Diverse Cyanobacteria Resource from North East Region of India for Valuable Biomolecules: Phycobiliprotein, Carotenoid, Carbohydrate and Lipid

Author(s): Ashmita Ghosh, Saumyakanti Khanra, Gopinath Haldar, Tridib Kumar Bhowmick*, Kalyan Gayen*.

Journal Name: Current Biochemical Engineering

Volume 5 , Issue 1 , 2019

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Abstract:

Background: North east region of India is well known as biodiversity hotspot with endemic flora and fauna. Organisms belonging to the cyanobacterial species are commonly known as blue green algae and are found in diverse categories in the environment of north-east India. Potentials of these cyanobacterial species are mostly unexplored. Present study aimed to isolate, identify and evaluate the potential cyanobacterial strains for the sustainable producers of biomolecules with agricultural, therapeutic and industrial significance.

Methods: Growth and biochemical characterization were performed with the isolated cyanobacterial species to investigate the growth kinetics, cellular pigments (carotenoid, phycobiliprotein and chlorophyll), protein, carbohydrate and lipid content.

Results: Three Phormidium sp., one Oscillatoria sp., and one Microcoleus sp. were isolated from the Tripura state (North-east region of India). Results revealed that isolated Oscillatoria sp. has high lipid (~20%), protein (~40%), and carbohydrate (~30%) yield. Further, two isolated Phormidium sp., produced significant amount of carotenoids (~23 mg/gm dry biomass), phycobiliprotein (~20-25%) and high protein (~55%). Microcoleus sp. produced 62% carbohydrate and 20% phycobiliprotein with significant amount of carotenoids (~17 mg/gm dry biomass).

Conclusion: Isolated Oscillatoria sp. is the promising resource for lipid and nutritional supplement due to high accumulated primary metabolites. Two Phormidium sp., can be used as animal and human nutritional food supplement and also can be further investigated for pigment production at industrial scale. Isolated Microcoleus sp. is the potential resource of carbohydrate and pigment. Isolated cyanobacterial strains are identified as viable candidates for the industrial production of biomass as well as other value added biomolecules.

Keywords: Cyanobacteria, north east india, phycobiliprotein, carotenoids, polysaccharide, fatty acid.

