Toward a systems-level understanding of gene regulatory, protein interaction, and metabolic networks in cyanobacteria

Frontiers in Genetics

Volumn 5, Issue JUL, 2014, Pages

  Hernández Prieto, Miguel A ^a   Semeniuk, Trudi A ^a   Futschik, Matthias E ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Cyanobacteria; Meta analysis; Metabolic pathways; Networks; Systems biology

Indexed keywords

CYANOBACTERIUM; DATA ANALYSIS; GENE CONTROL; GENE EXPRESSION; GENE MAPPING; GENETIC ANALYSIS; META ANALYSIS (TOPIC); METABOLOMICS; METAGENOMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROCHLOROCOCCUS; PROTEIN INTERACTION; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; PROTEOMICS; REVIEW; RNA SEQUENCE; SYNECHOCYSTIS; SYSTEMS BIOLOGY; TRANSCRIPTOMICS;

EID: 84906266629     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00191     Document Type: Review

References (172)

1. Abed, R. M. M., Dobretsov, S., and Sudesh, K. (2009). Applications of cyanobacteria in biotechnology. J. Appl. Microbiol. 106, 1-12. doi: 10.1111/j.1365-2672.2008.03918.x
2. Alagesan, S., Gaudana, S. B., Sinha, A., and Wangikar, P. P. (2013). Metabolic flux analysis of Cyanothece sp. ATCC 51142 under mixotrophic conditions. Photosynth. Res. 118, 191-198. doi: 10.1007/s11120-013-9911-5
3. Albert, R. (2007). Network inference, analysis, and modeling in systems biology. Plant Cell Online 19, 3327-3338. doi: 10.1105/tpc.107.054700
4. Arakawa, K., Yamada, Y., Shinoda, K., Nakayama, Y., and Tomita, M. (2006). GEM System: automatic prototyping of cell-wide metabolic pathway models from genomes. BMC Bioinformatics 7:168. doi: 10.1186/1471-2105-7-168
5. Arruda, S. C. C., Barbosa, H. D. S., Azevedo, R. A., and Arruda, M. A. Z. (2011). Two-dimensional difference gel electrophoresis applied for analytical proteomics: fundamentals and applications to the study of plant proteomics. Analyst 136, 4119-4126. doi: 10.1039/c1an15513j
6. Aryal, U., Stockel, J., Krovvidi, R., Gritsenko, M., Monroe, M., Moore, R., et al. (2011). Dynamic proteomic profiling of a unicellular cyanobacterium Cyanothece ATCC51142 across light-dark diurnal cycles. BMC Syst. Biol. 5:194. doi: 10.1186/1752-0509-5-194
7. Avrani, S., Wurtzel, O., Sharon, I., Sorek, R., and Lindell, D. (2011). Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474, 604-608. doi: 10.1038/nature10172
8. Axmann, I. M., Hertel, S., Wiegard, A., Dorrich, A. K., and Wilde, A. (2014). Diversity of KaiC-based timing systems in marine Cyanobacteria. Mar. Genomics 14, 3-16. doi: 10.1016/j.margen.2013.12.006
9. Blot, N., Mella-Flores, D., Six, C., Le Corguille, G., Boutte, C., Peyrat, A., et al. (2011). Light History influences the response of the marine cyanobacterium Synechococcus sp. WH7803 to oxidative stress. Plant Physiol. 156, 1934-1954. doi: 10.1104/pp.111.174714
10. Boele, J., Olivier, B. G., and Teusink, B. (2012). FAME, the flux analysis and modeling environment. BMC Syst. Biol. 6:8. doi: 10.1186/1752-0509-6-8
11. Bonneau, R., Reiss, D., Shannon, P., Facciotti, M., Hood, L., Baliga, N., et al. (2006). The Inferelator: an algorithm for learning parsimonious regulatory networks from systems-biology data sets de novo. Genome Biol. 7:R36. doi: 10.1186/gb-2006-7-5-r36
12. Burja, A. M., Dhamwichukorn, S., and Wright, P. C. (2003). Cyanobacterial postgenomic research and systems biology. Trends Biotechnol. 21, 504-511. doi: 10.1016/j.tibtech.2003.08.008
13. Buttigieg, P. L., Hankeln, W., Kostadinov, I., Kottmann, R., Yilmaz, P., Duhaime, M. B., et al. (2013). Ecogenomic perspectives on domains of unknown function: correlation-based exploration of marine metagenomes. PLoS ONE 8:e50869. doi: 10.1371/journal.pone.0050869
14. Caspi, R., Altman, T., Dreher, K., Fulcher, C. A., Subhraveti, P., Keseler, I. M., et al. (2012). The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 40, D742-D753. doi: 10.1093/nar/gkr1014
15. Chisholm, S. W., Olson, R. J., Zettler, E. R., Goericke, R., Waterbury, J. B., and Welschmeyer, N. A. (1988). A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334, 340-343. doi: 10.1038/334340a0
16. Church, M. J., Short, C. M., Jenkins, B. D., Karl, D. M., and Zehr, J. P. (2005). Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl. Environ. Microbiol. 71, 5362-5370. doi: 10.1128/AEM.71.9.5362-5370.2005
17. Cox, A. D., and Saito, M. A. (2013). Proteomic responses of oceanic Synechococcus WH8102 to phosphate and zinc scarcity and cadmium additions. Front. Microbiol. 4:387. doi: 10.3389/fmicb.2013.00387
18. Degnan, B. M., Hawkins, C. J., Lavin, M. F., McCaffrey, E. J., Parry, D. L., Van Den Brenk, A. L., et al. (1989). New cyclic peptides with cytotoxic activity from the ascidian Lissoclinum patella. J. Med. Chem. 32, 1349-1354. doi: 10.1021/jm00126a034
19. Devoid, S., Overbeek, R., Dejongh, M., Vonstein, V., Best, A., and Henry, C. (2013). "Automated genome annotation and metabolic model reconstruction in the SEED and model SEED," in Systems Metabolic Engineering, ed H. S. Alper (New York, NY: Humana Press), 17-45. doi: 10.1007/978-1-62703-299-5_2
