The quantitative proteomic response of Synechocystis sp. PCC6803 to phosphate acclimation
Tóm tắt
Inorganic phosphate (Pi) is a critical nutrient for all life and is periodically limiting in marine and freshwater provinces, yet little is understood how organisms acclimate to fluctuations in Pi within their environment. To investigate whole cell adaptation, we grew Synechocystis sp. PCC6803, a model freshwater cyanobacterium, in 3%, and 0.3% inorganic phosphate (Pi) media. The cells were allowed to acclimate over 60 days, and cells were harvested for quantitative high throughput mass spectrometry-based proteomics using the iTRAQ™ labelling technology. In total, 120 proteins were identified, and 52 proteins were considered differentially abundant compared to the control. Alkaline phosphatase (APase) activities correlated significantly (p < 0.05) with observed relative PhoA abundances. PstS1 and PstS2 were both observed, yet PstS1 was not differentially more abundant than the control. Phycobilisome protein abundances appeared to be coordinated, and are significantly less abundant in 0.3% Pi than 3% Pi cultures. Also, the central metabolic cell function appears to have shifted towards the production of (NADPH) reducing energy and nucleotide sugars. This acclimation response bears strong similarity to the previously reported response to nitrogen deprivation within Synechocystis sp. PCC 6803. However, it also demonstrates some characteristics of desiccation stress, such as the regulation of fatty acids and increased abundance of rehydrin in the 3% Pi culture.
Tài liệu tham khảo
Schutz K, Happe T, Troshina O, Lindblad P, Leitao E, Oliveira P, Tamagnini P: Cyanobacterial H(2) production - a comparative analysis. Planta. 2004, 218: 350-359. 10.1007/s00425-003-1113-5.
Frey KM, Oppermann-Sanio FB, Schmidt H, Steinbuchel A: Technical-scale production of cyanophycin with recombinant strains of Escherichia coli. Appl Environ Microbiol. 2002, 68: 3377-3384. 10.1128/AEM.68.7.3377-3384.2002.
Lagarde D, Beuf L, Vermaas W: Increased production of zeaxanthin and other pigments by application of genetic engineering techniques to Synechocystis sp. strain PCC 6803. Appl Environ Microbiol. 2000, 66: 64-72. 10.1128/AEM.66.1.64-72.2000.
Burja AM, Banaigsb B, Abou-Mansourc E, Burgess JG, Wright PC: Marine cyanobacteria-a prolific source of natural products. Tetrahedron. 2001, 57: 9347-9377. 10.1016/S0040-4020(01)00931-0.
Gill RT, Katsoulakis E, Schmitt W, Taroncher-Oldenburg G, Misra J, Stephanopoulos G: Genome-wide dynamic transcriptional profiling of the light-to-dark transition in Synechocystis sp. strain PCC 6803. J Bacteriol. 2002, 184: 3671-3681. 10.1128/JB.184.13.3671-3681.2002.
Burja AM, Dhamwichukorn S, Wright PC: Cyanobacterial postgenomic research and systems biology. Trends Biotechnol. 2003, 21: 504-511. 10.1016/j.tibtech.2003.08.008.
Gan CS, Reardon KF, Wright PC: Comparison of protein and peptide prefractionation methods for the shotgun proteomic analysis of Synechocystis sp. PCC 6803. Proteomics. 2005, 5: 2468-2478. 10.1002/pmic.200401266.
Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B, Hagemann M: Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics. 2006, 6: 2733-2745. 10.1002/pmic.200500538.
Wassen MJ, Venterink HO, Lapshina ED, Tanneberger F: Endangered plants persist under phosphorus limitation. Nature. 2005, 437: 547-550. 10.1038/nature03950.
Suzuki S, Ferjani A, Suzuki I, Murata N: The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in Synechocystis. J Biol Chem. 2004, 279: 13234-13240.
Allenby NE, O’Connor N, Pragai Z, Ward AC, Wipat A, Harwood CR: Genome-wide transcriptional analysis of the phosphate starvation stimulon of Bacillus subtilis. J Bacteriol. 2005, 187: 8063-8080. 10.1128/JB.187.23.8063-8080.2005.
Kocan M, Schaffer S, Ishige T, Sorger-Herrmann U, Wendisch VF, Bott M: Two-component systems of Corynebacterium glutamicum: deletion analysis and involvement of the PhoS-PhoR system in the phosphate starvation response. J Bacteriol. 2006, 188: 724-732. 10.1128/JB.188.2.724-732.2006.