[1]
N. Thajuddin, and G. Subramanian, "Cyanobacterial biodiver-sity and potential applications in biotechnology", Curr. Sci., vol. 89, pp. 47-57, 2005.
[2]
L. Barsanti, and P. Gualtieri, Algae: anatomy, biochemistry, and biotechnology., CRC press, 2014.
[3]
F.G. Flores, and A. Herrero, The cyanobacteria: molecular biology, genomics, and evolution., Horizon Scientific Press, 2008.
[4]
F. Metting Jr, "Biodiversity and application of microalgae", J. Ind. Microbiol., vol. 17, pp. 477-489, 1996.
[5]
P. Spolaore, C. Joannis-Cassan, E. Duran, and A. Isambert, "Commercial applications of microalgae", J. Biosci. Bioeng., vol. 101, no. 2, pp. 87-96, 2006.
[PMID: 16569602]
[6]
L.T. Tan, "Bioactive natural products from marine cyanobacteria for drug discovery", Phytochemistry, vol. 68, no. 7, pp. 954-979, 2007.
[PMID: 17336349]
[7]
K. Harada, "Production of secondary metabolites by freshwater cyanobacteria", Chem. Pharm. Bull. (Tokyo), vol. 52, no. 8, pp. 889-899, 2004.
[PMID: 15304980]
[8]
I.M. Ehrenreich, J.B. Waterbury, and E.A. Webb, "Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes", Appl. Environ. Microbiol., vol. 71, no. 11, pp. 7401-7413, 2005.
[PMID: 16269782]
[9]
S. Antonopoulou, H.C. Karantonis, T. Nomikos, A. Oikonomou, E. Fragopoulou, and A. Pantazidou, "Bioactive polar lipids from Chroococcidiopsis sp. (Cyanobacteria)", Comp. Biochem. Physiol. B Biochem. Mol. Biol., vol. 142, no. 3, pp. 269-282, 2005.
[PMID: 16198133]
[10]
R.W. Thacker, and V.J. Paul, "Morphological, chemical, and genetic diversity of tropical marine cyanobacteria Lyngbya spp. and Symploca spp. (Oscillatoriales)", Appl. Environ. Microbiol., vol. 70, no. 6, pp. 3305-3312, 2004.
[PMID: 15184125]
[11]
K. Skjånes, C. Rebours, and P. Lindblad, "Potential for green microalgae to produce hydrogen, pharmaceuticals and other high value products in a combined process", Crit. Rev. Biotechnol., vol. 33, no. 2, pp. 172-215, 2013.
[PMID: 22765907]
[12]
R.M.M. Abed, S. Dobretsov, and K. Sudesh, "Applications of cyanobacteria in biotechnology", J. Appl. Microbiol., vol. 106, no. 1, pp. 1-12, 2009.
[PMID: 19191979]
[13]
M.A. Borowitzka, Patents on cyanobacteria and cyanobacte-rial products and uses., John Wiley & Sons, Ltd, 2014, pp. 329-338.
[14]
J.S. Singh, A. Kumar, A.N. Rai, and D.P. Singh, "Cyanobacteria: A precious bio-resource in agriculture, ecosystem, and environmental sustainability", Front. Microbiol., vol. 7, p. 529, 2016.
[PMID: 27148218]
[15]
C.A. Kerfeld, "Water-soluble carotenoid proteins of cyanobacteria", Arch. Biochem. Biophys., vol. 430, no. 1, pp. 2-9, 2004.
[PMID: 15325905]
[16]
C. Liang, F. Zhao, W. Wei, Z. Wen, and S. Qin, "Carotenoid biosynthesis in cyanobacteria: structural and evolutionary scenarios based on comparative genomics", Int. J. Biol. Sci., vol. 2, no. 4, pp. 197-207, 2006.
[PMID: 16967101]
[17]
http://www.synthsys.ed.ac.uk/news/team-create-molecular-toolbox-boost-cyanobacterial-pigment-production
[18]
http://www.parrynutraceuticals.com/
[19]
http://www.oilgae.com/non_fuel_products/betacarotene.html
[20]
A.N. Glazer, "Phycobiliproteins — a family of valuable, widely used fluorophores", J. Appl. Phycol., vol. 6, pp. 105-112, 1994.
[21]
R.R. Sonani, R.P. Rastogi, R. Patel, and D. Madamwar, "Recent advances in production, purification and applications of phycobiliproteins", World J. Biol. Chem., vol. 7, no. 1, pp. 100-109, 2016.
