Biodiversity of Cyanobacteria in Azhagar hills, Madurai District of Tamil Nadu, India

INT J CURR SCI 2017, 20(1): E 79-86 RESEARCH ARTICLE ISSN 2250-1770 Abstract Biodiversity of Cyanobacteria in Azhagar hills, Madurai District of Tamil Nadu, India Palanivel S and Uma Rani V* Department of Plant Biology and Plant Biotechnology, Gill Research Institute, Guru Nanak College, Chennai-600 042, India *Corresponding author: umarani_gnc@yahoo.co.in Biodiversity of algae from different aquatic habitats were studied extensively in India. Among algae Cyanobacteria (BGA) is an important group of algae which makes valuable contribution to soil fertility by fixing atmospheric nitrogen. In the present study, biodiversity of Cyanobacteria were carried from Azhagar hills of Madurai district of South India. A total of 36 species of 10 genera, 3 families were characterized morphologically and described. Of these 11 were unicellular, 16 non-heterocystous filamentous and 9 heterocystous filamentous with the members of the family Oscillatoriaceae being predominant. Keywords: Cyanobacteria; Oscillatoriaceae; Nostocaceae; Chroococcaceae; Azhagar hills Received: 26 th November 2016; Revised: 19 th December; Accepted: 14 th January; IJCS New Liberty Group 2017 Introduction Cyanobacteria (Blue green algae) are diverse group of organisms that comprises of unicellular to multicellular prokaryotes, possess chlorophyll a and fertility and are considered as potential Biofertilizer component. In recent times, Cyanobacteria was proved to be a potential source of various biotechnological perform photosynthesis (Castenholz and Waterbury, applications. Blue-greens are the source of many 1989). They are diazotrophs, ubiquitous in nature; mostly aquatic but can also survive in extreme climatic conditions such as hot springs, (Castenholz, 1973), valuable products (Richmond, 1990) and because of such properties (proteins, vitamins and pigments) they are used in various fields such as food or fodder snow and ice (Kol, 1968; Laamanen, 1996). Many (Borowitzka and Borowitzka, 1988) fuel (Gao et al., species are capable of living in the soil and other terrestrial habitats, where they play important role in the functional processes of ecosystems (Whitton, 1992). The capacity of several cyanobacteria to fix the atmospheric nitrogen is a significant biological process of economic importance (Santra, 1993). The ability to fix atmospheric nitrogen by both heterocystous (Fogg, 1949) and non heterocystous (Anand, 1980). Cyanobacteria adds valuable contribution to soil 2012), pharmaceutical (Falch et al., 1995), industries (David and Rajan, 2014; Ansari et al., 2016) and so on. Recent study reveals that cyanobacteria has the capacity to degrade the environmental pollutants and can be used as an alternative source of energy (Ananya et al., 2014). Various studies regarding diversity and its applications were carried by many legendary algologists (Geitler, 1932; Fritsch, 1942; Desikachary, 1959; Anand, 1988). The contributions made by

