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Proteomic approaches in research of cyanobacterial photosynthesis

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Abstract

Oxygenic photosynthesis in cyanobacteria, algae, and plants is carried out by a fabulous pigment-protein machinery that is amazingly complicated in structure and function. Many different approaches have been undertaken to characterize the most important aspects of photosynthesis, and proteomics has become the essential component in this research. Here we describe various methods which have been used in proteomic research of cyanobacteria, and demonstrate how proteomics is implemented into on-going studies of photosynthesis in cyanobacterial cells.

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Abbreviations

1D:

One-dimensional

2D:

Two-dimensional

AEX:

Anion exchange chromatography

BN:

Blue native

CN:

Clear native

CID:

Collision-induced dissociation

Cyt b 6 f :

The Cyt b 6 f complex

DDA:

Data-dependent acquisition

DIGE:

Difference gel electrophoresis

DM:

Dodecyl β-d-maltoside

ECD:

Electron capture dissociation

emPAI:

Exponentially modified protein abundance index

ESI:

Electrospray ionization

ETD:

Electron transfer dissociation

FDR:

False discovery rate

FDPs or Flvs:

Flavodiiron proteins

GELFrEE:

Gel-eluted liquid fraction entrapment electrophoresis

HCD:

High energy collision dissociation

HPLC:

High-performance liquid chromatography

ICAT:

Isotope-coded affinity tags

IT:

Ion traps

IEF:

Isoelectric focusing

iTRAQ:

Isobaric tags for relative and absolute quantification

m/z :

Mass-to-charge

MALDI:

Matrix-assisted laser desorption/ionization

MRM:

Multiple reaction monitoring

MS:

Mass spectrometry

MS/MS:

Tandem mass spectrometry

MudPIT:

Multidimensional protein identification technology

NDH-1:

NAD(P)H:plastoquinone oxidoreductase type I

NDH-2:

NADH oxidoreductase type II

PAGE:

Polyacrylamide gel electrophoresis

PBS:

Phycobilisome

PM:

Plasma membrane

PQD:

Pulsed Q collision-induced dissociation

PSII:

Photosystem II

PSI:

Photosystem I

PTM:

Post-translational modification

Q:

Quadrupole

RF:

Reverse phase

SCX:

Cation exchange chromatography

SILAC:

Stable isotope labeling with amino acids in cell culture

SRM:

Single reaction monitoring

TM:

Thylakoid membrane

TMT:

Tandem mass tag

TOF:

Time of flight

References

  • Aebersold R, Mann M (2003) Mass sectrometry-based proteomics. Nature 422:198–207

    Article  CAS  PubMed  Google Scholar 

  • Agarwal R, Matros A, Melzer M, Mock H-P, Sainis JK (2010) Heterogeneity in thylakoid membrane proteome of Synechocystis 6803. J Proteomics 73:976–991

    Article  CAS  PubMed  Google Scholar 

  • Aggarwal K, Choe LH, Lee KH (2006) Shotgun proteomics using the iTRAQ isobaric tags. Brief Funct Genomic Proteomic 5:112–120

    Article  CAS  PubMed  Google Scholar 

  • Agrawal C, Sen S, Singh S, Rai S, Singh PK, Singh KV, Rai LC (2014) Comparative proteomics reveals association of early accumulated proteins in conferring butachlor tolerance in three N2-fixing Anabaena spp. J Proteomics 96:271–290

    Article  CAS  PubMed  Google Scholar 

  • Ahlf DR, Thomas PM, Kelleher NL (2013) Developing top down proteomics to maximize proteome and sequence coverage from cells and tissues. Curr Opin Chem Biol 17:787–794

    Article  CAS  PubMed  Google Scholar 

  • Allahverdiyeva Y, Ermakova M, Eisenhut M, Zhang P, Richaud P, Hagemann M, Cournac L, Aro EM (2011) Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. J Biol Chem 286:24007–24014

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro EM (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light in aquatic environments. Proc Natl Acad Sci USA 110:4111–4116

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Allen JF, Sanders CE, Holmes NG (1985) Correlation of membrane protein phosphorylation with excitation energy distribution in the cyanobacterium Synechococcus 6301. FEBS Lett 193:271–275

    Article  CAS  Google Scholar 

  • Anderson DC, Campbell EL, Meeks JC (2006) A Soluble 3D LC/MS/MS proteome of the filamentous cyanobacterium Nostoc punctiforme. J Proteome Res 5:3096–3104

  • Ansong C, Wu S, Meng D, Liu X, Brewer HM, Deatherage Kaiser BL, Nakayasu ES, Cort JR, Pevzner P, Smith RD (2013) Top-down proteomics reveals a unique protein S-thiolation switch in Salmonella typhimurium in response to infection-like conditions. Proc Natl Acad Sci USA 110:10153–10158

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aro EM, Suorsa M, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356

    Article  CAS  PubMed  Google Scholar 

  • Aryal UK, Stöckel J, Welsh EA, Gritsenko MA, Nicora CD, Koppenaal DW, Smith RD, Pakrasi HB, Jacobs JM (2012) Dynamic Proteome Analysis of Cyanothece sp. ATCC 51142 under constant light. J Proteome Res 11:609–619

    Article  CAS  PubMed  Google Scholar 

  • Bald D, Kruip J, Rögner M (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosynth Res 49:103–118

    Article  CAS  PubMed  Google Scholar 

  • Baldwin MA (2004) Protein identification by mass spectrometry: issues to be considered. Mol Cell Proteomics 3:1–9

    Article  CAS  PubMed  Google Scholar 

  • Baniulis D, Yamashita E, Whitelegge JP, Zatsman AI, Hendrich MP, Hasan SS, Ryan CM, Cramer AW (2009) Structure-function, stability, and chemical modification of the cyanobacterial cytochrome b 6 f complex from Nostoc sp. PCC 7120. J Biol Chem 284:9861–9869

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bantscheff M, Schirle M, Sweetman G, Rick J, Kuster B (2007) Quantitative mass spectrometry in proteomics: a critical review. Anal Bioanal Chem 389:1017–1031

    Article  CAS  PubMed  Google Scholar 

  • Barbato R, Polverino de Laureto P, Riconi F, de Martini E, Giacometti GM (1995) Pigment-protein complexes from the photosynthetic membrane of the cyanobacterium Synechocystis sp. PCC 6803. Eur J Biochem 234:459–465

    Article  CAS  PubMed  Google Scholar 

  • Barrios-Llerena ME, Chong PK, Gan CS, Snijders APL, Reardon KF, Wright PC (2006) Shotgun proteomics of cyanobacteria-applications of experimental and data-mining techniques. Brief Funct Genomics Proteomics 5:121–132

    Article  CAS  Google Scholar 

  • Barrios-Llerena ME, Reardon KF, Wright PC (2007) 2-DE proteomic analysis of the model cyanobacterium Anabaena variabilis. Electrophoresis 28:1624–1632

    Article  CAS  PubMed  Google Scholar 

  • Battchikova N, Aro EM (2007) Cyanobacterial NDH-1 complexes: multiplicity in function and subunit composition. Physiol Plant 131:22–32

