Diversity and regulation of ATP sulfurylase in photosynthetic organisms

. 2014 ; 5 () : 597. [epub] 20141105

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid25414712

ATP sulfurylase (ATPS) catalyzes the first committed step in the sulfate assimilation pathway, the activation of sulfate prior to its reduction. ATPS has been studied in only a few model organisms and even in these cases to a much smaller extent than the sulfate reduction and cysteine synthesis enzymes. This is possibly because the latter were considered of greater regulatory importance for sulfate assimilation. Recent evidences (reported in this paper) challenge this view and suggest that ATPS may have a crucial regulatory role in sulfate assimilation, at least in algae. In the ensuing text, we summarize the current knowledge on ATPS, with special attention to the processes that control its activity and gene(s) expression in algae. Special attention is given to algae ATPS proteins. The focus on algae is the consequence of the fact that a comprehensive investigation of ATPS revealed that the algal enzymes, especially those that are most likely involved in the pathway of sulfate reduction to cysteine, possess features that are not present in other organisms. Remarkably, algal ATPS proteins show a great diversity of isoforms and a high content of cysteine residues, whose positions are often conserved. According to the occurrence of cysteine residues, the ATPS of eukaryotic algae is closer to that of marine cyanobacteria of the genera Synechococcus and Prochlorococcus and is more distant from that of freshwater cyanobacteria. These characteristics might have evolved in parallel with the radiation of algae in the oceans and the increase of sulfate concentration in seawater.

Zobrazit více v PubMed

Allen E., Xie Z. X., Gustafson A. M., Carrington J. C. (2005). microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207–221. 10.1016/j.cell.2005.04.004 PubMed DOI

Balsera M., Uberegui E., Schuermann P., Buchanan B. B. (2014). Evolutionary development of redox regulation in chloroplasts. Antioxid. Redox Signaling. 21, 1327–1355. 10.1089/ars.2013.5817 PubMed DOI

Beynon J. D., Macrae I. J., Huston S. L., Nelson D. C., Segel I. H., Fisher A. J. (2001). Crystal structure of ATP sulfurylase from the bacterial symbiont of the hydrothermal vent tubeworm Riftia pachyptila. Biochemistry 40, 14509–14517. 10.1021/bi015643l PubMed DOI

Bick J. A., Leustek T. (1998). Plant sulfur metabolism - the reduction of sulfate to sulfite. Curr. Opin. Plant Biol. 1, 240–244. 10.1016/S1369-5266(98)80111-8 PubMed DOI

Bicknell R., Cullis P. M., Jarvest R. L., Lowe G. (1982). The stereochemical course of nucleotidyl transfer catalyzed by ATP sulfurylase. J. Biol. Chem. 257, 8922–8927. PubMed

Bochenek M., Etherington G. J., Koprivova A., Mugford S. T., Malin G., Kopriva S. (2013). Transcriptome analysis of the sulfate deficiency response in the marine microalga Emiliania huxleyi. New Phytol. 199, 650–662. 10.1111/nph.12303 PubMed DOI

Bradley M. E., Rest J. S., Li W.-H., Schwartz N. B. (2009). Sulfate activation enzymes: phylogeny and association with pyrophosphatase. J. Mol. Evol. 68, 1–13. 10.1007/s00239-008-9181-6 PubMed DOI

Bromke M. A., Hoefgen R., Hesse H. (2013). Phylogenetic aspects of the sulfate assimilation genes from Thalassiosira pseudonana. Amino Acids 44, 1253–1265. 10.1007/s00726-013-1462-8 PubMed DOI

Brunold C. (2000). Regulatory interactions between sulfate and nitrate assimilation, in Sulfur Nutrition and Sulfur Assimilation in Higher Plants, eds De Kok L. J., Stulen I., Rennenberg H., Brunold C., Rauser W. E. (Hague: SPB Academic Publishing; ), 6–75.

Brunold C., Schiff J. A. (1976). Studies of sulfate utilization of algae: 15. Enzymes of assimilatory sulfate reduction in euglena and their cellular localization. Plant Physiol. 57, 430–436. 10.1104/pp.57.3.430 PubMed DOI PMC

Brunold C., Suter M. (1984). Regulation of sulfate assimilation by nitrogen nutrition in the duckweed Lemna minor L. Plant Physiol. 76, 579–583. 10.1104/pp.76.3.579 PubMed DOI PMC

Buchanan B. B., Balmer Y. (2005). Redox regulation: a broadening horizon. Annu. Rev. Plant Biol. 56, 187–220. 10.1146/annurev.arplant.56.032604.144246 PubMed DOI

