Regulation of nitrogen metabolism in the marine diazotroph Trichodesmium IMS101 under varying temperatures and atmospheric CO2 concentrations

Environmental Microbiology

Volumn 12, Issue 7, 2010, Pages 1899-1912

  Levitan, Orly ^a   Brown, Christopher M ^b,d   Sudhaus, Stefanie ^c   Campbell, Douglas ^b   LaRoche, Julie ^c   Berman Frank, Ilana ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b MOUNT ALLISON UNIVERSITY   (Canada)

^c GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOBACTERIA; TRICHODESMIUM;

BACTERIAL PROTEIN; CARBON; CARBON DIOXIDE; MESSENGER RNA; NITROGEN; PHOSPHORUS;

AIR; ARTICLE; BIOSYNTHESIS; CYANOBACTERIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NITROGEN FIXATION; TEMPERATURE;

AIR; BACTERIAL PROTEINS; CARBON; CARBON DIOXIDE; CYANOBACTERIA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; NITROGEN; NITROGEN FIXATION; PHOSPHORUS; RNA, MESSENGER; TEMPERATURE;

EID: 77956682250     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02195.x     Document Type: Article

References (62)

1. 2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54: 609-622.
2. 2 concentrating mechanism. J Exp Bot 57: 249-265.
3. Berman-Frank, I., Lundgren, P., Chen, Y.B., Kupper, H., Kolber, Z., Bergman, B., and Falkowski, P. (2001a) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294: 1534-1537.
4. Berman-Frank, I., Cullen, J.T., Shaked, Y., Sherrell, R.M., and Falkowski, P.G. (2001b) Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol Oceanogr 46: 1249-1260.
5. Berman-Frank, I., Quigg, A., Finkel, Z.V., Irwin, A.J., and Haramaty, L. (2007) Nitrogen fixation strategies and Fe requirements in cyanobacteria. Limnol Oceanogr 52: 2260-2269.
6. Bonnet, S., Guieu, C., Bruyant, F., Prasil, O., Van Wambeke, F., Raimbault, P., et al. (2008) Nutrient limitation of primary productivity in the Southeast Pacific (BIOSOPE cruise). Biogeosciences 5: 215-225.
7. Bonnet, S., Biegala, I.C., Dutrieux, P., Slemons, L.O., and Capone, D.G. (2009) Nitrogen fixation in the western equatorial Pacific: rates, diazotrophic cyanobacterial size class distribution, and biogeochemical significance. Global Biogeochem Cycles 23: 1-13.
8. Breitbarth, E., Oschlies, A., and LaRoche, J. (2007) Physiological constraints on the global distribution of Trichodesmium -effect of temperature on diazotrophy. Biogeosciences 4: 53-61.
9. Brown, C.M., MacKinnon, J.D., Cockshutt, A.M., Villareal, T.A., and Campbell, D.A. (2008) Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico. Mar Biol 154: 413-422.
10. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., et al. (2009) The MIQE guidelines: minimum information for publication of quantitative realtime PCR experiments. Clin Chem 55: 611-622.
11. Capone, D.G. (1993) Determination of Nitrogenase activity in aquatic samples using the acetylene reduction procedure. In Handbook of Methods in Aquatic Microbial Ecology. Kemp, P.F., Sherr, B., Sherr, E., and Cole, J. (eds). New York, NY, USA: Lewis Publishers, pp. 621-631.
12. Capone, D.G., and Montoya, J.P. (2001) Nitrogen fixation and denitrification. Methods Microbiol 30: 501-515.
13. Capone, D.G., and Subramaniam, A. (2005) Seeing microbes from space -remote sensing is now a critical resource for tracking marine microbial ecosystem dynamics and their impact on global biogeochemical cycles. ASM News 71: 179-196.
14. Capone, D.G., Oneil, J.M., Zehr, J., and Carpenter, E.J. (1990) Basis for diel variation in nitrogenase activity in the marine planktonic cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol 56: 3532-3536.
15. Capone, D.G., Zehr, J.P., Paerl, H.W., Bergman, B., and Carpenter, E.J. (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276: 1221-1229.
16. Carpenter, E.J., and Capone, D.G. (2008) Nitrogen fixation in the marine environment. In Nitrogen in the Marine Environment, 2nd edn. Capone, D., Bronk, D., Mulholland, M., and Carpenter, E. (eds). San Diego, CA, USA: Academic Press, pp. 141-198.
