Growth and Nitrogen (N) Metabolizing Enzymes of Mesophilic and Psychrophilic Heterocystous Cyanobacteria—In Response to Temperature Regimes

Shan Ahamed Tharifkhan, Deviram Garlapati, Darshana Arulraj, Uma Lakshmanan, Dharmar Prabaharan


The increased NR & NiR activity, GS and nitrogenase activities at 25°C and 35°C in psychrophilic and mesophilic organisms indicates that the Arctic isolate is a psychrotolerant as it shows increased enzyme levels than its original temperature in which we isolated the organism though biomass was greater at 3°C. The biomass and enzyme data indicates cyanobacteria are the initiators of primary colonization in polar and alpine environments and are responsible for the nitrogen and carbon incorporation into biosphere. The nitrogenase activity as measured by ARA was high at 37°C mesophilic and 25°C was found to be optimum for psychrophilic. Likewise, NR & NiR was also optimal at 25°C.


Keywords: Arctic, cyanobacteria, glutamine synthetase, nitrate reductase, nitrite reductase, nostoc calcicole

Cite this Article

Shan Ahamed Tharifkhan, Deviram Garlapati, Dharshana Arulraj et al. Growth and Nitrogen (N) Metabolizing Enzymes of Mesophilic and Psychrophilic Heterocystous Cyanobacteria—In Response to Temperature Regimes. Research & Reviews: A Journal of Life Sciences. 2018; 8(3): 31–43p


Arctic, Cyanobacteria, Nitrate Reductase, Nitrite Reductase, Glutamine synthetase, Nostoc calcicola.

Full Text:




Ramos VMC, Castelo-Branco R, Leão PN, Martins J, Carvalhal-Gomes S, Sobrinho da Silva F, et al. Cyanobacterial Diversity in Microbial Mats from the Hypersaline Lagoon System of Araruama, Brazil: An In-depth Polyphasic Study. Front Microbiol [Internet].2017;8:1233.Availablefrom:

Premanandh J, Priya B, Prabaharan D, Uma L. Genetic heterogeneity of the marine cyanobacterium Leptolyngbya valderiana (Pseudanabaenaceae) evidenced by RAPD molecular markers and 16S rDNA sequence data. J Plankton Res [Internet]. 2009 Oct 1;31(10):1141–50. Available from:

Herrero A, Muro-Pastor AM, Flores E. Nitrogen control in cyanobacteria. J Bacteriol. 2001;183(2):411–25.

Staehr PA, Sand Jensen K. Seasonal changes in temperature and nutrient control of photosynthesis, respiration and growth of natural phytoplankton communities. Freshw Biol. 2006;51(2):249–62.

Thangaraj B, Rajasekar DP, Vijayaraghavan R, Garlapati D, Devanesan AA, Lakshmanan U. Cytomorphological and nitrogen metabolic enzyme analysis of psychrophilic and mesophilic Nostoc sp.: a comparative outlook. 3 Biotech [Internet]. 2017 May;7(2):107. Available from:

Elster J, Benson EE. Life in the polar terrestrial environment with a focus on algae and cyanobacteria. Life frozen state. 2004;111–50.

Margesin R, Häggblom MM. Thematic issue: Microorganisms in cold environments. FEMS Microbiol Ecol [Internet]. 2007;59(2):215–6. Available from:

Schopf JW. The fossil record: tracing the roots of the cyanobacterial lineage. In: The ecology of cyanobacteria. Springer; 2000. p. 13–35.

Vopel K, Hawes I. Photosynthetic performance of benthic microbial mats in Lake Hoare, Antarctica. Limnol Oceanogr [Internet]. 2006;51(4):1801–12. Available from:

Gibson JAE, Wilmotte A, Taton A, Van de Vijver B, Beyens L, Dartnall HJG. Biogeographic trends in Antarctic lake communities. In: Trends in Antarctic terrestrial and limnetic ecosystems. Springer; 2006. p. 71–99.

