Proteomic profiles of five strains of oxygenic photosynthetic cyanobacteria of the genus cyanothece

Journal of Proteome Research

Volumn 13, Issue 7, 2014, Pages 3262-3276

  Aryal, Uma K ^a,g   Callister, Stephen J ^a   McMahon, Benjamin H ^b   McCue, Lee Ann ^a   Brown, Joseph ^a   Stöckel, Jana ^c,f   Liberton, Michelle ^c   Mishra, Sujata ^d   Zhang, Xiaohui ^d   Nicora, Carrie D ^a   Angel, Thomas E ^a,e   Koppenaal, David W ^a   Smith, Richard D ^a   Pakrasi, Himadri B ^c   Sherman, Louis A ^d  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d PURDUE UNIVERSITY   (United States)

^e KINEMED INC   (United States)

^f MOgene Green Chemicals LC   (United States)

^g PURDUE UNIVERSITY   (United States)

Author keywords

Cyanobacteria; Cyanothece; orthologues; photosynthesis; proteome

Indexed keywords

PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RIBOSOME PROTEIN; BACTERIAL PROTEIN; PROTEOME;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; CELL FRACTIONATION; CYANOTHECE; GENE FUNCTION; GENE SEQUENCE; GENOME ANALYSIS; GENOMIC ISLAND; HORIZONTAL GENE TRANSFER; ION EXCHANGE CHROMATOGRAPHY; MEMBRANE TRANSPORT; MICROCYSTIS AERUGINOSA; NITROGEN FIXATION; NONHUMAN; PHOTOSYNTHESIS; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEOMICS; RNA METABOLISM; SYNECHOCYSTIS; TANDEM MASS SPECTROMETRY; GENE EXPRESSION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM;

BACTERIAL PROTEINS; CHROMATOGRAPHY, ION EXCHANGE; CYANOTHECE; GENE EXPRESSION; NITROGEN FIXATION; PHOTOSYNTHESIS; PHYLOGENY; PROTEOME; TANDEM MASS SPECTROMETRY;

EID: 84903723059     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5000889     Document Type: Article

References (45)

