Journal of Scientific &NAMPOOTHIRI Industrial Research et al: MICROBIAL BIODIVERSITY OF OF 617 Vol. 72, Sept - Oct 2013, pp. 617-623

Western Ghats of India: Rich source of microbial biodiversity

K Madhavan Nampoothiri*, B Ramkumar and Ashok Pandey Biotechnology Division, National Institute for Interdisciplinary Science and Technology, CSIR, Trivandrum 695 019, India

Received 19 March 2013; revised 17 May 2013; accepted 29 May 2013

Western Ghats is one of the unique biodiversity niches, with varied flora, fauna and landscapes. This review presents some data on microbial diversity of Western Ghats, emphasizing the prospects of exploiting them for potential applications that could be imperative for socio-economic development of India.

Keywords: Biodiversity Hotspots, Heritage tag, Western Ghats

Introduction forest in India. Within an area of 237.52 km2, it houses a Western Ghats of India, though covering an area of rich mosaic of varied habitats forming a unique preserve 180,000 km2, or just under 6% of the land area of India, of natural rainforests. Analyses of conservation outcomes contain more than 30% of all plant, fish, herpeto-fauna, reveal the presence of 332 globally threatened species bird, and mammal species found in India. Starting from and thousands of endemic species in the forests and hill southern tip of and extending from Satpura Range ranges of Western Ghats with over 450 birds and 5000 in the north traversing through the States of , vascular plants species, of which 35% and 30% , and , hills of Western Ghats ends respectively are endemic1, besides a vast array of fresh at southern tip of India, standing tall at an altitude of water fishes, invertebrates and amphibians, which are 2695 m () in Kerala. Being the “gene pool” endemic to the region. Among various ranges of harbouring millions of species of animals, plants and organisms in Western Ghats, microorganisms are a vast microbes, the heritage unit of UNESCO grants a section array of novel and unidentified microbes, which could be of Western Ghats lying in the states of Kerala, explored for potential applications. Karnataka, Maharashtra and Gujarat with a “heritage This review presents data on microbial diversity of tag”. In August, 2011, Western Ghats Ecology Expert Western Ghats of India, with an emphasis on exploiting Panel (WGEEP) designated entire Western Ghats as an them for potential applications for socio-economic Ecologically Sensitive Area (ESA) and, assigned three development of India. levels of ecological sensitivity to its different regions. Unique biodiversity of Western Ghats are protected and New microbial Isolates from Western Ghats conserved through the establishment of biosphere Bacteria and Actinomycetes reserves, national parks and several wildlife sanctuaries Bacterial species of 21 different genera (Table 1). Nilgiri Biosphere Reserve comprising 5500 [Proteobacteria (58%), Firmicutes (26%), km² of evergreen forests of Nagarahole; deciduous Actinobacteria (13%) and Bacteroidetes (3%)] were forests of ; Nugu in Karnataka isolated from water samples of Western Ghats region, and adjoining regions of Wayanad; Mudumalai National which shows an abundance of microbial diversity of Park and in the states of Kerala ecosystem2. Two new species from a group, Pontibacter and forms the largest contiguous protected niistensis sp. nov3 and Paracoccus niistensis sp. nov4, area in Western Ghats. Silent Valley National Park were isolated from soil samples of Western Ghat hotspot located in Nilgiri Hills in Palakkad district of Kerala is region. Similarly, 300 new isolates of Bacillus one among the last tracts of virgin tropical evergreen thuringiensis (Bt), isolated from Western Ghats, produce 7 different types of parasporal crystalline inclusions, *Author for correspondence predominantly cuboidal type (27%). Variation in mass of E-mail: [email protected] crystal proteins, purified from these isolates, revealed 618 J SCI IND RES VOL 72 SEPT - OCT 2013

Table 1—Major hot spots in Western Ghats

Major ‘Hot spots’ in Western Ghats State Bhagwan Mahavir Wildlife Sanctuary and Mollem National Park Goa

Anshi National Park, Bandipur National Park, Bhadra Wildlife Karnataka Sanctuary, Biligiri Rangaswamy Temple (BRT)Wildlife Sanctuary, National Park, Rajiv Gandhi National Park (Nagarhole) and Valley Wildlife Sanctuary

