Next Article in Journal
Epstein-Barr Virus miR-BART17-5p Promotes Migration and Anchorage-Independent Growth by Targeting Kruppel-Like Factor 2 in Gastric Cancer
Next Article in Special Issue
Adaptive Development of Soil Bacterial Communities to Ecological Processes Caused by Mining Activities in the Loess Plateau, China
Previous Article in Journal
Cuminal Inhibits Trichothecium roseum Growth by Triggering Cell Starvation: Transcriptome and Proteome Analysis
Previous Article in Special Issue
High Throughput Sediment DNA Sequencing Reveals Azo Dye Degrading Bacteria Inhabit Nearshore Sediments
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 8
Issue 2
10.3390/microorganisms8020257
microorganisms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Microbial Ecology from the Himalayan Cryosphere Perspective

by
Kusum Dhakar
1 and
Anita Pandey
2,*
1
Newe Ya’ar Research Center, Agricultural Research Organization, Ramat Yishay 30095, Israel
2
Department of Biotechnology, Graphic Era (Deemed to be University), Bell Road, Clement Town, Dehradun 248002, India
*
Author to whom correspondence should be addressed.
Microorganisms 2020, 8(2), 257; https://doi.org/10.3390/microorganisms8020257
Submission received: 12 January 2020 / Revised: 28 January 2020 / Accepted: 29 January 2020 / Published: 14 February 2020
(This article belongs to the Special Issue Microbial Diversity in Extreme Environments)
Browse Figures
Versions Notes

Abstract

:
Cold-adapted microorganisms represent a large fraction of biomass on Earth because of the dominance of low-temperature environments. Extreme cold environments are mainly dependent on microbial activities because this climate restricts higher plants and animals. Himalaya is one of the most important cold environments on Earth as it shares climatic similarities with the polar regions. It includes a wide range of ecosystems, from temperate to extreme cold, distributed along the higher altitudes. These regions are characterized as stressful environments because of the heavy exposure to harmful rays, scarcity of nutrition, and freezing conditions. The microorganisms that colonize these regions are recognized as cold-tolerant (psychrotolerants) or/and cold-loving (psychrophiles) microorganisms. These microorganisms possess several structural and functional adaptations in order to perform normal life processes under the stressful low-temperature environments. Their biological activities maintain the nutrient flux in the environment and contribute to the global biogeochemical cycles. Limited culture-dependent and culture-independent studies have revealed their diversity in community structure and functional potential. Apart from the ecological importance, these microorganisms have been recognized as source of cold-active enzymes and novel bioactive compounds of industrial and biotechnological importance. Being an important part of the cryosphere, Himalaya needs to be explored at different dimensions related to the life of the inhabiting extremophiles. The present review discusses the distinct facts associated with microbial ecology from the Himalayan cryosphere perspective.

Graphical Abstract

1. Introduction

1.1. Himalaya: Geographic Importance and Its Uniqueness

Our planet is a cold planet because the majority experiences temperatures below 15 °C throughout the year. Himalaya is one of the geographic locations that is recognized as a unique low-temperature environment since it holds the highest glacial coverage after the polar regions [1]. Dimensions of Himalaya are vast (>2000 km in plains and height up to >7000 m asl) and distributed widely in the Asian continent, and they control the weather conditions of the surrounding international landmarks/regions (Figure 1). Various ecosystems are found in the huge covering area of these mountain ranges. Himalaya is recognized with highly diverse regions in terms of geographical and biological aspects. It includes evergreen forests, lakes, hot springs, cold deserts, glaciers, grass lands, and so forth [2]. Further, the Himalayan mountain ranges offer a huge natural resource in the regions and support several rivers as source of water in the continent [3]. These distinct geographic regions have climatic dissimilarities that make the Himalayan region a hot spot of biodiversity. From foothills to the top, the mountain ranges are recorded to have unique and highly different biological components.
Besides the polar region, Himalaya possesses the highest altitude (approx. 8000 m asl) and represents similar environmental conditions to the other extreme colder regions on Earth. Its widely known low-temperature regions restrict the growth of higher plants and animals. The normal life in such locations is challenging; therefore, very few animals or plants can be seen surviving in these regions [4]. The extreme colder environments possess several other climatic factors that generate stress for life (e.g., high exposure to harmful radiation, low nutrient and water availability, desiccation, etc.) [5,6]. The extreme colder regions are mainly colonized by cold-adapted microorganisms only, “pyschrophiles/psychrotolerants” (cold-loving microorganisms) [7]. Such cold-loving microorganisms are known to have several modifications at cellular and biochemical levels to alleviate the effect of low temperatures and other associated stress conditions. These extreme low temperatures are dependent on these environment-specific microorganisms for their several ecological processes [8]. In the socio-economic perspective, Himalayan ranges serve as home to the population living in it. The mountains provide resources to the people where agriculture is one of the most important tasks that feeds the settlements and maintains the energy network in the system [9]. In the present review, we discuss the cold-adapted microorganisms in view of their contributions to the low-temperature environments of Himalaya.