Canfield D. E. (2004). The evolution of the Earth surface sulfur reservoir. Am. J. Sci. 304, 839–861 10.2475/ajs.304.10.839 DOI

Couturier J., Chibani K., Jacquot J.-P., Rouhier N. (2013). Cysteine-based redox regulation and signaling in plants. Front. Plant Sci. 4:105. 10.3389/fpls.2013.00105 PubMed DOI PMC

Cumming M., Leung S., McCallum J., McManus M. T. (2007). Complex formation between recombinant ATP sulfurylase and APS reductase of Allium cepa (L.). FEBS Lett. 581, 4139–4147. 10.1016/j.febslet.2007.07.062 PubMed DOI

Dixon D. P., Skipsey M., Grundy N. M., Edwards R. (2005). Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol. 138, 2233–2244. 10.1104/pp.104.058917 PubMed DOI PMC

Farley J. R., Cryns D. F., Yang Y. H., Segel I. H. (1976). Adenosine triphosphate sulfurylase from Penicillium chrysogenum. Steady state kinetics of the forward and reverse reactions. J. Biol. Chem. 251, 4389–4397. PubMed

Farley J. R., Nakayama G., Cryns D., Segel I. H. (1978). Adenosine triphosphate sulfurylase from Penicillium chrysogenum equilibrium binding, substrate hydrolysis, and isotope exchange studies. Arch. Biochem. Biophys. 185, 376–390. 10.1016/0003-9861(78)90180-7 PubMed DOI

Flombaum P., Gallegos J. L., Gordillo R. A., Rincon J., Zabala L. L., Jiao N., et al. . (2013). Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl. Acad. Sci. U.S.A. 110, 9824–9829. 10.1073/pnas.1307701110 PubMed DOI PMC

Giordano M. (2013). Homeostasis: an underestimated focal point of ecology and evolution. Plant Sci. 211, 92–101. 10.1016/j.plantsci.2013.07.008 PubMed DOI

Giordano M., Pezzoni V., Hell R. (2000). Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiol. 124, 857–864. 10.1104/pp.124.2.857 PubMed DOI PMC

Giordano M., Prioretti L. (2014). Sulphur and algae: metabolism, ecology and evolution, in The physiology of Microalgae, eds Borowitzka M. A., Beardall J., Raven J. A. (Dordrecht: Springer; ).

Giordano M., Raven J. A. (2014). Nitrogen and sulfur assimilation in plants and algae. Aquat. Bot. 118, 45–61. 10.1016/j.aquabot.2014.06.012 DOI

Glaeser K., Kanawati B., Kubo T., Schmitt-Kopplin P., Grill E. (2014). Exploring the Arabidopsis sulfur metabolome. Plant J. 77, 31–45. 10.1111/tpj.12359 PubMed DOI

Harjes S., Bayer P., Scheidig A. J. (2005). The crystal structure of human PAPS synthetase 1 reveals asymmetry in substrate binding. J. Mol. Biol. 347, 623–635. 10.1016/j.jmb.2005.01.005 PubMed DOI

Hatzfeld Y., Lee S., Lee M., Leustek T., Saito K. (2000). Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248, 51–58. 10.1016/S0378-1119(00)00132-3 PubMed DOI

Herrmann J., Ravilious G. E., McKinney S. E., Westfall C. S., Lee S. G., Baraniecka P., et al. . (2014). Structure and mechanism of soybean ATP sulfurylase and the committed step in plant sulfur assimilation. J. Biol. Chem. 289, 10919–10929. 10.1074/jbc.M113.540401 PubMed DOI PMC

Holmer M., Storkholm P. (2001). Sulphate reduction and sulphur cycling in lake sediments: a review. Freshw. Biol. 46, 431–451 10.1046/j.1365-2427.2001.00687.x DOI

Sonderby I. E., Geu F. F., Halkier B. A. (2010). Biosynthesis of glucosinolates - gene discovery and beyond. Trends Plant Sci. 15, 283–290. 10.1016/j.tplants.2010.02.005 PubMed DOI

Jagadeeswaran G., Li Y.-F., Sunkar R. (2014). Redox signaling mediates the expression of a sulfate-deprivation-inducible microRNA395 in Arabidopsis. Plant J. 77, 85–96. 10.1111/tpj.12364 PubMed DOI

Jones-Rhoades M. W., Bartel D. P. (2004). Computational identification of plant MicroRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14, 787–799. 10.1016/j.molcel.2004.05.027 PubMed DOI