1. Bryant, D. A.; Frigaard, N. U. Prokaryotic photosynthesis and phototrophy illuminated Trends Microbiol. 2006, 14, 488-96
2. Zehr, J. P.; Waterbury, J. B.; Turner, P. J.; Montoya, J. P.; Omoregie, E.; Steward, G. F.; Hansen, A.; Karl, D. M. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean Nature 2001, 412, 635-8
3. Colon-Lopez, M. S.; Sherman, L. A. Transcriptional and translational regulation of photosystem I and II genes in light-dark- and continuous-light- grown cultures of the unicellular cyanobacterium Cyanothece sp. strain ATCC 51142 J. Bacteriol. 1998, 180, 519-26
4. Welsh, E. A.; Liberton, M.; Stockel, J.; Loh, T.; Elvitigala, T.; Wang, C.; Wollam, A.; Fulton, R. S.; Clifton, S. W.; Jacobs, J. M.; Aurora, R.; Ghosh, B. K.; Sherman, L. A.; Smith, R. D.; Wilson, R. K.; Pakrasi, H. B. The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 15094-9
5. Toepel, J.; Welsh, E.; Summerfield, T. C.; Pakrasi, H. B.; Sherman, L. A. Differential transcriptional analysis of the cyanobacterium Cyanothece sp strain ATCC 51142 during light-dark and continuous-light growth J. Bacteriol. 2008, 190, 3904-3913
6. Stockel, J.; Welsh, E. A.; Liberton, M.; Kunnvakkam, R.; Aurora, R.; Pakrasi, H. B. Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes Proc. Natl. Acad. Sci. U.S. A. 2008, 105, 6156-61
7. Singh, A. K.; Bhattacharyya-Pakrasi, M.; Elvitigala, T.; Ghosh, B.; Aurora, R.; Pakrasi, H. B.; Systems-Level, A. Analysis of the effects of light quality on the metabolism of a cyanobacterium Plant Physiol. 2009, 151, 1596-1608
8. Aryal, U. K.; Stockel, J.; Krovvidi, R. K.; Gritsenko, M. A.; Monroe, M. E.; Moore, R. J.; Koppenaal, D. W.; Smith, R. D.; Pakrasi, H. B.; Jacobs, J. M. Dynamic proteomic profiling of a unicellular cyanobacterium Cyanothece ATCC51142 across light-dark diurnal cycles BMC Syst. Biol. 2011, 5, 194
9. Aryal, U. K.; Stockel, J.; Welsh, E. A.; Gritsenko, M. A.; Nicora, C. D.; Koppenaal, D. W.; Smith, R. D.; Pakrasi, H. B.; Jacobs, J. M. Dynamic proteome analysis of Cyanothece sp. ATCC 51142 under constant light J. Proteome Res. 2012, 11, 609-19
10. Stockel, J.; Jacobs, J. M.; Elvitigala, T. R.; Liberton, M.; Welsh, E. A.; Polpitiya, A. D.; Gritsenko, M. A.; Nicora, C. D.; Koppenaal, D. W.; Smith, R. D.; Pakrasi, H. B. Diurnal rhythms result in significant changes in the cellular protein complement in the cyanobacterium Cyanothece 51142 PLoS One 2011, 6, e16680
11. Bandyopadhyay, A.; Elvitigala, T.; Welsh, E.; Stockel, J.; Liberton, M.; Min, H.; Sherman, L. A.; Pakrasi, H. B. Novel metabolic attributes of the genus cyanothece, comprising a group of unicellular nitrogen-fixing Cyanothece MBio 2011, 2, e00214-11
12. Callister, S. J.; McCue, L. A.; Turse, J. E.; Monroe, M. E.; Auberry, K. J.; Smith, R. D.; Adkins, J. N.; Lipton, M. S. Comparative bacterial proteomics: analysis of the core genome concept PLoS One 2008, 3, e1542
13. Schrimpe-Rutledge, A. C.; Jones, M. B.; Chauhan, S.; Purvine, S. O.; Sanford, J. A.; Monroe, M. E.; Brewer, H. M.; Payne, S. H.; Ansong, C.; Frank, B. C.; Smith, R. D.; Peterson, S. N.; Motin, V. L.; Adkins, J. N. Comparative omics-driven genome annotation refinement: application across Yersiniae PLoS One 2012, 7, e33903
14. Berendzen, J.; Bruno, W. J.; Cohn, J. D.; Hengartner, N. W.; Kuske, C. R.; McMahon, B. H.; Wolinsky, M. A.; Xie, G. Rapid phylogenetic and functional classification of short genomic fragments with signature peptides BMC Res. Notes 2012, 5, 460
15. Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity BMC Bioinf. 2004, 5, 113
16. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 2004, 32, 1792-7
17. Guindon, S.; Dufayard, J. F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 Syst. Biol. 2010, 59, 307-21
18. Perriere, G.; Gouy, M. WWW-query: an on-line retrieval system for biological sequence banks Biochimie 1996, 78, 364-9
19. Overbeek, R.; Begley, T.; Butler, R. M.; Choudhuri, J. V.; Chuang, H. Y.; Cohoon, M.; de Crecy-Lagard, V.; Diaz, N.; Disz, T.; Edwards, R.; Fonstein, M.; Frank, E. D.; Gerdes, S.; Glass, E. M.; Goesmann, A.; Hanson, A.; Iwata-Reuyl, D.; Jensen, R.; Jamshidi, N.; Krause, L.; Kubal, M.; Larsen, N.; Linke, B.; McHardy, A. C.; Meyer, F.; Neuweger, H.; Olsen, G.; Olson, R.; Osterman, A.; Portnoy, V.; Pusch, G. D.; Rodionov, D. A.; Ruckert, C.; Steiner, J.; Stevens, R.; Thiele, I.; Vassieva, O.; Ye, Y.; Zagnitko, O.; Vonstein, V. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes Nucleic Acids Res. 2005, 33, 5691-702
20. Reddy, K. J.; Haskell, J. B.; Sherman, D. M.; Sherman, L. A. Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece J. Bacteriol. 1993, 175, 1284-92
21. Wegener, K. M.; Singh, A. K.; Jacobs, J. M.; Elvitigala, T.; Welsh, E. A.; Keren, N.; Gritsenko, M. A.; Ghosh, B. K.; Camp, D. G., 2nd; Smith, R. D.; Pakrasi, H. B. Global proteomics reveal an atypical strategy for carbon/nitrogen assimilation by a cyanobacterium under diverse environmental perturbations Mol. Cell Proteomics 2010, 9, 2678-89
22. Callister, S. J.; Dominguez, M. A.; Nicora, C. D.; Zeng, X.; Tavano, C. L.; Kaplan, S.; Donohue, T. J.; Smith, R. D.; Lipton, M. S. Application of the accurate mass and time tag approach to the proteome analysis of sub-cellular fractions obtained from Rhodobacter sphaeroides 2.4.1. Aerobic and photosynthetic cell cultures J. Proteome Res. 2006, 5, 1940-7
23. Jacobs, J. M.; Diamond, D. L.; Chan, E. Y.; Gritsenko, M. A.; Qian, W. J.; Stastna, M.; Baas, T.; Camp, D. G.; Carithers, R. L.; Smith, R. D.; Katze, M. G. Proteome analysis of liver cells expressing a full-length hepatitis C virus (HCV) replicon and biopsy specimens of posttransplantation liver from HCV-infected patients J. Virol. 2005, 79, 7558-69
24. Jacobs, J. M.; Mottaz, H. M.; Yu, L. R.; Anderson, D. J.; Moore, R. J.; Chen, W. N. U.; Auberry, K. J.; Strittmatter, E. F.; Monroe, M. E.; Thrall, B. D.; Camp, D. G.; Smith, R. D. Multidimensional proteome analysis of human mammary epithelial cells J. Proteome Res. 2004, 3, 68-75
25. Shen, Y.; Tolic, N.; Masselon, C.; Pasa-Tolic, L.; Camp, D. G.; Hixson, K. K.; Zhao, R.; Anderson, G. A.; Smith, R. D. Ultrasensitive proteomics using high-efficiency on-line micro-SPE-NanoLC-NanoESI MS and MS/MS Anal. Chem. 2004, 76, 144-54
26. Shen, Y. F.; Jacobs, J. M.; Camp, D. G.; Fang, R. H.; Moore, R. J.; Smith, R. D.; Xiao, W. Z.; Davis, R. W.; Tompkins, R. G. Ultra-high-efficiency strong cation exchange LC/RPLC/MS/MS for high dynamic range characterization of the human plasma proteome Anal. Chem. 2004, 76, 1134-44
27. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4, 207-14
28. Kim, S.; Gupta, N.; Pevzner, P. A. Spectral probabilities and generating functions of tandem mass spectra: A strike against decoy databases J. Proteome Res. 2008, 7, 3354-63
29. Remm, M.; Storm, C. E.; Sonnhammer, E. L. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons J. Mol. Biol. 2001, 314, 1041-52