Säwström C, Mumford P, Marshall W, Hodson A, Laybourn-Parry J. The microbial communities and primary productivity of cryoconite holes in an Arctic glacier (Svalbard 79°N). Polar Biol [Internet]. 2002;25(8):591–6. Available from:

Mueller DR, Vincent WF, Bonilla S, Laurion I. Extremotrophs, extremophiles and broadband pigmentation strategies in a high arctic ice shelf ecosystem. FEMS Microbiol Ecol [Internet]. 2005;53(1):73–87. Available from:

Saha SK, Das R, Bora KN, Uma L. Biodiversity of epilithic cyanobacteria from freshwater streams of Kakoijana reserve forest, Assam, India. Indian J Microbiol [Internet]. 2007 Sep;47(3):219–32. Available from:

Flores E, Herrero A. Nitrogen assimilation and nitrogen control in cyanobacteria. Portland Press Limited; 2005.

Bonilla S, Villeneuve V, Vincent W F. Benthic and planktonic algal communities in a high arctic lake: pigment structure and contrasting responses to nutrient enrichment. J Phycol [Internet]. 2005; 41 (6): 1120 – 30 . Available from:

Mishra P K, Mukherji S. Biosorption of diesel and lubricating oil on algal biomass. 3 Biotech. 2012 Dec; 2 (4) : 301 - 310. Available from:

Quesada A, Vincent WF. Cyanobacteria in the cryosphere: snow, ice and extreme cold. In: Ecology of cyanobacteria II. Springer; 2012. p. 387–99.

Komárek J, Kovacik L, Elster J, Komárek O. Cyanobacterial diversity of Petuniabukta, Billefjorden, central Spitsbergen. Vol. 33, Polish Polar Research. 2012.

Kvíderová J, Elster J, Šimek M. In situ response of Nostoc commune colonies to desiccation in Central Svalbard, Norwegian High Arctic. Fottea. 2011;11(1):87–97.

Stewart KJ, Coxson D, Grogan P. Nitrogen Inputs by Associative Cyanobacteria across a Low Arctic Tundra Landscape. Arctic, Antarct Alp Res [Internet]. 2011 May 1;43(2):267–78. Available from:

Desikachary T V. Cyanophyta, Indian Council of Agricultural Research, monographs on Algae. New Delhi, India. 1959;

Komárek J, Anagnostidis K. Subwasserflora von mitteleuropa: cyanoprokaryota. In: Subwasserflora von mitteleuropa: cyanoprokaryota. Gustav Fischer; 1999.

Daniel T, A. NB. Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. J Phycol [Internet]. 2001 Dec 25;36(1):251–8. Available from:

Seo P-S, Yokota A. The phylogenetic relationships of cyanobacteria inferred from 16S rRNA, gyrB, rpoC1 and rpoD1 gene sequences. J Gen Appl Microbiol. 2003;49(3):191–203.

Nübel U, Garcia-Pichel F, Muyzer G. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol [Internet]. 1997 Aug;63(8):3327–32. Available from:

Tillett D, Parker DL, Neilan BA. Detection of Toxigenicity by a Probe for the Microcystin Synthetase A Gene (mcyA) of the Cyanobacterial Genus Microcystis: Comparison of Toxicities with 16S rRNA and Phycocyanin Operon (Phycocyanin Intergenic Spacer) Phylogenies. Appl Environ Microbiol [Internet]. 2001 Jun 16;67(6) :2810–8. Available from:

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res [Internet]. 1997 Dec 15;25(24):4876–82. Available from:

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol [Internet]. 2013 Dec 16; 30 (12): 2725–9. Available from:

Mackinney G. Absorption of light by chlorophyll solutions. J Biol Chem [Internet]. 1941 Aug 1;140(2):315–22. Available from:

Craigie JS. Carrageenans and agars. Handbook of Phycol Methods, Physiol Biochem Methods. 1978;109–31.

