PtrA is required for coordinate regulation of gene expression during phosphate stress in a marine Synechococcus

ISME Journal

Volumn 4, Issue 7, 2010, Pages 908-921

  Ostrowski, Martin ^a   Mazard, Sophie ^a   Tetu, Sasha G ^b   Phillippy, Katherine ^c,e   Johnson, Aaron ^c   Palenik, Brian ^d   Paulsen, Ian T ^b,c   Scanlan, Dave J ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b MACQUARIE UNIVERSITY   (Australia)

^c J CRAIG VENTER INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Cyanobacteria; phosphorus metabolism; PtrA; Synechococcus; transcriptional activators

Indexed keywords

BACTERIAL PROTEIN; CYCLIC AMP BINDING PROTEIN; PHOSPHATASE; PHOSPHATE; PHOSPHORUS; SEA WATER;

BIOASSAY; BIOLOGICAL UPTAKE; CYANOBACTERIUM; ENVIRONMENTAL STRESS; GENE EXPRESSION; MARINE ECOSYSTEM; METABOLISM; METAL; PHOSPHATE (INORGANIC); PHOTOSYNTHESIS; PROTEIN;

ARTICLE; DNA MICROARRAY; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNECHOCOCCUS;

BACTERIAL PROTEINS; CYCLIC AMP RECEPTOR PROTEIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHATES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEAWATER; SYNECHOCOCCUS;

CYANOBACTERIA; SYNECHOCOCCUS; SYNECHOCOCCUS ELONGATUS PCC 6301; SYNECHOCOCCUS SP.;

EID: 77954084435     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2010.24     Document Type: Article

References (51)

