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Volume: 7, Issue: 4, July-August, 2019
DOI: 10.7324/JABB.2019.70415

Research Article

Biodiversity of psychrotrophic microbes and their biotechnological applications


Ajar Nath Yadav1, Neelam Yadav2, Shashwati Ghosh Sachan3, Anil Kumar Saxena4

  Author Affiliations


Abstract

The extreme cold environments harbor novel psychrotrophic microbes. The psychrotrophic microbes have been reported as plant growth promoters and biocontrol agents for sustainable agriculture, in industry as cold-adapted hydrolytic enzymes and in medicine as secondary metabolites and pharmaceutical important bioactive compounds. Inoculation with psychrotrophic/psychrotolerant strains significantly enhanced root/shoot biomass and nutrients uptake as compared to non-bacterized control. The psychrotrophic microbes play important role in alleviation of cold stress in plant growing at high hill and low temperature and conditions. The psychrotrophic microbes have been reported from worldwide from cold habitats and belong to all three domain archaea, bacteria, and eukarya including different phylum such as Actinobacteria, Ascomycota, Bacteroidetes, Basidiomycota, Chloroflexi, Chlamydiae, Planctomycetes, Cyanobacteria, Euryarchaeota, Firmicutes, Gemmatimonadetes, Verrucomicrobia, Mucoromycota, Proteobacteria, Spirochaetes, Thaumarchaeota and Nitrospirae. The most dominant genera belong to Arthrobacter, Bacillus, Exiguobacterium, Paenibacillus, Providencia, Pseudomonas, and Serratia have been reported from the cold habitats. The Psychrotrophic microbes have biotechnological applications in agriculture, medicine, industry, food, and allied sectors.

Keywords:

Adaptation, Biodiversity, Biotechnological applications, Cold adapted, Psychrotrophic.



Citation: Yadav AN, Yadav N, Sachan SG, Saxena AK. Biodiversity of psychrotrophic microbes and their biotechnological applications. J App Biol Biotech. 2019; 7(04):99-108. DOI: 10.7324/JABB.2019.70415


Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

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99. Zhang D-C, Wang H-X, Cui H-L, Yang Y, Liu H-C, Dong X-Z, Zhou P-J. Cryobacterium psychrotolerans sp. nov., a novel psychrotolerant bacterium isolated from the China No. 1 glacier. International Journal of Systematic and Evolutionary Microbiology. 2007; 57(4):866-869. https://doi.org/10.1099/ijs.0.64750-0

100. Reddy GSN, Pradhan S, Manorama R, Shivaji S. Cryobacterium roopkundense sp. nov., a psychrophilic bacterium isolated from glacial soil. International Journal of Systematic and Evolutionary Microbiology. 2010; 60(4):866-870. https://doi.org/10.1099/ijs.0.011775-0

101. Chaturvedi P, Reddy GSN, Shivaji S. Dyadobacter hamtensis sp. nov., from Hamta glacier, located in the Himalayas, India. International Journal of Systematic and Evolutionary Microbiology. 2005; 55(5):2113-2117. https://doi.org/10.1099/ijs.0.63806-0

102. Mou Y-Z, Qiu X-X, Zhao M-L, Cui H-L, Oh D, Dyall-Smith ML. Halohasta litorea gen. nov. sp. nov., and Halohasta litchfieldiae sp. nov., isolated from the Daliang aquaculture farm, China and from Deep Lake, Antarctica, respectively. Extremophiles. 2012; 16(6):895-901. https://doi.org/10.1007/s00792-012-0485-5

103. Mayilraj S, Kroppenstedt RM, Suresh K, Saini HS. Kocuria himachalensis sp. nov., an actinobacterium isolated from the Indian Himalayas. International Journal of Systematic and Evolutionary Microbiology. 2006; 56(8):1971-1975. https://doi.org/10.1099/ijs.0.63915-0

104. Gosink J, Herwig R, Staley J. Octadecabacter arcticus gen. nov., sp. nov., and O. antarcticus, sp. nov., nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. Syst Appl Microbiol. 1997; 20(3):356-365. https://doi.org/10.1016/S0723-2020(97)80003-3

