Skip to main content
SpringerLink
Log in

Gene Expression in the Cyanobacterium Anabaena sp. PCC7120 under Desiccation

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The N2-fixing cyanobacterium Anabaena sp. PCC7120 showed an inherent capacity for desiccation tolerance. A DNA microarray covering almost the entire genome of Anabaena was used to determine the genome-wide gene expression under desiccation. RNA was extracted from cells at intervals starting from early to late desiccation. The pattern of gene expression in DNA fragments was categorized into seven types, which include four types of up-regulated and three types of down-regulated fragments. Validation of the data was carried out by RT-PCR on selected up-regulated DNA fragments and was consistent with the changes in mRNA levels. Our conclusions regarding desiccation tolerance for Anabaena sp. PCC7120 are as follows: (i) Genes for osmoprotectant metabolisms and the K+ transporting system are up-regulated from early to mid-desiccation; (ii) genes induced by osmotic, salt, and low-temperature stress are up-regulated under desiccation; (iii) genes for heat shock proteins are up-regulated after mid-desiccation; (iv) genes for photosynthesis and the nitrogen-transporting system are down-regulated during early desiccation; and (v) genes for RNA polymerase and ribosomal protein are down-regulated between the early and the middle phase of desiccation. Profiles of gene expression are discussed in relation to desiccation acclimation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. MK Ashby CW Mullineaux (1999) ArticleTitleCyanobacterial ycf27 gene products regulate energy transfer from phycobilisomes to photosystems I and II. FEMS Microbiol Lett 181 253–260 Occurrence Handle10.1016/S0378-1097(99)00547-9 Occurrence Handle1:CAS:528:DyaK1MXns1agtrc%3D Occurrence Handle10585546

    Article  CAS  PubMed  Google Scholar 

  2. MG Caiola D Billi EI Friedmann (1996) ArticleTitleEffect of desiccation on envelopes of the cyanobacterium Chroococcidiopsis sp. (Chroococcales). Eur J Phycol 31 97–105

    Google Scholar 

  3. JH Crowe LM Crowe JF Carpenter AS Rudolph CA Winstrom BJ Spargo TJ Anchordoguy (1988) ArticleTitleInteractions of sugars with membranes. Biochim Biophys Acta 947 367–384 Occurrence Handle10.1016/0304-4157(88)90015-9 Occurrence Handle1:CAS:528:DyaL1cXktleqsrY%3D Occurrence Handle3285894

    Article  CAS  PubMed  Google Scholar 

  4. JH Crowe LM Crowe JF Carpenter CA Winstrom (1987) ArticleTitleStabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242 1–10 Occurrence Handle1:CAS:528:DyaL2sXpvVWqsg%3D%3D Occurrence Handle2954537

    CAS  PubMed  Google Scholar 

  5. JH Crowe FA Hoekstra LM Crowe (1989) ArticleTitleMembrane phase transitions are responsible for imbibitional damage in dry pollen. Proc Natl Acad Sci USA 86 520–523 Occurrence Handle1:CAS:528:DyaL1MXhtFWrurY%3D

    CAS  Google Scholar 

  6. L Curatti E Flores G Salerno (2002) ArticleTitleSucrose is involved in the diazotrophic metabolism of the heterocyst-forming cyanobacterium Anabaena sp. FEBS Lett 513 175–178 Occurrence Handle10.1016/S0014-5793(02)02283-4 Occurrence Handle1:CAS:528:DC%2BD38XitFejsrY%3D Occurrence Handle11904145

    Article  CAS  PubMed  Google Scholar 

  7. MB Eisen PO Brown (1999) ArticleTitleDNA arrays for analysis of gene expression. Methods Enzymol 303 179–205 Occurrence Handle1:CAS:528:DyaK1MXltFOns7o%3D Occurrence Handle10349646

    CAS  PubMed  Google Scholar 

  8. F Engelbrecht K Marin M Hagemann (1999) ArticleTitleExpression of the ggpS gene, involved in osmolyte synthesis in the marine cyanobacterium Synechococcus sp. strain PCC7002, revealed regulatory differences between this strain and the freshwater strain Synechocystis sp. strain PCC6803. Appl Environ Microbiol 65 4822–4829 Occurrence Handle1:CAS:528:DyaK1MXnt1WmtLo%3D Occurrence Handle10543792

    CAS  PubMed  Google Scholar 

  9. JE Frias E Flores A Herrero (1997) ArticleTitleNitrate assimilation gene cluster from the heterocyst-forming cyanobacterium Anabaena sp. strain PCC7120. J Bacteriol 179 477–486 Occurrence Handle8990301

