Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability

Molecular Systems Biology

Volumn 2, Issue , 2006, Pages

  Tolonen, Andrew C ^a   Aach, John ^b   Lindell, Debbie ^c   Johnson, Zackary I ^d   Rector, Trent ^b   Steen, Robert ^b   Church, George M ^b   Chisholm, Sallie W ^c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d UNIVERSITY OF HAWAII   (United States)

Author keywords

Cyanobacteria; Interstrain; Nitrogen; Prochlorococcus; Transcription

Indexed keywords

AMMONIA; CARBON; NITROGEN; BACTERIAL PROTEIN; CARRIER PROTEIN; NITROGEN REGULATORY PROTEIN; PIID REGULATORY PROTEIN, BACTERIA; SIGMA FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL FLORA; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBON METABOLISM; CHLOROPHYLL FLUORESCENCE; COMMUNITY ECOLOGY; CONTROLLED STUDY; CULTURE MEDIUM; ECOTYPE; ENVIRONMENTAL STRESS; GENE EXPRESSION REGULATION; NITROGEN AVAILABILITY; NITROGEN UTILIZATION; NONHUMAN; PHOTOCHEMICAL EFFICIENCY; PHOTOSYSTEM II; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROCHLOROCOCCUS; PROCHLOROCOCCUS MED4; PROCHLOROCOCCUS MIT9313; REGULATORY MECHANISM; REGULON; SEA; SPECIES COMPARISON; BIOSYNTHESIS; COMPARATIVE STUDY; ECOLOGY; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; OPERON; PHYSIOLOGY; RADIATION EXPOSURE; SPECIES DIFFERENCE;

CYANOBACTERIA; PROCHLOROCOCCUS;

BACTERIAL PROTEINS; CARBON; CARRIER PROTEINS; ECOLOGY; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; NITROGEN; OCEANS AND SEAS; OPERON; PHOTOSYSTEM II PROTEIN COMPLEX; PII NITROGEN REGULATORY PROTEINS; PROCHLOROCOCCUS; SIGMA FACTOR; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; WATER MICROBIOLOGY;

EID: 33750741940     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb4100087     Document Type: Article

References (68)

