A cytoplasmic chemoreceptor and reactive oxygen species mediate bacterial chemotaxis to copper
Open accessPublished version of a preprint
Abstract
Chemotaxis is a widespread strategy used by unicellular and multicellular living organisms to maintain their fitness in stressful environments. We previously showed that bacteria can trigger a negative chemotactic response to a copper (Cu)-rich environment. Cu ion toxicity on bacterial cell physiology has been mainly linked to mismetallation events and reactive oxygen species (ROS) production, although the precise role of Cu-generated ROS remains largely debated. Here, using inductively coupled plasma optical emission spectrometry on cell fractionates, we found that the cytoplasmic Cu ion content mirrors variations of the extracellular Cu ion concentration. ROS-sensitive fluorescent probe and biosensor allowed us to show that the increase of cytoplasmic Cu ion content triggers a dose-dependent oxidative stress, which can be abrogated by superoxide dismutase and catalase overexpression. The inhibition of ROS production in the cytoplasm not only improves bacterial growth but also impedes Cu chemotaxis, indicating that ROS derived from cytoplasmic Cu ions mediate the control of bacterial chemotaxis to Cu. We also identified the Cu chemoreceptor McpR, which binds Cu ions with low affinity, suggesting a labile interaction. In addition, we demonstrate that the cysteine 75 and histidine 99 within the McpR sensor domain are key residues in Cu chemotaxis and Cu coordination. Finally, we discovered that in vitro both Cu(I) and Cu(II) ions modulate McpR conformation in a distinct manner. Overall, our study provides mechanistic insights on a redox-based control of Cu chemotaxis, indicating that the cellular redox status can play a key role in bacterial chemotaxis.
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Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764 · see citing works
Krogh, A., Larsson, B., von Heijne, G., & Sonnhammer, E. L. L. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4315 · Cited by 12,654 · see citing works
Varadi, M., Anyango, S., Deshpande, M., Nair, S., Natassia, C., Yordanova, G., Yuan, D., Stroe, O., Wood, G., Laydon, A., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkab1061 · Cited by 7,850 · see citing works
The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences
Perez-Riverol, Y., Bai, J., Bandla, C., García-Seisdedos, D., Hewapathirana, S., Kamatchinathan, S., Kundu, D. J., Prakash, A., Frericks-Zipper, A., Eisenacher, M., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkab1038 · Cited by 6,125 · see citing works
SignalP 6.0 predicts all five types of signal peptides using protein language models
Teufel, F., Armenteros, J. J. A., Johansen, A. R., Gíslason, M. H., Pihl, S. I., Tsirigos, K. D., Winther, O., Brunak, S., von HEIJNE, G., & Nielsen, H. (2022) · Nature Biotechnology · doi:10.1038/s41587-021-01156-3 · Cited by 2,999 · see citing works
JPred4: a protein secondary structure prediction server
Drozdetskiy, A., Cole, C., Procter, J. B., & Barton, G. J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv332 · Cited by 1,714 · see citing works
Making sense of it all: bacterial chemotaxis
Wadhams, G. H., & Armitage, J. P. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1524 · Cited by 1,480 · see citing works
Stadtman, E. R. (1993) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.62.070193.004053 · Cited by 1,408 · see citing works
The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity
Macomber, L., & Imlay, J. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812808106 · Cited by 1,117 · see citing works
Zhang, J., Xin, L., Shan, B., Chen, W., Xie, M., Yuen, D., Zhang, W., Zhang, Z., Lajoie, G., & Ma, B. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.010587 · Cited by 1,073 · see citing works
MicrobeJ, a tool for high throughput bacterial cell detection and quantitative analysis
Ducret, A., Quardokus, E. M., & Brun, Y. V. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.77 · Cited by 950 · see citing works
Meier, F., Brunner, A., Koch, S., Koch, H., Lubeck, M., Krause, M., Goedecke, N., Decker, J., Kosinski, T., Park, M. A., et al. (2018) · Molecular & Cellular Proteomics · doi:10.1074/mcp.tir118.000900 · Cited by 946 · see citing works
The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation
Lee, J.-W., & Helmann, J. D. (2006) · Nature · doi:10.1038/nature04537 · Cited by 547 · see citing works
Complete genome sequence of Caulobacter crescentus
Nierman, W. C., Feldblyum, T. V., Laub, M. T., Paulsen, I. T., Nelson, K. E., Eisen, J. A., Heidelberg, J. F., Alley, M. R. K., Ohta, N., Maddock, J. R., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.061029298 · Cited by 518 · see citing works
Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells
EVINGER, M. J. Q., & Agabian, N. M. (1977) · Journal of Bacteriology · doi:10.1128/jb.132.1.294-301.1977 · Cited by 504 · see citing works
Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update
Parkinson, J. S., Hazelbauer, G. L., & Falke, J. J. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.03.003 · Cited by 414 · see citing works
The caulobacters: ubiquitous unusual bacteria
Poindexter, J. S. (1981) · Microbiological Reviews · doi:10.1128/mr.45.1.123-179.1981 · Cited by 377
Coordination chemistry of copper proteins: How nature handles a toxic cargo for essential function
Rubino, J. T., & Franz, K. J. (2011) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2011.11.024 · Cited by 369 · see citing works
Copper toxicity and the origin of bacterial resistance—new insights and applications
Dupont, C. L., Grass, G., & Rensing, C. (2011) · Metallomics · doi:10.1039/c1mt00107h · Cited by 365 · see citing works
Macomber, L., Rensing, C., & Imlay, J. A. (2007) · Journal of Bacteriology · doi:10.1128/jb.01357-06 · Cited by 356 · see citing works
Monitoring disulfide bond formation in the eukaryotic cytosol
Østergaard, H., Tachibana, C., & Winther, J. R. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200402120 · Cited by 333 · see citing works
The caulobacters: ubiquitous unusual bacteria
Poindexter, J. S. (1981) · Microbiological Reviews · doi:10.1128/mmbr.45.1.123-179.1981 · Cited by 294 · see citing works
Xiao, Z., Brose, J., Schimo, S., Ackland, S. M., Fontaine, S. L., & Wedd, A. G. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.213074 · Cited by 258 · see citing works
Molecular mechanism of transmembrane signaling by the aspartate receptor: a model.