    Article  CAS  PubMed  Google Scholar 

  • Battchikova N, Zhang PP, Rudd S, Aro EM (2005) Identification of NdhL and Ssl1690 (NdhO) in NDH-1L and NDH-1M complexes of Synechocystis sp. PCC 6803. J Biol Chem 280:2587–2595

    Article  CAS  PubMed  Google Scholar 

  • Battchikova N, Vainonen JP, Vorontsova N, Keranen M, Carmel D, Aro EM (2010) Dynamic changes in the proteome of Synechocystis 6803 in response to CO2 limitation revealed by quantitative proteomics. J Proteome Res 9:5896–5912

    Article  CAS  PubMed  Google Scholar 

  • Battchikova N, Aro EM, Nixon PJ (2011a) Structure and physiological function of NDH-1 complexes in cyanobacteria. In: Peschek GA, Obinger C, Renger G (eds) Bioenergetic processes of cyanobacteria: from evolutionary singularity to ecological diversity. Heidelberg, Springer Verlag, Berlin, New York, pp 445–467

    Chapter  Google Scholar 

  • Battchikova N, Eisenhut M, Aro EM (2011b) Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim Biophys Acta 1807:935–944

    Article  CAS  PubMed  Google Scholar 

  • Battchikova N, Wei L, Du L, Bersanini L, Aro EM, Ma W (2011c) Identification of novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH:plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC 6803. J Biol Chem 286:36992–37001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berla BM, Saha R, Immethun CM, Maranas CD, Moon TS, Pakrasi HB (2013) Synthetic biology of cyanobacteria: unique challenges and opportunities. Front Microbiol 4:246

    Article  PubMed Central  PubMed  Google Scholar 

  • Berman-Frank I, Lundgren P, Chen YB, Kupper H (2001) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294:1534–1537

    Article  CAS  PubMed  Google Scholar 

  • Bersanini L, Battchikova N, Jokel M, ur Rehman A, Vass I, Allahverdiyeva Y, Aro EM (2013) Flv2/Flv4 related photoprotective mechanism dissipates excitation pressure of photosystem II in co-operation with phycobilisomes in cyanobacteria. Plant Physiol 164:805–818

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bertone P, Snyder M (2005) Prospects and challenges in proteomics. Plant Physiol 138:560–562

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cardona T, Battchikova N, Agervald A, Zhang P, Nagel E, Aro EM, Styring S, Lindblad P, Magnuson A (2007) Isolation and characterization of thylakoid membranes from the filamentous cyanobacterium Nostoc punctiforme. Physiol Plant 131:622–634

    Article  CAS  PubMed  Google Scholar 

  • Cardona T, Battchikova N, Zhang P, Stensjö K, Aro EM, Lindblad P, Magnuson A (2009) Electron transfer protein complexes in the thylakoid membranes of heterocysts from the cyanobacterium Nostoc punctiforme. Biochim Biophys Acta 1787:252–263

    Article  CAS  PubMed  Google Scholar 

  • Castielli O, De la Cerda B, Navarro JA, Hervás M, De la Rosa MA (2009) Proteomic analyses of the response of cyanobacteria to different stress conditions. FEBS Lett 583:1753–1758

    Article  CAS  PubMed  Google Scholar 

  • Chen EI, Cociorva D, Norris JL, Yates JR III (2007) Optimization of mass spectrometry compatible surfactants for shotgun proteomics. J Proteome Res 6:2529–2538

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chevalier F (2010) Highlights on the capacities of “Gel-based”proteomics. Proteome Sci 8:23

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chitnis VP, Chitnis PR (1993) PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336:330–334

    Article  CAS  PubMed  Google Scholar 

  • Choi H, Nesvizhskii AI (2007) False discovery rates and related statistical concepts in mass spectrometry-based proteomics. J Proteome Res 7:47–50

    Article  PubMed  CAS  Google Scholar 

  • Choi H, Fermin D, Nesvizhskii AI (2008) Significance analysis of spectral count data in label-free shotgun proteomics. Mol Cell Proteomics 7:2373–2385

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cox AD, Saito MA (2013) Proteomic responses of oceanic Synechococcus WH8102 to phosphate and zinc scarcity and cadmium additions. Front Microbiol 4:387

    PubMed Central  PubMed  Google Scholar 

  • D’Agostino PM, Song X, Neilan BA, Moffitt MC (2014) Comparative proteomics reveals that a saxitoxin-producing and a nontoxic strain of Anabaena circinalis are two different ecotypes. J Proteome Res 13:1474–1484

    Article  PubMed  CAS  Google Scholar 

  • de Groot MJ, Daran-Lapujade P, van Breukelen B, Knijnenburg TA, de Hulster EAF, Reinders MJT, Pronk JT, Heck AJR, Slijper M (2007) Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals post-transcriptional regulation of key cellular processes. Microbiology 153:3864–3878

    Article  PubMed  CAS  Google Scholar 

  • Deschoenmaeker F, Facchini R, Leroy B, Badri H, Zhang CC, Wattiez R (2014) Proteomic and cellular views of Arthrospira sp. PCC 8005 adaptation to nitrogen depletion. Microbiology 160:1224–1236

    Article  CAS  PubMed  Google Scholar 

  • Diner BA, Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53:551–580

    Article  CAS  PubMed  Google Scholar 

  • Dühring U, Irrgang K-D, Lünser K, Kehr J, Wilde A (2006) Analysis of photosynthetic complexes from a cyanobacterial ycf37 mutant. Biochim Biophys Acta 1757:3–11

    Article  PubMed  CAS  Google Scholar 

  • Eberhard S, Finazzi G, Wollman F-A (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    Article  CAS  PubMed  Google Scholar 

  • Eisenhut M, Georg J, Klähn S, Sakurai I, Mustila H, Zhang P, Hess WR, Aro EM (2012) The antisense RNA As1_flv4 in the Cyanobacterium Synechocystis sp. PCC 6803 prevents premature expression of the flv4-2 operon upon shift in inorganic carbon supply. J Biol Chem 40:33153–33162

    Article  CAS  Google Scholar 

  • Ekman M, Ow SY, Holmqvist M, Zhang X, van Wagenen J, Wright PC, Stensjö K (2011) Metabolic adaptations in a H2 producing heterocyst-forming cyanobacterium: potentials and implications for biological engineering. J Proteome Res 10:1772–1784

    Article  CAS  PubMed  Google Scholar 

  • Elliott MH, Smith DS, Parker CE, Borchers C (2009) Current trends in quantitative proteomics. J Mass Spectrom 44:1637–1660

    CAS  PubMed  Google Scholar 

  • Elschenbroich S, Ignatchenko V, Sharma P, Schmitt-Ulms G, Gramolini AO, Kislinger T (2009) Peptide separations by on-line MudPIT compared to isoelectric focusing in an off-gel format: application to a membrane-enriched fraction from C2C12 mouse skeletal muscle cells. J Proteome Res 8:4860–4869

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ermakova M, Battchikova N, Allahverdiyeva Y, Aro EM (2013) Novel heterocyst-specific flavodiiron proteins in Anabaena sp. PCC 7120. FEBS Lett 587:82–87

