Nitrogen starvation induces extensive changes in the redox proteome of Prochlorococcus sp. strain SS120

Environmental Microbiology Reports

Volumn 4, Issue 2, 2012, Pages 257-267

  Mcdonagh, Brian ^a   Domínguez Martín, Ma Agustina ^a   Gómez Baena, Guadalupe ^a   López Lozano, Antonio ^a   Diez, Jesús ^a   Bárcena, Jose A ^a   García Fernández, Jose M ^a  

^a UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROCHLOROCOCCUS; PROCHLOROCOCCUS SP.;

EID: 84858611156     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/j.1758-2229.2012.00329.x     Document Type: Article

References (54)

1. Bottin, H., and Lagoutte, B. (1992) Ferredoxin and flavodoxin from the cyanobacterium Synechocystis sp PCC 6803. Biochim Biophys Acta 1101: 48-56.
2. Buchanan, B.B., and Balmer, Y. (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56: 187-220.
3. Capone, D. (2000) The marine microbial nitrogen cycle. In Microbial Ecology of the Oceans. Kirchman, D. (ed.). New York, NY, USA: Wiley-Liss, pp. 455-493.
4. Chisholm, S., Olson, R., Zettler, E., Goericke, R., Waterbury, J., and Welschmeyer, N. (1988) A novel free living prochlorophyte abundant in the oceanic euphotic zone. Nature 334: 340-343.
5. Coleman, M., and Chisholm, S. (2007) Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol 15: 398-407.
6. Coleman, M., Sullivan, M., Martiny, A., Steglich, C., Barry, K., Delong, E., and Chisholm, S. (2006) Genomic islands and the ecology and evolution of Prochlorococcus. Science 311: 1768-1770.
7. Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I., Barbe, V., etal. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100: 10020-10025.
8. El Alaoui, S., Diez, J., Humanes, L., Toribio, F., Partensky, F., and García-Fernández, J. (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.
9. El Alaoui, S., Diez, J., Toribio, F., Gómez-Baena, G., Dufresne, A., and García-Fernández, J. (2003) Glutamine synthetase from the marine cyanobacteria Prochlorococcus spp.: characterization, phylogeny and response to nutrient limitation. Environ Microbiol 5: 412-423.
10. Florencio, F., Perez-Perez, M., Lopez-Maury, L., Mata-Cabana, A., and Lindahl, M. (2006) The diversity and complexity of the cyanobacterial thioredoxin systems. Photosynth Res 89: 157-171.
11. García-Fernández, J., Tandeau de Marsac, N., and 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.
12. Goericke, R., and Welschmeyer, N. (1993) The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep-Sea Res Part I Oceanogr Res Pap 40: 2283-2294.
13. Gómez-Baena, G., Diez, J., García-Fernández, J., El Alaoui, S., and Humanes, L. (2001) Regulation of glutamine synthetase by metal-catalyzed oxidative modification in the marine oxyphotobacterium Prochlorococcus. Biochim Biophys Acta - Gen Sub 1568: 237-244.
14. Gómez-Baena, G., García-Fernández, J., Lopez-Lozano, A., Toribio, F., and Diez, J. (2006) Glutamine synthetase degradation is controlled by oxidative proteolysis in the marine cyanobacterium Prochlorococcus marinus strain PCC 9511. Biochim Biophys Acta 1760: 930-940.
15. Gómez-Garcia, M., and Serrano, A. (2002) Expression studies of two paralogous ppa genes encoding distinct Family I pyrophosphatases in marine unicellular cyanobacteria reveal inactivation of the typical cyanobacterial gene. Biochem Biophys Res Commun 295: 890-897.
16. Goto, T., Aoki, R., Minamizaki, K., and Fujita, Y. (2010) Functional differentiation of two analogous coproporphyrinogen III oxidases for heme and chlorophyll biosynthesis pathways in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 51: 650-663.