    PubMed  Google Scholar 

  10. RT Gill E Katsoulakis W Schmitt G Taroncher-Oldenburg J Misra G Stephanopoulos (2002) ArticleTitleGenome-wide dynamic transcriptional profiling of the light-to-dark transition in Synechocystis sp. strain PCC6803. J Bacteriol 184 3671–3681 Occurrence Handle10.1128/JB.184.13.3671-3681.2002 Occurrence Handle1:CAS:528:DC%2BD38Xkslyrtro%3D Occurrence Handle12057963

    Article  CAS  PubMed  Google Scholar 

  11. Y Hihara A Kamei M Kanehisa A Kaplan M Ikeuchi (2001) ArticleTitleDNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13 793–806 Occurrence Handle1:CAS:528:DC%2BD3MXjtFWqu7g%3D Occurrence Handle11283337

    CAS  PubMed  Google Scholar 

  12. DR Hill TW Keenan RF Helon M Potts LM Crowl JH Crowl (1997) ArticleTitleExtracellular polysaccharide of Nostoc commune (cyanobacteria) inhibits fusion of membrane vesicles during desiccation. J Appl Phycol 9 237–248 Occurrence Handle10.1023/A:1007965229567 Occurrence Handle1:CAS:528:DyaK2sXns1yhs78%3D

    Article  CAS  Google Scholar 

  13. TR Johnson JI Haynes 2nd JL Wealand LR Yarbrough R Hirschberg (1988) ArticleTitleStructure and regulation of genes encoding phycocyanin and allophycocyanin from Anabaena variabilis ATCC 29413. J Bacteriol 170 1858–1865 Occurrence Handle1:CAS:528:DyaL1cXhvF2isLY%3D Occurrence Handle2450871

    CAS  PubMed  Google Scholar 

  14. T Kaneko Y Nakamura CP Wolk T Kuritz S Sasamoto A Watanabe M Iriguchi A Ishikawa K Kawashima T Kimura Y Kishida M Kohara M Matsumoto A Matsuno A Muraki N Nakazaki S Shimpo M Sugimoto M Takazawa M Yamada M Yasuda S Tabata (2001) ArticleTitleComplete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC7120. DNA Res 8 205–213–227–253

    Google Scholar 

  15. Y Kanesaki I Suzuki SI Allakhverdiev K Mikami N Murata (2002) ArticleTitleSalt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 290 339–348 Occurrence Handle10.1006/bbrc.2001.6201 Occurrence Handle1:CAS:528:DC%2BD38XhsFCnuw%3D%3D Occurrence Handle11779175

    Article  CAS  PubMed  Google Scholar 

  16. H Katoh S Shiga Y Nakahira M Ohmori (2003) ArticleTitleIsolation and characterization of drought-tolerant cyanobacterium Nostoc sp. HK-01. Microb Environ 18 82–88 Occurrence Handle10.1264/jsme2.18.82

    Article  Google Scholar 

  17. SB Leslie E Israeli B Lighthart JH Crowe LM Crowe (1995) ArticleTitleTrehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl Environ Microbiol 61 3592–3597 Occurrence Handle1:CAS:528:DyaK2MXosFGnu7Y%3D Occurrence Handle7486995

    CAS  PubMed  Google Scholar 

  18. M Lonetto M Gribskov CA Gross (1992) ArticleTitleThe sigma-70 family: sequence conservation and evolutionary relationships. J Bacteriol 174 3843–3849 Occurrence Handle1:CAS:528:DyaK38XkvVGgsLY%3D

    CAS  Google Scholar 

  19. G Mackinney (1941) ArticleTitleAbsorption of light by chlorophyll solutions. J Biol Chem 140 315–322 Occurrence Handle1:CAS:528:DyaH3MXkt1GgsQ%3D%3D

    CAS  Google Scholar 

  20. K Maruta K Hattori T Nakada M Kubota T Sugimoto M Kurimoto (1996) ArticleTitleCloning and sequencing of trehalose biosynthesis genes from Arthrobacter sp. Q36. Biochim Biophys Acta 1289 10–13 Occurrence Handle10.1016/0304-4165(95)00139-5 Occurrence Handle1:CAS:528:DyaK28XhtlWht7g%3D Occurrence Handle8605217

    Article  CAS  PubMed  Google Scholar 

  21. A Mohamed C Jansson (1989) ArticleTitleInfluence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 13 693–700 Occurrence Handle1:CAS:528:DyaK3cXnsVSqtQ%3D%3D Occurrence Handle2518835