Kawashima C. G., Matthewman C. A., Huang S., Lee B.-R., Yoshimoto N., Koprivova A., et al. . (2011). Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J. 66, 863–876. 10.1111/j.1365-313X.2011.04547.x PubMed DOI

Kopriva S., Mugford S. G., Matthewman C., Koprivova A. (2009). Plant sulfate assimilation genes: redundancy versus specialization. Plant Cell Rep. 28, 1769–1780. 10.1007/s00299-009-0793-0 PubMed DOI

Koprivova A., Giovannetti M., Baraniecka P., Lee B.-R., Grondin C., Loudet O., et al. . (2013). Natural variation in the ATPS1 isoform of ATP sulfurylase contributes to the control of sulfate levels in Arabidopsis. Plant Physiol. 163, 1133–1141. 10.1104/pp.113.225748 PubMed DOI PMC

Lalor D. J., Schnyder T., Saridakis V., Pilloff D. E., Dong A., Tang H., et al. . (2003). Structural and functional analysis of a truncated form of Saccharomyces cerevisiae ATP sulfurylase: C-terminal domain essential for oligomer formation but not for activity. Protein Eng. 16, 1071–1079. 10.1093/protein/gzg133 PubMed DOI

Lappartient A. G., Touraine B. (1996). Demand-driven control of root ATP sulfurylase activity and SO42- uptake in intact canola - The role of phloem-translocated glutathione. Plant Physiol. 111, 147–157. PubMed PMC

Lappartient A. G., Touraine B. (1997). Glutathione-mediated regulation of ATP sulfurylase activity, SO4(2-) uptake, and oxidative stress response in intact canola roots. Plant Physiol. 114, 177–183. PubMed PMC

Lappartient A. G., Vidmar J. J., Leustek T., Glass A. D. M., Touraine B. (1999). Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J. 18, 89–95. 10.1046/j.1365-313X.1999.00416.x PubMed DOI

Leao G. A., Oliveira J. A., Farnese F. S., Gusman G. S., Felipe R. T. A. (2014). Sulfur metabolism: different tolerances of two aquatic macrophytes exposed to arsenic. Ecotoxicol. Environ. Saf. 105, 36–42. 10.1016/j.ecoenv.2014.03.011 PubMed DOI

Lee S., Leustek T. (1998). APS kinase from Arabidopsis thaliana: genomic organization, expression, and kinetic analysis of the recombinant enzyme. Biochem. Biophys. Res. Commun. 247, 171–175. 10.1006/bbrc.1998.8751 PubMed DOI

Lee S. M., Leustek T. (1999). The affect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci. 141, 201–207 10.1016/S0168-9452(98)00231-3 DOI

Leustek T., Murillo M., Cervantes M. (1994). Cloning of a cDNA-encoding ATP sulfurylase from Arabidopsis thaliana by functional expression in Saccharomyces cerevisiae. Plant Physiol. 105, 897–902. 10.1104/pp.105.3.897 PubMed DOI PMC

Leustek T., Saito K. (1999). Sulfate transport and assimilation in plants. Plant Physiol. 120, 637–643. 10.1104/pp.120.3.637 PubMed DOI PMC

Leyh T. S. (1993). The physical biochemistry and molecular genetics of sulfate activation. Crit. Rev. Biochem. Mol. Biol. 28, 515–542. 10.3109/10409239309085137 PubMed DOI

Leyh T. S., Taylor J. C., Markham G. D. (1988). The sulfate activation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization. J. Biol. Chem. 263, 2409–2416. PubMed

Lillig C. H., Schiffmann S., Berndt C., Berken A., Tischka R., Schwenn J. D. (2001). Molecular and catalytic properties of Arabidopsis thaliana adenylyl sulfate (APS)-kinase. Arch. Biochem. Biophys. 392, 303–310. 10.1006/abbi.2001.2453 PubMed DOI

Lindahl M., Florencio F. J. (2003). Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc. Natl. Acad. Sci. U.S.A. 100, 16107–16112. 10.1073/pnas.2534397100 PubMed DOI PMC

Liu C. X., Suo Y., Leyh T. S. (1994). The energetic linkage of GTP hydrolysis and the synthesis of activated sulfate. Biochemistry 33, 7309–7314. 10.1021/bi00189a036 PubMed DOI

Liu T., Chen J. A., Wang W., Simon M., Wu F., Hu W., et al. . (2014). A combined proteomic and transcriptomic analysis on sulfur metabolism pathways of Arabidopsis thaliana under simulated acid rain. PLoS ONE 9:e90120. 10.1371/journal.pone.0090120 PubMed DOI PMC