1. Allen MM (1984) Cyanobacterial cell inclusions. Annu Rev Microbiol 38: 1-25
2. Baldi P, Long AD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17: 509-519
3. Bertilsson S, Berglund O, Karl DM, Chisholm SW (2003) Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol Oceanogr 48: 1721-1731
4. Brahamsha B, Haselkorn R (1992) Identification of multiple RNA polymerase sigma factor homologs in the cyanobacterium Anabaena sp. strain PCC 7120: cloning, expression, and inactivation of the sigB and sigC genes. J Bacteriol 174: 7273-7282
5. Bulyk ML, Huang X, Choo Y, Church GM (2001) Exploring the DNA-binding specificities of zinc fingers with DNA microarrays. Proc Natl Acad Sci USA 98: 7158-7163
6. Campbell L, Landry MR, Constantinou J, Nolla HA, Brown SL, Liu H, Caron DA (1998) Response of microbial community structure to environmental forcing in the Arabian Sea. Deep-Sea Res II 45: 2301-2325
7. Caslake LF, Gruber TM, Bryant DA (1997) Expression of two alternative sigma factors of Synechococcus sp.strain PCC 7002 is modulated by carbon and nitrogen stress. Microbiology 143 (Part 12): 3807-3818
8. Choe SE, Boutros M, Michelson AM, Church GM, Halfon MS (2005) Preferred analysis methods for Affymetrix GeneChips revealed by a wholly defined control dataset. Genome Biol 6: R16
9. El Alaoui S, Diez J, Humanes L, Toribio F, Partensky F, Garcia-Fernandez JM (2001) In vivo regulation of glutamine synthetase activity in the marine chlorophyll b-containing cyanobacterium Prochlorococcus sp strain PCC 9511 (oxyphotobacteria). Appl Environ Microbiol 67: 2202-2207
10. El Alaoui S, Diez J, Toribio F, Gomez-Baena G, Dufresne A, Garcia-Fernandez JM (2003) Glutamine synthetase from the marine cyanobacteria Prochlorococcus spp.: characterization, phylogeny and response to nutrient limitation. Environ Microbiol 5: 412-423
11. Forchhammer K (1999) The PII protein in Synechococcus PCC 7942 senses and signals 2-oxoglutarate under ATP-replete conditions. In The Phototrophic Prokaryotes, Peschek GA, Löeffelhardt W, Schmetterer G (eds) pp 549-553. New York, NY: Kluwer Academic
12. II signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev 28: 319-333
13. II signal-transduction protein from Escherichia coli. Eur J Biochem 244: 869-875
14. II (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 177: 2033-2040
15. II protein) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 35: 723-734
16. Garcia-Fernandez JM, de Marsac NT, Diez J (2004) Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol Mol Biol Rev 68: 630-638
17. Gibbons FD, Roth FP (2002) Judging the quality of gene expression-based clustering methods using gene annotation. Genome Res 12: 1574-1581
18. 2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56: 99-131
19. Graziano LM, Geider RJ, Li WKW, Olaizola M (1996) Nitrogen limitation of North Atlantic phytoplankton: analysis of physiological condition in nutrient enrichment experiments. Aquatic Microb Ecol 11: 53-64
20. Havaux M, Guedeney G, He Q, Grossman AR (2003) Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. Biochim Biophys Acta 1557: 21-33
21. He Q, Dolganov N, Bjorkman O, Grossman AR (2001) The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276: 306-314
22. Herrero A, Muro-Pastor AM, Flores E (2001) Nitrogen control in cyanobacteria. J Bacteriol 183: 411-425
23. II regulates both inorganic carbon and nitrate uptake and is modified by a redox signal in Synechocystis PCC 6803. FEBS Lett 463: 216-220
24. Hughes JD, Estep PW, Tavazoie S, Church GM (2000) Computational identification of cis-regulatory elements associated with functionally coherent groups of genes in Saccharomyces cerevisiae. J Mol Biol 296: 1205-1214
25. Jiang F, Mannervik B, Bergman B (1997) Evidence for redox regulation of the transcription factor NtcA, acting both as an activator and a repressor, in the cyanobacterium Anabaena PCC 7120. Biochem J 327 (Part 2): 513-517
26. Jiang FY, Wisen S, Widersten M, Bergman B, Mannervik B (2000) Examination of the transcription factor NtcA-binding motif by in vitro selection of DNA sequences from a random library. J Mol Biol 301: 783-793
27. Johnson ZI (2004) Description and application of the background irradiance gradient-single turnover fluorometer (BIG-STf). Mar Ecol Prog Ser 283: 73-80
28. Johnson ZI, Zinser ER, Coe A, McNulty NP, Malcolm E, Woodward E, Chisholm SW (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311: 1737-1740
29. Kolber ZS, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367: 88-106
30. II (glnB) and influences its phosphorylation level in response to nitrogen and carbon supplies in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 181: 2697-2702
31. Lee TI, Rinaldi NJ, Robert F, Odom DT, Bar-Joseph Z, Gerber GK, Hannett NM, Harbison CT, Thompson CM, Simon I, Zeitlinger J, Jennings EG, Murray HL, Gordon DB, Ren B, Wyrick JJ, Tagne JB, Volkert TL, Fraenkel E, Gifford DK, Young RA (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298: 799-804
32. Li WKW (1994) Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: measurements from flow cytometric sorting. Limnol Oceanogr 39: 169-175