1.2. Adaptations: Flexibility of Metabolic Processes Under Cold Conditions

Cold-adapted microorganisms have evolved metabolic processes to cope with the adverse effects of low temperatures (Figure 2). Freezing temperatures cause cell damage due to desiccation and affects physiological reactions adversely. The cold-adapted microorganisms have evolved strategies at biochemical and molecular levels to withstand against the extreme low temperatures [10]. The cold-adapted microorganisms change their lipid composition (increased level of unsaturated fatty acids) to maintain cell membrane integrity under low-temperature environments. A recent study suggested that the microorganisms switch among different metabolic pathways in response to low temperature to obtain energy [11]. The accumulation of cryoprotectants such as trehalose, glycerol, mannitol, and so forth is responsible for maintaining homeostasis in the cell [12]. The cold-active enzymes have conformational flexibility to balance the low kinetic energy with high catalytic efficiency and increased turnover number under low-temperature environments [13]. The low-temperature effect is also associated with oxidative stress, which is overcome by antioxidants to retain a normal cellular environment [14]. Presence of cold shock proteins is reported from different groups such as prokaryotes, animals, and plants. In prokaryotic systems, up-regulation of chaperons (csp, ctr, rbps, etc.) has been studied to support growth under extreme low temperature [15,16]. These RNA-binding proteins (generally glycine-rich RNA binding domains) possess the ability to bind the RNA to destabilize the secondary structures and help in the proper functioning of the biochemical processes [17]. Antifreeze proteins (AFPs)/Ice binding proteins are one of the most important adaptations reported in the organisms (animals, plants, and microorganisms) inhabiting extreme low temperatures. They are the ice binding proteins and help to facilitate microbial growth by inhibiting the formation of ice crystals under extreme low temperatures [18,19]. Except for extreme temperatures, these environments are characterized with oligotrophy, desiccation, radiation, and so forth. The thriving microbes are capable of producing pigments to alleviate the effect of radiation and evolve to tolerate high salt concentration to avoid the adverse effect of desiccation. The pH tolerance of these microorganisms possesses the interesting fact that the microbial component associated with these cold regions has been found to tolerate a wide pH range (whereas the habitat is normal in terms of pH 5–7). Molecular investigations need to be done on the mechanisms behind this tolerance as it could be an important characteristic for novel biotechnological products [20]. Apart from these adaptations, the presence of pigments in cold-adapted microorganisms is recognized as an important adaptation against harmful radiation [21]. Recently, the production of various pigments in the microbiota of Himalayan soils has been reported and is likely to have a role in successional processes [22].
Investigations on the cold-adapted microorganisms have been focused on the most extreme low-temperature environments only. However, the climatic conditions in the Himalaya are somewhat different. Because of the relatively broad spectrum of environmental conditions that prevail, the Himalayan region favors colonization of the “tolerants” in comparison to “philes”. While growth of the latter is restricted to specific climatic conditions, the tolerants, being more diverse, can survive and colonize under a range of external factors. Investigations on the cellular and metabolic processes of these cold-tolerant microorganisms can help in revealing the connection between obligates (philes) and generalists (tolerants). The life processes associated with tolerants are more complicated and important in environmental and industrial perspectives.