30. Zhou, J. Y.; Schepmoes, A. A.; Zhang, X.; Moore, R. J.; Monroe, M. E.; Lee, J. H.; Camp, D. G.; Smith, R. D.; Qian, W. J. Improved LC-MS/MS spectral counting statistics by recovering low-scoring spectra matched to confidently identified peptide sequences J. Proteome Res. 2010, 9, 5698-704
31. Polpitiya, A. D.; Qian, W. J.; Jaitly, N.; Petyuk, V. A.; Adkins, J. N.; Camp, D. G.; Anderson, G. A.; Smith, R. D. DAnTE: a statistical tool for quantitative analysis of -omics data Bioinformatics 2008, 24, 1556-8
32. Andersson, I.; Backlund, A. Structure and function of Rubisco Plant Physiol. Biochem. 2008, 46, 275-91
33. Price, M. N.; Dehal, P. S.; Arkin, A. P. Orthologous transcription factors in bacteria have different functions and regulate different genes PLoS Comput. Biol. 2007, 3, 1739-50
34. Thompson, A. W.; Foster, R. A.; Krupke, A.; Carter, B. J.; Musat, N.; Vaulot, D.; Kuypers, M. M.; Zehr, J. P. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga Science 2012, 337, 1546-50
35. Nilsson, M.; Rasmussen, U.; Bergman, B. Competition among symbiotic cyanobacterial Nostoc strains forming artificial associations with rice (Oryza sativa) FEMS Microbiol. Lett. 2005, 245, 139-44
36. Aryal, U. K.; Callister, S. J.; Mishra, S.; Zhang, X.; Shutthanandan, J. I.; Angel, T. E.; Shukla, A. K.; Monroe, M. E.; Moore, R. J.; Koppenaal, D. W.; Smith, R. D.; Sherman, L. Proteome analyses of strains ATCC 51142 and PCC 7822 of the diazotrophic cyanobacterium Cyanothece sp. under culture conditions resulting in enhanced H(2) production Appl. Environ. Microbiol. 2013, 79, 1070-7
37. Turse, J. E.; Marshall, M. J.; Fredrickson, J. K.; Lipton, M. S.; Callister, S. J. An empirical strategy for characterizing bacterial proteomes across species in the absence of genomic sequences PLoS One 2010, 5, e13968
38. Liu, H.; Sadygov, R. G.; Yates, J. R., 3rd A model for random sampling and estimation of relative protein abundance in shotgun proteomics Anal. Chem. 2004, 76, 4193-201
39. Schneegurt, M. A.; Sherman, D. M.; Nayar, S.; Sherman, L. A. Oscillating behavior of carbohydrate granule formation and dinitrogen fixation in the cyanobacterium Cyanothece sp strain ATCC-51142 J. Bacteriol. 1994, 176, 1586-97
40. Raymond, J.; Zhaxybayeva, O.; Gogarten, J. P.; Gerdes, S. Y.; Blankenship, R. E. Whole-genome analysis of photosynthetic prokaryotes Science 2002, 298, 1616-20
41. Burke, D. H.; Hearst, J. E.; Sidow, A. Early evolution of photosynthesis: clues from nitrogenase and chlorophyll iron proteins Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 7134-8
42. Fujimori, T.; Hihara, Y.; Sonoike, K. PsaK2 subunit in photosystem I is involved in state transition under high light condition in the cyanobacterium Synechocystis sp. PCC 6803 J. Biol. Chem. 2005, 280, 22191-7
43. de Marsac, N. T.; Cohen-bazire, G. Molecular composition of cyanobacterial phycobilisomes Proc. Natl. Acad. Sci. U.S.A. 1977, 74, 1635-9
44. Wu, B.; Zhang, B. C.; Feng, X. Y.; Rubens, J. R.; Huang, R.; Hicks, L. M.; Pakrasi, H. B.; Tang, Y. J. J. Alternative isoleucine synthesis pathway in cyanobacterial species Microbiology 2010, 156, 596-602
45. Atsumi, S.; Wu, T. Y.; Eckl, E. M.; Hawkins, S. D.; Buelter, T.; Liao, J. C. Engineering the isobutanol biosynthetic pathway in Escherichia coli by comparison of three aldehyde reductase/alcohol dehydrogenase genes Appl. Microbiol. Biotechnol. 2010, 85, 651-7