Chervitz, S. A., & Falke, J. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.6.2545 · Cited by 238 · see citing works
Copper tolerance in bacteria requires the activation of multiple accessory pathways
Giachino, A., & Waldron, K. J. (2020) · Molecular Microbiology · doi:10.1111/mmi.14522 · Cited by 223 · see citing works
Methyl-accepting chemotaxis proteins: a core sensing element in prokaryotes and archaea
Ud-Din, A. I. M. S., & Roujeinikova, A. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2514-0 · Cited by 222 · see citing works
Polar localization of a bacterial chemoreceptor.Preprint
Alley, M. R., Maddock, J. R., & Shapiro, L. (1992) · Genes & Development · doi:10.1101/gad.6.5.825 · Cited by 214 · see citing works
Crystal structure of the copper chaperone for superoxide dismutase.
Rosenzweig, A. C., Lamb, A. L., Wernimont, A. K., Pufahl, R. A., Culotta, V., & O’Halloran, T. V. (1999) · Nature Structural Biology · doi:10.1038/11489 · Cited by 195 · see citing works
Sourjik, V., & Schmitt, R. (1998) · Biochemistry · doi:10.1021/bi972330a · Cited by 159 · see citing works
Webre, D. J., Wolanin, P. M., & Stock, J. B. (2003) · Current Biology · doi:10.1016/s0960-9822(02)01424-0 · Cited by 114 · see citing works
Location and architecture of the Caulobacter crescentus chemoreceptor array
Briegel, A., Ding, H. J., Li, Z., Werner, J., Gitai, Z., Dias, D. P., Jensen, R. B., & Jensen, G. J. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06219.x · Cited by 113 · see citing works
Requirement of the Carboxyl Terminus of a Bacterial Chemoreceptor for Its Targeted Proteolysis
Alley, M. R. K., Maddock, J. R., & Shapiro, L. (1993) · Science · doi:10.1126/science.8456303 · Cited by 113 · see citing works
Rubino, J. T., Chenkin, M. P., Keller, M., Riggs-Gelasco, P. J., & Franz, K. J. (2010) · Metallomics · doi:10.1039/c0mt00044b · Cited by 108 · see citing works
New Insights into Bacterial Chemoreceptor Array Structure and Assembly from Electron Cryotomography
Briegel, A., Wong, M. L., Hodges, H. L., Oikonomou, C. M., Piasta, K. N., Harris, M. J., Fowler, D. J., Thompson, L. K., Falke, J. J., Kiessling, L. L., et al. (2014) · Biochemistry · doi:10.1021/bi5000614 · Cited by 90 · see citing works
Differences in signalling by directly and indirectly binding ligands in bacterial chemotaxis
Neumann, S., Hansen, C. H., Wingreen, N. S., & Sourjik, V. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.224 · Cited by 86 · see citing works
Tsai, J.-W., & Alley, M. R. K. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.17.5001-5007.2001 · Cited by 78 · see citing works
Auxiliary phosphatases in two-component signal transduction
Silversmith, R. E. (2010) · Current Opinion in Microbiology · doi:10.1016/j.mib.2010.01.004 · Cited by 76 · see citing works
Khursigara, C. M., Wu, X., & Subramaniam, S. (2008) · Journal of Bacteriology · doi:10.1128/jb.00640-08 · Cited by 74 · see citing works
The C-Terminus of Human Copper Importer Ctr1 Acts as a Binding Site and Transfers Copper to Atox1
Kahra, D., Kovermann, M., & Wittung-Stafshede, P. E. (2016) · Biophysical Journal · doi:10.1016/j.bpj.2015.11.016 · Cited by 71 · see citing works
Nesper, J., Hug, I., Kato, S., Hee, C.-S., Habazettl, J. M., Manfredi, P., Grzesiek, S., Schirmer, T., Emonet, T., & Jenal, U. (2017) · eLife · doi:10.7554/elife.28842 · Cited by 64 · see citing works
Tiwari, M. K., Hägglund, P., Møller, I. M., Davies, M. J., & Bjerrum, M. J. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101262 · Cited by 61 · see citing works
Barnakov, A. N., Barnakova, L. A., & Hazelbauer, G. L. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.24.6713-6718.1998 · Cited by 61 · see citing works
Bacterial chemoreceptor dynamics correlate with activity state and are coupled over long distances
Samanta, D., Borbat, P. P., Dzikovski, B. G., Freed, J. H., & Crane, B. R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1414155112 · Cited by 41 · see citing works
Structure and Activity of the Flagellar Rotor Protein FliY