105. Yakimov MM, Giuliano L, Gentile G, Crisafi E, Chernikova TN, Abraham W-R, L\ünsdorf H, Timmis KN, Golyshin PN. Oleispira antarctica gen. nov., sp. nov., a novel hydrocarbonoclastic marine bacterium isolated from Antarctic coastal sea water. International Journal of Systematic and Evolutionary Microbiology. 2003; 53(3):779-785. https://doi.org/10.1099/ijs.0.02366-0

106. Mayilraj S, Saha P, Suresh K, Saini HS. Ornithinimicrobium kibberense sp. nov., isolated from the Indian Himalayas. International Journal of Systematic and Evolutionary Microbiology. 2006; 56(7):1657-1661. https://doi.org/10.1099/ijs.0.64138-0

107. Irgens R, Gosink J, Staley J. Polaromonas vacuolata gen. nov., sp. nov., a psychrophilic, marine, gas vacuolate bacterium from Antarctica. International Journal of Systematic and Evolutionary Microbiology. 1996; 46(3):822-826.

108. Lopez NI, Pettinari MJ, Stackebrandt E, Tribelli PM, Põtter M, Steinb\üchel A, M\éndez BS. Pseudomonas extremaustralis sp. nov., a poly (3-hydroxybutyrate) producer isolated from an Antarctic environment. Current microbiology. 2009; 59(5):514-519. https://doi.org/10.1007/s00284-009-9469-9

109. Bowman JP, McCammon SA, Lewis T, Skerratt JH, Brown JL, Nichols DS, McMeekin TA. Psychroflexus torquis gen. nov., sp. nov. a psychrophilic species from Antarctic sea ice, and reclassification of Flavobacterium gondwanense (Dobson et al. 1993) as Psychroflexus gondwanense gen. nov., comb. nov. Microbiology. 1998; 144(6):1601-1609. https://doi.org/10.1099/00221287-144-6-1601

110. Miyazaki M, Nogi Y, Fujiwara Y, Horikoshi K. Psychromonas japonica sp. nov., Psychromonas aquimarina sp. nov., Psychromonas macrocephali sp. nov. and Psychromonas ossibalaenae sp. nov., psychrotrophic bacteria isolated from sediment adjacent to sperm whale carcasses off Kagoshima, Japan. International Journal of Systematic and Evolutionary Microbiology. 2008; 58(7):1709-1714. https://doi.org/10.1099/ijs.0.65744-0

111. Anil Kumar P, Srinivas TNR, Sasikala C, Ramana CV. Rhodobacter changlensis sp. nov., a psychrotolerant, phototrophic alphaproteobacterium from the Himalayas of India. International Journal of Systematic and Evolutionary Microbiology. 2007; 57(11):2568-2571. https://doi.org/10.1099/ijs.0.65110-0

112. Shivaji S, Bhadra B, Rao RS, Pradhan S. Rhodotorula himalayensis sp. nov., a novel psychrophilic yeast isolated from Roopkund Lake of the Himalayan mountain ranges, India. Extremophiles. 2008; 12(3):375-381. https://doi.org/10.1007/s00792-008-0144-z

113. Bowman JP, McCammon SA, Nichols DS, Skerratt JH, Rea SM, Nichols PD, McMeekin TA. Shewanella gelidimarina sp. nov. and Shewanella frigidimarina sp. nov., novel Antarctic species with the ability to produce eicosapentaenoic acid (20: 5ω3) and grow anaerobically by dissimilatory Fe (III) reduction. International Journal of Systematic and Evolutionary Microbiology. 1997; 47(4):1040-1047.

114. Albert RA, Waas NE, Pavlons SC, Pearson JL, Ketelboeter L, Rossell\ó-M\óra R, Busse H-J. Sphingobacterium psychroaquaticum sp. nov., a psychrophilic bacterium isolated from Lake Michigan water. International Journal of Systematic and Evolutionary Microbiology. 2013; 63(3):952-958. https://doi.org/10.1099/ijs.0.043844-0

