Manganese co-localizes with calcium and phosphorus in Chlamydomonas acidocalcisomes and is mobilized in manganese-deficient conditions

Munkhtsetseg Tsednee, Madeli Castruita, Patrice A. Salomé, Ajay Sharma, Brianne E. Lewis, Stefan R. Schmollinger, Daniela Strenkert, Kristen Holbrook, Marisa S. Otegui, Kaustav Khatua, Sayani Das, Ankona Datta, Si Chen, Christina Ramon, Martina Ralle, Peter K. Weber, Timothy L. Stemmler, Jennifer Pett-Ridge, Brian M. Hoffman, Sabeeha S. Merchant

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Abstract

Exposing cells to excess metal concentrations well beyond the cellular quota is a powerful tool for understanding the molecular mechanisms of metal homeostasis. Such improved understanding may enable bioengineering of organisms with improved nutrition and bioremediation capacity. We report here that Chlamydomonas reinhardtii can accumulate manganese (Mn) in proportion to extracellular supply, up to 30-fold greater than its typical quota and with remarkable tolerance. As visualized by X-ray fluorescence microscopy and nanoscale secondary ion MS (nanoSIMS), Mn largely co-localizes with phosphorus (P) and calcium (Ca), consistent with the Mn-accumulating site being an acidic vacuole, known as the acidocalcisome. VacuolarMnstores are accessible reserves that can be mobilized in Mn-deficient conditions to support algal growth. We noted that Mn accumulation depends on cellular polyphosphate (polyP) content, indicated by 1) a consistent failure of C. reinhardtii vtc1 mutant strains, which are deficient in polyphosphate synthesis, to accumulate Mn and 2) a drastic reduction of theMnstorage capacity in P-deficient cells. Rather surprisingly, X-ray absorption spectroscopy, EPR, and electron nuclear double resonance revealed that only little Mn2 β is stably complexed with polyP, indicating that polyP is not the final Mn ligand. We propose that polyPs are a critical component of Mn accumulation in Chlamydomonas by driving Mn relocation from the cytosol to acidocalcisomes. Within these structures, polyP may, in turn, escort vacuolar Mn to a number of storage ligands, including phosphate and phytate, and other, yet unidentified, compounds.

Original languageEnglish (US)
Pages (from-to)17626-17641
Number of pages16
JournalJournal of Biological Chemistry
Volume294
Issue number46
DOIs
StatePublished - Nov 15 2019

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

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    Tsednee, M., Castruita, M., Salomé, P. A., Sharma, A., Lewis, B. E., Schmollinger, S. R., Strenkert, D., Holbrook, K., Otegui, M. S., Khatua, K., Das, S., Datta, A., Chen, S., Ramon, C., Ralle, M., Weber, P. K., Stemmler, T. L., Pett-Ridge, J., Hoffman, B. M., & Merchant, S. S. (2019). Manganese co-localizes with calcium and phosphorus in Chlamydomonas acidocalcisomes and is mobilized in manganese-deficient conditions. Journal of Biological Chemistry, 294(46), 17626-17641. https://doi.org/10.1074/jbc.RA119.009130