    Article  CAS  PubMed  Google Scholar 

  • Ermakova M, Battchikovaa N, Richaud P, Leino H, Kosourov S, Isojärvi J, Peltier G, Florese E, Courna F, Allahverdiyevaa Y, Aro E-M (2014) Heterocyst-specific flavodiiron protein Flv3B enables oxic diazotrophic growth of the filamentous cyanobacterium Anabaena sp. PCC 7120. Proc Natl Acad Sci USA 111:11205–11210

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Evans C, Noirel J, Ow SY, Salim M, Pereira-Medrano AG, Couto N, Pandhal J, Smith D, Pham TK, Karunakaran E, Zou X, Biggs CA, Wright PC (2012) An insight into iTRAQ: where do we stand now? Anal Bioanal Chem 404:1011–1027

    Article  CAS  PubMed  Google Scholar 

  • Fagerlund RD, Eaton-Rye JJ (2011) The lipoproteins of cyanobacterial photosystem II. J Photochem Photobiol B104:191–203

    Article  CAS  Google Scholar 

  • Fischer F, Poetsch A (2006) Protein cleavage strategies for an improved analysis of the membrane proteome. Proteome Sci 4:2

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fournier ML, Gilmore JM, Martin-Brown SA, Washburn MP (2007) Multidimensional separations-based shotgun proteomics. Chem Rev 107:3654–3686

    Article  CAS  PubMed  Google Scholar 

  • Fulda S, Huang F, Nilsson F, Hagemann M, Norling B (2000) Proteomics of Synechocystis sp. strain PCC 6803. Identification of periplasmic proteins in cells grown at low and high salt concentrations. Eur J Biochem 267:5900–5907

    Article  CAS  PubMed  Google Scholar 

  • Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B, Hagemann M (2006) Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics 6:2733–2745

    Article  CAS  PubMed  Google Scholar 

  • Fuszard MA, Wright PC, Biggs CA (2012) Comparative quantitative proteomics of Prochlorococcus ecotypes to a decrease in environmental phosphate concentrations. Aquat Biosyst 8:7

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fuszard MA, Ow SY, Gan CS, Noirel J, Ternan NG, McMullan G, Biggs CA, Reardon KF, Wright PC (2013) The quantitative proteomic response of Synechocystis sp. PCC6803 to phosphate acclimation. Aquat Biosyst 9:5

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gan CS, Reardon KF, Wright PC (2005) Comparison of protein and peptide prefractionation methods for the shotgun proteomic analysis of Synechocystis sp. PCC 6803. Proteomics 5:2468–2478

    Article  CAS  PubMed  Google Scholar 

  • Georg J, Voss B, Scholz I, Mitschke J, Wilde A, Hess WR (2009) Evidence for a major role of antisense RNAs in cyanobacterial gene regulation. Mol Syst Biol 5:305

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gerber SA, Rush J, Stemman O, Kirschner MW, Gygi SP (2003) Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc Natl Acad Sci USA 100:6940–6945

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gevaert K, Impens F, Ghesquière B, van Damme P, Lambrechts A, Vandekerckhove J (2008) Stable isotopic labeling in proteomics. Proteomics 8:4873–4885

    Article  CAS  PubMed  Google Scholar 

  • Ghaemmaghami S, Huh WK, Bowe K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425:737–741

    Article  CAS  PubMed  Google Scholar 

  • Gilmore JM, Washburn MP (2010) Advances in shotgun proteomics and the analysis of membrane proteomes. J Proteomics 73:2078–2091

    Article  CAS  PubMed  Google Scholar 

  • Gouw JW, Krijgsveld J, Heck AJ (2010) Quantitative proteomics by metabolic labeling of model organisms. Mol Cell Proteomics 9:11–24

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Griffin NM, Schnitzer JE (2011) Overcoming key technological challenges in using mass spectrometry for mapping cell surfaces in tissues. Mol Cell Proteomics 10:R110–R000935

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Grouneva I, Gollan PJ, Kangasjärvi S, Suorsa M, Tikkanen M, Aro EM (2013) Phylogenetic viewpoints on regulation of light harvesting and electron transport in eukaryotic photosynthetic organisms. Planta 237:399–412

    Article  CAS  PubMed  Google Scholar 

  • Grün D, Kirchner M, Thierfelder N, Stoeckius M, Selbach M, Rajewsky N (2014) Conservation of mRNA and protein expression during development of C. elegans. Cell Rep 6:565–577

    Article  PubMed  CAS  Google Scholar 

  • Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17:994–999

    Article  CAS  PubMed  Google Scholar 

  • Helbig AO, Heck AJR, Slijper M (2010) Exploring the membrane proteome—Challenges and analytical strategies. J Proteomics 73:868–878

    Article  CAS  PubMed  Google Scholar 

  • Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A (2003) Genes encoding A-type flavodiiron proteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235

    Article  CAS  PubMed  Google Scholar 

  • Herranen M, Battchikova N, Zhang P, Graf A, Sirpio S, Paakkarinen V, Aro EM (2004) Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol 134:470–481

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hongsthong A, Sirijuntarut M, Prommeenate P, Thammathorn S, Bunnag B, Cheevadhanarak S, Tanticharoen M (2007) Revealing differentially expressed proteins in two morphological forms of Spirulina platensis by proteomic analysis. Mol Biotechnol 36:123–130

    Article  CAS  PubMed  Google Scholar 

  • Hongsthong A, Sirijuntarut M, Prommeenate P, Lertladaluck K, Porkaew K, Cheevadhanarak S, Tanticharoen M (2008) Proteome analysis at the subcellular level of the cyanobacterium Spirulina platensis in response to low temperature stress conditions. FEMS Microbiol Lett 288:92–101

    Article  CAS  PubMed  Google Scholar 

  • Hongsthong A, Sirijuntarut M, Yutthanasirikul R, Senachak J, Kurdrid P, Cheevadhanarak S, Tanticharoen M (2009) Subcellular proteomic characterization of the high-temperature stress. Proteome Sci 7:1–19

    Article  CAS  Google Scholar 

  • Huang F, Parmryd I, Nilsson F, Persson AL, Pakrasi HB, Andersson B, Norling B (2002) Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins. Mol Cell Proteomics 1:956–966

    Article  CAS  PubMed  Google Scholar 

  • Huang F, Hedman E, Funk C, Kieselbach T, Schroder WP, Norling B (2004) Isolation of outer membrane of Synechocystis sp. PCC 6803 and its proteomic characterization. Mol Cell Proteomics 3:586–595

    Article  CAS  PubMed  Google Scholar 

  • Huang F, Fulda S, Hagemann M, Norling B (2006) Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 6:910–920

    Article  CAS  PubMed  Google Scholar 

  • Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M (2005) Exponentially modified protein abundance index (empai) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4:1265–1272

    Article  CAS  PubMed  Google Scholar 

  • Ivleva NB, Shestakov SV, Pakrasi HB (2000) The carboxyl-terminal extension of the precursor D1 Protein of Photosystem II is required for optimal photosynthetic performance of the Cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 124:1403–1412

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Järvi S, Suorsa M, Paakkarinen V, Aro EM (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem J 439:207–214