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1. INTRODUCTION

The extreme environment of low temperature is one of the major abiotic stresses acting as the limiting factor affecting the agricultural productivity. 20% of the Earth’s surfaces were covered frozen soils (permafrost), glaciers and ice sheets, and snow cover area. Extreme low temperature represents unique ecosystems which harbor novel biodiversity which has been extensively investigated in the past few years with a focus on culture-dependent and culture-independent techniques [1-6]. The psychrotrophic microbes have been reported from all three domains of life archaea, bacteria, and eukarya and belong to different phylum, namely Actinobacteria, Planctomycetes, Acidobacteria, Ascomycota, Bacteroidetes, Spirochaetes, Basidiomycota, Chlamydiae, Chloroflexi, Nitrospirae, Cyanobacteria, Verrucomicrobia, Firmicutes, Gemmatimonadetes, Mucoromycota, Proteobacteria, Thaumarchaeota, and Euryarchaeota [3-10]. The microbial diversity has opened up new possibilities for potential biotechnological agricultural and industrial applications of beneficial and efficient microbes for diverse sectors including agriculture, industry, and medicine. The cold-adapted microbes attracted the attention of the scientific community due to their aptitude in plant growth promotion, adaptation of plants at low-temperature conditions.

The novel microbes have been isolated using the culture-dependent techniques from cold environments worldwide including Actinoalloteichus spitiensis, RMV-378T [11], Agrococcus lahaulensis, K22-21T [12], Arthrobacter psychrochitiniphilus, GP3T [13], Azospirillum himalayense, ptl-3T [14], Bacillus lehensis, MLB2T [15], Desulforhopalus vacuolatus, ltk10 [16], Dioszegia antarctica, ANT-03-116T [17], Exiguobacterium himgiriensis, K22–26T [18], Exiguobacterium soli, DVS 3YT [19], Flavobacterium frigidarium, A2iT [20], Flavobacterium omnivorum, ZF-8T [21], Flavobacterium phocarum, SE14T [22], Flavobacterium urumqiense, Sr25T [23], Gelidibacter algens, ACAM 536 [24], Geopsychrobacter electrodiphilus, A1T [25], Glaciecola pallidula, ACAM 615T [26], Glaciimonas frigoris, N1-38T [27], Halobacterium lacusprofundi, ACAM 32T [28], Hymenobacter rubripertinctus, NY03-3-30T [29], Massilia eurypsychrophila, B528-3T [30], Nocardiopsis antarcticus [31], Paenibacillus glacialis, KFC91T [6], Pedobacter arcticus, A12T [32], Pseudomonas deceptionensis, M1T [33], Psychrobacter pocilloporae, S6-60T [34], Sphingobacterium antarcticus, 4BY [35], and Sulfitobacter brevis, EL-162T [Table 1] [36].

The cold habitats such as cold deserts, glaciers, and subglacial lakes are hot spots of a great microbial diversity of psychrophilic, psychrotolerant, and psychrotrophic microbiomes. The cold-adapted microbes possess diverse genes responsible for cold adaptation and genes for diverse molecules and alleles with potential applications in diverse fields. There are several reports on whole genome sequences of novel and potential psychrotrophic microbes such as Arthrobacter agilis [37], Cenarchaeum symbiosum [38], Clavibacter sp. [39], Colwellia chukchansi [40], Colwellia psychrerythraea [41], Exiguobacterium antarcticum [42], Exiguobacterium oxidotolerans [43], Exiguobacterium sibiricum [44], Methanococcoides burtonii [45], Octadecabacter antarcticus [46], Paenibacillus sp. [47], Planomicrobium glaciei [48], and Rheinheimera sp. [Table 2] [49]. The whole genome sequences of cold-adapted microbes help to understand the adaptation on microbe under the extreme cold habitats and also potential genes for functional attributes, for example, A. agilis L77, are an important psychrophilic bacteria isolated from Pangong lake, Northwest (NW) Himalayas, India. The strain L77 has abilities to produced cold-adapted hydrolytic enzymes and shows that the plant growth-promoting (PGP) attributes are different low-temperature conditions. The whole genome sequences of psychrophilic bacteria revealed different genes for adaptation and metabolic activities [37]. The novel psychrophilic/psychrotolerant microbes and their products will be applicable in broad range of agricultural, industrial, and medical processes. The cold-tolerant psychrotrophic microbes can be valuable in agriculture as inoculants biofertilizers and biocontrol agents. The present review describes the microbial diversity analysis from cold habitats and its potential applications in agriculture, industry, medicine, and allied sectors.