20. Dickson, D. J., Luterra, M. D., and Ely, R. L. (2012). Transcriptomic responses of Synechocystis sp. PCC 6803 encapsulated in silica gel. Appl. Microbiol. Biotechnol. 96, 183-196. doi: 10.1007/s00253-012-4307-6
21. Duce, R. A., Laroche, J., Altieri, K., Arrigo, K. R., Baker, A. R., Capone, D. G., et al. (2008). Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320, 893-897. doi: 10.1126/science.1150369
22. Dufresne, A., Garczarek, L., and Partensky, F. (2005). Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol. 6:R14. doi: 10.1186/gb-2005-6-2-r14
23. Dufresne, A., Ostrowski, M., Scanlan, D. J., Garczarek, L., Mazard, S., Palenik, B. P., et al. (2008). Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Genome Biol. 9:R90. doi: 10.1186/gb-2008-9-5-r90
24. Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I. M., Barbe, V., et al. (2003). Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc. Natl. Acad. Sci. U.S.A. 100, 10020-10025. doi: 10.1073/pnas.1733211100
25. Dupont, C. L., Johnson, D. A., Phillippy, K., Paulsen, I. T., Brahamsha, B., and Palenik, B. (2012). Genetic identification of a high-affinity Ni transporter and the transcriptional response to Ni deprivation in Synechococcus sp. strain WH8102. Appl. Environ. Microbiol. 78, 7822-7832. doi: 10.1128/AEM.01739-12
26. Edgar, R., Domrachev, M., and Lash, A. E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210. doi: 10.1093/nar/30.1.207
27. Elhai, J., Taton, A., Massar, J. P., Myers, J. K., Travers, M., Casey, J., et al. (2009). BioBIKE: a Web-based, programmable, integrated biological knowledge base. Nucleic Acids Res. 37, W28-W32. doi: 10.1093/nar/gkp354
28. Falkowski, P. (2012). OCEAN SCIENCE The power of plankton. Nature 483, S17-S20. doi: 10.1038/483S17a
29. Field, C. B., Behrenfeld, M. J., Randerson, J. T., and Falkowski, P. (1998). Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-240. doi: 10.1126/science.281.5374.237
30. Flaherty, B. L., Van Nieuwerburgh, F., Head, S. R., and Golden, J. W. (2011). Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp. strain PCC 7120 to combined-nitrogen deprivation. BMC Genomics 12:332. doi: 10.1186/1471-2164-12-332
31. Flombaum, P., Gallegos, J. L., Gordillo, R. A., Rincón, 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. doi: 10.1073/pnas.1307701110
32. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., et al. (2013). STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-D815. doi: 10.1093/nar/gks1094
33. Frigaard, N.-U., Sakuragi, Y., and Bryant, D. (2004). "Gene inactivation in the cyanobacterium Synechococcus sp. PCC 7002 and the green sulfur bacterium chlorobium tepidum using in vitro-made DNA constructs and natural transformation," in Photosynthesis Research Protocols, ed R. Carpentier (Totowa, NJ: Humana Press), 325-340. doi: 10.1385/1-59259-799-8:325
34. Fujisawa, T., Okamoto, S., Katayama, T., Nakao, M., Yoshimura, H., Kajiya-Kanegae, H., et al. (2014). CyanoBase and RhizoBase: databases of manually curated annotations for cyanobacterial and rhizobial genomes. Nucleic Acids Res. 42, D666-D670. doi: 10.1093/nar/gkt1145
35. Furumichi, M., Sato, Y., Omata, T., Ikeuchi, M., and Kanehisa, M. (2002). CYORF: community annotation of cyanobacteria genes. Genome Informatics 13, 402-403.
36. Fuszard, M. A., Wright, P. C., and Biggs, C. A. (2012). Comparative quantitative proteomics of prochlorococcus ecotypes to a decrease in environmental phosphate concentrations. Aquat. Biosyst. 8:7. doi: 10.1186/2046-9063-8-7
37. Garcia-Pichel, F., Belnap, J., Neuer, S., and Schanz, F. (2003). Estimates of global cyanobacterial biomass and its distribution. Arch. Hydrobiol. 109, 213-227. doi: 10.1127/1864-1318/2003/0109-0213
38. Garcia-Pichel, F., and Pringault, O. (2001). Microbiology: cyanobacteria track water in desert soils. Nature 413, 380-381. doi: 10.1038/35096640
39. Gardner, P. P., Daub, J., Tate, J., Moore, B. L., Osuch, I. H., Griffiths-Jones, S., et al. (2011). Rfam: Wikipedia, clans and the "decimal" release. Nucleic Acids Res. 39, D141-D145. doi: 10.1093/nar/gkq1129
40. Genini, S., Badaoui, B., Sclep, G., Bishop, S., Waddington, D., Pinard Van Der Laan, M.-H., et al. (2011). Strengthening insights into host responses to mastitis infection in ruminants by combining heterogeneous microarray data sources. BMC Genomics 12:225. doi: 10.1186/1471-2164-12-225
41. Georg, J., Voss, B., Scholz, I., Mitschke, J., Wilde, A., and Hess, W. R. (2009). Evidence for a major role of antisense RNAs in cyanobacterial gene regulation. Mol. Syst. Biol. 5:305. doi: 10.1038/msb.2009.63
42. Ginsburg, H. (2009). Caveat emptor: limitations of the automated reconstruction of metabolic pathways in Plasmodium. Trends Parasitol. 25, 37-43. doi: 10.1016/j.pt.2008.08.012
43. Goto, S., Kawashima, S., Okuji, Y., Kamiya, T., Miyazaki, S., Numatam, Y., et al. (2000). KEGG/EXPRESSION: a database for browsing and analysing microarray expression data. Genome Informatics 11, 222-223.
