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Trehalose-Producing Enzymes MTSase and MTHase in Anabaena 7120 Under NaCl Stress

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Abstract

Salt tolerance, a multigenic trait, necessitates knowledge about biosynthesis and function of candidate gene(s) at the cellular level. Among the osmolytes, trehalose biosynthesis in cyanobacteria facing NaCl stress is little understood. Anabaena 7120 filaments exposed to 150 mm NaCl fragmented and recovered on transfer to –NaCl medium with the increased heterocysts frequency (7%) over the control (4%). Cells failed to retain Na+ beyond a threshold [2.19 mm/cm3 (PCV)]. Whereas NaCl-stressed cells exhibited a marginal rise in K+ (1.1-fold) only at 30 h, for Na+ it was 130-fold at 48 h over cells in control. A time-course study (0–54 h) revealed reduction in intracellular Na+ beyond 48 h [0.80 mm/cm3 (PCV)] suggestive of ion efflux. The NaCl-stressed cells showed differential expression of maltooligosyltrehalose synthase (MTSase; EC 5.4.99.15) and maltooligosyltrehalose trehalohydrolase (MTHase; EC 3.2.1.141) depending on the time and the extent of intracellular Na+ buildup.

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References

  1. Adams DG (2000) Symbiotic interactions In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer Academic, Dordrecht, pp 523–561

    Google Scholar 

  2. Asthana RK, Srivastava S, Singh AP, Kayastha AM, Singh SP (2005) Identification of maltooligosyltrehalose synthase and maltooligosyltrehalose trehalohydrolase enzymes catalyzing trehalose biosynthesis in Anabaena 7120 exposed to NaCl stress. J Plant Physiol 162:1030–1037

    PubMed  CAS  Google Scholar 

  3. Avery SV, Codd GA, Gadd GM (1991) Caesium accumulation and interaction with other monovalent cations in the cyanobacterium Synechocystis PCC 6803. J Gen Microbiol 137:405–413

    CAS  Google Scholar 

  4. Ballal A, Apte SK (2005) Differential expression of two kdp operons in the nitrogen-fixing cyanobacterium Anabaena sp. Strain L-31. Appl Environ Microbiol 71(9):5297–5303

    Article  PubMed  CAS  Google Scholar 

  5. Blumwald E, Tel-Or E (1982) Structural aspects of the adaptation of Nostoc muscorum to salt. Arch Microbiol 132:163–167

    Article  CAS  Google Scholar 

  6. Cann M (2007) A subset of GAF domains are evolutionarily conserved sodium sensor. Mol Microbiol 64:461–472

    Article  PubMed  CAS  Google Scholar 

  7. Close TJ, Lammers PJ (1993) An osmotic stress protein of cyanobacteria is immunologically related to plant dehydrins. Plant Physiol 101:773–779

    Article  PubMed  CAS  Google Scholar 

  8. Curatti L, Folco E, Desplats P, et al. (1998) Sucrose–phosphate synthase from Synechocystis sp.strain PCC 6803: identification of the sps A gene and characterization of the enzyme expressed in Escherichia coli. J Bacteriol 180(24):6776–6779

    PubMed  CAS  Google Scholar 

  9. Davis VJ (1964) Disc electrophoresis: methods and implication to human serum protein. Ann NY Acad Sci 121:404–427

    Article  PubMed  CAS  Google Scholar 

  10. Ferjani A, Mustardy L, Sulpice R, Marin K, Hagemann M, Murata N (2003) Glucosyl glycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131:1628–1637

    Article  PubMed  CAS  Google Scholar 

  11. Gabbay-Azaria R, Schonfeld M, Tel-Or S, Messinger R, Tel-Or E (1992) Respiratory activity in the marine cyanobacterium Spirulina subsalsa and its role in salt tolerance. Arch Microbiol 1578:183–190

    Google Scholar 

  12. Gabby-Azaria R, Tel-Or E (1991) Regualtion of intracellular Na+ content during NaCl upshock in the marine cyanobacterium Spirulina subsalsa cell. Biores Technol 38:215–220

    Article  Google Scholar 

  13. Gonzalez-Hernandez JC, Jimenez- Estrada M, Pena A (2005) Comparative analysis of trehalose production by Debaryomyces hansenii and Saccharomyces cerevisiae under saline stress. Extremophiles 9:7–16

    Article  PubMed  CAS  Google Scholar 

  14. Herbert D, Phipps PJ, Strange RE (1971) Chemical analysis of microbial cells. In: Norris JR, Ribbons DW (eds) Methods in microbiology. Academic Press, London, pp 209–344

    Google Scholar 

  15. Higo A, Katoh H, Ohmori K, Ikeuchi M, Ohmori M (2006) The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 152:979–987

    Article  PubMed  CAS  Google Scholar 

  16. Imashimizu M, Yoshimura H, Katoh H, Ehira S, Ohmori M (2005) NaCl enhances cellular cAMP and upregulates genes related to heterocyst development in the cyanobacterium, Anabaena sp. strain PCC 7120. FEMS Microbiol Lett 253:97–103

    Article  Google Scholar 

  17. Jackman PJH (1985) Bacterial taxonomy based on electrophoretic whole cell protein pattern. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Society of Applied Bacteriology, London, pp 115–129

    Google Scholar 

  18. Joset F, Jeanjean R, Hagemann M (1996) Dynamics of the response of cyanobacteria to salt stress: deciphering the molecular events. Physiol Planta 96:738–744

    Article  CAS  Google Scholar 

  19. Kaneko T, Nakamura Y, Wolk CP, et al. (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:205–213, 227–253 (Suppl.)