Ganapati, 1940 (Temple tank); Thajuddin and Subramanian, 1992 (Marine); Sankaran, 2001 (Hilly region) are noteworthy. In this regard, the present study has been conducted on the diversity of Cyanobacteria of Azhagar Hills, Madurai district. Materials and Methods Study area Eastern Ghats (EG) is a long stretch of hills that spread through Eastern part of India, covering four states in which Tamil Nadu is one of the States. Azhagar Hills is in the extension part of Eastern Ghats and is located 21 km towards northeast of Madurai district which is known us 'City of Festivals' (Map 1). This hill is named as Azhagar Hills because of the famous Vaishnav Temple Azhagar Kovil located in the foothills. Fig. 1. Study area were temporarily stored in polythene vials and a part of the specimens were preserved in 4% formalin for future studies in the laboratory. The samples were observed and documented by using HOVERLABS Research Photo Microscopic Unit. Identification was done by using standard manuals and monographs (Geitler, 1932; Desikachary, 1959; Anand, 1988; Anagnostidis and Komarek, 1988). Results and Discussion A total number of 36 species of Cyanobacteria belonging to 3 families namely Chroococcaceae, Oscillatoriaceae and Nostocaceae were identified. The taxonomic descriptions are given below: Chroococcaceae 1. Aphanocapsa banaresense Bharadwaja (Pl. 1-Fig. a) (Desikachary, 1959, pp 133) Thallus mucilaginous, irregularly expanded, cells spherical, 4.0-4.6 µm diameter, sheath hyaline. 2. Aphanocapsa grevillei (Hass.) Rabenh (Pl. 1-Fig. b) (Geitler, 1932; Desikachary, 1959, pp 134) Thallus gelatinous, cells spherical, 3.6-4.6 µm broad, individual envelopes not distinct. 3. Aphanothece castagnei (Breb.) Rabenh (Pl. 1-Fig. c) (Geitler, 1932; Desikachary, 1959, pp 140) Thallus gelatinous, irregular in shape, slimy, cells ellipsoidal, cylindrical, 3.6-4.0 µm broad, 4.0-7.2 µm long, closely packed, sheath hyaline and diffluent. 4. Aphanothece conferta Richter (Pl. 1-Fig. d) (Desikachary, 1959, pp 140) Collection, observation and identification Samples were collected from the rocks, fine gravel, moist soil and stagnant and slow running water from May 2015 to April 2016. The collected samples Thallus gelatinous, expanded, cells single or in twos, oblong or spherical, 2.6-2.8 µm broad, 3.2-4.0 µm long 5. Chroococcus minor (Kuetz.) Naeg. (Pl. 1-Fig. e) (Geitler, 1932; Desikachary, 1959, pp 105)

Cells spherical, 3.2-4.0 µm diameter, single or in pairs, sheath thin, colourless and unlamellated. 6. Chroococcus minutus (Kuetz.) Naeg. (Pl. 1-Fig. f) (Geitler, 1932; Desikachary, 1959, pp 103) Cells sub spherical, single or in groups of 2-4, with sheath colony 7.6-10.8 µm broad, 10.0-12.0 µm long, sheath thin, colorless, unlamellated. 7. Gloeocapsa coracina Kuetz. (Pl. 1-Fig. g) (Desikachary, 1959, pp 121) Cells round, small, with sheath 6.0 µm broad, without sheath 3.0 µm broad, sheath lamellated. 8. Gloeocapsa crepidinum Thuret. (Pl. 1-Fig. h) (Geitler, 1932; Desikachary, 1959, pp 117) Thallus gelatinous, cells in groups of 2-4, without sheath 4.0-4.8 µm diameter. 9. Synechocystis aquatilis Sauv. (Pl. 1-Fig. i) Cells spherical, after division hemispherical, 3.0-3.5 µm broad, contents homogenous. Oscillatoriaceae: 12. Lyngbya aerugineo-coerulea (Kuetz.) Gomont (Pl. 1-Fig.l) (Geitler, 1932; Desikachary, 1959, p 315) Filaments 9.0-10.0 µm broad, trichome 8.0 µm broad, not constricted, cells 2.0-3.0 µm long, end cells rounded with a slightly thickened outer membrane. 