44. Gross, H. (2007). Strategies to unravel the function of orphan biosynthesis pathways: recent examples and future prospects. Appl. Microbiol. Biotechnol. 75, 267-277. doi: 10.1007/s00253-007-0900-5
45. Haas, B. J., Chin, M., Nusbaum, C., Birren, B. W., and Livny, J. (2012). How deep is deep enough for RNA-Seq profiling of bacterial transcriptomes? BMC Genomics 13:734. doi: 10.1186/1471-2164-13-734
46. Heidorn, T., Camsund, D., Huang, H. H., Lindberg, P., Oliveira, P., Stensjo, K., et al. (2011). Synthetic biology in cyanobacteria: engineering and analyzing novel functions. Methods Enzymol. 497, 539-579. doi: 10.1016/B978-0-12-385075-1.00024-X
47. Hernandez-Prieto, M. A., and Futschik, M. E. (2012). CyanoEXpress: a web database for exploration and visualisation of the integrated transcriptome of cyanobacterium Synechocystis sp. PCC6803. Bioinformation 8, 629-633. doi: 10.6026/97320630008634
48. Hernandez-Prieto, M. A., Schon, V., Georg, J., Barreira, L., Varela, J., Hess, W. R., et al. (2012). Iron deprivation in Synechocystis: inference of pathways, non-coding RNAs, and regulatory elements from comprehensive expression profiling. G3 (Bethesda) 2, 1475-1495. doi: 10.1534/g3.112.003863
49. Hihara, Y., Kamei, A., Kanehisa, M., Kaplan, A., and Ikeuchi, M. (2001). DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13, 793-806. doi: 10.1105/tpc.13.4.793
50. Hoffmann, L. (1999). Marine cyanobacteria in tropical regions: diversity and ecology. Eur. J. Phycol. 34, 371-379. doi: 10.1080/09670269910001736432
51. Ireland, C. M., Durso, A. R., Newman, R. A., and Hacker, M. P. (1982). Antineoplastic cyclic peptides from the marine tunicate Lissoclinum patella. J. Org. Chem. 47, 1807-1811. doi: 10.1021/jo00349a002
52. Jafari, P., and Azuaje, F. (2006). An assessment of recently published gene expression data analyses: reporting experimental design and statistical factors. BMC Med. Inform. Decis. Mak. 6:27. doi: 10.1186/1472-6947-6-27
53. Johnson, Z. I., Zinser, E. R., Coe, A., McNulty, N. P., Woodward, E. M. S., and Chisholm, S. W. (2006). Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311, 1737-1740. doi: 10.1126/science.1118052
54. Kaçar, B., and Gaucher, E. A. (2013). Experimental evolution of protein-protein interaction networks. Biochem. J. 453, 311-319. doi: 10.1042/BJ20130205
55. Kamennaya, N. A., and Post, A. F. (2011). Characterization of cyanate metabolism in marine Synechococcus and Prochlorococcus spp. Appl. Environ. Microbiol. 77, 291-301. doi: 10.1128/AEM.01272-10
56. Kaneko, T., Nakamura, Y., Wolk, C. P., Kuritz, T., Sasamoto, S., Watanabe, A., et al. (2001). Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 8, 205-213. doi: 10.1093/dnares/8.5.205
57. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., et al. (1996). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3, 109-136. doi: 10.1093/dnares/3.3.109
58. Karp, P. D., Paley, S. M., Krummenacker, M., Latendresse, M., Dale, J. M., Lee, T. J., et al. (2010). Pathway Tools version 13.0: integrated software for pathway/genome informatics and systems biology. Brief. Bioinform. 11, 40-79. doi: 10.1093/bib/bbp043
59. Kelly, L., Ding, H. M., Huang, K. H., Osburne, M. S., and Chisholm, S. W. (2013). Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent. ISME J. 7, 1827-1841. doi: 10.1038/ismej.2013.58
60. Kelly, L., Huang, K. H., Ding, H., and Chisholm, S. W. (2012). ProPortal: a resource for integrated systems biology of Prochlorococcus and its phage. Nucleic Acids Res. 40, D632-D640. doi: 10.1093/nar/gkr1022
61. Kettler, G. C., Martiny, A. C., Huang, K., Zucker, J., Coleman, M. L., Rodrigue, S., et al. (2007). Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet. 3:e231. doi: 10.1371/journal.pgen.0030231
62. Kim, W.-Y., Kang, S., Kim, B.-C., Oh, J., Cho, S., Bhak, J., et al. (2008). SynechoNET: integrated protein-protein interaction database of a model cyanobacterium Synechocystis sp. PCC 6803. BMC Bioinformatics 9:S20. doi: 10.1186/1471-2105-9-S1-S20
63. Klanchui, A., Khannapho, C., Phodee, A., Cheevadhanarak, S., and Meechai, A. (2012). iAK692: a genome-scale metabolic model of Spirulina platensis C1. BMC Syst. Biol. 6:71. doi: 10.1186/1752-0509-6-71
64. Knoop, H., Grundel, M., Zilliges, Y., Lehmann, R., Hoffmann, S., Lockau, W., et al. (2013). Flux balance analysis of cyanobacterial metabolism: the metabolic network of Synechocystis sp. PCC 6803. PLoS Comput. Biol. 9:e1003081. doi: 10.1371/journal.pcbi.1003081
65. Knoop, H., Zilliges, Y., Lockau, W., and Steuer, R. (2010). The metabolic network of Synechocystis sp. PCC 6803: systemic properties of autotrophic growth. Plant Physiol. 154, 410-422. doi: 10.1104/pp.110.157198
