Zinc deficiency impacts CO2 Assimilation and disrupts copper homeostasis in Chlamydomonas Reinhardtii

Journal of Biological Chemistry

Volumn 288, Issue 15, 2013, Pages 10672-10683

  Malasarn, Davin ^a   Kropat, Janette ^a   Hsieh, Scott I ^a   Finazzi, Giovanni ^c,d   Casero, David ^b   Loo, Joseph A ^a,b   Pellegrini, Matteo ^b   Wollman, Francis André ^c   Merchant, Sabeeha S ^a,b  

^a Department of Chemistry and Biochemistry ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON-CONCENTRATING MECHANISM; CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; COPPER HOMEOSTASIS; COPPER SENSOR; PROTEIN STRUCTURES; ZINC DEFICIENCY;

CARBON DIOXIDE; PHYSIOLOGY; ZINC;

COPPER;

CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE I; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE III; CARBONATE DEHYDRATASE IV; COPPER; PROTEOME; TRANSCRIPTOME; ZINC;

ARTICLE; CARBON DIOXIDE FIXATION; CATALYSIS; CELL SIZE; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; HOMEOSTASIS; IMMUNOBLOTTING; METALLATION; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEOMICS; REGULON; STOICHIOMETRY; ZINC DEFICIENCY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARBON DIOXIDE; CATION TRANSPORT PROTEINS; CHLAMYDOMONAS REINHARDTII; COPPER; HOMEOSTASIS; PLANT PROTEINS; ZINC;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII;

EID: 84876213081     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.455105     Document Type: Article

References (72)