Chinnar Wildlife Sanctuary, , Senduruney Kerala Wildlife Sanctuary, Parambikulam Wildife Sanctuary, , Silent Valley National Park and Wyanad Wildlife Sanctuary

Indira Gandhi (Anamalai) National Park, Kalakad-Mundanthurai Tamil Nadu Tiger Reserve (KMTR), , Mukurthi National Park, Sathyamangalam Wildlife Sanctuary, Grizzled Giant Squirrel Sanctuary and Kanyakumari Wildlife Sanctuary

unique molecular diversity of this bacterium in Western Capparaceae, Commelinaceae, Cyperaceae and Ghat regions5. A novel species of green phototrophic Portulacaceae) that are assumed to be non-mycorrhizal, bacterium, Rhodobacter viridis sp. nov. [Strain JA737 showed AM association for the first time. AM fungal (T)] of genus Rhodobacter (Family, Rhodo spores of 35 species belonging to Acaulospora, bacteraceae), was isolated from mud of a stream in Gigaspora, Glomus, Sclerocystis and Scutellospora Western Ghats. Strain JA737 (T) contained a were also reported. From fallen fruits of medicinal plant, bacteriochlorophyll and a carotenoid, neurosporene. Terminalia chebula, collected from forests of Western Strain clustered with members of genus Rhodobacter Ghats, two novel fungi of Gliocephalotrichum 6 of the class Alphaproteobacteria . longibrachium and G. bulbilium were isolated10. The first occurrence of Gliocephalotrichum simplex, a Fungal Species species not previously known from India, was reported11 Thermo-tolerance study with spores of mesophilic from Western Ghats region. Four new species of fungi subjected to dry season fire, isolated from a tropical hyphomycete genera (Phaeoramularia viz. semi-arid habitat in southern hills of Western Ghats, P.caesalpinae; Pseudocercospora viz. P. Tiliacearum; indicated that among 25 species of Ascomycota isolated and , occurring from leaf litter, nine were able to grow after incubation Stenella viz. S. argyreiae S. grewiae) on the plants of Western Ghats, were identified12. in a dry oven for 2 h at 100°C; spores of two species Muthukumar & Prabha13 studied extent and type of survived 2 h incubation at 110°C; and one survived exposure to 115°C for 2 h. Molecular and physiological AM and septate endophytic (SE) fungal associations in mechanisms of heat resistance shown by these fungi five lycophytes and 50 ferns collected from Western could be efficiently exploited for future genetic Ghats regions of India, and observed that from 54 species engineering applications7. White rot fungus8, Fomes (belonging to 31 genera) examined, AM fungal spore lividus, isolated from logs of Shorea robusta in Western morphotypes belonged to Claroideoglomus, Ghats region of Tamil Nadu, India, was tested for Funneliformis, Glomus and Rhizophagus. Similarly, decolorization of azo dyes (orange G, Congo red, amido Lakshmipathy et al14 reported abundance and diversity black 10 B) and also for colour removal from dye industry of AM fungi across a gradient of land use intensity and effluents. A survey of plants with arbuscular mycorrhizal their seasonal variations in Niligiri Biosphere (natural (AM) association9, growing in Western Ghats region of forest, grassland, acacia plantations, cardamom Southern India, indicated that from 329 plant species plantations, coffee plantations and paddy fields) of (representing 61 families) examined, 174 showed Western Ghats. Sridhar & Sudheep15 mapped mycorrhizal associations. About 81 plant species filamentous fungal association with mechanically hard belonging to several families (Amaranthaceae, and soft woody litter naturally deposited in a stream of NAMPOOTHIRI et al: MICROBIAL BIODIVERSITY OF WESTERN GHATS OF INDIA 619