[PMID: 26981199]
[22]
R.M. Chaloub, N.M.S. Motta, S.P. de Araujo, P.F. de Aguiar, and A.F. da Silva, "Combined effects of irradiance, temperature and nitrate concentration on phycoerythrin con-tent in the microalga Rhodomonas sp. (Cryptophyceae)", Algal Res., vol. 8, pp. 89-94, 2015.
[23]
A.R. Grossman, M.R. Schaefer, G.G. Chiang, and J.L. Collier, "The phycobilisome, a light-harvesting complex responsive to environmental conditions", Microbiol. Rev., vol. 57, no. 3, pp. 725-749, 1993.
[PMID: 8246846]
[24]
A.N. Glazer, "Structure and molecular organization of the photosynthetic accessory pigments of cyanobacteria and red algae", Mol. Cell. Biochem., vol. 18, no. 2-3, pp. 125-140, 1977.
[PMID: 415227]
[25]
C. Romay, J. Armesto, D. Remirez, R. González, N. Ledon, and I. García, "Antioxidant and anti-inflammatory properties of C-phycocyanin from blue-green algae", Inflamm. Res., vol. 47, no. 1, pp. 36-41, 1998.
[PMID: 9495584]
[26]
J. Riss, K. Décordé, T. Sutra, M. Delage, J.C. Baccou, N. Jouy, J.P. Brune, H. Oréal, J.P. Cristol, and J.M. Rouanet, "Phycobiliprotein C-phycocyanin from Spirulina platensis is powerfully responsible for reducing oxidative stress and NADPH oxidase expression induced by an atherogenic diet in hamsters", J. Agric. Food Chem., vol. 55, no. 19, pp. 7962-7967, 2007.
[PMID: 17696484]
[27]
V. Rimbau, A. Camins, C. Romay, R. González, and M. Pallàs, "Protective effects of C-phycocyanin against kainic acid-induced neuronal damage in rat hippocampus", Neurosci. Lett., vol. 276, no. 2, pp. 75-78, 1999.
[PMID: 10624795]
[28]
K.V. Sathyasaikumar, I. Swapna, P.V. Reddy, ChR. Murthy, and K.R. Roy, "A. Dutta Gupta, B. Senthilkumaran, and P. Reddanna, “Co-administration of C-Phycocyanin ameliorates thioacetamide-induced hepatic encephalopathy in Wistar rats", J. Neurol. Sci., vol. 252, no. 1, pp. 67-75, 2007.
[PMID: 17169376]
[29]
Y. Liu, L. Xu, N. Cheng, L. Lin, and C. Zhang, "Inhibitory effect of phycocyanin from Spirulina platensis on the growth of human leukemia K562 cells", J. Appl. Phycol., vol. 12, pp. 125-130, 2000.
[30]
Oilgae, "OILGAE DIGEST- The Algae Energy Industry Opportunities & Prospects", Chennai – 600034.
[31]
http://www.oilgae.com/non_fuel_products/phycoerythrin.html
[32]
C. Paliwal, T. Ghosh, B. George, I. Pancha, R. Maurya, and K. Chokshi, "Microalgal carotenoids: Potential nutraceuti-cal compounds with chemotaxonomic importance", Algal Res., vol. 15, pp. 24-31, 2016.
[33]
U.J. Jürgens, and J. Weckesser, "The fine structure and chemical composition of the cell wall and sheath layers of cyanobacteria", Ann. Inst. Pasteur Microbiol., vol. 136A, no. 1, pp. 41-44, 1985.
[PMID: 3923903]
[34]
S. Ball, C. Colleoni, U. Cenci, J.N. Raj, and C. Tirtiaux, "The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis", J. Exp. Bot., vol. 62, no. 6, pp. 1775-1801, 2011.
[PMID: 21220783]
[35]
D.F. Gómez Casati, M.A. Aon, and A.A. Iglesias, "Ultrasensitive glycogen synthesis in Cyanobacteria", FEBS Lett., vol. 446, no. 1, pp. 117-121, 1999.
[PMID: 10100626]
[36]
S.A. Angermayr, K.J. Hellingwerf, P. Lindblad, and M.J.T. de Mattos, "Energy biotechnology with cyanobacteria", Curr. Opin. Biotechnol., vol. 20, no. 3, pp. 257-263, 2009.
[PMID: 19540103]
[37]
I.M.P. Machado, and S. Atsumi, "Cyanobacterial biofuel production", J. Biotechnol., vol. 162, no. 1, pp. 50-56, 2012.
[PMID: 22446641]
[38]