1. Andreini, C., Banci, L., Bertini, I., and Rosato, A. (2006) Zinc through the three domains of life. J. Proteome Res. 5,3173-3178
2. Ehrensberger, K. M., and Bird, A. J. (2011) Hammering out details. Regulating metal levels in eukaryotes. Trends Biochem. Sci. 36, 524-531
3. Eide, D. J. (2009) Homeostatic and adaptive responses to zinc deficiency in Saccharomyces cerevisiae. J. Biol. Chem. 284, 18565-18569
4. Ryu, M. S., Lichten, L. A., Liuzzi, J. P., and Cousins, R. J. (2008) Zinc transporters ZnT1 (Slc30a1), Zip8 (Slc39a8), and Zip10 (Slc39a10) in mouse red blood cells are differentially regulated during erythroid development and by dietary zinc deficiency. J. Nutr. 138, 2076-2083
5. Dainty, S. J., Kennedy, C. A., Watt, S., Bahler, J., and Whitehall, S. K. (2008) Response of Schizosaccharomyces pombe to zinc deficiency. Eukaryot Cell 7, 454-464
6. Zhao, H., and Eide, D. (1996) The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J. Biol. Chem. 271, 23203-23210
7. Zhao, H., and Eide, D. (1996) The yeast ZRT1 gene encodes the zinc transporter protein of a high affinity uptake system induced by zinc limitation. Proc. Natl. Acad. Sci. U.S.A. 93, 2454-2458
8. Simm, C., Lahner, B., Salt, D., LeFurgey, A., Ingram, P., Yandell, B., and Eide, D. J. (2007) Saccharomyces cerevisiae vacuole in zinc storage and intracellular zinc distribution. Eukaryot. Cell 6, 1166-1177
9. Roh, H. C., Collier, S., Guthrie, J., Robertson, J. D., and Kornfeld, K. (2012) Lysosome-related organelles in intestinal cells are a zinc storage site in C. elegans. Cell Metab. 15, 88-99
10. Ballestin, R., Molowny, A., Marin, M. P., Esteban-Pretel, G., Romero, A. M., Lopez-Garcia, C., Renau-Piqueras, J., and Ponsoda, X. (2011) Ethanol reduces zincosome formation in cultured astrocytes. Alcohol. Alcohol. 46, 17-25
11. Williams, L. E., Pittman, J. K., and Hall, J. L. (2000) Emerging mechanisms for heavy metal transport in plants. Biochim. Biophys. Acta 1465, 104-126
12. Kambe, T., and Andrews, G. K. (2009) Novel proteolytic processing of the ectodomain of the zinc transporter ZIP4 (SLC39A4) during zinc deficiency is inhibited by acrodermatitis enteropathica mutations. Mol. Cell Biol. 29, 129-139
13. Davis, D. E., Roh, H. C., Deshmukh, K., Bruinsma, J. J., Schneider, D. L., Guthrie, J., Robertson, J. D., and Kornfeld, K. (2009) The cation diffusion facilitator gene cdf-2 mediates zinc metabolism in Caenorhabditis elegans. Genetics 182, 1015-1033
14. Blaby-Haas, C. E., and Merchant, S. S. (2012) The ins and outs of algal metal transport. Biochim. Biophys. Acta 1823, 1531-1552
15. Kim, D., Gustin, J. L., Lahner, B., Persans, M. W., Baek, D., Yun, D. J., and Salt, D. E. (2004) The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. Plant J. 39, 237-251
16. Podar, D., Scherer, J., Noordally, Z., Herzyk, P., Nies, D., and Sanders, D. (2012) Metal selectivity determinants in a family of transition metal transporters. J. Biol. Chem. 287, 3185-3196
17. 2 concentrating mechanisms in cyanobacteria. Molecular components, their diversity and evolution. J. Exp. Bot. 54, 609-622
18. 2 concentrating mechanisms in algae. Mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56, 99-131
19. Roberts, K., Granum, E., Leegood, R. C., and Raven, J. A. (2007) Carbon acquisition by diatoms. Photosynth. Res. 93, 79-88
20. 2 recapture. Photosynth. Res. 109, 115-122
21. Lane, T. W., and Morel, F. M. (2000) A biological function for cadmium in marine diatoms. Proc. Natl. Acad. Sci. U.S.A. 97, 4627-4631
22. Lane, T. W., and Morel, F. M. (2000) Regulation of carbonic anhydrase expression by zinc, cobalt, and carbon dioxide in the marine diatom Thalassiosira weissflogii. Plant Physiol. 123, 345-352
23. Yee, D., and Morel, F. M. M. (1996) In vivo substitution of zinc by cobalt in carbonic anhydrase of a marine diatom. Limnol. Oceanogr. 41, 573-577
24. Merchant, S. S., and Helmann, J. D. (2012) Elemental economy. Microbial strategies for optimizing growth in the face of nutrient limitation. Adv. Microb. Physiol. 60, 91-210
25. Merchant, S. S., Allen, M. D., Kropat, J., Moseley, J. L., Long, J. C., Tottey, S., and Terauchi, A. M. (2006) Between a rock and a hard place. Trace element nutrition in Chlamydomonas. Biochim. Biophys. Acta 1763, 578-594
26. Harris, E. H. (1989) The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use, Academic Press, Inc., San Diego,CA