    CAS  PubMed  Google Scholar 

  22. S Mori A Castoreno PJ Lammers (2002) ArticleTitleTranscript levels of rbcR1, ntcA, and rbcL/S genes in cyanobacterium Anabaena sp. PCC7120 are downregulated in response to cold and osmotic stress. FEMS Microbiol Lett 213 167–173 Occurrence Handle10.1016/S0378-1097(02)00815-7 Occurrence Handle1:CAS:528:DC%2BD38XmtVanur0%3D Occurrence Handle12167533

    Article  CAS  PubMed  Google Scholar 

  23. WH Nitschmann L Packer (1992) ArticleTitleNMR studies on Na+ transport in Synechococcus PCC6311. Arch Biochem Biophys 294 347–352 Occurrence Handle1:CAS:528:DyaK38XhvFSrsLo%3D

    CAS  Google Scholar 

  24. M Nylander P Heino E Helenius ET Palva H Ronne BV Welin (2001) ArticleTitleThe low-temperature- and salt-induced RCI2A gene of Arabidopsis complements the sodium sensitivity caused by a deletion of the homologous yeast gene SNA1. Plant Mol Biol 45 341–352 Occurrence Handle10.1023/A:1006451914231 Occurrence Handle1:CAS:528:DC%2BD3MXis1Kgt70%3D Occurrence Handle11292079

    Article  CAS  PubMed  Google Scholar 

  25. M Ohmori M Ikeuchi N Sato CP Wolk T Kaneko T Ogawa M Kanehisa S Goto S Kawashima S Okamoto H Yoshimura H Katoh T Fujisawa S Ehira A Kamei S Yoshihara R Narikawa S Tabata (2001) ArticleTitleCharacterization of genes encoding multi-domain proteins in the genome of the filamentous nitrogen-fixing Cyanobacterium Anabaena sp. strain PCC7120. DNA Res 8 271–284 Occurrence Handle1:CAS:528:DC%2BD38XhtFGhsL0%3D Occurrence Handle11858227

    CAS  PubMed  Google Scholar 

  26. T Onizuka H Akiyama S Endo S Kanai M Hirano S Tanaka H Miyasaka (2002) ArticleTitleCO2 response element and corresponding trans-acting factor of the promoter for ribulose-1,5-bisphosphate carboxylase/oxygenase genes in Synechococcus sp. PCC7002 found by an improved electrophoretic mobility shift assay. Plant Cell Physiol 43 660–667 Occurrence Handle10.1093/pcp/pcf082 Occurrence Handle1:CAS:528:DC%2BD38XkvVChtLo%3D Occurrence Handle12091720

    Article  CAS  PubMed  Google Scholar 

  27. M Page-Sharp CA Behm GD Smith (1999) ArticleTitleInvolvement of the compatible solutes trehalose and sucrose in the response to salt stress of a cyanobacterial Scytonema species isolated from desert soils. Biochim Biophys Acta 1472 519–528 Occurrence Handle10.1016/S0304-4165(99)00155-5 Occurrence Handle1:CAS:528:DyaK1MXntlCltr8%3D Occurrence Handle10564766

    Article  CAS  PubMed  Google Scholar 

  28. M Potts (1999) ArticleTitleMechanisms of desiccation tolerance in cyanobacteria. Eur J Phycol 34 319–328 Occurrence Handle10.1017/S0967026299002267

    Article  Google Scholar 

  29. RH Reed WDP Stewart (1985) ArticleTitleEvidence for target sensitive K+ influx in the cyanobacteria Anabaena variabilis ATCC 29413 and Synechocystis PCC6714. Biochim Biophys Acta 812 155–162 Occurrence Handle10.1016/0005-2736(85)90533-4 Occurrence Handle1:CAS:528:DyaL2MXnsFCnsA%3D%3D

    Article  CAS  Google Scholar 

  30. RH Reed LJ Borowitzka MA Mackay JA Chudek R Foster SRC Warr DJ Moore WDP Stewart (1986) ArticleTitleOrganic solute accumulation in osmotically stressed cyanobacteria. FEMS Microbiol Lett 39 51–56 Occurrence Handle10.1016/0378-1097(86)90060-1 Occurrence Handle1:CAS:528:DyaL28XktlyrsbY%3D

    Article  CAS  Google Scholar 

  31. PA Roger S Ardeles (1991) ArticleTitleThe IRRI blue-green algae collection and computerized information on the strain available for distribution. J Appl Physiol 3 375–376