13. Lyngbya allorgei Fremy (Pl. 2-Fig. a) (Desikachary, 1959, pp 313) Filaments solitary, trichome not constricted, 6.0-6.4 µm broad, sheath thin, prominent, 0.5 µm thick, cells nearly quadrate, 6.0-7.0 µm long, and end cell rounded. 14. Lyngbya birgei Smith G.M. (Pl. 2-Fig. b) (Geitler, 1932; Desikachary, 1959, pp 296) Filaments 20.0-21.0 µm broad, sheath firm, (Geitler, 1932; Desikachary, 1959, pp 144) unlamellated, 2.0-3.0 µm thick, trichome not Cells spherical, 5.4-6.0 µm broad. Fig. 2. Percentage composition of Cyanobacteria at family level constricted at cross walls, end cell rounded, domb shaped, 18.0-19.0 µm long, cell content granular. 15. Lyngbya gracilis (Menegh.) Rebenh. (Pl. 2-Fig. c) (Geitler, 1932; Desikachary, 1959, pp 285) Filaments straight, sheath thick, colourless, slightly 25% 30.50% Chroococcaceae constricted, 5.0-6.0 µm broad, end cell rounded. 16. Lyngbya hieronymusii Lemm. (Pl. 2-Fig. d) Oscillatoriaceae Nostocaceae (Geitler, 1932; Desikachary, 1959, pp 297) 44.44% Filaments straight, 12.0-12. 4 µm broad, trichome 8.0-8.4 µm broad, sheath prominent, persistent, thick, unlamellated, cells 2.5-3.0 µm long, not constricted and 10. Synechocystis crassa Woronichin (Pl. 1-Fig. j) (Geitler, 1932, pp 270) Cells 7.8-10 µm broad, cylindrical. 11. Synechocystis pevalekii Ercegovic (Pl. 1-Fig. k) (Geitler, 1932; Desikachary, 1959, pp 145) cell flatly rounded. 17. Oscillatoria acuminata Gomont (Pl. 2-Fig. e) (Geitler, 1932; Desikachary, 1959, pp 240) Thallus blue green, trichome straight, not constricted, 3.5-4.1 µm broad, end cell pointed, bent, not capitate.

18. Oscillatoria acuta Bruhl et Biswas, Orth, mut. Geitler (Pl. 2-Fig. f) (Geitler, 1932; Desikachary, 1959, pp 240) Thallus parallel, not constricted, 5.2-6.0 µm broad, ends bent, cells 3.2-4.0 µm long, contents granular. 19. Oscillatoria animalis Ag. ex. Gomont (Pl. 2-Fig. g) (Geitler, 1932; Desikachary, 1959, pp 239) Thallus dark blue green, trichome straight, not constricted, slightly attenuated at the ends and bent, 3.2-4.0 µm broad, end cell pointed, acute, not capitate. 20. Oscillatoria perornata Skuja (Pl. 2-Fig. h) (Desikachary, 1959, pp 205) Trichome erect, constricted at the cross walls, 13.5-14.7 µm broad, granular, septa more or less granulated, end cell hemispherical. 21. Oscillatoria proboscidea Gomont (Pl. 2-Fig. i) (Geitler, 1932; Desikachary, 1959, pp 211) Thallus dull green, trichome more or less straight, not constricted, 9.0-9.4 µm broad, ends distinctly attenuated, curved, not granulated at cross walls, end cell flatly rounded, capitate with slightly thickened membrane. 22. Oscillatoria raoi De Toni, J (Pl. 2-Fig. j) (Desikachary, 1959, pp 223) Thallus straight, uniform thickness, slightly tapering at the end, cells 5.2-5.8 µm broad, rounded, not capitate. 23. Oscillatoria rubescens DC ex Gomont (Pl. 2-Fig. k) (Geitler, 1932; Desikachary, 1959, pp 235) Trichome straight, 6.5-7.2 µm broad, not constricted at the cross walls, cells broader than long, granulated at the septa end cell with convex calyptra. 