66. Kolowrat, C., Partensky, F., Mella-Flores, D., Le Corguille, G., Boutte, C., Blot, N., et al. (2010). Ultraviolet stress delays chromosome replication in light/dark synchronized cells of the marine cyanobacterium Prochlorococcus marinus PCC9511. BMC Microbiol. 10:204. doi: 10.1186/1471-2180-10-204
67. Krishnakumar, S., Durai, D. A., Wangikar, P. P., and Viswanathan, G. A. (2013). SHARP: genome-scale identification of gene-protein-reaction associations in cyanobacteria. Photosyn. Res. 118, 181-190. doi: 10.1007/s11120-013-9910-6
68. Kunert, A., Vinnemeier, J., Erdmann, N., and Hagemann, M. (2003). Repression by Fur is not the main mechanism controlling the iron-inducible isiAB operon in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol. Lett. 227, 255-262. doi: 10.1016/S0378-1097(03)00689-X
69. Langlois, R. J., Hummer, D., and Laroche, J. (2008). Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean. Appl. Environ. Microbiol. 74, 1922-1931. doi: 10.1128/AEM.01720-07
70. Li, H., Singh, A. K., McIntyre, L. M., and Sherman, L. A. (2004). Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803. J. Bacteriol. 186, 3331-3345. doi: 10.1128/JB.186.11.3331-3345.2004
71. Li, W. K., Rao, D. V., Harrison, W. G., Smith, J. C., Cullen, J. J., Irwin, B., et al. (1983). Autotrophic picoplankton in the tropical ocean. Science 219, 292-295. doi: 10.1126/science.219.4582.292
72. Licata, L., Briganti, L., Peluso, D., Perfetto, L., Iannuccelli, M., Galeota, E., et al. (2012). MINT, the molecular interaction database: 2012 update. Nucleic Acids Res. 40, D857-D861. doi: 10.1093/nar/gkr930
73. Lindell, D., Jaffe, J. D., Coleman, M. L., Futschik, M. E., Axmann, I. M., Rector, T., et al. (2007). Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83-86. doi: 10.1038/nature06130
74. Liu, L., Li, Y., Li, S., Hu, N., He, Y., Pong, R., et al. (2012). Comparison of Next-Generation Sequencing Systems. J. Biomed. Biotechnol. 2012, 11. doi: 10.1155/2012/251364
75. Lopes, C. T., Franz, M., Kazi, F., Donaldson, S. L., Morris, Q., and Bader, G. D. (2010). Cytoscape Web: an interactive web-based network browser. Bioinformatics 26, 2347-2348. doi: 10.1093/bioinformatics/btq430
76. Lorenz, P., and Eck, J. (2005). Metagenomics and industrial applications. Nat. Rev. Microbiol. 3, 510-516. doi: 10.1038/nrmicro1161
77. Ludwig, M., and Bryant, D. A. (2012). Synechococcus sp. strain PCC 7002 transcriptome: acclimation to temperature, salinity, oxidative stress and mixotrophic growth conditions. Front. Microbiol. 3:354. doi: 10.3389/fmicb.2012.00354
78. Ma, C.-Y., Lin, S.-H., Lee, C.-C., Tang, C. Y., Berger, B., and Liao, C.-S. (2013). Reconstruction of phyletic trees by global alignment of multiple metabolic networks. BMC Bioinformatics 14:S12. doi: 10.1186/1471-2105-14-S2-S12
79. Maarleveld, T. R., Boele, J., Bruggeman, F. J., and Teusink, B. (2014). A data integration and visualization resource for the metabolic network of Synechocystis sp. PCC 6803. Plant Physiol. 164, 1111-1121. doi: 10.1104/pp.113.224394
80. Malmstrom, R. R., Rodrigue, S., Huang, K. H., Kelly, L., Kern, S. E., Thompson, A., et al. (2013). Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis. ISME J. 7, 184-198. doi: 10.1038/ismej.2012.89
81. Mao, X., Chen, X., Zhang, Y., Pangle, S., and Xu, Y. (2012). CINPER: an interactive web system for pathway prediction for prokaryotes. PLoS ONE 7:e51252. doi: 10.1371/journal.pone.0051252
82. Markowitz, V. M., Chen, I.-M. A., Palaniappan, K., Chu, K., Szeto, E., Grechkin, Y., et al. (2012). IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res. 40, D115-D122. doi: 10.1093/nar/gkr1044
83. Martiny, A. C., Huang, Y., and Li, W. (2009a). Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions. Environ. Microbiol. 11, 1340-1347. doi: 10.1111/j.1462-2920.2009.01860.x
84. Martiny, A. C., Kathuria, S., and Berube, P. M. (2009b). Widespread metabolic potential for nitrite and nitrate assimilation among Prochlorococcus ecotypes. Proc. Natl. Acad. Sci. U.S.A. 106, 10787-10792. doi: 10.1073/pnas.0902532106
85. Massar, J. P., Travers, M., Elhai, J., and Shrager, J. (2005). BioLingua: a programmable knowledge environment for biologists. Bioinformatics 21, 199-207. doi: 10.1093/bioinformatics/bth465
86. Massé, E., Escorcia, F. E., and Gottesman, S. (2003). Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 17, 2374-2383. doi: 10.1101/gad.1127103
87. Masse, E., and Gottesman, S. (2002). A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 99, 4620-4625. doi: 10.1073/pnas.032066599
88. McDermott, J. E., Oehmen, C. S., McCue, L. A., Hill, E., Choi, D. M., Stockel, J., et al. (2011). A model of cyclic transcriptomic behavior in the cyanobacterium Cyanothece sp. ATCC 51142. Mol. Biosyst. 7, 2407-2418. doi: 10.1039/c1mb05006k