    Google Scholar 

  32. N Sato (1992) ArticleTitleCloning of a low-temperature-induced gene lti2 from the cyanobacterium Anabaena variabilis M3 that is homologous to alpha-amylases. Plant Mol Biol 18 165–170 Occurrence Handle1:CAS:528:DyaK3sXhs1enurg%3D Occurrence Handle1731972

    CAS  PubMed  Google Scholar 

  33. M Schena D Shalon RW Davis PO Brown (1995) ArticleTitleQuantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270 467–470 Occurrence Handle1:CAS:528:DyaK2MXovVersLk%3D Occurrence Handle7569999

    CAS  PubMed  Google Scholar 

  34. SH Schwartz TA Black K Jager JM Panoff CP Wolk (1998) ArticleTitleRegulation of an osmoticum-responsive gene in Anabaena sp. strain PCC 7120. J Bacteriol 180 6332–6337 Occurrence Handle1:CAS:528:DyaK1cXnslyisLs%3D Occurrence Handle9829944

    CAS  PubMed  Google Scholar 

  35. M Seki M Narusaka J Ishida T Nanjo M Fujita Y Oono A Kamiya M Nakajima A Enju T Sakurai M Satou K Akiyama T Taji K Yamaguchi-Shinozaki P Carninci J Kawai Y Hayashizaki K Shinozaki (2002) ArticleTitleMonitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31 279–292 Occurrence Handle10.1046/j.1365-313X.2002.01359.x Occurrence Handle1:CAS:528:DC%2BD38XntFelsLg%3D Occurrence Handle12164808

    Article  CAS  PubMed  Google Scholar 

  36. RY Stanier R Kunisawa M Mandel G Cohen-Bazire (1971) ArticleTitlePurification and properties of unicellular blue-green alga (order Chroococcales). Bacteriol Rev 35 171–205 Occurrence Handle1:STN:280:CS6B2srgs1E%3D Occurrence Handle4998365

    CAS  PubMed  Google Scholar 

  37. W Tezara VJ Mitchell SD Driscoll DW Lawlor (1999) ArticleTitleWater stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401 914–917 Occurrence Handle1:CAS:528:DyaK1MXntFyltbo%3D

    CAS  Google Scholar 

  38. J Vinnemeier A Kunert M Hagemann (1998) ArticleTitleTranscriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC6803. FEMS Microbiol Lett 169 323–330 Occurrence Handle10.1016/S0378-1097(98)00478-9 Occurrence Handle1:CAS:528:DyaK1cXnvVSqtrY%3D Occurrence Handle9868777

    Article  CAS  PubMed  Google Scholar 

  39. WQ Xie D Tice M Potts (1995) ArticleTitleCell-water deficit regulates expression of rpoC1C2 (RNA polymerase) at the level of mRNA in desiccation-tolerant Nostoc commune UTEX 584 (Cyanobacteria). FEMS Microbiol Lett 126 159–164 Occurrence Handle10.1016/0378-1097(95)00004-O Occurrence Handle1:CAS:528:DyaK2MXjs1CqsLw%3D

    Article  CAS  Google Scholar 

  40. R Zhou CP Wolk (2002) ArticleTitleIdentification of an akinete marker gene in Anabaena variabilis. J Bacteriol 184 2529–2532 Occurrence Handle1:CAS:528:DC%2BD38XjvFeisL8%3D Occurrence Handle11948167

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. S. Kuhara and Dr. K. Tashiro, Kyushu University, for construction of the DNA microarray, as well as Mrs. N. Tamura for her technical support. This work was supported by a grant from the Bio-oriented Technology Research Advancement Institution, Japan, and by a Grant-in-Aid for Scientific Research on Priority Areas (12206002) and a Grant-in-Aid (12440223) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. R.K. Asthana acknowledges the financial support received under the INSA-JSPS exchange program.

Author information

Authors and Affiliations

  1. Department of Life Sciences (Biology), University of Tokyo, Komaba 3-8-1, Meguro, Tokyo 153-8902, Japan

    H. Katoh & M. Ohmori

  2. Bio-oriented Technology Research Advancement Institution (BRAIN), 1-40-2 Nisshin, Saitama, Saitama 331-8537, Japan

    H. Katoh

  3. Department of Botany, Banaras Hindu University, B.H.U. Varanasi-221 005, India

    R. K. Asthana

Authors
  1. H. Katoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. K. Asthana
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Ohmori
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Ohmori.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Katoh, H., Asthana, R. & Ohmori, M. Gene Expression in the Cyanobacterium Anabaena sp. PCC7120 under Desiccation . Microb Ecol 47, 164–174 (2004). https://doi.org/10.1007/s00248-003-1043-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-003-1043-6

Keywords

Search

Navigation