Table 1: Novel psychrotrophic microbes from diverse cold habitats

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Table 2: Genome sequencing of psychrophilic and psychrotrophic microbes isolated from diverse cold habitats worldwide

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2. BIODIVERSITY PSYCHROTROPHIC MICROBES

The extreme of cold represents hot spots of microbial biodiversity for psychrotrophic, psychrophilic, and psychrotolerant microbiomes [9,50,51]. The biodiversity of psychrotrophic microbes inhabiting cold habitats has been extensively investigated worldwide and has been reported from phylum, namely Actinobacteria, Gemmatimonadetes, Ascomycota, Acidobacteria, Bacteroidetes, Basidiomycota, Chlamydiae, Chloroflexi, Proteobacteria, Cyanobacteria, Firmicutes, Mucoromycota, Verrucomicrobia, Nitrospirae, Planctomycetes, Spirochaetes, Thaumarchaeota, and Euryarchaeota [Figure 1]. The microbiomes of cold habitats including the subglacial lakes, Antarctic, Arctic glacier, permanently ice-covered sea, permafrost, and Himalayan and Mountain lakes have been investigated for the diversity of psychrotrophic, psychrophilic, and psychrotolerant microbes [52-56,19,57-62].

The biodiversity of cold-adapted bacteria was deciphered from northern hills zone of India. A total of 247 culturable bacteria have been isolated using serial dilution and spread plate methods from different sites in Indian Himalayan regions. The bacteria have been identified using 16S rRNA gene sequencing and BLAST analysis. All sequences have been analyzed for phylogenetic profiling and revealed that the sequences are affiliated to four phyla, namely Firmicutes, Proteobacteria, Bacteroidetes, and Actinobacteria. The selected strains have been found to be PGP attributes, which included phosphorus, K, and Zn solubilization; NH3, HCN, indole-3-acetic acid (C10H9NO2), and Fe-chelating compounds production; and the activity of 1-aminocyclopropane-1-carboxylate (ACC) deaminase and biological nitrogen fixation. The psychrotrophic bacteria also possess biological control against the different pathogens such as Macrophomina phaseolina, Rhizoctonia solani, and Fusarium graminearum. These PGP psychrotrophic and psychrotolerant bacteria could be applicable as biofertilizers and biocontrol agents for crops cultivated under the low-temperature conditions and hilly regions [2].

The Indian cold deserts are suitable for the selection of psychrotrophic and psychrotolerant bacteria, archaea, and fungi with potential biotechnological application in diverse sectors, microbes. Yadav et al. [63] investigated microbiome of the cold deserts of Northwestern Himalayas, India, using culture-dependent and culture-independent method and reported different genera, belonging to different phyla, namely Bacteroidetes, Firmicutes, Actinobacteria, and Proteobacteria. The selected microbe showed PGP attributes of the production of NH3, HCN, gibberellic acid, Fe-chelating compounds (catecholates [phenolates], hydroxamates, and carboxylates), and indole acetic acids; P, K, and Zn solubilization and ACC deaminase activity. The microbiomes with psychrotrophic ability with different PGP traits may be used as biofertilizers/bioinoculants and biocontrol agents for hilly crops. The report by Yadav et al. [63] shows the presence of Pseudomonas cedrina, Brevundimonas terrae, Arthrobacter nicotianae, and Paenibacillus tylopili in cold habitats for the 1st time and exhibits multifarious PGP attributes at low-temperature conditions. In another investigation by Yadav et al. [64], the culturable biodiversity of microbiomes in Leh Ladakh region and found that bacteria belong to four phyla, namely Proteobacteria, Firmicutes, Bacteroidetes, and Actinobacteria which included different genera Bacillus, Desemzia, Pseudomonas, Sporosarcina, Arthrobacter, Psychrobacter, Exiguobacterium, Flavobacterium, Alishewanella, Staphylococcus, Brachybacterium, Klebsiella, Providencia, Paracoccus, Planococcus, Sinobaca, Janthinobacterium, Sphingobacterium, Kocuria, Aurantimonas, Citricoccus, Cellulosimicrobium, Brevundimonas, Stenotrophomonas, Vibrio, and Sanguibacter. These microbes possess PGP attributes and may be applicable as bioinoculants and biocontrol for crops in hilly area.