17. Carpenter, E.J., Bergman, B., Dawson, R., Siddiqui, P.J., Soderback, E., and Capone, D.G. (1992) Glutamine synthetase and nitrogen cycling in colonies of the marine diazotrophic cyanobacteria Trichodesmium spp. Appl Environ Microbiol 58: 3122-3129.
18. Chen, Y.B., Zehr, J.P., and Mellon, M. (1996) Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp IMS 101 in defined media: Evidence for a circadian rhythm. J Phycol 32: 916-923.
19. Chen, Y.B., Dominic, B., Mellon, M.T., and Zehr, J.P. (1998) Circadian rhythm of nitrogenase gene expression in the diazotrophic filamentous nonheterocystous Cyanobacterium Trichodesmium sp strain IMS101. J Bacteriol 180: 3598-3605.
20. Chen, Y.B., Dominic, B., Zani, S., Mellon, M.T., and Zehr, J.P. (1999) Expression of photosynthesis genes in relation to nitrogen fixation in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp IMS 101. Plant Mol Biol 41: 89-104.
21. Church, M.J., Bjorkman, K.M., Karl, D.M., Saito, M.A., and Zehr, J.P. (2008) Regional distributions of nitrogen-fixing bacteria in the Pacific Ocean. Limnol Oceanogr 53: 63-77.
22. 2 fixing colonial cyanobacterium Trichodesmium. Science 312: 1517-1520.
23. Dominic, B., Chen, Y.B., and Zehr, J.P. (1998) Cloning and transcriptional analysis of the nifUHDK genes of Trichodesmium sp. IMS101 reveals stable nifD, nifDK and nifK transcripts. Microbiology-UK 144: 3359-3368.
24. El-Shehawy, R., Lugomela, C., Ernst, A., and Bergman, B. (2003) Diurnal expression of hetR and diazocyte development in the filamentous non-heterocystous cyanobacterium Trichodesmium erythraeum. Microbiology-Sgm 149: 1139-1146.
25. Flores, E., and Herrero, A. (1994) Assimilatory nitrogen metabolism and its regulation. In The Molecular Biology of Cyanobacteria. Bryant, D.A. (ed.). Dordrecht, the Netherlands: Kluwer Scientific Publications, pp. 487-517.
26. Hageman, R.V., and Burris, R.H. (1978) Kinetic studies on electron-transfer and interaction between nitrogenase components from Azotobacter vinelandii. Biochemistry 17: 4117-4124.
27. 2 fixation rate, biomass, and C:N:P stoichiometry. J Phycol 44: 929-937.
28. 2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol Oceanogr 52: 1293-1304.
29. Kramer, J.G., Wyman, M., Zehr, J.P., and Capone, D.G. (1996) Diel variability in transcription of the structural gene for glutamine synthetase (glnA) in natural populations of the marine diazotrophic cyanobacterium Trichodesmium thiebautii. FEMS Microbiol Ecol 21: 187-196.
30. 2 and diurnal changes. Limnol Oceanogr 54: 548-559.
31. Krauk, J.M., Villareal, T.A., Sohm, J.A., Montoya, J.P., and Capone, D.G. (2006) Plasticity of N: P ratios in laboratory and field populations of Trichodesmium spp. Aquat Microb Ecol 42: 243-253.
32. Küpper, H., Ferimazova, N., Setlik, I., and Berman-Frank, I. (2004) Traffic lights in Trichodesmium. Regulation of photosynthesis for nitrogen fixation studied by chlorophyll fluorescence kinetic microscopy. Plant Physiol (Rockville) 135: 2120-2133.
33. Küpper, H., Setlik, I., Seibert, S., Prasil, O., Setlikova, E., Strittmatter, M., et al. (2008) Iron limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation. New Phytol 179: 784-798.
34. Lanzilotta, W.N., and Seefeldt, L.C. (1996) Electron transfer from the nitrogenase iron protein to the [8Fe-(7/8)S] clusters of the molybdenum-iron protein. Biochemistry 35: 16770-16776.
35. LaRoche, J., and Breitbarth, E. (2005) Importance of the diazotrophs as a source of new nitrogen in the ocean. J Sea Res 53: 67-91.
36. 2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Global Change Biol 13: 531-538.
37. Lin, S.J., Henze, S., Lundgren, P., Bergman, B., and Carpenter, E.J. (1998) Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Appl Environ Microbiol 64: 3052-3058.