X. Lu, "A perspective: photosynthetic production of fatty acid-based biofuels in genetically engineered cyanobacteria", Biotechnol. Adv., vol. 28, no. 6, pp. 742-746, 2010.
[PMID: 20561924]
[39]
A. Ghosh, S. Khanra, M. Mondal, G. Halder, O.N. Tiwari, and S. Saini, "Progress toward isolation of strains and genet-ically engineered strains of microalgae for production of bio-fuel and other value added chemicals: A review", Energy Convers. Manage., vol. 113, pp. 104-118, 2016.
[40]
K. Lee, M.L. Eisterhold, F. Rindi, S. Palanisami, and P.K. Nam, "Isolation and screening of microalgae from natural habitats in the midwestern United States of America for biomass and biodiesel sources", J. Nat. Sci. Biol. Med., vol. 5, no. 2, pp. 333-339, 2014.
[PMID: 25097410]
[41]
M.B. Syiem, B.B. Nongbri, A. Pinokiyo, A. Bhattacharjee, N.A. Nongrum, and L. Hynniewta, "Significance of cyanobacte-rial diversity in different ecological conditions of Meghalaya, India", J. Appl. Nat. Sci., vol. 2, pp. 134-139, 2010.
[42]
A. Singh, O. Gunapati, and O. Singh, "Isolation of fresh water Cyanobacterial DNA of north east India by modified Xan-thogenate method", Int. J. Res. Biosci., vol. 2, pp. 75-82, 2013.
[43]
P. Feng, Z. Deng, Z. Hu, Z. Wang, and L. Fan, "Characterization of Chlorococcum pamirum as a potential biodiesel feedstock", Bioresour. Technol., vol. 162, pp. 115-122, 2014.
[PMID: 24747389]
[44]
M. Muthuraj, V. Kumar, B. Palabhanvi, and D. Das, "Evaluation of indigenous microalgal isolate Chlorella sp. FC2 IITG as a cell factory for biodiesel production and scale up in outdoor conditions", J. Ind. Microbiol. Biotechnol., vol. 41, no. 3, pp. 499-511, 2014.
[PMID: 24445403]
[45]
K. Schütz, T. Happe, O. Troshina, P. Lindblad, E. Leitão, P. Oliveira, and P. Tamagnini, "Cyanobacterial H(2) production -- a comparative analysis", Planta, vol. 218, no. 3, pp. 350-359, 2004.
[PMID: 14564521]
[46]
G. Mackinney, "Absorption of light by chlorophyll solutions", J. Biol. Chem., vol. 140, pp. 315-322, 1941.
[47]
K. Habib, S. Kumar, N. Manikar, S. Zutshi, and T. Fatma, "Biochemical effect of carbaryl on oxidative stress, antioxidant enzymes and osmolytes of cyanobacterium Calothrix brevissima", Bull. Environ. Contam. Toxicol., vol. 87, no. 6, pp. 615-620, 2011.
[PMID: 21979138]
[48]
M. Kumar, J. Kulshreshtha, and G.P. Singh, "Growth and biopigment accumulation of cyanobacterium Spirulina platensis at different light intensities and temperature", Braz. J. Microbiol., vol. 42, no. 3, pp. 1128-1135, 2011.
[PMID: 24031731]
[49]
A. Jensen, Chlorophylls and carotenoids"Handbook of Phycological Methods: Physiological And Biochemical Methods", Hellebust. J. A, and Craigie. J., Eds., Cambridge University Press., 1978, pp. 59-70.
[50]
C. Juin, J-R. Chérouvrier, V. Thiéry, A-L. Gagez, J-B. Bérard, N. Joguet, R. Kaas, J.P. Cadoret, and L. Picot, "Microwave-assisted extraction of phycobiliproteins from Porphyridium purpureum", Appl. Biochem. Biotechnol., vol. 175, no. 1, pp. 1-15, 2015.
[PMID: 25231233]
[51]
A. Patel, S. Mishra, R. Pawar, and P.K. Ghosh, "Purification and characterization of C-Phycocyanin from cyanobacterial species of marine and freshwater habitat", Protein Expr. Purif., vol. 40, no. 2, pp. 248-255, 2005.
[PMID: 15766866]
[52]
A. Bennett, and L. Bogorad, "Complementary chromatic adaptation in a filamentous blue-green alga", J. Cell Biol., vol. 58, no. 2, pp. 419-435, 1973.