27. Kropat, J., Hong-Hermesdorf, A., Casero, D., Ent, P., Castruita, M., Pellegrini, M., Merchant, S. S., and Malasarn, D. (2011) A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii. Plant J. 66, 770-780
28. Page, M. D., Kropat, J., Hamel, P. P., and Merchant, S. S. (2009) Two Chlamydomonas CTR copper transporters with a novel Cys-Met motif are localized to the plasma membrane and function in copper assimilation. Plant Cell 21, 928-943
29. Allen, M. D., del Campo, J. A., Kropat, J., and Merchant, S. S. (2007) FEA1, FEA2, and FRE1, encoding two homologous secreted proteins and a candidate ferrireductase, are expressed coordinately with FOX1 and FTR1 in iron-deficient Chlamydomonas reinhardtii. Eukaryot. Cell 6, 1841-1852
30. Allen, M. D., Kropat, J., Tottey, S., Del Campo, J. A., and Merchant, S. S. (2007) Manganese deficiency in Chlamydomonas results in loss of photosystem II and MnSOD function, sensitivity to peroxides, and secondary phosphorus and iron deficiency. Plant Physiol. 143, 263-277
31. La Fontaine, S., Quinn, J. M., Nakamoto, S. S., Page, M. D., Göhre, V., Moseley, J. L., Kropat, J., and Merchant, S. (2002) Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot. Cell 1, 736-757
32. Kropat, J., Tottey, S., Birkenbihl, R. P., Depège, N., Huijser, P., and Merchant, S. (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc. Natl. Acad. Sci. U.S.A. 102, 18730-18735
33. Yamasaki, H., Hayashi, M., Fukazawa, M., Kobayashi, Y., and Shikanai, T. (2009) SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21, 347-361
34. Bernal, M., Casero, D., Singh, V., Wilson, G. T., Grande, A., Yang, H., Dodani, S. C., Pellegrini, M., Huijser, P., Connolly, E. L., Merchant, S. S., and Kramer, U. (2012) Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24, 738-761
35. Castruita, M., Casero, D., Karpowicz, S. J., Kropat, J., Vieler, A., Hsieh, S. I., Yan, W., Cokus, S., Loo, J. A., Benning, C., Pellegrini, M., and Merchant, S. S. (2011) Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23, 1273-1292
36. Quinn, J. M., Barraco, P., Eriksson, M., and Merchant, S. (2000) Coordinate copper-and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. J. Biol. Chem. 275, 6080-6089
37. Sommer, F., Kropat, J., Malasarn, D., Grossoehme, N. E., Chen, X., Giedroc, D. P., and Merchant, S. S. (2010) The CRR1 nutritional copper sensor in Chlamydomonas contains two distinct metal-responsive domains. Plant Cell 22, 4098-4113
38. Merchant, S., and Bogorad, L. (1986) Regulation by copper of the expression of plastocyanin and cytochrome c552 in Chlamydomonas reinhardtii. Mol. Cell Biol. 6, 462-469
39. Quinn, J. M., and Merchant, S. (1998) Copper-responsive gene expression during adaptation to copper deficiency. Methods Enzymol. 297, 263-279
40. Joliot, P., and Joliot, A. (2002) Cyclic electron transfer in plant leaf. Proc. Natl. Acad. Sci. U.S.A. 99, 10209-10214
41. Schloss, J. A. (1990) A Chlamydomonas gene encodes a G protein β subunit-like polypeptide. Mol. Gen. Genet. 221, 443-452
42. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2βββCT method. Methods 25, 402-408
43. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S. L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25
44. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNASeq. Nat. Methods 5, 621-628
45. Anders, S., and Huber, W. (2010) Differential expression analysis for sequence count data. Genome Biol. 11, R106
46. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate. A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289-300
47. Howe, G., and Merchant, S. (1992) The biosynthesis of membrane and soluble plastidic c-type cytochromes of Chlamydomonas reinhardtii is dependent on multiple common gene products. EMBO J. 11, 2789-2801
48. Hsieh, S. I., Castruita, M., Malasarn, D., Urzica, E., Erde, J., Page, M. D., Yamasaki, H., Casero, D., Pellegrini, M., Merchant, S. S., and Loo, J. A. (2013) The proteome of copper, iron, zinc, and manganese micronutrient deficiency in Chlamydomonas reinhardtii. Mol. Cell Proteomics 12, 65-86
49. Bailleul, B., Cardol, P., Breyton, C., and Finazzi, G. (2010) Electrochromism: a useful probe to study algal photosynthesis. Photosynth. Res. 106, 179-189