89. Michaut, M., Kerrien, S., Montecchi-Palazzi, L., Chauvat, F., Cassier-Chauvat, C., Aude, J. C., et al. (2008). InteroPORC: automated inference of highly conserved protein interaction networks. Bioinformatics 24, 1625-1631. doi: 10.1093/bioinformatics/btn249
90. Mitschke, J., Georg, J., Scholz, I., Sharma, C. M., Dienst, D., Bantscheff, J., et al. (2011). An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc. Natl. Acad. Sci. U.S.A. 108, 2124-2129. doi: 10.1073/pnas.1015154108
91. Montagud, A., Zelezniak, A., Navarro, E., De Córdoba, P. F., Urchueguía, J. F., and Patil, K. R. (2011). Flux coupling and transcriptional regulation within the metabolic network of the photosynthetic bacterium Synechocystis sp. PCC6803. Biotechnol. J. 6, 330-342. doi: 10.1002/biot.201000109
92. Moore, L. R., Rocap, G., and Chisholm, S. W. (1998). Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393, 464-467. doi: 10.1038/30965
93. Nakamura, Y., Kaneko, T., Hirosawa, M., Miyajima, N., and Tabata, S. (1998). CyanoBase, a www database containing the complete nucleotide sequence of the genome of Synechocystis sp. strain PCC6803. Nucleic Acids Res. 26, 63-67. doi: 10.1093/nar/26.1.63
94. Nakao, M., Okamoto, S., Kohara, M., Fujishiro, T., Fujisawa, T., Sato, S., et al. (2010). CyanoBase: the cyanobacteria genome database update 2010. Nucleic Acids Res. 38, D379-D381. doi: 10.1093/nar/gkp915
95. Nelson, N. (2011). Photosystems and global effects of oxygenic photosynthesis. Biochim. Biophys. Acta 1807, 856-863. doi: 10.1016/j.bbabio.2010.10.011
96. Ngounou Wetie, A., Sokolowska, I., Woods, A., Roy, U., Deinhardt, K., and Darie, C. (2014). Protein-protein interactions: switch from classical methods to proteomics and bioinformatics-based approaches. Cell. Mol. Sci. 71, 205-228. doi: 10.1007/s00018-013-1333-1
97. Nixon, P. J., Michoux, F., Yu, J., Boehm, M., and Komenda, J. (2010). Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. 106, 1-16. doi: 10.1093/aob/mcq059
98. Nogales, J., Gudmundsson, S., Knight, E. M., Palsson, B. O., and Thiele, I. (2012). Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. Proc. Natl. Acad. Sci. U.S.A. 109, 2678-2683. doi: 10.1073/pnas.1117907109
99. Ntzani, E. E., and Ioannidis, J. P. (2003). Predictive ability of DNA microarrays for cancer outcomes and correlates: an empirical assessment. Lancet 362, 1439-1444. doi: 10.1016/S0140-6736(03)14686-7
100. Orchard, S., Ammari, M., Aranda, B., Breuza, L., Briganti, L., Broackes-Carter, F., et al. (2014). The MIntAct project-IntAct as a common curation platform for 11 molecular interaction databases. Nucleic Acids Res. 42, D358-D363. doi: 10.1093/nar/gkt1115
101. Ostrowski, M., Mazard, S., Tetu, S. G., Phillippy, K., Johnson, A., Palenik, B., et al. (2010). PtrA is required for coordinate regulation of gene expression during phosphate stress in a marine Synechococcus. ISME J. 4, 908-921. doi: 10.1038/ismej.2010.24
102. Ow, S. Y., and Wright, P. C. (2009). Current trends in high throughput proteomics in cyanobacteria. FEBS Lett. 583, 1744-1752. doi: 10.1016/j.febslet.2009.03.062
103. Palenik, B., Brahamsha, B., Larimer, F. W., Land, M., Hauser, L., Chain, P., et al. (2003). The genome of a motile marine Synechococcus. Nature 424, 1037-1042. doi: 10.1038/nature01943
104. Palenik, B., Ren, Q., Tai, V., and Paulsen, I. T. (2009). Coastal Synechococcus metagenome reveals major roles for horizontal gene transfer and plasmids in population diversity. Environ. Microbiol. 11, 349-359. doi: 10.1111/j.1462-2920.2008.01772.x
105. Partensky, F., and Garczarek, L. (2010). Prochlorococcus: advantages and limits of minimalism. Ann. Rev. Mar. Sci. 2, 305-331. doi: 10.1146/annurev-marine-120308-081034
106. Partensky, F., Hess, W. R., and Vaulot, D. (1999). Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106-127.
107. Paul, S., Dutta, A., Bag, S. K., Das, S., and Dutta, C. (2010). Distinct, ecotype-specific genome and proteome signatures in the marine cyanobacteria Prochlorococcus. BMC Genomics 11:103. doi: 10.1186/1471-2164-11-103
108. Postier, B. L., Wang, H. L., Singh, A., Impson, L., Andrews, H. L., Klahn, J., et al. (2003). The construction and use of bacterial DNA microarrays based on an optimized two-stage PCR strategy. BMC Genomics 4:23. doi: 10.1186/1471-2164-4-23
109. Prommeenate, P., Lennon, A. M., Markert, C., Hippler, M., and Nixon, P. J. (2004). Subunit composition of NDH-1 complexes of Synechocystis sp. PCC 6803. J. Biol. Chem. 279, 28165-28173. doi: 10.1074/jbc.M401107200
110. Quek, L.-E., Wittmann, C., Nielsen, L., and Kromer, J. (2009). OpenFLUX: efficient modelling software for 13C-based metabolic flux analysis. Microb. Cell Fact. 8:25. doi: 10.1186/1475-2859-8-25
111. Reddy, K. J., Haskell, J. B., Sherman, D. M., and Sherman, L. A. (1993). Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus cyanothece. J. Bacteriol. 175, 1284-1292.
