Stress responses in Prochlorococcus MIT9313 vs. SS120 involve differential expression of genes encoding proteases ClpP, FtsH and Lon

Research in Microbiology

Volumn 160, Issue 8, 2009, Pages 567-575

  Gómez Baena, Guadalupe ^a   Rangel, Oriol Alberto ^a   López Lozano, Antonio ^a   García Fernández, Jose Manuel ^a   Diez, Jesús ^a  

^a UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

Cyanobacteria; Gene expression; Prochlorococcus; Protease; Protein degradation; Stress response

Indexed keywords

2,5 DIBROMO 6 ISOPROPYL 3 METHYLBENZOQUINONE; ADENOSINE TRIPHOSPHATE; AZASERINE; DIURON; ENDOPEPTIDASE CLP; ENDOPEPTIDASE LA; FTSH PROTEIN; METALLOPROTEINASE; UNCLASSIFIED DRUG;

AGING; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM CULTURE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DARKNESS; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROCHLOROCOCCUS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; STARVATION; STRAIN DIFFERENCE;

BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; PEPTIDE HYDROLASES; PROCHLOROCOCCUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PHYSIOLOGICAL;

CYANOBACTERIA; PROCHLOROCOCCUS;

EID: 70350534258     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2009.08.009     Document Type: Article

References (56)