MacRae I. J., Segel I. H., Fisher A. J. (2001). Crystal structure of ATP sulfurylase from Penicillium chrysogenum: insights into the allosteric regulation of sulfate assimilation. Biochemistry 40, 6795–6804. 10.1021/bi010367w PubMed DOI

MacRae I. J., Segel I. H., Fisher A. J. (2002). Allosteric inhibition via R-state destabilization in ATP sulfurylase from Penicillium chrysogenum. Nat. Struct. Mol. Biol. 9, 945–949. 10.1038/nsb868 PubMed DOI

Marchand C., Le Marechal P., Meyer Y., Decottignies P. (2006). Comparative proteomic approaches for the isolation of proteins interacting with thioredoxin. Proteomics 6, 6528–6537. 10.1002/pmic.200600443 PubMed DOI

Maruyama-Nakashita A., Nakamura Y., Tohge T., Saito K., Takahashi H. (2006). Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18, 3235–3251. 10.1105/tpc.106.046458 PubMed DOI PMC

Montechiaro F., Giordano M. (2010). Compositional homeostasis of the dinoflagellate Protoceratium reticulatum grown at three different pCO2. J. Plant Physiol. 167, 110–113. 10.1016/j.jplph.2009.07.013 PubMed DOI

Mougous J. D., Lee D. H., Hubbard S. C., Schelle M. W., Vocadlo D. J., Berger J. M., et al. . (2006). Molecular basis for G protein control of the prokaryotic ATP sulfurylase. Mol. Cell 21, 109–122. 10.1016/j.molcel.2005.10.034 PubMed DOI

Mueller J. W., Shafqat N. (2013). Adenosine-5-phosphosulfate - a multifaceted modulator of bifunctional 3-phospho-adenosine-5-phosphosulfate synthases and related enzymes. FEBS J. 280, 3050–3057. 10.1111/febs.12252 PubMed DOI PMC

Murillo M., Leustek T. (1995). Adenosine-5′-triphosphate-sulfurylase from Arabidopsis thaliana and Escherichia coli are functionally equivalent but structurally and kinetically divergent - nucleotide sequence of two adenosine-5′-triphosphate-sulfurylase cDNAs from Arabidopsis thaliana and analysis of a recombinant enzyme. Arch. Biochem. Biophys. 323, 195–204. 10.1006/abbi.1995.0026 PubMed DOI

Parey K., Demmer U., Warkentin E., Wynen A., Ermler U., Dahl C. (2013). Structural, biochemical and genetic characterization of dissimilatory ATP sulfurylase from Allochromatium vinosum. PLoS ONE 8:e74707. 10.1371/journal.pone.0074707 PubMed DOI PMC

Patron N. J., Durnford D. G., Kopriva S. (2008). Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol. Biol. 8:39. 10.1186/1471-2148-8-39 PubMed DOI PMC

Phartiyal P., Kim W.-S., Cahoon R. E., Jez J. M., Krishnan H. B. (2006). Soybean ATP sulfurylase, a homodimeric enzyme involved in sulfur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch. Biochem. Biophys. 450, 20–29. 10.1016/j.abb.2006.03.033 PubMed DOI

Ratti S., Knoll A. H., Giordano M. (2011). Did sulfate availability facilitate the evolutionary expansion of chlorophyll a plus c phytoplankton in the oceans? Geobiology 9, 301–312. 10.1111/j.1472-4669.2011.00284.x PubMed DOI

Rauen H. M. (1964). Biochemisches Taschenbuch. Berlin; Heidelberg: Springer.

Ravilious G. E., Herrmann J., Lee S. G., Westfall C. S., Jez J. M. (2013). Kinetic mechanism of the dimeric ATP sulfurylase from plants. Biosci. Rep. 33, 585–591. 10.1042/BSR20130073 PubMed DOI PMC

Rosenwasser S., Van Creveld S. G., Schatz D., Malitsky S., Tzfadia O., Aharoni A., et al. . (2014). Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment. Proc. Natl. Acad. Sci. U.S.A. 111, 2740–2745. 10.1073/pnas.1319773111 PubMed DOI PMC

Rotte C., Leustek T. (2000). Differential subcellular localization and expression of ATP sulfurylase and 5′-adenylylsulfate reductase during ontogenesis of Arabidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may have specialized functions. Plant Physiol. 124, 715–724. 10.1104/pp.124.2.715 PubMed DOI PMC

Schiff J. A., Hodson R. C. (1973). The metabolism of sulfate. Annu. Rev. Plant Physiol. 24, 381–414 10.1146/annurev.pp.24.060173.002121 DOI

Schwedock J., Long S. R. (1990). ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348, 644–647. 10.1038/348644a0 PubMed DOI

Segel I. H. (1976). Biochemical Calculations: How to Solve Mathematical Problems in General Biochemistry. New York, NY: John Wiley & Sons Inc.