112. Rees, C., Demeter, J., Matese, J., Botstein, D., and Sherlock, G. (2004). GeneXplorer: an interactive web application for microarray data visualization and analysis. BMC Bioinformatics 5:141. doi: 10.1186/1471-2105-5-141
113. Rocap, G., Larimer, F. W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N. A., et al. (2003). Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424, 1042-1047. doi: 10.1038/nature01947
114. Rotilio, D., Della Corte, A., D'Imperio, M., Coletta, W., Marcone, S., Silvestri, C., et al. (2012). Proteomics: bases for protein complexity understanding. Thromb. Res. 129, 257-262. doi: 10.1016/j.thromres.2011.12.035
115. Ruffing, A. (2013). RNA-Seq analysis and targeted mutagenesis for improved free fatty acid production in an engineered cyanobacterium. Biotechnol. Biofuels 6, 1-15. doi: 10.1186/1754-6834-6-113
116. Ruffing, A. M. (2011). Engineered cyanobacteria: teaching an old bug new tricks. Bioeng. Bugs 2, 136-149. doi: 10.4161/bbug.2.3.15285
117. Rusch, D. B., Halpern, A. L., Sutton, G., Heidelberg, K. B., Williamson, S., Yooseph, S., et al. (2007). The Sorcerer II global ocean sampling expedition: northwest atlantic through eastern tropical pacific. PLoS Biol. 5:e77. doi: 10.1371/journal.pbio.0050077
118. Rusch, D. B., Martiny, A. C., Dupont, C. L., Halpern, A. L., and Venter, J. C. (2010). Characterization of Prochlorococcus clades from iron-depleted oceanic regions. Proc. Natl. Acad. Sci. U.S.A. 107, 16184-16189. doi: 10.1073/pnas.1009513107
119. Rustici, G., Kolesnikov, N., Brandizi, M., Burdett, T., Dylag, M., Emam, I., et al. (2013). ArrayExpress update-trends in database growth and links to data analysis tools. Nucleic Acids Res. 41, D987-D990. doi: 10.1093/nar/gks1174
120. Salwinski, L., Miller, C. S., Smith, A. J., Pettit, F. K., Bowie, J. U., and Eisenberg, D. (2004). The database of interacting proteins: 2004 update. Nucleic Acids Res. 32, D449-D451. doi: 10.1093/nar/gkh086
121. Sandh, G., Ran, L., Xu, L., Sundqvist, G., Bulone, V., and Bergman, B. (2011). Comparative proteomic profiles of the marine cyanobacterium Trichodesmium erythraeum IMS101 under different nitrogen regimes. Proteomics 11, 406-419. doi: 10.1002/pmic.201000382
122. Sato, S., Shimoda, Y., Muraki, A., Kohara, M., Nakamura, Y., and Tabata, S. (2007). A large-scale protein-protein interaction analysis in Synechocystis sp. PCC6803. DNA Res. 14, 207-216. doi: 10.1093/dnares/dsm021
123. Scanlan, D. J., Ostrowski, M., Mazard, S., Dufresne, A., Garczarek, L., Hess, W. R., et al. (2009). Ecological genomics of marine picocyanobacteria. Microbiol. Mol. Biol. Rev. 73, 249-299. doi: 10.1128/MMBR.00035-08
124. Schmidt, E. W., Nelson, J. T., Rasko, D. A., Sudek, S., Eisen, J. A., Haygood, M. G., et al. (2005). Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc. Natl. Acad. Sci. U.S.A. 102, 7315-7320. doi: 10.1073/pnas.0501424102
125. Schriek, S., Kahmann, U., Staiger, D., Pistorius, E. K., and Michel, K. P. (2009). Detection of an L-amino acid dehydrogenase activity in Synechocystis sp. PCC 6803. J. Exp. Bot. 60, 1035-1046. doi: 10.1093/jxb/ern352
126. Schwarz, D., Orf, I., Kopka, J., and Hagemann, M. (2013). Recent applications of metabolomics toward cyanobacteria. Metabolites 3, 72-100. doi: 10.3390/metabo3010072
127. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., et al. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504. doi: 10.1101/gr.1239303
128. Shastri, A. A., and Morgan, J. A. (2005). Flux balance analysis of photoautotrophic metabolism. Biotechnol. Prog. 21, 1617-1626. doi: 10.1021/bp050246d
129. Shcolnick, S., Summerfield, T. C., Reytman, L., Sherman, L. A., and Keren, N. (2009). The Mechanism of iron homeostasis in the unicellular cyanobacterium Synechocystis sp. PCC 6803 and its relationship to oxidative stress. Plant Physiol. 150, 2045-2056. doi: 10.1104/pp.109.141853
130. Shi, T., and Falkowski, P. G. (2008). Genome evolution in cyanobacteria: the stable core and the variable shell. Proc. Natl. Acad. Sci. U.S.A. 105, 2510-2515. doi: 10.1073/pnas.0711165105
131. Shi, Y., Tyson, G. W., and Delong, E. F. (2009). Metatranscriptomics reveals unique microbial small RNAs in the ocean/'s water column. Nature 459, 266-269. doi: 10.1038/nature08055
132. Shih, P. M., Wu, D., Latifi, A., Axen, S. D., Fewer, D. P., Talla, E., et al. (2013). Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. U.S.A. 110, 1053-1058. doi: 10.1073/pnas.1217107110
133. Singh, A. K., Elvitigala, T., Bhattacharyya-Pakrasi, M., Aurora, R., Ghosh, B., and Pakrasi, H. B. (2008). Integration of carbon and nitrogen metabolism with energy production is crucial to light acclimation in the cyanobacterium Synechocystis. Plant Physiol. 148, 467-478. doi: 10.1104/pp.108.123489