    Article  PubMed  CAS  Google Scholar 

  • Johnson LN (2009) The regulation of protein phosphorylation. Biochem Soc Trans 37:627–641

    Article  CAS  PubMed  Google Scholar 

  • Julka S, Regnier F (2004) Quantification in proteomics through stable isotope coding: a review. J Proteome Res 3:350–363

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. Strain PCC6803. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    Article  CAS  PubMed  Google Scholar 

  • Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB (2002) Proteomic analysis of a highly active Photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41:8004–8012

    Article  CAS  PubMed  Google Scholar 

  • Khouri GA, Baliban RC, Floudas CA (2011) Proteome-wide post-translational modification statistics: frequency analysis and curation of the swiss-prot database. Sci Rep 1:90

    Google Scholar 

  • Kim YH, Parka KH, Kim S-Y, Ji ES, Kim JY, Lee SK, Yoo JS, Kim HS, Park YM (2011) Identification of trimethylation at C-terminal lysine of pilin in the cyanobacterium Synechocystis PCC 6803. Biochem Biophys Res Commun 404:587–592

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick DS, Gerber S, Gygi SP (2005) The absolute quantification strategy: a general procedure for the quantification of proteins and post-translational modifications. Methods 35:265–273

    Article  CAS  PubMed  Google Scholar 

  • Klinkert B, Ossenbühl F, Sikorski M, Berry S, Eichacker L, Nickelsen J (2004) PratA, a periplasmic tetratricopeptide repeat protein involved in biogenesis of photosystem II in Synechocystis sp. PCC 6803. J Biol Chem 279:44639–44644

    Article  CAS  PubMed  Google Scholar 

  • Klotz AV, Glazer AN (1987) γ-N-methylasparagine in phycobiliproteins. Occurrence, location, and biosynthesis. J Biol Chem 262:17350–17355

    CAS  PubMed  Google Scholar 

  • Komenda J, Lupίnkova L, Kopeckÿ J (2002) Absence of the psbH gene product destabilizes photosystem II complex and bicarbonate binding on its acceptor side in Synechocystis PCC 6803. Eur J Biochem 269:610–619

    Article  CAS  PubMed  Google Scholar 

  • Komenda J, Sobotka R, Nixon PJ (2012) Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol 15:245–251

    Article  CAS  PubMed  Google Scholar 

  • Kubota H, Sakurai I, Katayama K, Mizusawa N, Ohashi S, Kobayashi M, Zhang P, Aro EM, Wada H (2010) Purification and characterization of photosystem I complex from Synechocystis sp. PCC 6803 by expressing histidine-tagged subunits. Biochim Biophys Acta 1797:98–105

    Article  CAS  PubMed  Google Scholar 

  • Kumar K, Mella-Herrera RA, Golden JW (2009) Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol 2:a000315

    Google Scholar 

  • Kurdrid P, Senachak J, Sirijuntarut M, Yutthanasirikul R, Phuengcharoen P, Jeamton W, Roytrakul S, Cheevadhanarak S, Hongsthong A (2011) Comparative analysis of the Spirulina platensis subcellular proteome in response to low- and high-temperature stresses: uncovering cross-talk of signaling components. Proteome Sci 9:39

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kurian D, Jansén T, Mäenpää P (2006a) Proteomic analysis of heterotrophy in Synechocystis sp. PCC 6803. Proteomics 6:1483–1494

    Article  CAS  PubMed  Google Scholar 

  • Kurian D, Phadwai K, Mäenpää P (2006b) Proteomic characterization of acid response in Synechocystis sp. PCC 6803. Proteomics 6:3614–3624

    Article  CAS  PubMed  Google Scholar 

  • Kwon J-H, Oh J, Park C, Cho K, Kim SI, Kim S, Lee S, Bhak J, Norling B, Choi JS (2010) Systematic cyanobacterial membrane proteome analysis by combining acid hydrolysis and digestive enzymes with nano-liquid chromatography-Fourier transform mass spectrometry. J Chromatogr A 1217:285–293

    Article  CAS  PubMed  Google Scholar 

  • Kwon J-H, Bernát G, Wagner H, Rögner M, Rexroth S (2013) Reduced light-harvesting antenna: consequences on cyanobacterial metabolism and photosynthetic productivity. Algal Res 2:188–195

    Article  Google Scholar 

  • Ladig R, Sommer MS, Hahn A, Leisegang MS, Papasotiriou DG, Ibrahim M, Elkehal R, Karas M, Zickermann V, Gutensohn M, Brandt U, Klösgen RB, Schleiff E (2011) A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes. Plant J 67:181–194

    Article  CAS  PubMed  Google Scholar 

  • Lange V, Picotti P, Domon B, Aebersold R (2008) Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 4:222–2008

    Article  PubMed Central  PubMed  Google Scholar 

  • Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jørgensen TJD (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxidemicrocolumns. Mol Cell Proteomics 4:873–886

    Article  CAS  PubMed  Google Scholar 

  • Li T, Yang HM, Cui SX, Suzuki I, Zhang LF, Li L, Bo TT, Wang J, Murata N, Huang F (2012) Proteomic study of the impact of Hik33 mutation in Synechocystis sp. PCC 6803 under normal and salt stress conditions. J Proteome Res 11:502–514

    Article  CAS  PubMed  Google Scholar 

  • Liang W, Zhou Y, Wang L, Xiangrong Y, Zhang Y, Cheng C-L, Chen W (2012) Ultrastructural, physiological and proteomic analysis of Nostoc flagelliforme in response to dehydration and rehydration. J Proteomics 75:5604–5627

    Article  CAS  PubMed  Google Scholar 

  • Liang W, Wang L, Zhang Y, Lei X, Yang J, You X, Cheng C-L, Zhou Y, Wei C (2013) Comparative proteomic and physiological analysis of diurnal changes in Nostoc flagelliforme. J Appl Phycol 25:1709–1721

    Article  CAS  Google Scholar 

  • Liberton M, Berg RH, Heuser J, Roth R, Pakrasi HB (2006) Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Protoplasma 227:129–138

    Article  PubMed  Google Scholar 

  • Liberton M, Austin JR, Berg RH, Pakrasi HB (2011) Unique thylakoid membrane architecture of a unicellular N2-fixing cyanobacterium revealed by electron tomography. Plant Physiol 155:1656–1666

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu H, Sadygov RG, Yates JR (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76:4193–4201

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Chen L, Wang J, Qiao J, Zhang W (2012) Proteomic analysis reveals resistance mechanism against biofuel hexane in Synechocystis sp. PCC 6803. Biotechnol Biofuels 5:68

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Macek B, Mijakovic I (2011) Site-specific analysis of bacterial phosphoproteomes. Proteomics 11:3002–3011

    Article  CAS  PubMed  Google Scholar 

  • Magdeldin S, Enany S, Yoshida Y, Xu B, Zhang Y, Zureena Z, Yamamoto T (2014) Basics and recent advances of two dimensional polyacrylamide gel electrophoresis. Clin Proteomics 11:16

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mangels D, Kruip J, Berry S, Rögner M, Boekema EJ, Koenig F (2002) Photosystem I from the unusual cyanobacterium Gloeobacter violaceus. Photosynth Res 72:307–319