Seubert P. A., Hoang L., Renosto F., Segel I. H. (1983). ATP sulfurylase from Penicillium chrysogenum: measurements of the true specific activity of an enzyme subject to potent product inhibition and a reassessment of the kinetic mechanism. Arch. Biochem. Biophys. 225, 679–691. 10.1016/0003-9861(83)90079-6 PubMed DOI

Seubert P. A., Renosto F., Knudson P., Segel I. H. (1985). Adenosinetriphosphate sulfurylase from Penicillium chrysogenum: steady-state kinetics of the forward and reverse reactions, alternative substrate kinetics, and equilibrium binding studies. Arch. Biochem. Biophys. 240, 509–523. 10.1016/0003-9861(85)90057-8 PubMed DOI

Shaw W. H., Anderson J. W. (1974). The enzymology of adenosine triphosphate sulphurylase from spinach leaf tissue. Biochem. J. 139, 27–35. PubMed PMC

Shu L., Hu Z. (2012). Characterization and differential expression of microRNAs elicited by sulfur deprivation in Chlamydomonas reinhardtii. BMC Genomics 13:108. 10.1186/1471-2164-13-108 PubMed DOI PMC

Song P., Li L., Liu J. (2013). Proteomic analysis in nitrogen-deprived Isochrysis galbana during lipid accumulation. PLoS ONE 8:e82188. 10.1371/journal.pone.0082188 PubMed DOI PMC

Suga H., Chen Z., de Mendoza A., Sebe-Pedros A., Brown M. W., Kramer E., et al. . (2013). The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat. Commun. 4, 2325. 10.1038/ncomms3325 PubMed DOI PMC

Sun M., Leyh T. S. (2006). Channeling in sulfate activating complexes. Biochemistry 45, 11304–11311. 10.1021/bi060421e PubMed DOI

Taguchi Y., Sugishima M., Fukuyama K. (2004). Crystal structure of a novel zinc-binding ATP sulfurylase from Thermus thermophilus HB8. Biochemistry 43, 4111–4118. 10.1021/bi036052t PubMed DOI

Takahashi H., Kopriva S., Giordano M., Saito K., Hell R. (2011). Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62, 157–184. 10.1146/annurev-arplant-042110-103921 PubMed DOI

Ullrich T. C., Blaesse M., Huber R. (2001). Crystal structure of ATP sulfurylase from Saccharomyces cerevisiae, a key enzyme in sulfate activation. EMBO J. 20, 316–329. 10.1093/emboj/20.3.316 PubMed DOI PMC

Vauclare P., Kopriva S., Fell D., Suter M., Sticher L., Von Ballmoos P., et al. . (2002). Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J. 31, 729–740. 10.1046/j.1365-313X.2002.01391.x PubMed DOI

Wang M., Wang Q., Zhang B. (2013). Response of miRNAs and their targets to salt and drought stresses in cotton (Gossypium hirsutum L.). Gene 530, 26–32. 10.1016/j.gene.2013.08.009 PubMed DOI

Yatusevich R., Mugford S. G., Matthewman C., Gigolashvili T., Frerigmann H., Delaney S., et al. . (2010). Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J. 62, 1–11. 10.1111/j.1365-313X.2009.04118.x PubMed DOI

Yildiz F. H., Davies J. P., Grossman A. R. (1996). Sulfur availability and the SAC1 gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii. Plant Physiol. 112, 669–675. 10.1104/pp.112.2.669 PubMed DOI PMC

Yu Z., Lansdon E. B., Segel I. H., Fisher A. J. (2007). Crystal structure of the bifunctional ATP sulfurylase - APS kinase from the chemolithotrophic thermophile Aquifex aeolicus. J. Mol. Biol. 365, 732–743. 10.1016/j.jmb.2006.10.035 PubMed DOI

Zhang Z., Shrager J., Jain M., Chang C. W., Vallon O., Grossman A. R. (2004). Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot. Cell 3, 1331–1348. 10.1128/EC.3.5.1331-1348.2004 PubMed DOI PMC

Zhaxybayeva O., Gogarten J. P., Charlebois R. L., Doolittle W. F., Papke R. T. (2006). Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res. 16, 1099–1108. 10.1101/gr.5322306 PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Effect of sulfate availability on phytoplankton stoichiometry

. 2025 Aug ; 61 (4) : 895-910. [epub] 20250625

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...