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Title: Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas

Here we identified a Cu-accumulating structure with a dynamic role in intracellular Cu homeostasis. During Zn limitation, Chlamydomonas reinhardtii hyperaccumulates Cu, a process dependent on the nutritional Cu sensor CRR1, but it is functionally Cu deficient. Visualization of intracellular Cu revealed major Cu accumulation sites coincident with electron-dense structures that stained positive for low pH and polyphosphate, suggesting that they are lysosome-related organelles. Nano-secondary ion MS showed colocalization of Ca and Cu, and X-ray absorption spectroscopy was consistent with Cu + accumulation in an ordered structure. Zn resupply restored Cu homeostasis concomitant with reduced abundance of these structures. Cu isotope labeling demonstrated that sequestered Cu + became bioavailable for the synthesis of plastocyanin, and transcriptome profiling indicated that mobilized Cu became visible to CRR1. Cu trafficking to intracellular accumulation sites may be a strategy for preventing protein mismetallation during Zn deficiency and enabling efficient cuproprotein metallation or remetallation upon Zn resupply.
Authors:
 [1] ;  [1] ;  [1] ;  [1] ;  [2] ;  [2] ;  [3] ;  [2] ;  [4] ;  [5] ;  [6] ;  [6] ;  [3] ;  [2] ;  [7]
  1. Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Materials Science and Engineering
  2. Univ. of California-Berkeley, Berkeley, CA (United States). Dept. of Chemistry; Univ. of California-Berkeley, Berkeley, CA (United States). Howard Hughes Medical Inst.
  3. Wayne State Univ., Detroit, MI (United States). Dept. of Pharmaceutical Sciences
  4. Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Biological Chemistry
  5. Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Materials Science and Engineering; Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Biological Chemistry; Univ. of California-Los Angeles, Los Angeles, CA (United States).Inst. for Genomics and Proteomics
  6. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Chemical Sciences Division
  7. Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Materials Science and Engineering; Univ. of California-Los Angeles, Los Angeles, CA (United States).Inst. for Genomics and Proteomics
Publication Date:
Report Number(s):
LLNL-JRNL-652416
Journal ID: ISSN 1552-4450; nchembio.1662
Grant/Contract Number:
FC02-02ER63421; AC52-07NA27344; T32HL120822; D1242134
Type:
Accepted Manuscript
Journal Name:
Nature Chemical Biology
Additional Journal Information:
Journal Volume: 10; Journal Issue: 12; Journal ID: ISSN 1552-4450
Publisher:
Nature Publishing Group
Research Org:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org:
USDOE; National Institutes of Health (NIH)
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 47 OTHER INSTRUMENTATION; Metals; Membrane trafficking; Bacteria; 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL AND ANALYTICAL CHEMISTRY; bacteria; bioinorganic chemistry; membrane trafficking; metals
OSTI Identifier:
1282166
Alternate Identifier(s):
OSTI ID: 1321442

Hong-Hermesdorf, Anne, Miethke, Marcus, Gallaher, Sean D., Kropat, Janette, Dodani, Sheel C., Chan, Jefferson, Barupala, Dulmini, Domaille, Dylan W., Shirasaki, Dyna I., Loo, Joseph A., Weber, Peter K., Pett-Ridge, Jennifer, Stemmler, Timothy L., Chang, Christopher J., and Merchant, Sabeeha S.. Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas. United States: N. p., Web. doi:10.1038/nchembio.1662.
Hong-Hermesdorf, Anne, Miethke, Marcus, Gallaher, Sean D., Kropat, Janette, Dodani, Sheel C., Chan, Jefferson, Barupala, Dulmini, Domaille, Dylan W., Shirasaki, Dyna I., Loo, Joseph A., Weber, Peter K., Pett-Ridge, Jennifer, Stemmler, Timothy L., Chang, Christopher J., & Merchant, Sabeeha S.. Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas. United States. doi:10.1038/nchembio.1662.
Hong-Hermesdorf, Anne, Miethke, Marcus, Gallaher, Sean D., Kropat, Janette, Dodani, Sheel C., Chan, Jefferson, Barupala, Dulmini, Domaille, Dylan W., Shirasaki, Dyna I., Loo, Joseph A., Weber, Peter K., Pett-Ridge, Jennifer, Stemmler, Timothy L., Chang, Christopher J., and Merchant, Sabeeha S.. 2014. "Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas". United States. doi:10.1038/nchembio.1662. https://www.osti.gov/servlets/purl/1282166.
@article{osti_1282166,
title = {Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas},
author = {Hong-Hermesdorf, Anne and Miethke, Marcus and Gallaher, Sean D. and Kropat, Janette and Dodani, Sheel C. and Chan, Jefferson and Barupala, Dulmini and Domaille, Dylan W. and Shirasaki, Dyna I. and Loo, Joseph A. and Weber, Peter K. and Pett-Ridge, Jennifer and Stemmler, Timothy L. and Chang, Christopher J. and Merchant, Sabeeha S.},
abstractNote = {Here we identified a Cu-accumulating structure with a dynamic role in intracellular Cu homeostasis. During Zn limitation, Chlamydomonas reinhardtii hyperaccumulates Cu, a process dependent on the nutritional Cu sensor CRR1, but it is functionally Cu deficient. Visualization of intracellular Cu revealed major Cu accumulation sites coincident with electron-dense structures that stained positive for low pH and polyphosphate, suggesting that they are lysosome-related organelles. Nano-secondary ion MS showed colocalization of Ca and Cu, and X-ray absorption spectroscopy was consistent with Cu+ accumulation in an ordered structure. Zn resupply restored Cu homeostasis concomitant with reduced abundance of these structures. Cu isotope labeling demonstrated that sequestered Cu+ became bioavailable for the synthesis of plastocyanin, and transcriptome profiling indicated that mobilized Cu became visible to CRR1. Cu trafficking to intracellular accumulation sites may be a strategy for preventing protein mismetallation during Zn deficiency and enabling efficient cuproprotein metallation or remetallation upon Zn resupply.},
doi = {10.1038/nchembio.1662},
journal = {Nature Chemical Biology},
number = 12,
volume = 10,
place = {United States},
year = {2014},
month = {10}
}