Figure 1: Phylogenetic tree showed the relationship among psychrotrophic, isolated from diverse cold habitats worldwide

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The subglacial lakes are also hot spots of microbial diversity of psychrotrophic and psychrotolerant bacteria with functional attributes of cold-adapted and cold stable active extracellular hydrolytic enzymes productions [65]. On the basis of DNA isolation, polymerase chain reaction amplification of 16S rRNA gene and their sequencing using universal primers reveled that isolated bacilli belong to different genera, namely Exiguobacterium, Virgibacillus, Staphylococcus, Lysinibacillus, Jeotgalicoccus, Desemzia, Bacillus, Paenibacillus, Planococcus, Pontibacillus, Sinobaca, and Sporosarcina. The identified genera affiliated to different families Bacillales incertae sedis, Carnobacteriaceae, Bacillaceae, Planococcaceae, Paenibacillaceae, Staphylococcaceae, and Sporolactobacillaceae. The selected isolates found to exhibit cold-active enzymes such as amylase, chitinase, pectinase, β-glucosidase, protease, cellulase, xylanase, β-galactosidase, laccase, and lipase by different genera, namely P. terrae, Bacillus amyloliquefaciens, Exiguobacterium indicum, Bacillus marisflavi, Pontibacillus sp., Sporosarcina globispora, and Sporosarcina psychrophila.

The PGP psychrotrophic bacilli were investigated from different sites in NW Himalayas India [66] and bacteria have been reported from different genera, namely Desemzia, Exiguobacterium, Lysinibacillus, Sporosarcina, Jeotgalicoccus, Planococcus, Paenibacillus, Sinobaca, Pontibacillus, Staphylococcus, and Virgibacillus. Among all the identified bacterial strains, Bacillus muralis, Bacillus licheniformis, Sporosarcina globispora, P. tylopili, and Desemzia incerta, were found to be an important biofertilizers for Indian Himalayan agriculture.

Cold-adapted microbes are ubiquitous in nature and can be isolated from permanently ice-covered lakes, cloud glaciers, and hilly regions [8]. Microbes recovered using isolation techniques using different growth media as selective and complex and using 16S rRNA gene sequencing the bacteria were affiliated to genera Stenotrophomonas, Virgibacillus, Citricoccus, Enterobacter, Brevundimonas, Providencia, Pseudomonas, Flavobacterium, Pantoea, Planococcus, Paenibacillus, Pontibacillus, Methylobacterium, Psychrobacter, Cellulosimicrobium, Exiguobacterium, Janthinobacterium, Lysinibacillus, Rhodococcus, Sanguibacter, Arthrobacter, Sphingobacterium, Bacillus, Staphylococcus, and Sporosarcina. The identified bacteria affiliated to different phylum on the phylogenetic profiling using Actinobacteria, Proteobacteria, Basidiomycota, Chlamydiae, Chloroflexi, Bacteroidetes, Cyanobacteria, and Firmicutes using Mega 4 analysis.

Cold-adapted microbial communities can be studies using culture-dependent and culture-independent techniques. The microbiomes reported using both techniques culture dependent and culture independent revealed the occurrence of different and diverse major groups viz., Actinobacteria, Ascomycota, Bacteroidetes, Verrucomicrobia, Thaumarchaeota, Spirochaetes, Proteobacteria, Planctomycetes, Nitrospirae, Mucoromycota, Gemmatimonadetes, Firmicutes, Euryarchaeota, Cyanobacteria, Chloroflexi, Chlamydiae, and Basidiomycota. On review of isolated cold-adapted microbes, it was found that proteobacteria were most dominant phylum followed by Firmicutes and Actinobacteria [10].


3. BIOTECHNOLOGICAL APPLICATIONS

The psychrotrophic microbes exhibited multifarious PGP attributes such as ACC deaminase activity, potassium zinc and phosphorus solubilization, biological N2 fixation, and production of different bioactive compounds such as gibberellic acids, ammonia, cytokinins, Fe-chelating compounds, hydrogen cyanide, and indole-3-acetic acid. The use of PGP microbes improves plant growth by supplying plant nutrients, which can help sustain environmental health and soil productivity [10]. Psychrotrophic PGP microbes were found in several genera, including Arthrobacter, Bacillus, Burkholderia, Pseudomonas, Exiguobacterium, Janthinobacterium, Lysinibacillus, Methylobacterium, Microbacterium, Paenibacillus, Providencia, and Serratia [67-70]. The microbes having ACC deaminase activity help plant to alleviate cold stress [Table 3] [2,66,71,72].

