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

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

doi:10.1074/jbc.RA119.009130

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

Journal Article · Fri Nov 01 00:00:00 EDT 2019 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.RA119.009130· OSTI ID:1766099

Tsednee, Munkhtsetseg; Castruita, Madeli;

; Sharma, Ajay;

; Schmollinger, Stefan R.; Strenkert, Daniela; Holbrook, Kristen;

; Khatua, Kaustav; Das, Sayani; Datta, Ankona;

; Ramon, Christina; Ralle, Martina; Weber, Peter K.; Stemmler, Timothy L.; Pett-Ridge, Jennifer; Hoffman, Brian M.; Merchant, Sabeeha S.

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 manga- nese (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 sec- ondary ion MS (nanoSIMS), Mn largely co-localizes with phos- phorus (P) and calcium (Ca), consistent with the Mn-accumu- lating site being an acidic vacuole, known as the acidocalcisome. Vacuolar Mn stores 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. rein- hardtii vtc1 mutant strains, which are deficient in polyphos- phate synthesis, to accumulate Mn and 2) a drastic reduction of the Mn storage capacity in P-deficient cells. Rather surprisingly, X-ray absorption spectroscopy, EPR, and electron nuclear double resonance revealed that only little Mn 2 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 relo- cation from the cytosol to acidocalcisomes. Within these structures, polyP may, in turn, escort vacuolar Mn to a num- ber of storage ligands, including phosphate and phytate, and other, yet unidentified, compounds.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Argonne National Laboratory (ANL), Argonne, IL (United States); University of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC52-07NA27344; AC02-06CH11357; FG02-04ER15529

OSTI ID:: 1766099

Alternate ID(s):: OSTI ID: 1603239; OSTI ID: 1607396; OSTI ID: 1922673

Report Number(s):: LLNL-JRNL-772298; S0021925820307511; PII: S0021925820307511

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 294 Journal Issue: 46; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 36 works

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59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
algae
antioxidant
calcium
Chlamydomonas
histidine
imaging
lysosomal acidification
lysosome
manganese
metal homeostasis
H+-PPase
NRAMP
organelle
photosynthesis
polyphosphate

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

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