1. Adam Z. Chloroplast proteases: possible regulators of gene expression?. Biochimie 82 (2000) 647-654
2. Adam Z., Rudella A., and van Wijk K.J. Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Curr. Opin. Plant Biol. 9 (2006) 234-240
3. Alfonso M., Perewoska I., and Kirilovsky D. Redox control of ntcA gene expression in Synechocystis sp. PCC 6803. Nitrogen availability and electron transport regulate the levels of the NtcA protein. Plant Physiol. 125 (2001) 969-981
4. Alfonso M., Perewoska I., and Kirilovsky D. Redox control of psbA gene expression in the cyanobacterium Synechocystis PCC 6803. Involvement of the cytochrome b(6)/f complex. Plant Physiol. 122 (2000) 505-516
5. Bieniossek C., Schalch T., Bumann M., Meister M., Meier R., and Baumann U. The molecular architecture of the metalloprotease FtsH. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 3066-3071
6. Bota D.A., Van Remmen H., and Davies K.J. Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress. FEBS Lett. 532 (2002) 103-106
7. + alpha domain of E. coli Lon protease at 1.9 Å resolution. J. Struct. Biol. 146 (2004) 113-122
8. Chisholm S.W., Olson R.J., Zettler E.R., Goericke R., Waterbury J.B., and Welschmeyer N.A. A novel free living prochlorophyte abundant in the oceanic euphotic zone. Nature 334 (1988) 340-343
9. Chung C.H., Yoo S.J., Seol J.H., and Kang M.S. Characterization of energy-dependent proteases in bacteria. Biochem. Biophys. Res. Commun. 241 (1997) 613-616
10. Clarke A.K. ATP-dependent Clp proteases in photosynthetic organism- a cut above the rest!. Ann. Bot. 83 (1999) 593-599
11. Clarke A.K., Schelin J., and Porankiewicz J. Inactivation of the clpP1 gene for the proteolytic subunit of the ATP-dependent Clp protease in the cyanobacterium Synechococcus limits growth and light acclimatation. Plant Mol. Biol. 37 (1998) 791-801
12. Coleman M.L., Sullivan M.B., Martiny A.C., Steglich C., Barry K., Delong E.F., and Chisholm S.W. Genomic islands and the ecology and evolution of Prochlorococcus. Science 311 (2006) 1768-1770
13. Dufresne A., Salanoubat M., Partensky F., Artiguenave F., Axmann I.M., Barbe V., Duprat S., Galperin M.Y., et al. Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 10020-10025
14. El Alaoui S., Diez J., Toribio F., Gómez-Baena G., Dufresne A., and García-Fernández J.M. Glutamine synthetase from the marine cyanobacteria Prochlorococcus spp.: characterization, phylogeny and response to nutrient limitation. Environ. Microbiol. 5 (2003) 412-423
15. El Bissati K., and Kirilovsky D. Regulation of psbA and psaE expression by light quality in Synechocystis species PCC 6803. A redox control mechanism. Plant Physiol. 125 (2001) 1988-2000
16. Fedhila S., Msadek T., Nel P., and Lereclus D. Distinc clpP genes control specific adaptive responses in Bacillus thuringiensis. J. Bacteriol. 184 (2002) 5554-5562
17. II protein) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol. Biol. 35 (1997) 723-734
18. García-Fernández J.M., and Diez J. Adaptive mechanisms of the nitrogen and carbon assimilatory pathways in the marine cyanobacteria Prochlorococcus. Res. Microbiol. 155 (2004) 795-802
19. García-Fernández J.M., Tandeau de Marsac N., and Diez J. Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol. Mol. Biol. Rev. 68 (2004) 630-638
20. Gottesman S. Proteases and their targets in Escherichia coli. Annu. Rev. Genet. 30 (1996) 465-506
21. Hengge R., and Bukau B. Proteolysis in prokaryotes: protein quality control and regulatory principles. Mol. Microbiol. 49 (2003) 1451-1462
22. Hihara Y., Sonoike K., Kanehisa M., and Ikeuchi M. DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 185 (2003) 1719-1725
23. Ito K., and Akiyama Y. Cellular functions, mechanism of action, and regulation of FtsH protease. Annu. Rev. Microbiol. 59 (2005) 211-231
24. Kettler G.C., Martiny A.C., Huang K., Zucker J., Coleman M.L., Rodrigue S., Chen F., Lapidus A., et al. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet. 3 (2007) 2515-2528
25. Kuroda A. A polyphosphate-lon protease complex in the adaptation of Escherichia coli to amino acid starvation. Biosci. Biotechnol. Biochem. 70 (2006) 325-331
26. Li W.K.W. Primary production of prochlorophytes, cyanobacteria, and eukaryotic ultraphytoplankton - Measurements from flow cytometric sorting. Limnol. Oceanogr. 39 (1994) 169-175
27. Mann N.H., Novac N., Mullineaux C.W., Newman J., Bailey S., and Robinson C. Involvement of a FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 479 (2000) 72-77
28. Martiny A.C., Coleman M.L., and Chisholm S.W. Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 12552-12557
29. Mary I., Tu C.-J., Grossman A., and Vaulot D. Effects of high light on transcripts of stress-associated genes for the cyanobacteria Synechocystis sp. PCC 6803 and Prochlorococcus MED4 and MIT9313. Microbiology 150 (2004) 1271-1281
30. Maurizi M.R. Proteases and protein degradation in Escherichia coli. Experientia 48 (1992) 178-201
31. Moore L.R., Rocap G., and Chisholm S.W. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393 (1998) 464-467
32. Muro-Pastor M.I., Reyes J.C., and Florencio F.J. Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J. Biol. Chem. 276 (2001) 38320-38328
33. Nair J.S., and Ramaswamy N.K. Chloroplast proteases. Biol. Plantarum 48 (2004) 321-326
34. Navarro F., Martinfigueroa E., and Florencio F.J. Electron transport controls transcription of the thioredoxin gene (Trxa) in the cyanobacterium Synechocystis Sp PCC-6803. Plant Mol. Biol. 43 (2000) 23-32
35. Palenik B., Brahamsha B., Larimer F., Land M., Hauser L., Chain P., Lamerdin J., Regala W., et al. The genome of a motile marine Synechococcus. Nature 424 (2003) 1037-1042
36. Partensky F., Hess W.R., and Vaulot D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63 (1999) 106-127
37. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) (9), e45
38. Post A.F. Nutrient limitation of marine cyanobacteria. In: Huisman J., Matthijs H., and Visser (Eds). Harmful Cyanobacteria (2005), Kluwer Academic Publisher
39. Rangel O.A., Gómez-Baena G., López-Lozano A., Diez J., and García-Fernández J.M. Physiological role and regulation of glutamate dehydrogenase in Prochlorococcus MIT9313. Environ. Microbiol. Rep. 1 (2009) 56-64
40. Reyes J.C., Crespo J.L., García-Domínguez M., and Florencio F.J. Electron transport controls glutamine synthetase activity in the facultative heterotrophic cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 109 (1995) 899-905
41. Reyes J.C., and Florencio F.J. Electron transport controls transcription of the glutamine synthetase gene (glnA) from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol. Biol. 27 (1995) 789-799
42. 6f complex. Biochim. Biophys. Acta 108 (1991) 1188-1195
43. 2-containing cyanobacterium (Oxyphotobacteria). Int. J. Syst. Evol. Microbiol. 50 (2000) 1833-1847
44. Rocap G., Larimer F.W., Lamerdin J., Malfatti S., Chain P., Ahlgren N.A., Arellano A., Coleman, et al. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424 (2003) 1042-1047
45. Sakamoto W. Protein degradation machineries in plastids. Annu. Rev. Plant Biol. 57 (2006) 599-621
46. Schelin J., Lindmark F., and Clarke A.K. The clpP multigene family for the ATP-dependent Clp protease in the cyanobacterium Synechococcus. Microbiology 148 (2002) 2255-2265
47. Schwarz R., and Forchhammer K. Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiology 151 (2005) 2503-2514
48. Silva P., Thompson E., Bailey S., Kruse O., Mullineaux C.W., Robinson C., Mann N.H., and Nixon P.J. FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. Plant Cell 15 (2003) 2152-2164
49. Stanier R.Y., and Cohen-Bazire G. Phototrophic prokaryotes: the cyanobacteria. Annu. Rev. Microbiol. 31 (1977) 225-274
50. Stanne T.M., Pojidaeva E., Andersson F.I., and Clarke A.K. Distinctive types of ATP-dependent Clp proteases in cyanobacteria. J. Biol. Chem. 282 (2007) 14394-14402
51. Steglich C., Futschik M., Rector T., Steen R., and Chisholm S.W. Genome-wide analysis of light sensing in Prochlorococcus. J. Bacteriol. 188 (2006) 7796-7806
52. Stirnberg M., Fulda S., Huckauf J., Hagemann M., Krämer R., and Marin K. A membrane-bound FtsH protease is involved in osmoregulation in Synechocystis sp. PCC 6803: the compatible solute synthesizing enzyme GgpS is one of the targets for proteolysis. Mol. Microbiol. 63 (2007) 86-102
53. Tolonen A.C., Aach J., Lindell D., Johnson Z.I., Rector T., Steen R., Church G.M., and Chisholm W. Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol. Syst. Biol. 2 (2006) 53
54. Trebst A. Inhibitors in the electron flow. In: San Pietro A. (Ed). Methods Enzymol vol. 69 (1980) 675-715
55. Wang J., Hartling J.A., and Flanagan J.M. The structure of ClpP at 2.3 Å resolution suggests a model for ATP dependent proteolysis. Cell 91 (1997) 447-456
56. Weichart D., Querfurth N., Dreger M., and Hengge-Aronis R. Global role for ClpP-containing proteases in stationary-phase adaptation of Escherichia coli. J. Bacteriol. 185 (2003) 115-125