Western Ghats. In hardwood sections, 17 lignicolous symbiotic associations between tropical plants and fungi fungi (4 ascomycetes and 13 mitosporic) and 10 Ingoldian in Western Ghats regions, Riviere et al21 investigated fungi (9 lignicolous) and 3 Ingoldian as core-group taxa ectomycorrhizal (ECM) basidiomycete diversity, using a were recovered. In softwood, 10 lignicolous fungi (10 fragment of mitochondrial large subunit rRNA gene, to mitosporic) and 26 Ingoldian fungi (6 lignicolous) and 12 type 140 sporocarps and 54 ectomycorrhizas, thereby Ingoldian as core-group taxa were recovered. providing preliminary insights into taxonomic diversity, ECM status, and biogeographic patterns of ECM fungi Endophytic Fungi in tropical rain forest ecosystems. Several new endophytic fungal strains with potential applications were isolated from tropical rain forest region Microalgae of Western Ghats, viz., Fusarium solani isolated from Freshwater algae are a rich source of novel and Apodytes dimidiate (Icacinaceae), a medium sized biologically active metabolites. In recent years, algal bushy tree. Two strains of F. solani (MTCC 9667 and biofuel has become one of the most promising new MTCC 9668) were found to produce camptothecin and generation biofuel with potential industrial applications 10-hydroxy camptothecin, important precursors for due to fast and efficient growth cycle of microalgae. synthesis of clinically useful anticancer drugs, topotecan For effective use and industrial exploitation, mapping and and irinotecan16. Raviraja et al17 isolated 18 species of enlisting all these microalgal taxa is highly important. John endophytic fungi from bark, steam and leaf segments of & Francis22 conducted a systematic mapping of medicinal plants grown in Western Ghats. The greatest microalgal resources of Kerala in Western Ghats, India. numbers of endophytic fungal species were found within Out of 33 taxa of algae recorded, 19 belongs to the group, Callicarpa tomentosa (11 sp.), whereas Chlorophyceae, five of Euglenineae, four of Lobelia nicotinifolia harboured the lowest number of Bacillariophyceae, two of Rhodophyceae, and one fungal endophytes (5 sp.). Sudheep & Sridhar18 reported each of Xanthophyceae, Dinophyceae and presence of endophytic fungal communities in three tissue Cyanophyceae, of which three are new reports (1 from types of two dominant orchids (Bulbophyllum Rhodophyceae and 2 from Euglenineae). neilgherrense and Vanda testacea) of Kaiga forest of Western Ghats. About 118 fungal isolates were obtained Microbes for Biotechnological Applications from root, bulb and leaves of B. neilgherrense, consisting Plant Growth Promoting Rhizobacteria (PGPR) of 17 anamorphic taxa (range 10-15 taxa) with 1.3 fungal Western Ghats soil samples are rich sources of taxa per segment (range, 1.2-1.4 taxa). A total of 130 PGPR, which shows multiple plant growth promoting fungal isolates from roots, stems and leaves of V. attributes [phosphate solubilization activity, indole acetic testacea yielded 20 anamorphic taxa (range 11-15 taxa) acid (IAA) production, siderophore and HCN production with 1.4 fungal taxa per segment (range 1.4-1.5 taxa). etc.]. B. thioparus (NII0902)23 and Microcous sp. Aspergillus flavus, A. niger, A. ochraceus, (NII0909)24 from Silent valley soil samples enhanced Gliocladium viride, Penicillium sp. and Morpho sp. growth of black pepper and cow pea, showed significant belonged to the core group. Suryanarayanan et al19 antifungal activity against various phytopathogens, and reported fungal endophytes of dicotyledonous tropical hence could be used as potential PGPR. trees belonging to 33 families and growing in three different types of tropical forests of Niligiri Biosphere Industrial Applications Reserve (NBR) of Western Ghats. Endophytic fungal Microbial diversity of Western Ghats is an immense diversity in Western Ghats forests is limited due to source of potent microorganisms that could be potentially reduced host affiliations among endophytes and it exploited for various industrial and medicinal applications. appears that environment has a larger role in determining Selvam et al25 collected 56 samples of wood rot fungi endophyte assemblage of a host plant than its taxonomic from Western Ghats area of Tamil Nadu and Karnataka position. Muthkumar et al20 studied roots of 107 medicinal in and screened for their ligninolytic activity and aromatic plants (MAPs) in southern part of Western based on their ability to oxidize dyes, poly R-478 and Ghats for AM and dark septate endophyte (DSE) remazol brilliant blue, to degrade native lignin and further associations and found that more than 30 MAPs had confirmation was done by liberation of ethylene from both AM and DSE association. In order to understand KTBA (2-keto-4-thiomethyl butyric acid). Isolated fungal 620 J SCI IND RES VOL 72 SEPT - OCT 2013