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem [Internet]. 1951 Nov 1;193(1):265–75. Available from:

Herrero A, Flores E, Guerrero MG. Regulation of nitrate reductase levels in the cyanobacteria Anacystis nidulans, Anabaena sp. strain 7119, and Nostoc sp. strain 6719. J Bacteriol [Internet]. 1981 Jan 1;145(1):175–80. Available from:

Shapiro BM, Stadtman ERBT-M in E. [130] Glutamine synthetase (Escherichia coli). In: Metabolism of Amino Acids and Amines Part A [Internet]. Academic Press; 1970. p. 910–22. Available from:

Stewart WD, Fitzgerald GP, Burris RH. In situ studies on N2 fixation using the acetylene reduction technique. Proc Natl Acad Sci [Internet]. 1967 Nov 1;58(5):2071 LP-2078. Available from:

Makhalanyane TP, Van Goethem MW, Cowan DA. Microbial diversity and functional capacity in polar soils. Curr Opin Biotechnol [Internet]. 2016;38:159–66. Available from:

Grzesiak J, Górniak D, Świątecki A, Aleksandrzak-Piekarczyk T, Szatraj K, Zdanowski MK. Microbial community development on the surface of Hans and Werenskiold Glaciers (Svalbard, Arctic): a comparison. Extremophiles. 2015;19(5):885–97.

Chakraborty S, Santra S, Bhattacharya T. Seasonal variation of enzyme activity and stress metabolites in eight benthic macro algae with fluctuations in salinity of Sunderban estuary, India. Vol. 39, Indian Journal of Marine Sciences. 2010. 429-43 p.

Gonzalez PJ, Correia C, Moura I, Brondino CD, Moura JJG. Bacterial nitrate reductases: molecular and biological aspects of nitrate reduction. J Inorg Biochem. 2006;100(5–6):1015–23.

Jepson BJN, Anderson LJ, Rubio LM, Taylor CJ, Butler CS, Flores E, et al. Tuning a Nitrate Reductase for Function the first spectropotentiometric characterization of a bacterial assimilatory nitrate reductase reveals novel redox properties. J Biol Chem. 2004;279(31):32212–8.

Mérida A, Candau P, Florencio FJ. Regulation of glutamine synthetase activity in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803 by the nitrogen source: effect of ammonium. J Bacteriol [Internet]. 1991;173(13):4095–100. Available from:

Chow F, Capociama F V, Faria R, Oliveira MC de. Characterization of nitrate reductase activity in vitro in Gracilaria caudata J. Agardh (Rhodophyta, Gracilariales). Brazilian J Bot. 2007;30(1):123–9.

Suzuki I, Kikuchi H, Nakanishi S, Fujita Y, Sugiyama T, Omata T. A novel nitrite reductase gene from the cyanobacterium Plectonema boryanum. J Bacteriol [Internet]. 1995; 177 (21) : 6137 – 43. Available from:

Kuznetsova S, Knaff DB, Hirasawa M, Lagoutte B, Sétif P. Mechanism of spinach chloroplast ferredoxin-dependent nitrite reductase: spectroscopic evidence for intermediate states. Biochemistry. 2004;43(2):510–7.

Moreno-Vivián C, Cabello P, Martínez-Luque M, Blasco R, Castillo F. Prokaryotic Nitrate Reduction: Molecular Properties and Functional Distinction among Bacterial Nitrate Reductases. J Bacteriol [Internet]. 1999;181(21):6573–84. Available from:

Flores E, Frías JE, Rubio LM, Herrero A. Photosynthetic nitrate assimilation in cyanobacteria. Photosynth Res [Internet]. 2005;83(2):117–33. Available from:

Jungblut A, F. Vincent W. Cyanobacteria in Polar and Alpine Ecosystems. Psychrophiles: From Biodiversity to Biotechnology: Second Edition. 2017. 181-206 p.

Braker G, Schwarz J, Conrad R. Influence of temperature on the composition and activity of denitrifying soil communities. FEMS Microbiology Ecology. 2010 Jun 3;73(1):134-48.



  • There are currently no refbacks.