1. Aiba H, Mizuno T. (1994). A novel gene whose expression is regulated by the response-regulator, SphR, in response to phosphate limitation in Synechococcus species PCC7942. Mol Microbiol 13: 25-34. (Pubitemid 24220540)
2. Aiba H, Nagaya M, Mizuno T. (1993). Sensor and regulator proteins from the cyanobacterium Synechococcus species PCC7942 that belong to the bacterial signaltransduction protein families-implication in the adaptive response to phosphate limitation. Mol Microbiol 8: 81-91. (Pubitemid 23114824)
3. Ammerman JW, Hood RR, Case DA, Cotner JB. (2003). Phosphorus deficiency in the Atlantic: an emerging paradigm in oceanography. EOS 84: 165-170.
4. 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. (Pubitemid 37207580)
5. Bessey OA, Lowry OH, Brock MJ. (1946). A method for the rapid determination of alkaline phosphatase with five cubic millimeters of serum. J Biol Chem 164: 321-329.
6. Blindauer CA. (2008). Zinc-handling in cyanobacteria: an update. Chem Biodiv 5: 1990-2013.
7. Brahamsha B. (1996). A genetic manipulation system for oceanic cyanobacteria of the genus Synechococcus. Appl Environ Microbiol 62: 1747-1751. (Pubitemid 26143453)
8. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C et al. (2001). Minimum information about a microarray experiment (MIAME) toward standards for microarray data. Nat Genet 29: 365-371. (Pubitemid 34326681)
9. Coleman JE. (2003). Structure and mechanism of alkaline phosphatase. Ann Rev Biophys Biomol Struct 21: 441-483.
10. Cotner JB, Ammerman JW, Peele ER, Bentzen E. (1997). Phosphorus-limited bacterioplankton growth in the Sargasso Sea. Aquat Microb Ecol 13: 141-149. (Pubitemid 127472851)
11. Dufresne A, Ostrowski M, Scanlan DJ, Garczarek L, Mazard S, Palenik BP et al. (2008). Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Genome Biol 9: R90. (Pubitemid 351974340)
12. Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe Vet al. (2003). Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100: 10020-10025. (Pubitemid 37087061)
13. Elledge SJ, Zhou Z, Allen JB. (1992). Ribonucleotide reductase: regulation, regulation, regulation. Trends Biochem Sci 17: 119-123.
14. Heldal M, Scanlan DJ, Norland S, Thingstad F, Mann NH. (2003). Elemental composition of single cells of various strains of marine Prochlorococcus and Synechococcus using X-ray microanalysis. Limnol Oceanogr 48: 1732-1743. (Pubitemid 37207581)
15. Herrero A, Muro-Pastor AM, Flores E. (2001). Nitrogen control in cyanobacteria. J Bacteriol 183: 411-425. (Pubitemid 32049030)
16. Hirani TA, Suzuki I, Murata N, Hayashi H, Eaton-Rye JJ. (2001). Characterization of a two-component signal transduction system involved in the induction of alkaline phosphatase under phosphate-limiting conditions in Synechocystis sp. PCC 6803. Plant Mol Biol 45: 133-144. (Pubitemid 32228599)
17. Itaya K, Ui M. (1966). A new micromethod for the colorimetric determination of inorganic phosphate. Clinica Chimica Acta 14: 361-366.
18. Karl DM, Tien G. (1997). Temporal variability in dissolved phosphorus concentrations in the subtropical North Pacific Ocean. Mar Chem 56: 77-96. (Pubitemid 27111855)
19. Korner H, Sofia HJ, Zumft WG. (2003). Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 27: 559-592. (Pubitemid 37456858)
20. Lindell D, Padan E, Post AF. (1998). Regulation of ntcA expression and nitrite uptake in the marine Synechococcus sp. strain WH7803. J Bacteriol 180: 1878-1886. (Pubitemid 28173070)
21. Lohan MC, Statham PJ, Crawford DW. (2002). Total dissolved zinc in the upper water column of the subarctic North East Pacific. Deep-Sea Res Part II 49: 5793-5808.
22. Luque I, Flores E, Herrero A. (1994). Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13: 2862-2869. (Pubitemid 24191696)
23. Mackey KRM, Paytan A, Grossman AR, Bailey S. (2008). A photosynthetic strategy for coping in a high-light, low-nutrient environment. Limnol Oceanogr 53: 900-913. (Pubitemid 351821688)
24. Martiny AC, Coleman ML, Chisholm SW. (2006). Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA 103: 12552-12557.
25. McCarren J, Brahamsha B. (2005). Transposon mutagenesis in a marine Synechococcus strain: isolation of swimming motility mutants. J Bacteriol 187: 4457-4462. (Pubitemid 40880956)
26. McCarren J, Brahamsha B. (2007). SwmB, a 1.12-megadalton protein that is required for nonflagellar swimming motility in Synechococcus. J Bacteriol 189: 1158-1162. (Pubitemid 46183893)
27. Moore LR, Ostrowski M, Scanlan DJ, Feren K, Sweetsir T. (2005). Ecotypic variation in phosphorus acquisition mechanisms within marine picocyanobacteria. Aquat Microb Ecol 39: 257-269. (Pubitemid 40962702)
28. Morel FMM, Rueter JG, Anderson DM, Guillard RRL. (1979). Aquil-chemically defined phytoplankton culture-medium for trace-metal studies. J Phycol 15: 135-141.
29. Palenik B, Brahamsha B, Larimer FW, Land M, Hauser L, Chain P et al. (2003). The genome of a motile marine Synechococcus. Nature 424: 1037-1042.
30. Palenik B, Ren QH, Dupont CL, Myers GS, Heidelberg JF, Badger JH et al. (2006). Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proc Natl Acad Sci USA 103: 13555-13559. (Pubitemid 44380146)
31. Partensky F, Hess WR, Vaulot D. (1999). Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127. (Pubitemid 29116088)
32. Salgado H, Gama-Castro S, Martinez-Antonio A, Diaz-Peredo E, Sanchez-Solano F, Peralta-Gil M et al. (2004). RegulonDB (version 4.0): transcriptional regulation, operon organization and growth conditions in Escherichia coli K-12. Nucleic Acids Res 32: D303-D306. (Pubitemid 38081663)
33. Scanlan DJ, Bourne JA, Mann NH. (1997a). A putative transcriptional activator of the Crp/Fnr family from the marine cyanobacterium Synechococcus sp WH7803. J Appl Phycol 8: 565-567.
34. Scanlan DJ, Mann NH, Carr NG. (1993). The response of the picoplanktonic marine cyanobacterium Synechococcus species WH7803 to phosphate starvation involves a protein homologous to the periplasmic phosphate-binding protein of Escherichia coli. Mol Microbiol 10: 181-191.
35. Scanlan DJ, Silman NJ, Donald KM, Wilson WH, Carr NG, Joint I et al. (1997b). An immunological approach to detect phosphate stress in populations and single cells of photosynthetic picoplankton. Appl Environ Microbiol 63: 2411-2420. (Pubitemid 27232946)
36. Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR et al. (2009). Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73: 249-299.
37. Snyder DS, Brahamsha B, Azadi P, Palenik B. (2009). Structure of compositionally simple lipopolysaccharide from marine Synechococcus. J Bacteriol 191: 5499-5509.
38. Silberbach M, Hüser A, Kalinowski J, Pühler A, Walter B, Kramer R et al. (2005). DNA microarray analysis of the nitrogen starvation response of Corynebacterium glutamicum. J Biotech 119: 357-367. (Pubitemid 41330754)
39. Su ZC, Dam P, Chen X, Olman V, Jiang T, Palenik B et al. (2003). Computational inference of regulatory pathways in microbes. An application to phosphorus assimilation pathways in Synechococcus WH8102. Genome Inform 14: 3-13.
40. Su ZC, Olman V, Mao FL, 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. (Pubitemid 41487824)
41. Su ZC, Olman V, Xu Y. (2007). Computational prediction of Pho regulons in cyanobacteria. BMC Genomics 8: 156. (Pubitemid 47039446)
42. Suzuki S, Ferjani A, Suzuki I, Murata N. (2004). The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in Synechocystis. J Biol Chem 279: 13234-13240. (Pubitemid 38445902)
43. Tai V, Paulsen IT, Phillippy K, Johnson DA, Palenik B. (2009). Whole-genome microarray analyses of Synechococcus- Vibrio interactions. Environ Microbiol 11: 2698-2709.
44. Tetu SG, Brahamsha B, Johnson DA, 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.
45. Thingstad TF, Krom MD, Mantoura RFC, Flaten GAF, Groom S, Herut B et al. (2005). Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309: 1068-1071. (Pubitemid 41134463)
46. Tusher VG, Tibshirani R, Chu G. (2001). Significance Analysis of Microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121. (Pubitemid 32397092)
47. Van Mooy BAS, Rocap G, Fredricks HF, Evans CT, Devol AH. (2006). Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci USA 103: 8607-8612. (Pubitemid 43878067)
48. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74. (Pubitemid 38451457)
49. Waterbury JB, Willey JM. (1988). Isolation and growth of marine planktonic cyanobacteria. Methods Enzymol 167: 100-105.
50. Zubkov MV, Mary I, Woodward EMS, Warwick PE, Fuchs BM, Scanlan DJ et al. (2007). Microbial control of phosphate in the nutrient-depleted North Atlantic subtropical gyre. Environ Microbiol 9: 2079-2089. (Pubitemid 47057361)
51. Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D et al. (2008). Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10: 147-161.