    Article  CAS  PubMed  Google Scholar 

  • Mann NH (1994) Protein phosphorylation in cyanobacteria. Microbiology 140:3207–3215

    Article  CAS  PubMed  Google Scholar 

  • Marcotte EM (2007) How do shotgun proteomics algorithms identify proteins? Nat Biotechnol 25:755–757

    Article  CAS  PubMed  Google Scholar 

  • Matzke MM, Brown JN, Gritsenko MA, Metz TO, Pounds JG, Rodland KD, Shukla AK, Smith RD, Waters KM, McDermott JE, Webb-Robertson BJ (2013) A comparative analysis of computational approaches to relative protein quantification using peptide peak intensities in label-free LC–MS proteomics experiments. Proteomics 13:493–503

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Michalski A, Damoc E, Hauschild JP, Lange O, Wieghaus A, Makarov A, Nagaraj N, Cox J, Mann M, Horning S (2011) Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Mol Cell Proteomics 10:M111–M011015

    Article  PubMed Central  PubMed  Google Scholar 

  • Mikkat S, Fulda S, Hagemann M (2014) A 2D gel electrophoresis-based snapshot of the phosphoproteome in the cyanobacterium Synechocystis sp. strain PCC 6803. Microbiology. doi:10.1099/mic.0.074443-0

  • M-k Yang, Z-x Qiao, W-y Zhang, Xiong Q, Zhang J, Li T, Ge F, Zhao J (2013) Global phosphoproteomic analysis reveals diverse functions of serine/threonine/tyrosine phosphorylation in the model cyanobacterium Synechococcus sp. strain PCC 7002. J Proteome Res 12:1909–1923

    Article  CAS  Google Scholar 

  • Mukhopadhyay A, Kennelly PJ (2011) A low molecular weight protein tyrosine 580 phosphatase from Synechocystis sp. strain PCC 6803: enzymatic characterization and 581 identification of its potential substrates. J Biochem 149:551–556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mullineaux CW (2014) Electron transport and light-harvesting switches in cyanobacteria. Front Plant Sci 5:7

    Article  PubMed Central  PubMed  Google Scholar 

  • Nakamura T, Oda Y (2007) Mass spectrometry-based quantitative proteomics. Biotechnol Gen Eng Rev 24:147–164

    Article  CAS  Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, Tsuchiya T, Sasamoto S, Watanabe A, Kawashima K, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Takeuchi C, Yamada M, Tabata S (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10:137–145

    Article  CAS  PubMed  Google Scholar 

  • Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5:971–982

    Article  CAS  PubMed  Google Scholar 

  • Nickelsen J, Rengstl B, Stengel A, Schottkowski M, Soll J, Ankele E (2011) Biogenesis of the cyanobacterial thylakoid membrane system: an update. FEMS Microbiol Lett 315:1–5

    Article  CAS  PubMed  Google Scholar 

  • Nierzwicki-Bauer SA, Balkwill DL, Stevens SE Jr (1983) Three-dimensional ultrastructure of a unicellular cyanobacterium. J Cell Biol 97:713–722

    Article  CAS  PubMed  Google Scholar 

  • Norling B, Zak E, Andersson B, Pakrasi H (1998) 2D-isolation of pure plasma and thylakoid membranes from the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 436:189–192

    Article  CAS  PubMed  Google Scholar 

  • Nowaczyk MM, Hebeler R, Schlodder E, Meyer HE, Warscheid B, Rögner M (2006) Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell 18:3121–3131

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nowaczyk MM, Wulfhorst H, Ryan CM, Souda P, Zhang H, Cramer WA, Whitelegge JP (2011) NdhP and NdhQ: two novel small subunits of the cyanobacterial NDH-1 complex. Biochemistry 50:1121–1124

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ogawa T, Mi H (2007) Cyanobacterial NADPH dehydrogenase complexes. Photosynth Res 93:69–77

    Article  CAS  PubMed  Google Scholar 

  • Old WM, Meyer-Arendt K, Aveline-Wolf L, Pierce KG, Mendoza A, Sevinsky JR, Resing KA, Ahn NG (2005) Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol Cell Proteomics 4:1487–1502

    Article  CAS  PubMed  Google Scholar 

  • Olsen JV, Blagoev B, Florian G, Macek B, Kumar C, Peter M, Mann M (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:635–648

    Article  CAS  PubMed  Google Scholar 

  • Olsen JV, Schwartz JC, Griep-Raming J, Nielsen ML, Damoc E, Denisov E, Lange O, Remes P, Taylor D, Splendore M, Wouters ER, Senko M, Makarov A, Mann M, Horning S (2009) A dual pressure linear ion trap Orbitrap instrument with very high sequencing speed. Mol Cell Proteomics 8:2759–2769

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Omata T, Murata N (1983) Isolation and characterization of the cytoplasmic membranes from the blue-green alga (cyanobacterium) Anacystis nidulans. Plant Cell Physiol 24:1101–1112

    CAS  Google Scholar 

  • Ong SE, Mann M (2005) Mass spectrometry-based proteomics turns quantitative. Nature Chem Biol 1:252–262

    Article  CAS  Google Scholar 

  • Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1:376–386

    Article  CAS  PubMed  Google Scholar 

  • Ow SY, Cardona T, Taton A, Magnuson A, Lindblad P, Stensjö K, Wright PC (2008) Quantitative shotgun proteomics of enriched heterocysts from Nostoc sp. PCC 7120 using 8-plex isobaric peptide tags. J Proteome Res 7:1615–1628

    Article  CAS  PubMed  Google Scholar 

  • Ow SY, Noirel J, Cardona T, Taton A, Lindblad P, Stensjö K, Wright PC (2009) Quantitative overview of N2 fixation in Nostoc punctiforme ATCC 29133 through cellular enrichments and iTRAQ shotgun proteomics. J Proteome Res 8:187–198

    Article  CAS  PubMed  Google Scholar 

  • Pandey S, Rai R, Rai LC (2012) Proteomics combines morphological, physiological and biochemical attributes to unravel the survival strategy of Anabaena sp. PCC7120 under arsenic stress. J Proteomics 75:921–937

    Article  CAS  PubMed  Google Scholar 

  • Pandhal J, Wright PC, Biggs CA (2007) A quantitative proteomic analysis of light adaptation in a globally significant marine cyanobacterium Prochlorococcus marinus MED4. J Proteome Res 6:996–1005

    Article  CAS  PubMed  Google Scholar 

  • Pereira SB, Ow SY, Barrios-Llerena ME, Wright PC, Moradas-Ferreira P, Tamagnini P (2011) iTRAQ-based quantitative proteomic analysis of Gloeothece sp. PCC 6909: comparison with its sheathless mutant and adaptations to nitrate deficiency and sulfur limitation. J Proteomics 75:270–283

    Article  CAS  PubMed  Google Scholar 

  • Perkins DN, Pappin DJ, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551–3567

    Article  CAS  PubMed  Google Scholar 

  • Picotti P, Aebersold R (2012) Selected reaction monitoring–based proteomics: workflows, potential, pitfalls and future directions. Nat Methods 9:555–566