24. Phormidium ambiguum var. majus Lammermann (Pl. 2-Fig. l) (Geitler, 1932; Desikachary, 1959, pp 266) Trichome 9.0-9.5 µm broad, cells 2.5-3.0 µm long. 25. Phormidium anomala Rao, C.B. (Pl. 3-Fig. a) (Desikachary, 1959, pp 266) Filament straight, trichome of uniform width, trichome 8.0-9.2 µm broad, not constricted, sheath thin and colourless, not attenuated, not constricted at cross walls, end cell bluntly rounded, not capitate. 26. Phormidium calcicola Gardner (Pl. 3-Fig. b) (Geitler, 1932; Desikachary, 1959, pp 267) Filaments 7.6-8.1 µm broad, sheath thick, not lamellated, trichome 5.8-6.2 µm broad. 27. Phormidium cebennense Gomont (Pl. 3-Fig. c) (Geitler, 1932; Desikachary, 1959, pp 262) Thallus thin, expanded, filaments nearly parallel and straight, sheath thin, diffluent, trichome 2.0-3.2 µm broad, not constricted at cross walls, end cell rounded. Nostocaceae 28. Anabaena anomala Fritsch (Pl. 3-Fig. d) (Desikachary, 1959, pp 398) Thallus thin, trichomes densely arranged, cells 2.0-3.0 µm long, barrel shaped, end cell rounded, heterocyst single, intercalary, spherical 4.0-5.2 µm in diameter. 29. Anabaena doliolum Bharadwaja (Pl. 3-Fig. e) (Desikachary, 1959, pp 410) Trichomes contorted, cells 3.8-4.2 µm broad, apical cell rounded, heterocyst both terminal and intercalary, single, barrel shaped, 5.2-5.8 µm broad, spores in long series, away from the heterocyst, ellipsoidal with rounded ends, 4.0-5.0 µm broad, 6.0-8.0 µm long. 30. Anabaena fertillisima Rao, C.B. (Pl. 3-Fig. f) (Desikachary, 1959, pp 398) Thallus amorphous, cells barrel shaped, 4.8-5.2 µm broad, 5.5-6.0 µm long, end cell rounded, heterocyst spherical, 6.4-7.0 µm in diameter, spores in chain,

away from heterocyst, spherical 5.5-7.0 µm broad, 4.5-6.5 µm long. 31. Nostoc carnaeum Ag. ex Born. et Flah (Pl. 3-Fig. g) (Geitler, 1932; Desikachary, 1959, pp 381) Thallus macroscopic, filaments flexuous, loosely arranged, sheath not distinct, trichome 3.6-4.0 µm broad, cells twice as long as broad, heterocyst oblong, 5.4-6.0 µm broad, spores not observed. Plate 1. a-aphanocapsa banaresense, b-aphanocapsa grevillei, c-aphanothece castagnei, d-aphanothece conferta, e-chroococcus minor, f-chroococcus minutes, g-gloeocapsa corocina, h-gloeocapsa crepidinum, i-synechocystis aquatilis, j-synechocystis crassa, k-synechocystis pevalekii, l-lyngbya aerugineo-coerulea Plate 2. a-lyngbya allorgei, b-lyngbya birgei, c-lyngbya gracilis, d-lyngbya hieronymusii, e-oscillatoria acuminate, f-oscillatoria acuta, g-oscillatoria animalis, h-oscillatoria perornata, i-oscillatoria proboscidiea, j- Oscillatoria raoi, k-oscillatoria rubescens, l-phormidium ambiguum