[PMID: 4199659]
[53]
S. Kumar, K. Habib, and T. Fatma, "Endosulfan induced biochemical changes in nitrogen-fixing cyanobacteria", Sci. Total Environ., vol. 403, no. 1-3, pp. 130-138, 2008.
[PMID: 18584851]
[54]
O.N. Tiwari, R. Khangembam, M. Shamjetshabam, A.S. Sharma, G. Oinam, and J.J. Brand, "Characterization and Optimization of Bioflocculant Exopolysaccharide Production by Cyanobacteria Nostoc sp. BTA97 and Anabaena sp. BTA990 in Culture Conditions", Appl. Biochem. Biotechnol., vol. 176, no. 7, pp. 1950-1963, 2015.
[PMID: 26041059]
[55]
R.G. Spiro, "Analysis of sugars found in glycoproteins", Methods in Enzymol.. vol. 8, 1966, pp. 3-26.
[56]
K. Phadwal, and P.K. Singh, "Effect of nutrient depletion on β-carotene and glycerol accumulation in two strains of Dunaliella sp", Bioresour. Technol., vol. 90, no. 1, pp. 55-58, 2003.
[PMID: 12835057]
[57]
D. Herbert, P. Phipps, and R. Strange, "Chemical analysis of microbial cells", Methods in Microbiol.. 1971, pp. 209-344.
[58]
M. Mondal, A. Ghosh, A.S. Sharma, O.N. Tiwari, K. Gayen, and M.K. Mandal, "Mixotrophic cultivation of Chlorella sp. BTA 9031 and Chlamydomonas sp. BTA 9032 isolated from coal field using various carbon sources for biodiesel produc-tion", Energy Convers. Manage., vol. 124, pp. 297-304, 2016.
[59]
T.V. Desikachary, Cyanophyta., Indian Council of Agriculture Research, 1959.
[60]
T.A. Sarma, Handbook of Cyanobacteria., CRC Press, 2012.
[61]
S. International Association for Cyanophyte Research, Proceedings of the 13th Symposium of the International As-sociation for Cyanophyte Research (IAC), 1995 Frascati (Italy)
[62]
O. Strunecký, J. Komárek, J. Johansen, A. Lukešová, and J. Elster, "Molecular and morphological criteria for revision of the genus Microcoleus (Oscillatoriales, Cyanobacteria)", J. Phycol., vol. 49, no. 6, pp. 1167-1180, 2013.
[PMID: 27007635]
[63]
T.E. Jensen, "Fine structure of elongate polyhedral bodies (carboxysomes) in two Oscillatoria (Cyanophyceae) isolates", Microbios, vol. 79, no. 321, pp. 203-214, 1994.
[PMID: 7837992]
[64]
D. Tashyreva, J. Elster, and D. Billi, "A novel staining protocol for multiparameter assessment of cell heterogeneity in Phormidium populations (cyanobacteria) employing fluorescent dyes", PLoS One, vol. 8, no. 2, 2013.e55283
[PMID: 23437052]
[65]
J. Komárek, and K. Anagnostidis, Cyanoprokaryota. 1. Teil: Chroococcales, .
[66]
J. Komárek, and K. Anagnostidis, Süßwasserflora von Mitteleuropa, Bd. 19/2: Cyanoprokaryota
[67]
J. Komárek, Cyanoprokaryota. Heterocytous genera, Süsswasserflora von Mitteleuropa, Bd. 19/3
[68]
N. Singh, N. Singh, G. Devi, and S. Singh, "Cyanobacterial flora of rice field soils of Tripura", Phykos, vol. 36, pp. 121-126, 1997.
[69]
J. Dihingia, and P.P. Baruah, "Population dynamics of cyano-bacteria in alluvial rice grown soils of lower Brahmaputra floodplain", Phykos, vol. 45, pp. 54-62, 2015.
[70]
S.K. Saha, R. Das, K.N. Bora, and L. Uma, "Biodiversity of epilithic cyanobacteria from freshwater streams of Kakoijana reserve forest, Assam, India", Indian J. Microbiol., vol. 47, no. 3, pp. 219-232, 2007.
[PMID: 23100670]
[71]
H.G. Truper, "Prokaryotes: an overview with respect to bio-diversity and environmental importance", Biodivers. Conserv., vol. 1, pp. 227-236, 1992.
[72]
K. Ojit Singh, T. Indrama, O. Gunapati, O. Avijeet Singh, S. Minerva, and C. Silvia, "Morphological and molecular char-acterization of potential cyanobacteria isolated from Loktak Lake", Int. J. Adv. Res. (Indore), vol. 3, pp. 19-27, 2015.