134. Singh, A. K., Elvitigala, T., Cameron, J. C., Ghosh, B. K., Bhattacharyya-Pakrasi, M., and Pakrasi, H. B. (2010). Integrative analysis of large scale expression profiles reveals core transcriptional response and coordination between multiple cellular processes in a cyanobacterium. BMC Syst. Biol. 4:105. doi: 10.1186/1752-0509-4-105
135. Stanley, D. N., Raines, C. A., and Kerfeld, C. A. (2013). Comparative analysis of 126 cyanobacterial genomes reveals evidence of functional diversity among homologs of the redox-regulated CP12 protein. Plant Physiol. 161, 824-835. doi: 10.1104/pp.112.210542
136. Steele, E., and Tucker, A. (2008). Consensus and Meta-analysis regulatory networks for combining multiple microarray gene expression datasets. J. Biomed. Inform. 41, 914-926. doi: 10.1016/j.jbi.2008.01.011
137. Steglich, C., Futschik, M. E., Lindell, D., Voss, B., Chisholm, S. W., and Hess, W. R. (2008). The Challenge of regulation in a minimal photoautotroph: non-coding RNAs in Prochlorococcus. PLoS Genet. 4:e1000173. doi: 10.1371/journal.pgen.1000173
138. Stockel, J., Jacobs, J. M., Elvitigala, T. R., Liberton, M., Welsh, E. A., Polpitiya, A. D., et al. (2011). Diurnal rhythms result in significant changes in the cellular protein complement in the cyanobacterium cyanothece 51142. PLoS ONE 6:e16680. doi: 10.1371/journal.pone.0016680
139. Stockel, J., Welsh, E. A., Liberton, M., Kunnvakkam, R., Aurora, R., and Pakrasi, H. B. (2008). Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes. Proc. Natl. Acad. Sci. U.S.A. 105, 6156-6161. doi: 10.1073/pnas.0711068105
140. Stuart, R. K., Dupont, C. L., Johnson, D. A., Paulsen, I. T., and Palenik, B. (2009). Coastal strains of marine synechococcus species exhibit increased tolerance to copper shock and a distinctive transcriptional response relative to those of open-ocean strains. Appl. Environ. Microbiol. 75, 5047-5057. doi: 10.1128/AEM.00271-09
141. Su, Z., Mao, F., Dam, P., Wu, H., Olman, V., Paulsen, I. T., et al. (2006). Computational inference and experimental validation of the nitrogen assimilation regulatory network in cyanobacterium Synechococcus sp. WH 8102. Nucleic Acids Res. 34, 1050-1065. doi: 10.1093/nar/gkj496
142. Su, Z. C., Olman, V., Mao, F. L., and Xu, Y. (2005). Comparative genomics analysis of NtcA regulons in cyanobacteria: regulation of nitrogen assimilation and its coupling to photosynthesis. Nucleic Acids Res. 33, 5156-5171. doi: 10.1093/nar/gki817
143. Sun, J., Heck, D., Xu, W., Chitnis, V., and Chitnis, P. (1999). "Abundance of photosystem I proteins in cyanobacteria and chloroplasts," in The Chloroplast: From Molecular Biology to Biotechnology, eds J. Argyroudi-Akoyunoglou and H. Senger (Netherlands: Springer), 227-232. doi: 10.1007/978-94-011-4788-0_36
144. Sun, R., Fu, X., Guo, F., Ma, Z., Goulbourne, C., Jiang, M., et al. (2009). A strategy for meta-analysis of short time series microarray datasets. Front. Biosci. (Landmark Ed) 14, 4058-4070. doi: 10.2741/3512
145. Suzuki, I., Kanesaki, Y., Mikami, K., Kanehisa, M., and Murata, N. (2001). Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol. Microbiol. 40, 235-244. doi: 10.1046/j.1365-2958.2001.02379.x
146. Tanaka, R., Rothbart, M., Oka, S., Takabayashi, A., Takahashi, K., Shibata, M., et al. (2010). LIL3, a light-harvesting-like protein, plays an essential role in chlorophyll and tocopherol biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 107, 16721-16725. doi: 10.1073/pnas.1004699107
147. Tetu, S. G., Brahamsha, B., Johnson, D. A., Tai, V., Phillippy, K., Palenik, B., et al. (2009). Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. ISME J. 3, 835-849. doi: 10.1038/ismej.2009.31
148. Thompson, A. W., Huang, K., Saito, M. A., and Chisholm, S. W. (2011). Transcriptome response of high- and low-light-adapted Prochlorococcus strains to changing iron availability. ISME J. 5, 1580-1594. doi: 10.1038/ismej.2011.49
149. Thompson, C., Silva, G. Z., Vieira, N., Edwards, R., Vicente, A., and Thompson, F. (2013). Genomic taxonomy of the genus prochlorococcus. Microb. Ecol. 66, 752-762. doi: 10.1007/s00248-013-0270-8
150. Toepel, J., Welsh, E., Summerfield, T. C., Pakrasi, H. B., and Sherman, L. A. (2008). Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth. J. Bacteriol. 190, 3904-3913. doi: 10.1128/JB.00206-08
151. Tolonen, A. C., Aach, J., Lindell, D., Johnson, Z. I., Rector, T., Steen, R., et al. (2006). Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol. Syst. Biol. 2:53. doi: 10.1038/msb4100087
152. Vermaas, W. F. (2001). "Photosynthesis and respiration in cyanobacteria," in eLS (Chichester: John Wiley and Sons Ltd). doi: 10.1038/npg.els.0001670
153. Vijayan, V., Jain, I., and O'Shea, E. (2011). A high resolution map of a cyanobacterial transcriptome. Genome Biol. 12:R47. doi: 10.1186/gb-2011-12-5-r47
154. Voigt, K., Sharma, C. M., Mitschke, J., Joke Lambrecht, S., Voss, B., Hess, W. R., et al. (2014). Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity. ISME J. doi: 10.1038/ismej.2014.57. [Epub ahead of print].