    Article  CAS  PubMed  Google Scholar 

  • Pisareva T, Shumskaya M, Maddalo G, Ilag L, Norling B (2007) Proteomics of Synechocystis sp. PCC 6803. Identification of novel integral plasma membrane proteins. FEBS Lett 274:791–804

    Article  CAS  Google Scholar 

  • Pisareva T, Kwon J, Oh J, Kim S, Ge C, Wieslander Å, Choi J-S, Norling B (2011) Model for membrane organization and protein sorting in the cyanobacterium Synechocystis sp. PCC 6803 inferred from proteomics and multivariate sequence analyses. J Proteome Res 10:3617–3631

    Article  CAS  PubMed  Google Scholar 

  • Piven I, Ajlani G, Sokolenko A (2005) Phycobilisome linker proteins are phosphorylated in Synechocystis sp. PCC 6803. J Biol Chem 280:21667–21672

    Article  CAS  PubMed  Google Scholar 

  • Prommeenate P, Lennon AM, Markert C, Hippler M, Nixon PJ (2004) Subunit composition of NDH-1 complexes of Synechocystis sp PCC 6803: identification of two new ndh gene products with nuclear-encoded homologues in the chloroplast Ndh complex. J Biol Chem 279:28165–28173

    Article  CAS  PubMed  Google Scholar 

  • Qiao J, Wang J, Chen L, Tian X, Huang S, Ren X, Zhang W (2012) Quantitative iTRAQ LC–MS/MS proteomics reveals metabolic responses to biofuel ethanol in cyanobacterial Synechocystis sp. PCC 6803. J Proteome Res 11:5286–5300

    Article  CAS  PubMed  Google Scholar 

  • Qiao J, Huang S, Te R, Wang J, Chen L, Zhang W (2013) Integrated proteomic and transcriptomic analysis reveals novel genes and regulatory mechanisms involved in salt stress responses in Synechocystis sp. PCC 6803. Appl Microbiol Biotechnol 97:8253–8264

    Article  CAS  PubMed  Google Scholar 

  • Quan L, Liu M (2013) CID, ETD and HCD fragmentation to study protein. Post-translational modifications. Mod Chem Appl 1:e102

    Google Scholar 

  • Rabilloud T, Lelong C (2011) Two-dimensional gel electrophoresis in proteomics: a tutorial. J Proteomics 74:1829–1841

    Article  CAS  PubMed  Google Scholar 

  • Rabilloud T, Chevallet M, Luche S, Lelong C (2010) Two-dimensional gel electrophoresis in proteomics: past, present and future. J Proteomics 7:2064–2077

    Article  CAS  Google Scholar 

  • Race HL, Gounaris K (1993) Identification of the psbH gene product as a 6 kDa phosphoprotein in the cyanobacterium Synechocystis 6803. FEBS Lett 323:35–39

    Article  CAS  PubMed  Google Scholar 

  • Rai S, Singh S, Shrivastava AK, Rai LC (2013) Salt and UV-B induced changes in Anabaena PCC 7120: physiological, proteomic and bioinformatic perspectives. Photosynth Res 118:105–114

    Article  CAS  PubMed  Google Scholar 

  • Rai S, Agrawal C, Shrivastava AK, Singh PK, Rai LC (2014) Comparative proteomics unveils cross species variations in Anabaena under salt stress. J Proteomics 98:254–270

    Article  CAS  PubMed  Google Scholar 

  • Ramanan R, Vinayagamoorthy N, Sivanesan SD, Kannan K, Chakrabarti T (2012) Influence of CO2 concentration on carbon concentrating mechanisms in cyanobacteria and green algae: a proteomic approach. Algae 27:295–301

    Article  CAS  Google Scholar 

  • Ran L, Huang F, Ekman M, Klint J, Bergman B (2007) Proteomic analyses of the photoauto and diazotrophically grown cyanobacterium Nostoc sp. PCC 73102. Microbiology 153:608–618

    Article  CAS  PubMed  Google Scholar 

  • Rexroth S, Mullineaux CW, Ellinger D, Sendtko E, Rögner M, Koenig F (2011) The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains. Plant Cell 23:2379–2390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Riviere ME, Arrio B, Steffan I, Molitor V, Kuntner O, Peschek GA (1990) Changes of some physical properties of isolated and purified plasma and thylakoid membrane vesicles from the freshwater cyanobacterium Synechococcus 6301 (Anacystis nidulans) during adaptation to salinity. Arch Biochem Biophys 280:159–166

    Article  CAS  PubMed  Google Scholar 

  • Rögner M, Dekker JP, Boekema EJ, Witt HT (1987) Size, shape and mass of the oxygen-evolving Photosystem II complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 219:207–211

    Article  Google Scholar 

  • Rögner M, Muhlenhoff U, Boekema EJ, Witt HT (1990) Mono-, di- and trimeric PSI reaction center complexes isolated from the thermophilic cyanobacterium Synechococcus sp. Size, shape and activity. Biochim Biophys Acta 101:415–424

    Article  Google Scholar 

  • Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3:1154–1169

    Article  CAS  PubMed  Google Scholar 

  • Rowland JG, Simon WJ, Nishiyama Y, Slabas AR (2010) Differential proteomic analysis using iTRAQ reveals changes in thylakoids associated with photosystem II-acquired thermotolerance in Synechocystis sp. PCC 6803. Proteomics 10:1917–1929

    Article  CAS  PubMed  Google Scholar 

  • Rowland JG, Simon WJ, Prakash JSS, Slabas AR (2011) Proteomics reveals a role for the RNA helicase crhrr in the modulation of multiple metabolic pathways during cold acclimation of Synechocystis sp. PCC6803. J Proteome Res 10:3674–3689

    Article  CAS  PubMed  Google Scholar 

  • Sanders CE, Melis A, Allen JF (1989) In vivo phosphorylation of proteins in the cyanobacterium Synechococcus 6301 after chromatic acclimation to photosystem I or photosystem II light. Biochim Biophys Acta 976:168–172

    Article  CAS  Google Scholar 

  • Sandh G, Ran L, Xu L, Sundqvist G, Bulone V, Bergman B (2011) Comparative proteomic profiles of the marine cyanobacterium Trichodesmium erythraeum IMS101 under different nitrogen regimes. Proteomics 11:406–419

    Article  CAS  PubMed  Google Scholar 

  • Santoni V, Molloy M, Rabilloud T (2000) Membrane proteins and proteomics: un amour impossible. Electrophoresis 21:1054–1070

    Article  CAS  PubMed  Google Scholar 

  • Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223–231

    Article  PubMed  Google Scholar 

  • Schägger H, Cramer WA, von Jagow G (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem 217:220–230

    Article  PubMed  Google Scholar 

  • Scheer H, Zhao KH (2008) Biliprotein maturation: the chromophore attachment. Mol Microbiol 68:263–276

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shih PM, Wua D, Latifid A, Axena SD, Fewere DP, Tallad E, Calteauf A, Caia F, Tandeau de Marsacd N, Rippkag R, Herdmang M, Sivonene K, Coursinh T, Laurenth T, Goodwini L, Nolana M, Davenporti KW, Hani CS, Rubina EM, Eisena JA, Woykea T, Guggerh M, Kerfelda CA (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA 110:1053–1058