Martiny AC, Coleman ML, Chisholm SW: Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci U S A. 2006, 103: 12552-12557. 10.1073/pnas.0601301103.
Eymann C, Mach H, Harwood CR, Hecker M: Phosphate-starvation-inducible proteins in Bacillus subtilis: a two-dimensional gel electrophoresis study. Microbiology. 1996, 142: 3163-3170. 10.1099/13500872-142-11-3163.
Antelmann H, Scharf C, Hecker M: Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J Bacteriol. 2000, 182: 4478-4490. 10.1128/JB.182.16.4478-4490.2000.
Madhusudhan KT, McLaughlin R, Komori N, Matsumoto H: Identification of a major protein upon phosphate starvation of Pseudomonas aeruginosa PAO1. J Basic Microbiol. 2003, 43: 36-46. 10.1002/jobm.200390002.
He Z, Zhong H, Hu Y, Xiao S, Liu J, Xu J, Li G: Analysis of differential-expressed proteins of Acidithiobacillus ferrooxidans grown under phosphate starvation. J Biochem Mol Biol. 2005, 38: 545-549. 10.5483/BMBRep.2005.38.5.545.
Fuszard MA, Wright PC, Biggs CA: Cellular acclimation strategies of a minimal picocyanobacterium to phosphate stress. FEMS Microbiol Lett. 2010, 306: 127-134. 10.1111/j.1574-6968.2010.01942.x.
Fuszard M, Wright PC, Biggs CA: Comparative quantitative proteomics of Prochlorococcus ecotypes to a decrease in environmental phosphate concentrations. Aquat Biosystems. 2012, 8: 7-10.1186/2046-9063-8-7.
Tetu SG, Brahamsha B, Johnson DA, Tai V, Phillippy K, Palenik B, Paulsen IT: Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. ISME J. 2009, 3: 835-849. 10.1038/ismej.2009.31.
Ishige T, Krause M, Bott M, Wendisch VF, Sahm H: The phosphate starvation stimulon of Corynebacterium glutamicum determined by DNA microarray analyses. J Bacteriol. 2003, 185: 4519-4529. 10.1128/JB.185.15.4519-4529.2003.
Pitt FD, Mazard S, Humphreys L, Scanlan DJ: Functional characterization of synechocystis sp. Strain PCC 6803 pst1 and pst2 gene clusters reveals a novel strategy for phosphate uptake in a freshwater cyanobacterium. J Bacteriol. 2010, 192: 3512-3523. 10.1128/JB.00258-10.
Adams MM, Gomez-Garcia MR, Grossman AR, Bhaya D: Phosphorus deprivation responses and phosphonate utilization in a thermophilic synechococcus sp. From microbial mats. J Bacteriol. 2008, 190: 8171-8184. 10.1128/JB.01011-08.
Orchard ED, Webb EA, Dyhrman ST: Molecular analysis of the phosphorus starvation response in Trichodesmium spp. Environ Microbiol. 2009, 11: 2400-2411. 10.1111/j.1462-2920.2009.01968.x.
Juntarajumnong W, Hirani T, Simpson J, Incharoensakdi A, Eaton-Rye J: Phosphate sensing in Synechocystis sp. PCC 6803: SphU and the SphS–SphR two-component regulatory system. Arch Microbiol. 2007, 188: 389-402. 10.1007/s00203-007-0259-0.
Hirani TA, Suzuki I, Murata N, Hayashi H, Eaton-Rye JJ: Characterization of a two-component signal transduction system involved in the induction of alkaline phosphatase under phosphate-limiting conditions in Synechocystis sp. PCC 6803. Plant Mol Biol. 2001, 45: 133-144. 10.1023/A:1006425214168.
Morohoshi T, Maruo T, Shirai Y, Kato J, Ikeda T, Takiguchi N, Ohtake H, Kuroda A: Accumulation of inorganic polyphosphate in phoU mutants of Escherichia coli and Synechocystis sp. strain PCC6803. Appl Environ Microbiol. 2002, 68: 4107-4110. 10.1128/AEM.68.8.4107-4110.2002.
Bhaya D, Vaulot D, Amin P, Takahashi AW, Grossman AR: Isolation of regulated genes of the cyanobacterium Synechocystis sp. strain PCC 6803 by differential display. J Bacteriol. 2000, 182: 5692-5699. 10.1128/JB.182.20.5692-5699.2000.