17. Graziano, L., Geider, R., Li, W., and Olaizola, M. (1996) Nitrogen limitation of North Atlantic phytoplankton - analysis of physiological condition in nutrient enrichment experiments. Aquat Microb Ecol 11: 53-64.
18. Grzymski, J.J., and Dussaq, A.M. (2012) The significance of nitrogen cost minimization in proteomes of marine microorganisms. ISME J. 6: 71-80.
19. Hama, H., Kayahara, T., Tsuda, M., and Tsuchiya, T. (1991) Inhibition of homoserine dehydrogenase I by L-serine in Escherichia coli. J Biochem 109: 604-608.
20. Howarth, R. (1988) Nutrient limitation of net primary production in marine ecosystems. Annu Rev Ecol Syst 19: 89-110.
21. Johnson, Z., Zinser, E., Coe, A., McNulty, N., Woodward, E., and Chisholm, S. (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311: 1737-1740.
22. Jung, Y.S., Vassiliev, I.R., Yu, J., McIntosh, L., and Golbeck, J.H. (1997) Strains of Synechocystis sp. PCC 6803 with altered PsaC. II. EPR and optical spectroscopic properties of FA and FB in aspartate, serine, and alanine replacements of cysteines 14 and 51. J Biol Chem 272: 8040-8049.
23. Kettler, G., Martiny, A., Huang, K., Zucker, J., Coleman, M., Rodrigue, S., etal. (2007) Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3: 2515-2528.
24. Kim, Y., Konno, H., Sugano, Y., and Hisabori, T. (2011) Redox regulation of rotation of the cyanobacterial F1-ATPase containing thiol regulation switch. J Biol Chem 286: 9071-9078.
25. Layer, G., Moser, J., Heinz, D.W., Jahn, D., and Schubert, W.D. (2003) Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J 22: 6214-6224.
26. Lindahl, M., and Florencio, F. (2003) Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc Natl Acad Sci USA 100: 16107-16112.
27. Lindahl, M., and Kieselbach, T. (2009) Disulphide proteomes and interactions with thioredoxin on the track towards understanding redox regulation in chloroplasts and cyanobacteria. J Proteomics 72: 416-438.
28. Liu, H., Nolla, H., and Campbell, L. (1997) Prochlorococcus growth rate and contribution to primary production in the Equatorial and Subtropical North Pacific ocean. Aquat Microb Ecol 12: 39-47.
29. López-Lozano, A., Diez, J., El Alaoui, S., Moreno-Vivián, C., and García-Fernández, J. (2002) Nitrate is reduced by heterotrophic bacteria but not transferred to Prochlorococcus in non axenic cultures. FEMS Microbiol Ecol 41: 151-160.
30. López-Lozano, A., Gómez-Baena, G., Muñoz-Marín, M., Rangel, O., Diez, J., and García-Fernández, J. (2009) Expression of genes involved in nitrogen assimilation and the C/N balance sensing in Prochlorococcus sp. strain SS120. Gene Expr 14: 279-289.
31. Luque, I., and Forchhammer, K. (2008) Nitrogen assimilation and C/N balance sensing. In The Cyanobacteria Molecular Biology, Genomics and Evolution. Herrero, A., and Flores, E. (eds). Norfolk, UK: Caister Academic Press, pp. 335-382.
32. McDonagh, B., Ogueta, S., Lasarte, G., Padilla, C., and Barcena, J. (2009) Shotgun redox proteomics identifies specifically modified cysteines in key metabolic enzymes under oxidative stress in Saccharomyces cerevisiae. J Proteomics 72: 677-689.
33. McDonagh, B., Padilla, C.A., Pedrajas, J.R., and Barcena, J.A. (2011a) Biosynthetic and iron metabolism is regulated by thiol proteome changes dependent on glutaredoxin-2 and mitochondrial peroxiredoxin-1 in Saccharomyces cerevisiae. J Biol Chem 286: 15565-15576.
34. McDonagh, B., Requejo, R., Fuentes-Almagro, C.A., Ogueta, S., Barcena, J.A., and Padilla, C.A. (2011b) Thiol redox proteomics identifies differential targets of cytosolic and mitochondrial glutaredoxin-2 isoforms in Saccharomyces cerevisiae. Reversible S-glutathionylation of DHBP synthase (RIB3). J Proteomics 74: 2487-2497.