50. Finazzi, G., Buschlen, S., de Vitry, C., Rappaport, F., Joliot, P., and Wollman, F. A. (1997) Function-directed mutagenesis of the cytochrome b6f complex in Chlamydomonas reinhardtii. Involvement of the cd loop of cytochrome b6 in quinol binding to the Qo site. Biochemistry 36, 2867-2874
51. Harris, E. H. (2009) Introduction to Chlamydomonas and Its Laboratory Use, Elsevier, San Diego, CA
52. Hutner, S. H., Provasoli, L., Schatz, A., and Haskins, C. P. (1950) Some approaches to the study of the role of metals in the metabolism of microorganisms. Proc. Am. Philos. Soc. 94, 152-170
53. Hanikenne, M., Krämer, U., Demoulin, V., and Baurain, D. (2005) A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. Plant Physiol. 137, 428-446
54. 2-concentrating mechanism regulator CIA5/ CCM1. Plant Cell 24, 1876-1893
55. Haas, C. E., Rodionov, D. A., Kropat, J., Malasarn, D., Merchant, S. S., and de Crécy-Lagard, V. (2009) A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. BMC Genomics 10, 470 PMC2770081
56. Tachiki, A., Fukuzawa, H., and Miyachi, S. (1992) Characterization of carbonic anhydrase isozyme CA2, which is the CAH2 gene product, in Chlamydomonas reinhardtii. Biosci. Biotechnol. Biochem. 56, 794-798
57. Villarejo, A., Rolland, N., Martinez, F., and Sültemeyer, D. F. (2001) A new chloroplast envelope carbonic anhydrase activity is induced during acclimation to low inorganic carbon concentrations in Chlamydomonas reinhardtii. Planta 213, 286-295
58. Ynalvez, R. A., Xiao, Y., Ward, A. S., Cunnusamy, K., and Moroney, J. V. (2008) Identification and characterization of two closely related-carbonic anhydrases from Chlamydomonas reinhardtii. Physiol. Plant. 133, 15-26
59. Moroney, J. V., Ma, Y., Frey, W. D., Fusilier, K. A., Pham, T. T., Simms, T. A., DiMario, R. J., Yang, J., and Mukherjee, B. (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii. Intracellular location, expression, and physiological roles. Photosynth. Res. 109, 133-149
60. Dancis, A., Haile, D., Yuan, D. S., and Klausner, R. D. (1994) The Saccharomyces cerevisiae copper transport protein (Ctr1p). Biochemical characterization, regulation by copper, and physiologic role in copper uptake. J. Biol. Chem. 269, 25660-25667
61. Rutherford, J. C., and Bird, A. J. (2004) Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot. Cell 3, 1-13
62. Eide, D. J. (2006) Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 1763, 711-722
63. Sinclair, S. A., and Kramer, U. (2012) The zinc homeostasis network of land plants. Biochim. Biophys. Acta 1823, 1553-1567
64. Yamano, T., Miura, K., and Fukuzawa, H. (2008) Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol. 147, 340-354
65. Toepel, J., Albaum, S. P., Arvidsson, S., Goesmann, A., la Russa, M., Rogge, K., and Kruse, O. (2011) Construction and evaluation of a whole genome microarray of Chlamydomonas reinhardtii. BMC Genomics 12, 579
66. Sinetova, M. A., Kupriyanova, E. V., Markelova, A. G., Allakhverdiev, S. I., and Pronina, N. A. (2012) Identification and functional role of the carbonic anhydrase Cah3 in thylakoid membranes of pyrenoid of Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1817, 1248-1255
67. Lane, T. W., Saito, M. A., George, G. N., Pickering, I. J., Prince, R. C., and Morel, F. M. (2005) Biochemistry. A cadmium enzyme from a marine diatom. Nature 435, 42
68. Zhang, B., Egli, D., Georgiev, O., and Schaffner, W. (2001) The Drosophila homolog of mammalian zinc finger factor MTF-1 activates transcription in response to heavy metals. Mol. Cell Biol. 21, 4505-4514
69. Dièz, M., Cerdàn, F. J., Arroyo, M., and Balibrea, J. L. (1989) Use of the copper/zinc ratio in the diagnosis of lung cancer. Cancer 63, 726-730
70. Mezzetti, A., Pierdomenico, S. D., Costantini, F., Romano, F., De Cesare, D., Cuccurullo, F., Imbastaro, T., Riario-Sforza, G., Di Giacomo, F., Zuliani, G., and Fellin, R. (1998) Copper/zinc ratio and systemic oxidant load. Effect of aging and aging-related degenerative diseases. Free Radic. Biol. Med. 25, 676-681
71. 2 availability. Proc. Natl. Acad. Sci. U.S.A. 98, 5347-5352
72. Page, M. D., Allen, M. D., Kropat, J., Urzica, E. I., Karpowicz, S. J., Hsieh, S. I., Loo, J. A., and Merchant, S. S. (2012) Fe sparing and Fe recycling contribute to increased superoxide dismutase capacity in iron-starved Chlamydomonas reinhardtii. Plant Cell 24, 2649-2665