[73]
T. Rezanka, I. Dor, A. Prell, and V.M. Dembitsky, "Fatty acid composition of six freshwater wild cyanobacterial species", Folia Microbiol. (Praha), vol. 48, no. 1, pp. 71-75, 2003.
[PMID: 12744080]
[74]
S. Rodjaroen, N. Juntawong, A. Mahakhant, and K. Miya-moto, "High biomass production and starch accumulation in native green algal strains and cyanobacterial strains of Thai-land", Witthayasan Kasetsat Witthayasat, vol. 41, pp. 570-575, 2007.
[75]
A. Parikh, and D. Madamwar, "Partial characterization of extracellular polysaccharides from cyanobacteria", Bioresour. Technol., vol. 97, no. 15, pp. 1822-1827, 2006.
[PMID: 16256343]
[76]
J.G. Ormerod, Physiology of the Photosynthetic Prokary-otes., Springer, US, 1992, pp. 93-120.
[77]
A. Hosikian, S. Lim, R. Halim, and M.K. Danquah, "Chloro-phyll extraction from microalgae: A review on the process engineering aspects", Int. J. Chem. Eng., vol. 2010, p. 11, 2010.
[78]
A. Wilson, G. Ajlani, J.M. Verbavatz, I. Vass, C.A. Kerfeld, and D. Kirilovsky, "A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria", Plant Cell, vol. 18, no. 4, pp. 992-1007, 2006.
[PMID: 16531492]
[79]
J.A. Del Campo, M. García-González, and M.G. Guerrero, "Outdoor cultivation of microalgae for carotenoid production: current state and perspectives", Appl. Microbiol. Biotechnol., vol. 74, no. 6, pp. 1163-1174, 2007.
[PMID: 17277962]
[80]
N.K. Singh, A. Parmar, and D. Madamwar, "Optimization of medium components for increased production of C-phycocyanin from Phormidium ceylanicum and its purification by single step process", Bioresour. Technol., vol. 100, no. 4, pp. 1663-1669, 2009.
[PMID: 18954974]
[81]
B. Soni, B. Kalavadia, U. Trivedi, and D. Madamwar, "Extrac-tion, purification and characterization of phycocyanin from Oscillatoria quadripunctulata—Isolated from the rocky shores of Bet-Dwarka, Gujarat, India", Process Biochem., vol. 41, pp. 2017-2023, 2006.
[82]
C. Hu, Y. Liu, B.S. Paulsen, D. Petersen, and D. Klaveness, "Extracellular carbohydrate polymers from five desert soil al-gae with different cohesion in the stabilization of fine sand grain", Carbohydr. Polym., vol. 54, pp. 33-42, 2003.
[83]
K.B. Möllers, D. Cannella, H. Jørgensen, and N.U. Frigaard, "Cyanobacterial biomass as carbohydrate and nutrient feedstock for bioethanol production by yeast fermentation", Biotechnol. Biofuels, vol. 7, p. 64, 2014.
[PMID: 24739806]
[84]
G. Subramanian, M. Anusha, G.B.A. Leela, R. Latha, J. Sasikala, and R. Chandrasakaran, "Carbohydrate and Protein content of five species of Marine Cyanobacteria from Pamban and Vadakadu (Rameswaram) coastal regions, Tamil Nadu, India", Int J Adv Interdiscipl Res, vol. 1, pp. 18-24, 2014.
[85]
K. Sharathchandra, and M. Rajashekhar, "Total lipid and fatty acid composition in some freshwater cyanobacteria", J Algal Biomass Util, vol. 2, pp. 83-97, 2011.
[86]
E. Abedi, and M.A. Sahari, "Long-chain polyunsaturated fatty acid sources and evaluation of their nutritional and functional properties", Food Sci. Nutr., vol. 2, no. 5, pp. 443-463, 2014.
[PMID: 25473503]


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VOLUME: 5
ISSUE: 1
Year: 2019
Page: [21 - 33]
Pages: 13
DOI: 10.2174/2212711905666180817105828

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