    Google Scholar 

  20. Kim YH, Kwon TK, Park S, et al. (2000) Trehalose synthesis by sequential reactions of recombinant maltooligosyltrehalose synthase and maltooligosyltrehalose trehalohydrolase from Brevibacterium helvolum. Appl Environ Microbiol 66(11):4620–4624

    Article  PubMed  CAS  Google Scholar 

  21. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of Bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  22. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurements with the Folin-phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  23. Maestri O, Joset F (2000) Regulation by external pH and stationary growth phase of the acetolactate synthase from Synechocystis PCC 6803. Mol Microbiol 37(4):828–838

    Article  PubMed  CAS  Google Scholar 

  24. Marin K, Suzuki I, Yamaguchi K, et al. (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 100(15):9061–9066

    Article  PubMed  CAS  Google Scholar 

  25. Maruta K, Hattori K, Nakada T, Kubota M, Sugimoto T, Kurimoto M (1996) Cloning and sequencing of trehalose biosynthesis genes from Arthrobacter sp. Q36. Biochim Biophys Acta 1289:10–13

    PubMed  Google Scholar 

  26. Ning SB, Guo HL, Wang L, Song YC (2002) Salt stress induces programmed cell death in prokaryotic organism Anabaena. J Appl Microbiol 93:15–28

    Article  PubMed  CAS  Google Scholar 

  27. Page-Sharp M, Behm CA, Smith GD (1999) Involvement 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

    PubMed  CAS  Google Scholar 

  28. Paula D, Eduardo F, Salerno GL (2005) Sucrose may play an additional role to that of an osmolyte in Synechocystis sp. PCC6803 salt-shocked cells. Plant Physiol Biochem 43:133–138

    Article  Google Scholar 

  29. Porchia AC, Salerno GL (1996) Sucrose biosynthesis in a prokaryotic organism: presence of two sucrose–phosphate synthases in Anabaena with remarkable differences compared with the plant enzymes. Proc Natl Acad Sci USA 93:13,600–13,604

    Article  CAS  Google Scholar 

  30. Reed RH, Stewart WDP (1988) The responses of cyanobacteria to salt stress. In: Rogers LJ, Gallan JR (eds) Biochemistry of the algae and cyanobacteria. Vol. 12. Clarendon Press, Oxford, pp 217–231

    Google Scholar 

  31. Reed RH, Warr SRC, Richardson DL, Moore DJ, Stewart WDP (1985) Multiphasic osmotic adjustment in a euryhaline cyanobacterium. FEMS Microbiol Lett 28:225–229

    Article  CAS  Google Scholar 

  32. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  33. Schiraldi C, Di Lernia I, De Rosa M (2002) Trehalose production: exploiting novel approaches. Trends Biotechnol 20(10):420–425

    Article  PubMed  CAS  Google Scholar 

  34. Sorokin C (1973) Dry weight, packed cell volume and optical density. In: Stein JR (ed) Handbook of phycological methods culture methods and growth measurements. Cambridge University Press, Cambridge, pp 322–343

    Google Scholar 

  35. Sue HL, Pringle JR (1980) Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143:1384–1394

    Google Scholar 

  36. Warr SRC, Reed RH, Stewart WDP (1987) Low molecular-weight carbohydrate biosynthesis and the distribution of cyanobacteria (blue-green algae) in marine environments. Br Phycol J 22:175–180

    Article  Google Scholar 

  37. Zar JH (1974) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, NJ

    Google Scholar 

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Acknowledgments

We are grateful to the Head and Programme Coordinator, CAS in Botany, Banaras Hindu University for lab facilities and the Head, Regional Sophisticated Instrumentation Centre, Central Drug Research Institute, Lucknow for HPLC. Financial support from CSIR, New Delhi 9/13(90)/06-EMR-I to Subhasha Nigam and (CSIR F.No. 9113 (008)/2004-EMR-I) to Archana Maurya is gratefully acknowledged.

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Authors and Affiliations

  1. Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, 221005, India

    Ravi K. Asthana, Subhasha Nigam, Archana Maurya & Sureshwar P. Singh

  2. School of Biotechnology, Banaras Hindu University, Varanasi, 221005, India

    Arvind M. Kayastha

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  1. Ravi K. Asthana
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  2. Subhasha Nigam
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  3. Archana Maurya
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  4. Arvind M. Kayastha
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Correspondence to Ravi K. Asthana.

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Asthana, R.K., Nigam, S., Maurya, A. et al. Trehalose-Producing Enzymes MTSase and MTHase in Anabaena 7120 Under NaCl Stress. Curr Microbiol 56, 429–435 (2008). https://doi.org/10.1007/s00284-008-9121-0

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