155. Vu, T. T., Stolyar, S. M., Pinchuk, G. E., Hill, E. A., Kucek, L. A., Brown, R. N., et al. (2012). Genome-scale modeling of light-driven reductant partitioning and carbon fluxes in diazotrophic unicellular cyanobacterium Cyanothece sp. ATCC 51142. PLoS Comput. Biol. 8:1002460. doi: 10.1371/journal.pcbi.1002460
156. Waldbauer, J. R., Rodrigue, S., Coleman, M. L., and Chisholm, S. W. (2012). Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle. PLoS ONE 7:e43432. doi: 10.1371/journal.pone.0043432
157. Wallach, T., Schellenberg, K., Maier, B., Kalathur, R. K. R., Porras, P., Wanker, E. E., et al. (2013). Dynamic circadian protein-protein interaction networks predict temporal organization of cellular functions. PLoS Genet. 9:e1003398. doi: 10.1371/journal.pgen.1003398
158. Wang, B., Wang, J., Zhang, W., and Meldrum, D. R. (2012). Application of synthetic biology in cyanobacteria and algae. Front. Microbiol. 3:344. doi: 10.3389/fmicb.2012.00344
159. Welsh, E. A., Liberton, M., Stockel, J., Loh, T., Elvitigala, T., Wang, C., et al. (2008). The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle. Proc. Natl. Acad. Sci. U.S.A. 105, 15094-15099. doi: 10.1073/pnas.0805418105
160. West, N. J., Lebaron, P., Strutton, P. G., and Suzuki, M. T. (2011). A novel clade of Prochlorococcus found in high nutrient low chlorophyll waters in the South and Equatorial Pacific Ocean. ISME J. 5, 933-944. doi: 10.1038/ismej.2010.186
161. West, N. J., Schonhuber, W. A., Fuller, N. J., Amann, R. I., Rippka, R., Post, A. F., et al. (2001). Closely related Prochlorococcus genotypes show remarkably different depth distributions in two oceanic regions as revealed by in situ hybridization using 16S rRNA-targeted oligonucleotides. Microbiology 147, 1731-1744.
162. Williams, A. B., and Jacobs, R. S. (1993). A marine natural product, patellamide D, reverses multidrug resistance in a human leukemic cell line. Cancer Lett. 71, 97-102. doi: 10.1016/0304-3835(93)90103-G
163. Winter, G., and Kromer, J. O. (2013). Fluxomics-connecting 'omics analysis and phenotypes. Environ. Microbiol. 15, 1901-1916. doi: 10.1111/1462-2920.12064
164. Yang, Q., Pando, B. F., Dong, G., Golden, S. S., and Van Oudenaarden, A. (2010). Circadian gating of the cell cycle revealed in single cyanobacterial cells. Science 327, 1522-1526. doi: 10.1126/science.1181759
165. Yao, D., Kieselbach, T., Komenda, J., Promnares, K., Prieto, M. A., Tichy, M., et al. (2007). Localization of the small CAB-like proteins in photosystem II. J. Biol. Chem. 282, 267-276. doi: 10.1074/jbc.M605463200
166. Yu, D., Kim, M., Xiao, G., and Hwang, T. H. (2013). Review of biological network data and its applications. Genomics Inform. 11, 200-210. doi: 10.5808/GI.2013.11.4.200
167. Zehr, J. P., Bench, S. R., Carter, B. J., Hewson, I., Niazi, F., Shi, T., et al. (2008). Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322, 1110-1112. doi: 10.1126/science.1165340
168. Zehr, J. P., Bench, S. R., Mondragon, E. A., McCarren, J., and Delong, E. F. (2007). Low genomic diversity in tropical oceanic N2-fixing cyanobacteria. Proc. Natl. Acad. Sci. U.S.A. 104, 17807-17812. doi: 10.1073/pnas.0701017104
169. Zhang, A., Sun, H., Wang, P., Han, Y., and Wang, X. (2012). Modern analytical techniques in metabolomics analysis. Analyst 137, 293-300. doi: 10.1039/c1an15605e
170. Zhang, S. Y., and Bryant, D. A. (2011). The tricarboxylic acid cycle in cyanobacteria. Science 334, 1551-1553. doi: 10.1126/science.1210858
171. Zhang, Z., Pendse, N. D., Phillips, K. N., Cotner, J. B., and Khodursky, A. (2008). Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. BMC Genomics 9:344. doi: 10.1186/1471-2164-9-344
172. Zinser, E. R., Lindell, D., Johnson, Z. I., Futschik, M. E., Steglich, C., Coleman, M. L., et al. (2009). Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus. PLoS ONE 4:e5135. doi: 10.1371/journal.pone.0005135