Table 2—Microbial isolates reported from Western Ghats and their applications

Sl No. Microorganisms Applications 1 Streptomyces sp. ERI-26, ERI-3, Antimicrobial activity ERI-0432-34 2 Methylobacterium sp. ERI-13535 Cytotoxic (A 549) and Antimicrobial effects 3 Streptomyces aurantiacus AAA536 Quinine-related antibiotic resistomycin 4 Streptomyces sp., Bacillus sp.37 inhibition of extended spectrum β-lactamase (ESBL) 5 Bacillus subtilis C938, Anti-phytopathogenic, 6 Pseudomonas sp.39 Antibacterial activity 7 Streptomyces Sp (TA22)30 Anticancer enzyme: asparaginase 8 Serratia marcescenes strain SN5gR31 Enzyme: Lipase Production 9 Bacillus thioparus (NII0902), Indole acetic acid (IAA), Siderophore Microcous sp (NII 090923,24 and HCN production 10 Rhodobacter viridis Sp.nov (Strain JA737T)6 Bioactive production 11 Chryseobacterium Sp, WG4A26 Bioactive: aromatic compound 12 Pseudomonas fluorescence sp.27 Enzymes and antimicrobial metabolites. 13 Exiguobacterium sp. AFB-11 and AFB 1829 Amylolytic enzyme 14 Tolypocladium spp. Ti-1, Ti-2 and Ti-328 Antimicrobial activity 15 Fomes lividus8 Dye decolorization in industry effluents 16 Fusarium solani17 For anticancer 17 Polyporus hirsutus, Daedalea flavida, Enzyme production Phellinus sp.25 18 Microalgae: Rhodophyceae & Euglenineae22 Biofuel

strains (Polyporus hirsutus, Daedalea flavida, (pCC1FOS) and screened for biocatalytic properties. Phellinus sp.) proved to have potential applications. Clones showed amylolytic activity and enzyme exhibited Chryseobacterium indologenes Strain WG4 (Family, stability at elevated temperature with 60°C being optimum, Flavobacteriaceae), isolated from water sample retaining more than 30% activity after 60 min incubation collected from the Western Ghats, India, at 80°C. It also showed more than 70% activity retention produces a fruity aroma26 due to the presence of in 1.5 M NaCl solution with optimum pH 5.0. 16S rRNA aromatic compounds, ethyl-2-methylbutyrate and ethyl- gene sequence (GenBank accession number HQ680979) 3-methylbutyrate. Megha et al27 isolated 52 fluorescent BLAST showed 95% similarities with Exiguobacterium Pseudomonas sp. from forest soils of Western Ghats of sp. AFB-11 and AFB 18, with query sequence coverage Uttara district in Karnataka, India, and indicated of 99%. This study hence revealed potential of that isolates possesse various beneficial traits and exhibit metagenomic approach in Western Ghats region for biocontrol activity against four plant pathogens, screening enzymes with novel properties for improved (Ralstonia solanacearum, Xanthomonas compestris, industrial applications. Priya et al30 reported production Fusarium oxysporum and Rhizoctonia bataticola). All of anticancer enzyme, L-asparginase from actinomyces 52 isolates solubilized tri-calcium phosphate (TCP) strain, Streptomyces Sp (TA22) isolated from soil sample produced IAA and GA, while some showed HCN collected from Western Ghats, near Thirunelveli district, production. Ramachandran et al28 isolated soil fungi Tamil Nadu. An extracellular lipase-producing bacterium, Tolypocladium spp. designated as Ti-1, Ti-2, Ti-3 from Serratia marcescenes strain SN5gR, was isolated from soil samples of forest of Western Ghats. Fungi a fecal sample of lion-tailed macaque (Macaca silenus), showed potential antimicrobial activity and produced an endangered Old World monkey that is endemic to Cyclosporine-related compound, which could be explored Western Ghats of South India31. as an effective immunosuppressant drug in the market. Microbial Bioactives Enzymes Several bacterial and actinomyctes strains isolated Western Ghats soil samples collected from silent from Western Ghats soil samples showed wide spectrum valley region were used by Jalaja et al29 for isolation antimicrobial activity (Table 2). Ignacimuthu et al32-34 and characterization of a novel α-amylase, and a reported several Streptomyces sp. designated as ERI- metagenomic library was constructed in a fosmid vector 26, ERI-3, ERI-04 etc, isolated from southern Western NAMPOOTHIRI et al: MICROBIAL BIODIVERSITY OF WESTERN GHATS OF INDIA 621