Sustainable agriculture requires the use of strategies to increase or maintain the current rate of crops and food production using eco-friendly manners. PGP microbe can affect plant growth directly under the low-temperature condition through nitrogen-fixing bacteria such as Arthrobacter, Azoarcus, Azospirillum, Azotobacter, Bacillus, Enterobacter, Gluconacetobacter, Herbaspirillum, Klebsiella, Pseudomonas, and Serratia [1,2,69,73,74]; ACC deaminase activity by Acinetobacter, Achromobacter, Agrobacterium, Alcaligenes, Azospirillum, Bacillus, Burkholderia, Enterobacter, Pseudomonas, Ralstonia, Serratia, and Rhizobium [75-78] and through indirect mechanism by releasing siderophores, β-1, 3-glucanase, chitinases, antibiotics, and fluorescent pigment or by cyanide production by Alcaligenes sp., Bacillus pumilus, B. subtilis, B. megaterium, Clavibacter michiganensis, Curtobacterium sp., Flavobacterium sp., Kluyvera sp., Microbacterium sp., Pseudomonas alcaligenes, P. putida, and P. fluorescens [79-85].

Table 3: Psychrotrophic microbes with multifunctional plant growth promoting attributes

[Click here to view]

The psychrophilic, psychrotolerant, and psychrotrophic microbes are important for many reasons, particularly because they exhibited antifreezing compounds, antibiotics, and bioactive compounds production [1] and production of extracellular hydrolytic enzymes with potential biotechnological applications in different processes. These enzymes included β-glucosidase, β-galactosidase, xylanase, protease, pectinase, laccase, lipase, chitinase, cellulase, and amylase [37,65,86]. Cold-active enzymes are produced by psychrophilic microbes, namely Acinetobacter, Aquaspirillum, Arthrobacter, Moraxella, Bacillus, Moritella, Carnobacterium, Planococcus, Clostridium, Cytophaga, Shewanella, Vibrio, Flavobacterium, Marinomonas, Paenibacillus, Pseudoalteromonas, Pseudomonas, Psychrobacter, and Xanthomonas [9,37,65,87-89]. Enzymes from psychrophilic and psychrotrophic microbes have become interesting for different processes in industry, pharmaceuticals, medicine, and food and feed industry. Antifreezing compounds from psychrophilic microbes are useful in cryosurgery and also in the cryopreservation of whole organisms, isolated organs, cell lines, and tissues [1,9,37].


4. CONCLUSION AND FUTURE VISION

The psychrophilic, psychrotolerant and psychrotrophic microbiomes have been isolated from different cold habitats worldwide. The microbial diversity of cold environments has attracted the consideration of the scientific community dues to production of cold active enzymes production, anti-freezing compounds, secondary metabolites and bioactive compounds by psychrotrophic microbes. The psychrotolerant/psychrotrophic microbes have potential biotechnological applications in industry, pharmaceuticals, medicine, food and feed for human. The psychrotrophic microbes with multifarious

PGP attributes could be used as biofertilizers and biocontrol agents for crops growing in hilly and low temperature condition for enhance crops production and soil health for sustainable agriculture. The psychrotrophic microbes having biodegradation ability could be used for bioremediation, and waste water treatments for sustainable environments. These cold-adapted microbes may be used for biofuels and biodiesel production for future energy systems. The psychrotrophic microbiomes are widely distributed and have been reported to promote plant growth and alleviation of cold stress in plants. Although the most research work conducted so far has largely focused on psychrophilic and psychrotolerant microbes, it is a welcome sign that many agriculturally important resourceful microbes are being described from various parts of the earth.


5. ACKNOWLEDGMENT

The authors are grateful to Prof. Harcharan Singh Dhaliwal, Vice Chancellor, Eternal University, Baru Sahib, Himachal Pradesh, India, for providing infrastructural facilities and constant encouragement.


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