Sircar, R., Greenswag, A. R., Bilwes, A. M., Gonzalez-Bonet, G., & Crane, B. R. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.445171 · Cited by 40 · see citing works
Proteolysis of the McpA Chemoreceptor Does Not Require the Caulobacter Major Chemotaxis Operon
Tsai, J.-W., & Alley, M. R. K. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.2.504-507.2000 · Cited by 35 · see citing works
Berne, C., & Brun, Y. V. (2019) · Journal of Bacteriology · doi:10.1128/jb.00071-19 · Cited by 35 · see citing works
Degradation of a Caulobacter Soluble Cytoplasmic Chemoreceptor Is ClpX Dependent
Potocka, I., Thein, M. C., Østerås, M., Jenal, U., & Alley, M. R. K. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.23.6635-6642.2002 · Cited by 30 · see citing works
Lertsethtakarn, P., Howitt, M. R., Castellon, J., Amieva, M. R., & Ottemann, K. M. (2015) · Molecular Microbiology · doi:10.1111/mmi.13086 · Cited by 29 · see citing works
Caulobacter crescentus intrinsic dimorphism provides a prompt bimodal response to copper stress
Lawarée, E., Gillet, S., Louis, G., Tilquin, F., Blastier, S. L., Cambier, P., & Matroule, J. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.98 · Cited by 29 · see citing works
Self-citationDecoding the chemotactic signal
Thomas, M. A., Kleist, A. B., & Volkman, B. F. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.1mr0218-044 · Cited by 28 · see citing works
The Aerotactic Response of Caulobacter crescentus
Morse, M., Colin, R., Wilson, L. G., & Tang, J. X. (2016) · Biophysical Journal · doi:10.1016/j.bpj.2016.03.028 · Cited by 24 · see citing works
Flack, C. E., & Parkinson, J. S. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204161119 · Cited by 18 · see citing works
Maertens, L., Cherry, P., Tilquin, F., Houdt, R. V., & Matroule, J. (2021) · Microorganisms · doi:10.3390/microorganisms9061116 · Cited by 15 · see citing works
Self-citationMicrochannel-Nanopore Device for Bacterial Chemotaxis Assays
Kovarik, M. L., Brown, P., Kysela, D. T., Berne, C., Kinsella, A. C., Brun, Y. V., & Jacobson, S. C. (2010) · Analytical Chemistry · doi:10.1021/ac101977f · Cited by 15 · see citing works
Effects of oxidation on redox and cytotoxic properties of copper complex of Aβ1–16 peptide
Ramteke, S., Walke, G. R., Joshi, B. N., Rapole, S., & Kulkarni, P. P. (2014) · Free Radical Research · doi:10.3109/10715762.2014.960412 · Cited by 6 · see citing works
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Passos, C., Tomares, D. T., Yassine, H., Schnorr, W. E., Hunter, H., Wolfe-Feichter, H. K., Velier, J., Dzurik, K. G., Grillo, J., Gega, A., et al. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110648 · Cited by 6 · see citing works
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- Authors
- Louis, G., Cherry, P., Michaux, C., Rahuel-Clermont, S., Dieu, M., Tilquin, F., Maertens, L., Van Houdt, R., Renard, P., Perpete, E., & Matroule, J.-Y.
- Affiliations
- University of Namur (BE)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Matroule, Jean-Yves
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2023-10
- Volume
- 299
- Issue
- 10
- Pages
- 105207
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC10579534
- OpenAlex
- W4386366684
- Cited by
- 17
- References
- 54
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 3
- FWCI
- 2.70
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- Repository of the University of Namur (submittedVersion, cc-by)
- Funders
- Université de Namur
- Namur Institute of Structured Matter, University of Namur
- Fonds De La Recherche Scientifique - FNRS
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Keywords
- reactive oxygen species, oxidative stress, bacterial chemotaxis, superoxide dismutase, catalase, redox signaling, copper coordination, copper toxicity
- MeSH terms
- Methyl-Accepting Chemotaxis Proteins, Bacterial Proteins, Chemotaxis, Copper, Cytoplasm, Escherichia coli, Reactive Oxygen Species, Oxidative Stress
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