33. Lindell D, Erdner D, Marie D, Prasil O, Koblizek M, Le Gall F, Rippka R, Partensky F, Scanlan DJ, Post AF (2002) The nitrogen stress response of Prochlorococcus strain PCC 9511 (Oxyphotobacteria) involves contrasting regulation of ntcA and amt1. J Phycol 38: 1113-1124
34. Lindell D, Post AF (2001) Ecological aspects of ntcA gene expression and its use as an indicator of the nitrogen status of marine Synechococcus spp. Appl Environ Microbiol 67: 3340-3349
35. Lipschultz F (2001) A time-series assessment of the nitrogen cycle at BATS. Deep-Sea Res II 48: 1897-1924
36. Luque I, Flores E, Herrero A (1994) Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13: 2862-2869
37. Marcotte EM, Pellegrini M, Ng HL, Rice DW, Yeates TO, Eisenberg D (1999) Detecting protein function and protein-protein interactions from genome sequences. Science 285: 751-753
38. Moore LR, Chisholm SW (1999) Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol Oceanogr 44: 628-638
39. Moore LR, Post AF, Rocap G, Chisholm SW (2002) Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol Oceanogr 47: 989-996
40. Moore LR, Rocap G, Chisholm SW (1998) Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464-467
41. Muro-Pastor MI, Reyes JC, Florencio FJ (1996) The NADP + -isocitrate dehydrogenase gene (icd) is nitrogen regulated in cyanobacteria. J Bacteriol 178: 4070-4076
42. Muro-Pastor MI, Reyes JC, Florencio FJ (2001) Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J Biol Chem 276: 38320-38328
43. Muro-Pastor MI, Reyes JC, Florencio FJ (2005) Ammonium assimilation in cyanobacteria. Photosynth Res 83: 135-150
44. Nakamura Y, Kaneko T, Hirosawa M, Miyajima N, 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
45. II signal transduction proteins. Trends Microbiol 8: 172-179
46. 15N tracer studies of the primary nitrite maximum. J Mar Res 39: 1033-1051
47. Palinska KA, Jahns T, Rippka R, Tandeau De Marsac N (2000) Prochlorococcus marinus strain PCC 9511, a picoplanktonic cyanobacterium, synthesizes the smallest urease. Microbiology 146 (Part 12): 3099-3107
48. Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127
49. II (glnB gene product) on NtcA-dependent genes in Synechococcus sp. PCC 7942. FEBS Lett 543: 42-46
50. Pellegrini M, Marcotte EM, Thompson MJ, Eisenberg D, Yeates TO (1999) Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc Natl Acad Sci USA 96: 4285-4288
51. Ramasubramanian TS, Wei TF, Golden JW (1994) Two Anabaena Sp strain Pcc 7120 DNA-binding factors interact with vegetative cell-specific and heterocyst-specific genes. J Bacteriol 176: 1214-1223
52. Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46: 205-221
53. Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047
54. Rocap G, Distel DL, Waterbury JB, Chisholm SW (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68: 1180-1191
55. Roth FP, Hughes JD, Estep PW, Church GM (1998) Finding DNA regulatory motifs within unaligned non-coding sequences by whole-genome mRNA quantitation. Nat Biotechnol 16: 939-945
56. Sauer J, Gorl M, Forchhammer K (1999) Nitrogen starvation in Synechococcus PCC 7942: involvement of glutamine synthetase and NtcA in phycobiliprotein degradation and survival. Arch Microbiol 172: 247-255
57. Schwarz R, Forchhammer K (2005) Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiology 151 (Part 8): 2503-2514
58. Su Z, Mao F, Dam P, Wu H, Olman V, Paulson IT, Palenik B, Xu Y (2006) Computational inference and experimental validation of the nitrogen assimilation regulatory network in cyanobacterium Synechococcus sp. WH 8102. Nucleic Acids Res 34: 1050-1065
59. Su Z, Olman V, Mao F, 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
60. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545-15550
61. Tandeau de Marsac N, Lee HM (1999) Regulation of carbon and nitrogen metabolism in the unicellular cyanobacterium Synechococcus spp. In The Phototrophic Prokaryotes, Peschek GA, Löeffelhardt W, Schmetterer G (eds) pp 539-548. New York, NY: Kluwer Academic
62. Tanigawa R, Shirokane M, Maeda Si S, Omata T, Tanaka K, Takahashi H (2002) Transcriptional activation of NtcA-dependent promoters of Synechococcus sp. PCC 7942 by 2-oxoglutarate in vitro. Proc Natl Acad Sci USA 99: 4251-4255
63. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2003) The COG database: an updated version includes eukaryotes. BMC Bioinform 4: 41
64. Valera DE, Harrison PJ (1999) Seasonal variability in nitrogenous nutrition of phytoplankton assemblages in the northeastern subarctic Pacific Ocean. Deep-Sea Res II 46: 2505-2538
65. Valladares A, Montesinos ML, Herrero A, Flores E (2002) An ABC-type, high-affinity urea permease identified in cyanobacteria. Mol Microbiol 43: 703-715
66. Vazquez-Bermudez MF, Herrero A, Flores E (2002) 2-Oxoglutarate increases the binding affinity of the NtcA (nitrogen control) transcription factor for the Synechococcus glnA promoter. FEBS Lett 512: 71-74
67. Vega-Palas MA, Madueño F, Herrero A, Flores E (1990) Identification and cloning of a regulatory gene for nitrogen assimilation in the cyanobacterium synechococcus sp. strain PCC 7942. J Bacteriol 172: 643-647
68. West NJ, Schonhuber WA, Fuller NJ, Amann RI, Rippka R, Post AF, Scanlan DJ (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 (Part 7): 1731-1744