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Simon WJ, Hall JJ, Suzuki I, Murata N, Slabas AR (2002) Proteomic study of the soluble proteins from the unicellular cyanobacterium Synechocystis sp. PCC6803 using automated matrix-assisted laser desorption/ionization-time of flight peptide mass fingerprinting. Proteomics 2:1735–1742

    Article  CAS  PubMed  Google Scholar 

  • Singh KP, Rai S, Pandey S, Agrawal C, Shrivastava AK, Kumar S, Rai LC (2012) Cadmium and UV-B induced changes in proteome and some biochemical attributes of Anabaena sp. PCC 7120. Phykos 42:39–50

    Google Scholar 

  • Slabas AR, Suzuki I, Murata N, Simon WJ, Hall JJ (2006) Proteomic analysis of the heat shock response in Synechocystis PCC6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 gene. Proteomics 6:845–864

    Article  CAS  PubMed  Google Scholar 

  • Srivastava R, Pisareva T, Norling B (2005) Proteomic studies of the thylakoid membrane of Synechocystis sp. PCC 6803. Proteomics 5:4905–4916

    Article  CAS  PubMed  Google Scholar 

  • Stahl DC, Swiderek KM, Davis MT, Lee TD (1996) Data-controlled automation of liquid chromatography/tandem mass spectrometry analysis of peptide mixtures. J Am Soc Mass Spectrom 7:532–540

    Article  CAS  PubMed  Google Scholar 

  • Stensjö K, Ow SY, Barrios-Llerena ME, Lindblad P, Wright PC (2007) An iTRAQ-based quantitative analysis to elaborate the proteomic response of Nostoc sp. PCC 7120 under N2 fixing conditions. J Proteome Res 6:621–635

    Article  PubMed  CAS  Google Scholar 

  • Stöckel J, Welsh EA, Liberton M, Kunnvakkam R, Aurora R, Pakrasi HB (2008) Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes. Proc Natl Acad Sci USA 105:6156–6161

    Article  PubMed Central  PubMed  Google Scholar 

  • Stöckel J, Jacobs JM, Elvitigala TR, Liberton M, Welsh EA, Polpitiya AD, Gritsenko MA, Nicora CD, Koppenaal DW, Smith RD, Pakrasi HB (2011) Diurnal rhythms result in significant changes in the cellular protein complement in the cyanobacterium Cyanothece 51142. PLoS One 6:e16680

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Suzuki I, Simon W, Slabas AR (2006) The heat shock response of Synechocystis sp. PCC 6803 analysed by transcriptomics and proteomics. J Exp Bot 57:1573–1578

    Article  CAS  PubMed  Google Scholar 

  • Swanson R, Glazer AN (1990) Phycobiliprotein methylation: effect of the γ-N-methylasparagine residue on energy transfer in phycocyanin and the phycobilisome. J Mol Biol 214:787–796

    Article  CAS  PubMed  Google Scholar 

  • Takahashi Y, Koike H, Katoh S (1982) Multiple forms of chlorophyll–protein complexes from a thermophilic cyanobacterium Synechococcus sp. Arch Biochem Biophys 219:209–218

    Article  CAS  PubMed  Google Scholar 

  • Taylor SW, Fahy E, Zhang B, Glenn GM, Warnock DE, Wiley S, Murphy AN, Gaucher SP, Capaldi RA, Gibson BW, Ghosh SS (2003) Characterization of the human heart mitochondrial proteome. Nat Biotechnol 21:281–286

    Article  CAS  PubMed  Google Scholar 

  • Thingholm TE, Jensen ON, Larsen MR (2009) Analytical strategies for phosphoproteomics. Proteomics 9:1451–1468

    Article  CAS  PubMed  Google Scholar 

  • Thompson A, Schafer J, Kuhn K (2003) Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75:1895–1904

    Article  CAS  PubMed  Google Scholar 

  • Tian X, Lei C, Wang J, Qiao J, Zhang W (2013) Quantitative proteomics reveals dynamic responses of Synechocystis sp. PCC 6803 to next-generation biofuel butanol. J Proteomics 78:326–345

    Article  CAS  PubMed  Google Scholar 

  • Ting L, Rad R, Gygi SP, Haas W (2011) MS3 eliminates ratio distortion in isobaric labeling-based multiplexed quantitative proteomics. Nat Methods 8:937–940

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tran JC, Zamdborg L, Ahlf DR, Lee JE, Catherman AD, Durbin KR, Tipton JD, Vellaichamy A, Kellie JF, Li M, Wu C, Sweet SM, Early BP, Siuti N, LeDuc RD, Compton PD, Thomas PM, Kelleher NL (2011) Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature 480:254–258

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Trautmann D, Voß B, Wilde A, Al-Babili S, Hess WR (2012) Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803. DNA Res 19:435–448

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ujihara T, Sakurai I, Mizusawa N, Wada H (2008) A method for analyzing lipid-modified proteins with mass spectrometry. Anal Biochem 374:429–431

    Article  CAS  PubMed  Google Scholar 

  • Ünlü M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: a single method for detecting changes in protein extracts. Electrophoresis 18:2071–2077

    Article  PubMed  Google Scholar 

  • van de Meene AML, Hohmann MF, Vermass WFJ, Robertson RW (2006) The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol 184:259–270

    Article  CAS  PubMed  Google Scholar 

  • van den Bergh G, Arckens L (2003) Fluorescent two-dimensional difference gel electrophoresis unveils the potential of gel-based proteomics. Curr Opin Biotechnol 15:38–43

    Article  CAS  Google Scholar 

  • van Oudenhove L, Devreese B (2013) A review on recent developments in mass spectrometry instrumentation and quantitative tools advancing bacterial proteomics. App Microbiol Biotechnol 97:4749–4762

    Article  CAS  Google Scholar 

  • Waldbauer JR, Rodrigue S, Coleman ML, Chisholm SW (2012) Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle. PLoS One 7:e43432

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Y, Sun J, Chitnis PR (2000) Proteomic study of the peripheral proteins from thylakoid membranes of the cyanobacterium Synechocystis sp. PCC 6803. Electrophoresis 21:1746–1754

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Xu W, Chitnis PR (2009) Identification and bioinformatic analysis of the membrane proteins of Synechocystis sp. PCC 6803. Proteoeme Sci 7:11

    Article  CAS  Google Scholar 

  • Wang B, Wang J, Zhang W, Meldrum DR (2012a) Application of synthetic biology in cyanobacteria and algae. Front Microbiol 3:344

    PubMed Central  PubMed  Google Scholar 

  • Wang H, Alvarez S, Hicks LM (2012b) Comprehensive comparison of iTRAQ and label-free LC-based quantitative proteomics approaches using two Chlamydomonas reinhardtii strains of interest for biofuels engineering. J Proteome Res 11:487–501

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Bian Y, Cheng K, Gu L-F, Ye M, Zou H, Sai-Ming Sun S, He J-X (2012c) A large-scale protein phosphorylation analysis reveals novel phosphorylation motifs and phosphoregulatory networks in Arabidopsis. J Proteomics 78:486–498