Ghats regions mainly from Nilgiri hills. Streptomyces sp. acetate extract of the culture broth of isolate C9 that ERI-26 exhibited resistance to Streptomycin and showed proves the potential agricultural application of bacterial activity against several bacteria (B. subtilis, isolates. Saravanan et al39 isolated from forest soil of Staphylococcus aureus, S. epidermidis, Enterococcus Western Ghats strains of Pseudomonas sp. with potent faecalis) and fungi (Candida albicans, A. flavus, A. antibacterial activity against a wide range of Gram niger etc.). MIC concentration of ethyl acetate extract positive and Gram negative bacteria. Madhaiyana et al40 of ERI-3 was determined as 0.25 mg/ml for S. reported for the first time occurrence of an endophytic epidermidis, C. albicans etc. MIC of organic extract bacterium, Gluconacetobacter diazotrophicus, in of Streptomyces sp. ER-04 against A. niger was 62.5µg/ tropical and subtropical plants of Western Ghats. All ml and 125µg/ml for T. rubrum, E. floccosum, M. grisea isolates showed potential plant growth promoting traits and T. simii. Extracellular product of isolates exhibits [nitrogenase activity, phosphorus & zinc solubilization and moderate antifeedant activity against Helicoverpa production of phytohormone: indole acetic acid (IAA)]. armigera and Spodoptera litura. Strain ERI-135 identified as Methylobacterium sp., isolated from Conclusions Doddabetta forest, showed cytotoxic (A 549) and Western Ghats are known to be an active hotspot antimicrobial effects35. A new actinomycetes strain, region with enormous biodiversity wealth. Despite isolated from humus soils of Western Ghats, identified extensive research and analysis made to explore as S. aurantiacus AAA5 produced a reddish-brown biodiversity potential of Western Ghats, there still remains pigmented compound during secondary metabolite phase. a huge gap on biological richness of these conservation A yellow compound derived from extracted pigment was sites. Innovative and effective approaches should be identified as quinine-related antibiotic resistomycin36. made to strengthen fledgling participation of various Isolate was found to produce large quantities of research groups and civil societies to catalyze exploitation resistomycin (52.5 mg/ml) that showed potent cytotoxic and conservation of Western Ghats biodiversity especially activity against cell lines [HepG2 (hepatic carcinoma) microbial population. From existing studies, it will never and HeLa (cervical carcinoma)] in vitro studies. This be an embellishment to call Western Ghats as the strain also exhibited broad antimicrobial activities against “Treasure House” of microbial biodiversity. Gram positive and Gram negative bacteria. Mohandas et al37 carried out exploitation of microbial biodiversity Acknowledgements from Western Ghats of Kerala for screening of bioactives Authors thank CSIR and DBT for research funding having β-lactamase inhibitory activities. A total of 700 for exploration of microbial wealth of Western Ghats of pure cultures were isolated and screened for antibacterial Kerala belt for various studies. Authors also thank Kerala activity against a β-lactam resistant B. cereus strain Forest Department for data provided on Western Ghats (PL 10) isolated from the same niche. Bioactive extracts and also for approval for soil sample collection from Silent made from 45 isolates showed inhibitory activities against valley. 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