Stone, K. L. (2024) · Life · doi:10.3390/life14020171 · Cited by 7 · see citing works
Tum, S., Katayama, T., Miyata, N., Watanabe, M., Hashimoto, Y., Nishikata, M., & Yasutaka, T. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e40363 · Cited by 7 · see citing works
Whitty-Léveillé, L., VanAernum, Z. L., Pavon, J. A., Murphy, C., Neal, K., Forrest, W. P., Gao, X., Zhong, W., Richardson, D. D., & Schuessler, H. A. (2023) · mAbs · doi:10.1080/19420862.2023.2199466 · Cited by 7 · see citing works
Sawabe, T., Kudo, R., Yu, J., Nguyen, T. N., Rossi, A., Sakai, Y., & Mino, S. (2025) · Current Microbiology · doi:10.1007/s00284-025-04138-9 · Cited by 6 · see citing works
Gao, Y., Song, G., Xu, Y., Sun, Y., Feng, Y., Tan, H., & Tian, W. (2025) · Chinese Journal of Chemical Engineering · doi:10.1016/j.cjche.2024.11.023 · Cited by 6 · see citing works
Kilias, S. P., Ivarsson, M., Fru, E. C., Rattray, J. E., Gustafsson, H., Naden, J., & Detsi, K. (2020) · Minerals · doi:10.3390/min10060536 · Cited by 6 · see citing works
Ayon, N. J. (2025) · AppliedChem · doi:10.3390/appliedchem5040035 · Cited by 5 · see citing works
Trace elements and their isotopes in streams and rivers
Herndon, E. M., Ma, L., Newcomer, M., & Shiller, A. M. (2024) · Treatise on Geochemistry · doi:10.1016/b978-0-323-99762-1.00022-x · Cited by 5 · see citing works
Biosynthesis, Biofunctionalization, and Bioapplications of Manganese Nanomaterials: An Overview
Panda, B., Lenka, A., Dixit, P. K., & Dash, S. K. (2023) · Springer eBooks · doi:10.1007/978-981-19-8501-0_3 · Cited by 5 · see citing works
Fu, W., Hyler, F. P., Sanchez, J., Jaramillo, T. F., Velázquez, J. M., Tao, L., & Britt, R. D. (2024) · ACS Catalysis · doi:10.1021/acscatal.3c06119 · Cited by 5 · see citing works
A Bioinformatic Study of the Distribution of Mn Oxidation Proteins in Sequenced Bacterial GenomesPreprint
Kurdi, M. Z., Olichney, J. A., & Geszvain, K. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.10.515945 · Cited by 5 · see citing works
Smolyakov, D. D., Beletsky, A. V., Rudenko, T. S., Gureeva, M. V., Ravin, N. V., & Grabovich, M. Y. (2025) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2025.126666 · Cited by 4 · see citing works
Xu, Y., Wu, T., Zhang, G., & Niu, Y. (2024) · ACS ES&T Water · doi:10.1021/acsestwater.4c00089 · Cited by 4 · see citing works
Liu, S., Feng, K., Zhang, D., Liu, Y., Wang, J., Lu, B., & Xing, D. (2025) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2025.139776 · Cited by 3 · see citing works
Tsukamoto, Y., & Kakegawa, T. (2022) · Life · doi:10.3390/life12060816 · Cited by 3 · see citing works
Biochemical properties of CumA multicopper oxidase from plant pathogen, Pseudomonas syringae
Ishida, K., Tsukamoto, Y., Horitani, M., Ogawa, T., & Tanaka, Y. (2021) · Bioscience Biotechnology and Biochemistry · doi:10.1093/bbb/zbab123 · Cited by 3 · see citing works
Zhao, L.-N., Huang, Q., Pi, D.-H., Yi, Z., Ding, D.-Q., & Ahmet, S. (2025) · Ore Geology Reviews · doi:10.1016/j.oregeorev.2025.106855 · Cited by 2 · see citing works
Huang, Y., Huangfu, X., Zhao, Z., Zhang, Y., & He, Q. (2026) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2026.141120 · Cited by 2 · see citing works
Ca2+ effects on manganese oxidation by the bacterial multicopper oxidase complex Mnx
Soldatova, A. V., Romano, C. A., Wilson, J., Zhou, M., Tebo, B. M., & Spiro, T. G. (2026) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2026.113396 · Cited by 2 · see citing works
Self-citationAn in-Silico Study of the Distribution of Mn Oxidation Proteins in Sequenced Bacterial GenomesPreprint
Kurdi, M. Z., Olichney, J. A., & Geszvain, K. (2023) · Research Square · doi:10.21203/rs.3.rs-2451893/v1 · Cited by 2 · see citing works
Reid, D. J., Thibert, S. M., Wilson, J., Soldatova, A. V., Tebo, B. M., Spiro, T. G., & Zhou, M. (2023) · International Journal of Mass Spectrometry · doi:10.1016/j.ijms.2023.117172 · Cited by 1 · see citing works
Self-citationYu, W., Polgári, M., Zhou, Q. F., Du, Y., Gong, Y., Yang, M., Wei, W., Liu, Z., Xu, L., Zhen, X., et al. (2025) · Earth Science-Journal of China University of Geosciences · doi:10.3799/dqkx.2025.002 · Cited by 1 · see citing works
Wang, Y., Liu, S., Zheng, Z., Ma, J., Xiang, Y., Wu, L., Ding, C., & Shi, Y. (2025) · Microorganisms · doi:10.3390/microorganisms14010015 · Cited by 1 · see citing works