    Article  PubMed  CAS  Google Scholar 

  • Wasinger VC, Zeng M, Yau Y (2013) Current status and advances in quantitative proteomic mass spectrometry. Int J Proteomics 2013:1–12

    Article  CAS  Google Scholar 

  • Watanabe M, Iwai M, Narikawa R, Ikeuchi M (2009) Is the photosystem II complex a monomer or a dimer? Plant Cell Physiol 50:1674–1680

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Kubota H, Wada H, Narikawa R, Ikeuchi M (2011) Novel supercomplex organization of Photosystem I in Anabaena and Cyanophora paradoxa. Plant Cell Physiol 52:162–168

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Semchonok DA, Webber-Birungi MT, Ehira S, Kondo K, Narikawa R, Ohmori M, Boekema EJ, Ikeuchi M (2014) Attachment of phycobilisomes in an antenna-Photosystem I supercomplex of cyanobacteria. Proc Natl Acad Sci USA 111:2512–2517

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wegener KM, Singh AK, Jacobs JM, Elvitigala T, Welsh EA, Keren N, Gritsenko MA, Ghosh BK, Camp DG, Smith RD, Pakrasi HB (2010) Global proteomics reveal an atypical strategy for carbon/nitrogen assimilation by a cyanobacterium under diverse environmental perturbations. Mol Cell Proteomics 9:2678–2689

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whitelegge JP (2013) Integral membrane proteins and bilayer proteomics. Anal Chem 85:2558–2568

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whitelegge J, Halgand F, Souda P, Zabrouskov V (2006) Top-down mass spectrometry of integral membrane proteins. Expert Rev Proteomics 3:585–596

    Article  CAS  PubMed  Google Scholar 

  • Wiese S, Reidegeld KA, Meyer HE, Warscheid B (2007) Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics 3:340–350

    Article  Google Scholar 

  • Wijffels RH, Kruse O, Hellingwerf KJ (2013) Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Curr Opin Biotechnol 24:405–513

    Article  CAS  PubMed  Google Scholar 

  • Wilkins MR, Sanchez JC, Gooley AA, Appel RD, Humphery-Smith I, Hochstrasser DF, Williams KL (1996) From proteins to proteomes: large scale protein identification by two-dimensional electrophoresis and arnino acid analysis. Nat Biotechnol 14:61–65

    Article  CAS  Google Scholar 

  • Wittig I, Braun HP, Schägger H (2006) Blue native PAGE. Nat Protoc 1:418–428

    Article  CAS  PubMed  Google Scholar 

  • Wittig I, Karas M, Schägger H (2007) High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol Cell Proteomics 6:1215–1225

    Article  CAS  PubMed  Google Scholar 

  • Witze ES, Old WM, Resing KA, Ahn NG (2007) Mapping protein post-translational modifications with mass spectrometry. Nat Methods 4:798–806

    Article  CAS  PubMed  Google Scholar 

  • Wolf-Yadlin A, Hautaniemi S, Lauffenburger DA, White FM (2007) Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networks. Proc Natl Acad Sci USA 104:5860–5865

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wolters DA, Washburn MP, Yates JR (2001) An automated multidimensional protein identification technology for shotgun proteomics. Anal Chem 73:5683–5690

    Article  CAS  PubMed  Google Scholar 

  • Wulfhorst H, Franken LE, Wessinghage T, Boekema EJ, Nowaczyk MM (2014) The 5 kDa protein NdhP is essential for stable NDH-1L assembly in Thermosynechococcus elongatus. PLoS One 9:e103584

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Xu M, Ogawa T, Pakrasi HB, Mi H (2008) Identification and localization of the CupB protein involved in constitutive CO2 uptake in the cyanobacterium Synechocystis sp strain PCC 6803. Plant Cell Physiol 49:994–997

    Article  PubMed  CAS  Google Scholar 

  • Yates JR III, Eng JK, McCormack AL, Schieltz D (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67:1426–1436

    Article  CAS  PubMed  Google Scholar 

  • Yates JR, Ruse CI, Nakorchevsky A (2009) Proteomics by mass spectrometry: approaches, advances, and applications. Annu Rev Biomed Eng 11:49–79

    Article  CAS  PubMed  Google Scholar 

  • Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB (2001) The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc Natl Acad Sci USA 98:13443–13448

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang P, Battchikova N, Jansen T, Appel J, Ogawa T, Aro EM (2004) Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp. PCC 6803. Plant Cell 16:3326–3340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang P, Battchikova N, Paakkarinen V, Katoh H, Iwai M, Ikeuchi M, Pakrasi HB, Ogawa T, Aro EM (2005) Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. Biochem J 390:513–520

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang LF, Yang HM, Cui SX, Hu J, Wang J, Kuang TY, Norling B, Huang F (2009a) Proteomic analysis of plasma membranes of cyanobacterium Synechocystis sp. strain PCC 6803 in response to high pH stress. J Proteome Res 8:2892–2902

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Allahverdiyeva Y, Eisenhut M, Aro EM (2009b) Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS One 4:e5331

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang P, Eisenhut M, Brandt AM, Carmel D, Silén H, Vass I, Allahverdiyeva Y, Salminen T, Aro EM (2012) Operon flv4-flv2 provides cyanobacterial photosystem II with flexibility of electron transfer. Plant Cell 24:1952–1971

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zilliges Y, Kehr J-C, Mikkat S, Bouchier C, Tandeau de Marsac N, Börner T, Dittmann E (2008) An extracellular glycoprotein is implicated in cell-cell contacts in the toxic cyanobacterium Microcystis aeruginosa PCC 7806. J Bacteriol 190:2871–2879

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zilliges Y, Kehr J-C, Meissner S, Ishida K, Mikkat S, Hagemann M, Kaplan A, Börner T, Dittmann E (2011) The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of microcystis under pxidative stress conditions. PLoS One 6:e17615

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zorina A, Stepanchenko N, Novikova GV, Sinetova M, Panichkin VB, Moshkov IE, Zinchenko VV, Shestakov SV, Suzuki I, Murata N, Los DA (2011) Eukaryotic-like Ser/Thr protein kinases SpkC/F/K are involved in phosphorylation of GroES in the cyanobacterium Synechocystis. DNA Res 18:137–151

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

Research in the laboratory of authors is supported by Academy of Finland Center of Excellence Projects 141121 and 271832 and by Academy Professor Grants Aro (2272230 and 273870) to Eva-Mari. This work has received funding from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme FP7/2007-2013/under REA Grant agreement no 317184. This material reflects only the author’s views and the Union is not liable for any use that may be made of the information contained therein.

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  1. Laboratory of Molecular Plant Biology, Department of Biochemistry, University of Turku, 20014, Turku, Finland

    Natalia Battchikova, Martina Angeleri & Eva-Mari Aro

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  1. Natalia Battchikova
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  2. Martina Angeleri
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  3. Eva-Mari Aro
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Correspondence to Natalia Battchikova.

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Battchikova, N., Angeleri, M. & Aro, EM. Proteomic approaches in research of cyanobacterial photosynthesis. Photosynth Res 126, 47–70 (2015). https://doi.org/10.1007/s11120-014-0050-4

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