35. Malmstrom, J., Lee, H., and Aebersold, R. (2007) Advances in proteomic workflows for systems biology. Curr Opin Biotechnol 18: 378-384.
36. Maruyama, K., Sato, N., and Ohta, N. (1999) Conservation of structure and cold-regulation of RNA-binding proteins in cyanobacteria: probable convergent evolution with eukaryotic glycine-rich RNA-binding proteins. Nucleic Acids Res 27: 2029-2036.
37. Mata-Cabana, A., Florencio, F.J., and Lindahl, M. (2007) Membrane proteins from the cyanobacterium Synechocystis sp. PCC 6803 interacting with thioredoxin. Proteomics 7: 3953-3963.
38. Moore, L., Coe, A., Zinser, E., Saito, M., Sullivan, M., Lindell, D., etal. (2007) Culturing the marine cyanobacterium Prochlorococcus. Limnol Oceanogr 5: 353-362.
39. +-isocitrate dehydrogenase gene (icd) is nitrogen regulated in cyanobacteria. J Bacteriol 178: 4070-4076.
40. Nakai, M., Goto, A., Nohara, T., Sugita, D., and Endo, T. (1994) Identification of the SecA protein homolog in pea chloroplasts and its possible involvement in thylakoidal protein transport. J Biol Chem 269: 31338-31341.
41. Nilsson, T., Mann, M., Aebersold, R., Yates, J.R., 3rd, Bairoch, A., and Bergeron, J.J. (2010) Mass spectrometry in high-throughput proteomics: ready for the big time. Nat Methods 7: 681-685.
42. Partensky, F., and Garczarek, L. (2003) The photosynthetic apparatus of chlorophyll b- and d-containing oxyphotobacteria. In Photosynthesis in Algae. Larkum, A., Douglas, S., and Raven, J. (eds). Dordrecht: Kluwer Academic Publishers, pp. 29-62.
43. Partensky, F., and Garczarek, L. (2010) Prochlorococcus: advantages and limits of minimalism. Annu Rev Mar Sci 2: 305-331.
44. Partensky, F., Blanchot, J., and Vaulot, D. (1999a) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In Marine Cyanobacteria. Charpy, L., and Larkum, A. (eds). Monaco: Bulletin de l'Institut Océanographique, Numéro spécial, pp. 457-476.
45. Partensky, F., Hess, W., and Vaulot, D. (1999b) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127.
46. Perez-Perez, M.E., Florencio, F.J., and Lindahl, M. (2006) Selecting thioredoxins for disulphide proteomics: target proteomes of three thioredoxins from the cyanobacterium Synechocystis sp. PCC 6803. Proteomics 6 (Suppl. 1): S186-S195.
47. Rocap, G., Larimer, F., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N., etal. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047.
48. Tolonen, A., Aach, J., Lindell, D., Johnson, Z., Rector, T., Steen, R., etal. (2006) Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol Syst Biol 2: 53.
49. Valladares, A., Montesinos, M.L., Herrero, A., and Flores, E. (2002) An ABC-type, high-affinity urea permease identified in cyanobacteria. Mol Microbiol 43: 703-715.
50. Van Mooy, B., Rocap, G., Fredricks, H., Evans, C., and Devol, A. (2006) Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci USA 103: 8607-8612.
51. Warangkar, S.C., and Khobragade, C.N. (2010) Purification, characterization, and effect of thiol compounds on activity of the Erwinia carotovora L-asparaginase. Enzyme Res 2010: 165878.
52. Wegener, K., Singh, A., Jacobs, J., Elvitigala, T., Welsh, E., Keren, N., etal. (2010) Global proteomics reveal an atypical strategy for Carbon/Nitrogen assimilation by a cyanobacterium under diverse environmental perturbations. Mol Cell Proteomics 9: 2678-2689.
53. Zehr, J.P., and Kudela, R.M. (2011) Nitrogen cycle of the open ocean: from genes to ecosystems. Ann Rev Mar Sci 3: 197-225.
54. Zhang, L., Paakkarinen, V., van Wijk, K.J., and Aro, E.M. (2000) Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into photosystem II. Plant Cell 12: 1769-1782.