Guo, Y., Liu, Y., Li, F., Pan, H., Yi, X., Liu, Y., & Zhou, H. (2026) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2026.151530 · Cited by 1 · see citing works
Morales, E., Brown, J., Runge, C., York, M., Dennis, G., Johnson, C., Baudino, A. M., Paz-Ramirez, N., Samson, L., Romal, J. R. A., et al. (2026) · Oxygen · doi:10.3390/oxygen6020013 · Cited by 1 · see citing works
Coordinated plant and microbial transcriptional responses to oil-sands process–affected water
Nweze, J. E., Morvan, S., Samad, A., Bergeron, M., Degenhardt, D., Tremblay, J., Symonds, K., Muench, D. G., Martineau, C., & Yergeau, É. (2026) · ISME Communications · doi:10.1093/ismeco/ycag152 · Cited by 1 · see citing works
Manganese Biomineralization by a Multicopper Oxidase Protein Complex
Soldatova, A. V., Tebo, B. M., & Spiro, T. G. (2026) · Chemical Reviews · doi:10.1021/acs.chemrev.6c00213 · Cited by 1 · see citing works
Self-citationTakeda, A., Oki, T., Yokoo, H., Kawamoto, K., Nakano, Y., Ochiai, A., Winarni, I. D., Kitahara, M., Miyoshi, K., Fukuyama, K., et al. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.137526 · Cited by 1 · see citing works
Miyata, N., & Tani, Y. (2020) · KAGAKU TO SEIBUTSU · doi:10.1271/kagakutoseibutsu.58.562 · Cited by 1 · see citing works
A novel cuproptosis-related gene signature can predict prognosis in acute myeloid leukemiaPreprint
Zhou, X., Xu, Z., Ma, H., Weng, Z., & Li, J. (2022) · Research Square · doi:10.21203/rs.3.rs-1628980/v1 · Cited by 1 · see citing works
Bio‐inspired Nanocomposites for Remediation of Pharmaceutical Pollutants
Gautam, P. K., Shivalkar, S., Singh, A. K., Pingali, M. S., Chaudhary, S., Banerjee, S., Varadwaj, P. K., & Samanta, S. K. (2022) · doi:10.1002/9783527834143.ch17 · Cited by 1 · see citing works
Yates, J. R. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.732531772.793557936
崔, 喜. (2024) · Advances in Microbiology · doi:10.12677/amb.2024.134026
Wang, Y., Liu, S., Zheng, Z., Ma, J., Xiang, Y., Wu, L., & Ding, C. (2025) · Research Square · doi:10.21203/rs.3.rs-7036046/v1
Photochemically facilitated todorokite nanoparticle formation in circumneutral pH environments
Jung, H., Gao, Z., & Jun, Y. (2026) · Environmental Science Nano · doi:10.1039/d5en01203a
Wang, Z., Liu, Y., Dai, J., Cui, Y., Li, Y., Zhang, S., Liu, J., Wang, C., Ji, X., Xu, H., et al. (2026) · Microchemical Journal · doi:10.1016/j.microc.2026.117987
Draft genome sequence of Salibacterium sp. K-3, a halophilic Mn(II)-oxidizing bacterium
Abdulwahed, L., & Greene, A. C. (2026) · Microbiology Resource Announcements · doi:10.1128/mra.01475-25
- Authors
- Romano, C. A., Zhou, M., Song, Y., Wysocki, V. H., Dohnalkova, A. C., Kovarik, L., Paša-Tolić, L., & Tebo, B. M.
- Affiliations
- Oregon Health & Science University (US)
- Pacific Northwest National Laboratory (US)
- The Ohio State University (US)
- Corresponding author
- Romano, Christine A.
- Zhou, Mowei
- Tebo, Bradley M.
- Venue
- Nature Communications
- Published
- 2017-09-29
- Volume
- 8
- Issue
- 1
- Pages
- 746-746
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC5622069
- OpenAlex
- W2760615945
- Cited by
- 102
- References
- 66
- Citations by year
- 2026: 11 · 2025: 14 · 2024: 10 · 2023: 12 · 2022: 11 · 2021: 14 · 2020: 11 · 2019: 13 · 2018: 6
- FWCI
- 3.14
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (1410688, 1202859)
- U.S. Department of Energy
- Bentham-Moxon Trust
- National Institutes of Health
- Office of Science
- National Institute of General Medical Sciences (R01GM113658)
- Division of Chemistry (CHE-1410688)
- Biological and Environmental Research
- Pacific Northwest National Laboratory
- Topics
- Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Physical Sciences › Earth and Planetary Sciences › Geochemistry and Petrology › Geochemistry and Elemental Analysis
- Keywords
- biogenic manganese oxides, multicopper oxidase, manganese nanoparticles, copper binding, native mass spectrometry, high-resolution electron microscopy
- MeSH terms
- Bacillus, Bacterial Proteins, Copper, Manganese, Oxides, Oxidoreductases, Mass Spectrometry, Manganese Compounds, Microscopy, Electron, Transmission, Nanoparticles
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review