38. -ΔΔCt method. Methods 25: 402-408.
39. MacIntyre, H.L., and Cullen, J.J. (2005) Using cultures to investigate the physiological ecology of microalgae. In Algal Culturing Techniques. Anderson, R.A. (ed.). Burlington, MA, USA: Elsevier Academic Press, pp. 287-326.
40. 2 fixation. Am J Sci 305: 546-595.
41. Milligan, A.J., Berman-Frank, I., Gerchman, Y., Dismukes, G.C., and Falkowski, P.G. (2007) Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection. J Phycol 43: 845-852.
42. Mills, M.M., Ridame, C., Davie, M., La Roche, J., and Geider, R.J. (2004) Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429: 292-294.
43. Mulholland, M.R., and Capone, D.G. (1999) Nitrogen fixation, uptake and metabolism in natural and cultured populations of Trichodesmium spp. Mar Ecol Prog Ser 188: 33-49.
44. 2 fixing cyanobacteria Trichodesmium spp. Trends Plant Sci 5: 148-153.
45. 2 fixation in cultures of Trichodesmium NIBB1067. J Phycol 35: 977-988.
46. Ohkawa, H., Sonoda, M., Shibata, M., and Ogawa, T. (2001) Localization of NAD(P)H dehydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183: 4938-4939.
47. Postgate, J.R. (1998) Nitrogen Fixation. Cambridge, UK: Cambridge University Press.
48. 2 fixation. Funct Plant Biol 29: 117-121.
49. Ramakers, C., Ruijter, J.M., Deprez, R.H.L., and Moorman, A.F.M. (2003) Assumption-free analysis of quantitative real-time PCR data. Neurosci Lett 339: 62-66.
50. Ramos, B.J., Biswas, H., Schulz, K., LaRoche, J., and Riebesell, U. (2007) Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Global Biogeochem Cycles 21: 1-6.
51. Raven, J.A. (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27: 85-209.
52. Raymond, J., Siefert, J.L., Staples, C.R., and Blankenship, R.E. (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554.
53. Reade, J.P.H., Dougherty, L.J., Rogers, L.J., and Gallon, J.R. (1999) Synthesis and proteolytic degradation of nitrogenase in cultures of the unicellular cyanobacterium Gloeothece strain ATCC 27152. Microbiology-UK 145: 1749-1758.
54. Scanlan, D.J., and Wilson, W.H. (1999) Application of molecular techniques to addressing the role of P as key effector in marine ecosystems. Hydrobiologia 401: 149-175.
55. Tandeau De Marsac, N., and Houmard, J. (1988) Complementary chromatic adaptation: physiological conditions and action spectra. In Cyanobacteria. Packer, L., and Glazer, A.N. (eds). San Diego, CA, USA: Academic Press, pp. 318-328.
56. Tortell, P.D., Rau, G.H., and Morel, M.M.F. (2000) Inorganic carbon acquisition in costal Pacific phytoplankton communities. Limnol Oceanogr 45: 1485-1500.
57. Vichitphan, K. (2001) Azotobacter vinelandii Nitrogenase: Effect of Amino-acid Substitutions at the aGln-191 Residue of the MoFe Protein on Substrate Reduction and CO Inhibition. PhD Thesis. Blacksburg, VA, USA: Virginia Polytechnic Institute and State University.
58. White, A.E., Spitz, Y.H., Karl, D.M., and Letelier, R.M. (2006) Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications. Limnol Oceanogr 51: 1777-1790.
59. Zehr, J.P., Ohki, K., and Fujita, Y. (1991) Arrangement of nitrogenase structural genes in an aerobic filamentous nonheterocystous cyanobacterium. J Bacteriol 173: 7055-7058.
60. Zehr, J.P., Wyman, M., Miller, V., Duguay, L., and Capone, D.G. (1993) Modification of the Fe protein of nitrogenase in Natural populations of Trichodesmium thiebautii. Appl Environ Microbiol 59: 669-676.
61. Zehr, J.P., Harris, D., Dominic, B., and Salerno, J. (1997) Structural analysis of the Trichodesmium nitrogenase iron protein: implications for aerobic nitrogen fixation activity. FEMS Microbiol Lett 153: 303-309.
62. Zhang, J.-Y., Chen, W.-L., and Zhang, C.-C. (2009) hetR and patS, two genes necessary for heterocyst pattern formation, are widespread in filamentous nonheterocyst-forming cyanobacteria. Microbiology 155: 1418-1426.