Plate 3. a-phormidium anomala, b-phormidium calcicola, c-phormidium cebennense, d-anabaena anomala, e- Anabaena doliolum, f-anabaena fertillisima, g-nostoc carnaeum, h-nostoc commune, i-nostoc ellipsosporum (Desm.) Rabenh, j-nostoc ellipsosporum var. violacea, k-nostoc rivulare, l-nostoc sphaericum Table 1. List of unicellular/colonial, filamentous forms S. No Morphology Name of the Species 1 2 3 S. No Morphology Name of the Species Chroococcaceae Aphanocapsa banaresense Oscillatoria animalis Ag. ex. Bharadwaja 19 Gomont Aphanocapsa grevillei (Hass.) Rabenh 20 Oscillatoria perornata Skuja Aphanothece castagnei (Breb.) Rabenh 21 Oscillatoria proboscidea Gomont 7 Gloeocapsa corocina Kuetz. 25 Phormidium anomala Rao, C.B. 8 Gloeocapsa crepidinum Thuret. 26 Phormidium calcicola Gardner 9 Synechocystis aquatilis Sauv. 27 Phormidium cebennense Gomont 10 Synechocystis crassa Woroniccchin Nostocaceae 11 Synechocystis pevalekii Ercegovic 28 Anabaena anomala Fritsch 4 Aphanothece conferta Richter 22 Non- Oscillatoria raoi De Toni,J Heterocystous Oscillatoria rubescens DC ex 5 Unicellular Chroococcus minor (Kuetz.) Naeg. 23 Filamentous Gomont Chroococcus minutus (Kuetz.) Phormidium ambiguum var. 6 Naeg. 24 major Lammermann Oscillatoriaceae 29 Anabaena doliolum Bharadwaja Lyngbya aerugineo-coerulea 12 (Kuetz.) Gomont 30 Anabaena fertillisima Rao, C.B. Nostoc carnaeum Ag. ex Born. et 13 Lyngbya allorgei Fremy 31 Flah 14 Nostoc commune Vaucher ex Non- Lyngbya birgei Smith G.M. 32 Heterocystous Born et Flah Heterocysto Lyngbya gracilis (Menegh.) Filamentous Nostoc ellipsosporum (Desm.) 15 us Rebenh. 33 Rabenh. Filamentous Nostoc ellipsosporum var. 16 Lyngbya hieronymusii Lemm. 34 violacea Rao, C.B. Nostoc rivulare Kuetz. ex Born. 17 Oscillatoria acuminata Gomont 35 et Flah Oscillatoria acuta Bruhl et Biswas, Nostoc sphaericum Vaucher ex 18 Orth, mut. Geitler 36 Born. et Flah

32. Nostoc commune Vaucher ex Born et Flah (Pl. 3- Fig. h) (Geitler, 1932; Desikachary, 1959, pp 387) Thallus large, membranous with firm layer, trichome 4.5-5.0 µm broad, heterocyst nearly spherical, 5.0 µm broad, spores not observed. 33. Nostoc ellipsosporum (Desm.) Rabenh. (Pl. 3-Fig. i) (Geitler, 1932; Desikachary, 1959, pp 383) Macroscopic thallus, entangled filaments, trichome less coiled, cells cylindrical, heterocyst sub spherical, 6.0-8.0 µm long, spores ellipsoidal, 7.2-12.0 µm long. 34. Nostoc ellipsosporum var. violacea Rao CB (Pl. 3- Fig. j) (Desikachary, 1959, pp 383) Thallus gelatinous, irregularly expanded, filaments loosely arranged, trichome 3.0-3.4 µm broad, slightly constricted at the cross walls, cells cylindrical, and heterocyst spherical with rounded ends, 4.2-5.0 µm broad, 5.0-5.8 µm long, spores ellipsoidal, spherical or cylindrical 4.0 µm diameter. 35. Nostoc rivulare Kuetz. ex Born. et Flah (Pl. 3-Fig. k) (Geitler, 1932; Desikachary, 1959, pp 379) Thallus macroscopic, globose, filaments loosely entangled, highly coiled, sheath diffluent, distinct at the periphery of the thallus, cells 3.4-4.0 µm broad, heterocyst oblong, 5.0-5.6 µm broad, spores oblong, 6.0-6.6 µm broad, 7.2-8.0 µm long. 36. Nostoc sphaericum Vaucher ex Born. et Flah (Pl. 3-Fig. l) (Geitler, 1932; Desikachary, 1959, pp 390) Thallus globose, 6.0 µm in diameter, filaments densely In the present study, total number of 36 species of Cyanobacteria were recorded. It includes unicellular/colonial, filamentous non-heterocystous and heterocystous forms (Table 1). Analysis of the data further shows that the species belongs to Oscillatoriaceae (44.5%) was dominant followed by Chroococcaceae (30.5%) and Nostocaceae (25%) at the family level (Fig. 2). References Anand N (1988). Culture Studies and Taxonomy of blue green algae-certain identification problems. Arch Fur Hydrobiol 50-53: 141-147. Bisby FA (1995). Characterization of biodiversity. In: VH Heywood, RT Watson [Eds] Global Biodiversity Assessment. Cambridge University Press, Cambridge, UK 21-106. Borowitzka MA, Borowitzka LJ (1988). Micro-algal Biotechnology. Cambridge University Press, Cambridge, UK 477 pp. Castenholz RW, Waterbury JB (1989). In: JT Staley, MP Bryant, N Pfennig, JG Holt [Eds] Bergey's Manual of Systematic Bacteriology. Vol. 3: Williams and Wilkins, Baltimore, USA 1710. Castenholz RW (1973). Ecology of blue-green algae in hot springs. In: Carr NG, BA Whitton [Eds]. The Biology of Blue-Green Algae. Blackwell Scientific Publications, Oxford, UK 379. Desikachary TV (1959). Cyanophyta. Indian Council for Agricultural Research, New Delhi, India: pp entangled, trichomes 4.0-4.5 µm broad, cells 686. compressed, spherical, heterocyst 5.5 µm broad sub spherical, spores oval, 4.5-5.0 µm broad, spores globose, 6.0-7.0 µm broad in long chains. Drouet F (1968). Revision of the Classification of the Oscillatoriaceae. Monograph of the academy of Natural Sciences, Philadelphia, USA 15: pp334.

Falch BS, König GM, Wright AD, Sticher O, Angerhofer CK, Pezzuto JM, Bachmann H (1995). Biological activities of cyanobacteria: evaluation of extracts and pure compounds. Planta Med 61: 321-328. Fritsch FE (1942). The interrelations and classification of the Myxophyceae (Cyanophyceae). New Phytol 41: 134-148. Ganapati SV (1940). The ecology of the temple tank containing a permanent bloom of Microystis aeruginosa Kuetzing J Bomb Nat Hist Soc 42(1): 65-77. Santra SC (1993). Biology of rice fields blue green algae. Daya Publishing House. Delhi, India. Starmach K (1996). Cyanophyta-Sinice, Glaucophyta- Glaukofity, Flora slodkowodna Polski, tom 2, Warszawa, Poland pp. 800. Thajuddin N, Subramanian G (1992). Survey of cyanobacterial flora of the southern east coast of India. Bot Mar 35: 305-311. Whitton BA (1992). Diversity, ecology and taxonomy of the cyanobacteria. In: NH Mann and NG Carr [Eds] Photosynthetic Prokaryotes. Plenum Press, New York, USA pp 1-51. Geitler L (1932). Cyanophyceae. In: L Rabenhorst [Ed.] Kryptogamen-Flora. 14. Band. Akademische Verlagsgesellschaft, Leipzig, 1196 pp. Kol E (1968). Kryobiologie. I Kryovegetation. In: HJ Elster, W Ohle [Eds] Die Binnengewässer, Band XXIV. E. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart, 216 pp. Komarek J, Anagnostidis K (2005). Cyanoprokaryota 2.Teil/2nd part: Oscillatoriales, [in:] Budel B, Krienitz L, Gartner G, Schagerl M (eds.), Susswasser flora von Mitteleuropa, 19(2), Elsevier/Spektrum, Heidelberg. pp 759. Laamanen M (1996). Cyanoprokaryotes in the Baltic Sea ice and winter plankton. Arch Hydrobiol Suppl. 117: Algological Studies 83: 423-433. Richmond A (1990). Large scale microalgal culture and applications. Prog Phycol Res 7: 269-330. Sankaran V (2001). Bluegreen algae from the Anamaly Hill ranges of Tamil Nadu and Kerala. In Algal Biotechnology (ed.) Trivedi PC, Pointer Publishers, Jaipur, India pp. 116-134.