Gomez-Garcia MR, Losada M, Serrano A: Concurrent transcriptional activation of ppa and ppx genes by phosphate deprivation in the cyanobacterium Synechocystis sp. strain PCC 6803. Biochem Biophys Res Commun. 2003, 302: 601-609. 10.1016/S0006-291X(03)00162-1.
Chong PK, Gan CS, Pham TK, Wright PC: Isobaric tags for relative and absolute quantitation (iTRAQ) reproducibility: implication of multiple injections. J Proteome Res. 2006, 5: 1232-1240. 10.1021/pr060018u.
Gan CS, Chong PK, Pham TK, Wright PC: Technical, experimental and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ). J Proteome Res. 2007, 6: 821-827. 10.1021/pr060474i.
Osorio G, Jerez CA: Adaptive response of the archaeon Sulfolobus acidocaldarius BC65 to phosphate starvation. Microbiology. 1996, 142: 1531-1536. 10.1099/13500872-142-6-1531.
Ticconi CA, Delatorre CA, Abel S: Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol. 2001, 127: 963-972. 10.1104/pp.010396.
Ray JM, Bhaya D, Block MA, Grossman AR: Isolation, transcription, and inactivation of the gene for an atypical alkaline phosphatase of Synechococcus sp. strain PCC 7942. J Bacteriol. 1991, 173: 4297-4309.
Doonan BB, Jensen TE: Physiological aspects of alkaline phosphatase in selected cyanobacteria. Microbios. 1980, 29: 185-207.
Bacsi I, Vasas G, Suranyi G, M-Hamvas M, Mathe C, Toth E, Grigorszky I, Gaspar A, Toth S, Borbely G: Alteration of cylindrospermopsin production in sulfate- or phosphate-starved cyanobacterium Aphanizomenon ovalisporum. FEMS Microbiol Lett. 2006, 259: 303-310. 10.1111/j.1574-6968.2006.00282.x.
MacColl R: Cyanobacterial phycobilisomes. J Struct Biol. 1998, 124: 311-334. 10.1006/jsbi.1998.4062.
Allen MM, Smith AJ: Nitrogen chlorosis in blue-green algae. Arch Microbiol. 1969, 69: 114-120.
Elmorjani K, Herdman M: Metabolic control of phycocyanin degradation in the cyanobacterium synechocystis PCC 6803: a glucose effect. J Gen Microbiol. 1987, 133: 1685-1694.
Battchikova N, Vainonen JP, Vorontsova N, Keranen M, Carmel D, Aro E-M: Dynamic changes in the proteome of synechocystis 6803 in response to CO2 limitation revealed by quantitative proteomics. J Proteome Res. 2010, 9: 5896-5912. 10.1021/pr100651w.
Wang H-L, Postier BL, Burnap RL: Alterations in global patterns of gene expression in synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem. 2004, 279: 5739-5751.
Eisenhut M, von Wobeser EA, Jonas L, Schubert H, Ibelings BW, Bauwe H, Matthijs HCP, Hagemann M: Long-term response toward inorganic carbon limitation in wild type and glycolate turnover mutants of the cyanobacterium synechocystis sp. strain PCC 6803. Plant Physiol. 2007, 144: 1946-1959. 10.1104/pp.107.103341.
Collier JL, Grossman AR: Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacteriol. 1992, 174: 4718-4726.
Wegener KM, Singh AK, Jacobs JM, Elvitigala T, Welsh EA, Keren N, Gritsenko MA, Ghosh BK, Campll DG, Smith RD, Pakrasi HB: Global proteomics reveal an atypical strategy for carbon/nitrogen assimilation by a cyanobacterium under diverse environmental peturbations. Mol Cell Proteomics. 2010, 9: 12-
Seidler A: The extrinsic polypeptides of photosystem II. Biochim Biophys Acta. 1996, 1277: 35-60. 10.1016/S0005-2728(96)00102-8.
Shen JR, Inoue Y: Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12-kDa protein, in cyanobacterial photosystem II. Biochemistry. 1993, 32: 1825-1832. 10.1021/bi00058a017.
Inoue-Kashino N, Kashino Y, Satoh K, Terashima I, Pakrasi HB: PsbU provides a stable architecture for the oxygen-evolving system in cyanobacterial photosystem II. Biochemistry. 2005, 44: 12214-12228. 10.1021/bi047539k.
Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB: Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry. 2002, 41: 8004-8012. 10.1021/bi026012+.
Dobakova M, Sobotka R, Tichy M, Komenda J: Psb28 Protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium synechocystis sp. PCC 6803. Plant Physiol. 2009, 149: 1076-1086.
van Thor JJ, Gruters OWM, Matthijs HCP, Hellingwerf KJ: Localization and function of ferredoxin:NADP + reductase bound to the phycobilisomes of Synechocystis. EMBO J. 1999, 18: 4128-4136. 10.1093/emboj/18.15.4128.
Stryer L: Biochemistry. 1995, New York: W.H. Freeman Co, 4
Osanai T, Imamura S, Asayama M, Shirai M, Suzuki I, Murata N, Tanaka K: Nitrogen induction of sugar catabolic gene expression in synechocystis sp. PCC 6803. DNA Res. 2006, 13: 185-195. 10.1093/dnares/dsl010.
Clarke AK: ATP-dependent Clp proteases in photosynthetic organisms- a Cut above the rest!. Ann Bot. 1999, 83: 593-599. 10.1006/anbo.1999.0878.
Clarke A: Variations on a theme: combined molecular chaperone and proteolysis functions in Clp/HSP100 proteins. J Biosci. 1996, 21: 161-177. 10.1007/BF02703106.
Clarke AK, Eriksson M-J: The cyanobacterium Synechococcus sp. PCC 7942 possesses a close homologue to the chloroplast ClpC protein of higher plants. Plant Mol Biol. 1996, 31: 721-730. 10.1007/BF00019460.
Stanne TM, Pojidaeva E, Andersson FI, Clarke AK: Distinctive types of ATP-dependent Clp proteases in cyanobacteria. J Biol Chem. 2007, 282: 14394-14402. 10.1074/jbc.M700275200.
Pandhal J, Wright PC, Biggs CA: A quantitative proteomic analysis of light adaptation in a globally significant marine cyanobacterium Prochlorococcus marinus MED4. J Proteome Res. 2007, 6: 996-1005. 10.1021/pr060460c.
Oliver MJ: Desiccation tolerance in vegetative plant cells. Physiol Plant. 1996, 97: 779-787. 10.1111/j.1399-3054.1996.tb00544.x.
Bannister JV, Bannister WH, Rotilio G: Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit Rev Biochem. 1987, 22: 111-180. 10.3109/10409238709083738.
Singh SC, Sinha RP, Hader D-P: Role of lipids and fatty acids in stress tolerance in cyanobacteria. Acta Protozool. 2002, 41: 297-308.
Bandyopadhyay U, Das D, Banerjee RK: Reactive oxygen species: oxidative damage and pathogenesis. Curr Sci. 1999, 77: 658-666.
Hudson JJ, Taylor WD, Schindler DW: Phosphate concentrations in lakes. Nature. 2000, 406: 54-56. 10.1038/35017531.
Marcus Y, Gurevitz M: Activation of cyanobacterial RuBP-carboxylase/oxygenase is facilitated by inorganic phosphate via two independent mechanisms. Eur J Biochem. 2000, 267: 5995-6003. 10.1046/j.1432-1327.2000.01674.x.
Allen MM: Simple conditions for growth of unicellular blue-green algae on plates. J Phycol. 1968, 4: 1-4.
Axmann IM, Kensche P, Vogel J, Kohl S, Herzel H, Hess WR: Identification of cyanobacterial non-coding RNAs by comparative genome analysis. Genome Biol. 2005, 6: R73-10.1186/gb-2005-6-9-r73.
O’Loughlin SN, Graham RLJ, McMullan G, Ternan NG: A role for carbon catabolite repression in the metabolism of phosphonoacetate by Agromyces fucosus Vs2. FEMS. 2006
Fiske CH, SubbaRow Y: The colourimetric determination of phosphorus. J Biol Chem. 1925, 66: 375-400.
Mukherjee J, Ow SY, Noirel J, Biggs CA: Quantitative protein expression and cell surface characteristics of Escherichia coli MG1655 biofilms. Proteomics. 2011, 11: 339-351. 10.1002/pmic.201000386.
Pham TK, Roy S, Noirel J, Douglas I, Wright PC, Stafford GP: A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia. Proteomics. 2010, 10: 3130-3141. 10.1002/pmic.200900448.