2. Microbial Diversity: Compositional and Functional Spectrum

Himalaya is one of the regions representing low-temperature environments (also considered as the “third pole” because of its environmental similarity to the polar regions) on Earth [23]. Earlier, it was thought that these extreme colder regions were sterile and did not contain any life, but the advancement in science and technology revealed a huge and complicated world of these tiny warriors inhabiting in the extreme low-temperature environments (glaciers, snow, ice, etc.) and playing key roles in the environmental processes [24]. The cryosphere, in general, has become a major fraction of global ecology. The fast upgradation in technology stretched the resolution for microbial ecology and revealed the colonization of all the three domains of life in colder regions. The upcoming techniques are likely to provide more information about the dead and the live microbial communities and their activities. Omics approaches have already brought huge information at the molecular level with respect to taxonomic aspects of the microbial communities, enhancing our understanding on microbial interactions in specific niches [25,26]. Similarly, the microbial diversity of an important fraction of the cryosphere, the Himalayas, is being investigated by several research groups with various traditional and high-throughput methods [27].
The existing studies from different regions of Himalaya show the complicated composition of microbial communities [28,29,30,31,32] and diverse metabolic potential [27,33,34] through various culture-dependent and culture-independent methods. In the last two decades, a lot of information associated with the microbial communities of Himalaya has been generated. In the early stages, prokaryotes were highly targeted among the microbial components because of their high involvement in diverse ecological processes [35]. Only few studies are dedicated to the distribution of fungi in the Himalayan region, indicating the significantly high abundance of Ascomycota [5,36,37]. The investigations on these inhabiting micro-eukaryotes are now increasing continuously [29,38,39] because of their high bioprospection values in agriculture and other biotechnology-based industries [27].
Towards bacterial communities, Gangwar et al. [40] reported high dominance of Proteobacteria in culture-dependent and culture-independent studies from the soil of different altitudes of Himalaya, with a reduction in the bacterial genera along the increasing altitude. Even the change in bacterial diversity from subalpine to subtropical regions was observed through TTGE (temporal temperature gradient gel electrophoresis) [41]. The presence of temperature-sensitive and tolerant bacterial isolates has been reported from the glacial sites of Mount Everest, which is an indication of the diversity richness even in the most extreme and harsh regions [42]. Except this, several known glaciers of Himalaya (such as Changme Khangpu, Hamta, Pindari, Kafni, and Roopkund) have been investigated for their bacterial communities through 16S rRNA gene amplicon sequencing along with the traditional approach [43,44,45,46]. In fact, these regions have also been reported as a source of novel species [47,48,49]. The phototrophic microbial communities of the Ladakh region were assessed and reported with a diverse composition of cyanobacteria and eukaryotic algae across the altitude between 3700–5900 m asl [50]. Diversity of cold-adapted bacilli has also been investigated in subglacial lakes located in Indian Himalaya following the amplified ribosomal DNA restriction analysis (ARDRA) method. Further, the bacterial diversity has been recognized for its potential in the production of cold-active enzymes [51]. In addition, records from similar regions revealed the presence of sulfate-reducing and anaerobic bacteria through the phosphor lipid fatty acids (PLFA) analysis [52]. Metagenomic investigations of Pangong Lake located in Himalaya revealed a complex composition of microbiota along with the dominance of bacteria (where Proteobacteria >50%). The microbial communities were found to be mainly associated with the biogeochemical cycle of carbon and nitrogen [53]. In a recent study, the culture-dependent bacterial diversity (high abundance of Firmicutes and Proteobacteria) of the glacial sites of Himalaya has been reported, which showed the importance of Matrix-Assisted Laser Desorption/Ionization–Time Of Flight (MALDI-TOF) mass spectrometry along with nucleic acid based methods, in the identification of cold-tolerant bacterial strains [54].
The abundance of Actinobacteria, Proteobacteria, and Firmicutes in the Himalayan region was similar to the bacterial genera found in the other colder regions (such as Antarctic and Arctic) [46,55]. Because of the environmental similarities between polar areas, microbial components have been found similar, to some extent, in both the colder regions. However, the barren soils of dry valleys located in Himalaya are found to have a rich photoautotrophic microbial diversity in the low-mineral soils, similar to Antarctic dry valleys [56,57]. Yet, more investigations on the molecular level are awaited. These valleys are characterized by mineral-limited soils at high elevation along with extreme temperature fluctuations at a large scale across the freezing temperature. The associated microbial diversity has shown similarity to the Antarctic arid soils and other high-altitude regions, indicating the close relationship of their climatic conditions. Such comparative studies have an advantage towards the distribution of biogeochemical processes across the globe and to understand the analog extremes of Mars, which is characterized by low-mineral soils with extreme cold [57,58].
The soils at high altitude at the retreating of glaciers have become an important ecosystem in the climate change perspective as these barren soils are transforming due to colonization of various new microbial communities. These communities consist of diverse microorganisms, heterotrophs to chemotrophs, that contribute significantly to the biogeochemical cycles in the developing stage of soils. The abundance of cyanobacteria indicates their key role in increasing soil carbon and nitrogen content through other environmental processes [59]. Similar results on the significant contribution of the heterotrophs in the carbon and nitrogen inputs have been reported from the debris covering glaciers [60]. The periglacial soils from different regions (Rocky, Andes, and Himalayas) of the world revealed the unity in the inhabiting fungal component. It has been widely recognized that soils in colder regions are dominated by Ascomycota and Basidiomycota. In contrast, high elevations of mountains that experience high snow falls have been found to be abundant in Chytridiomycota, the zoosporic fungi [61,62]. Probably, the continuous freeze-and-thaw cycles and moisture content lead to the dominance of such lower fungi that are linked between the aquatic and terrestrial ecosystems.
The Tibetan Plateau represents the world’s highest plateau that contains glaciers with extremely cold and unique habitats for colonization of microorganisms in the ice sheets [32]. Probably, aeolian activities contribute towards the microbial transport. An extensive bacterial diversity (15 genera approximately) with prevalence of Proteobacteria has been reported through the molecular methods [63,64]. The autotrophic microbial communities (consisting of Rhizobiales, Burkholderiales, and Actinomycetales) are mainly responsible for the biological processes and nutrient cycling (including carbon and nitrogen) in the semiarid/arid ecological conditions with restricted vegetation [65]. The wetlands located in the region (Tibetan Plateau) are considered as a significant contributor to the biogeochemical cycling of carbon and other nutrients. However, they have been less explored for their microbial communities because of their heterogenous biogeography [66].
Besides glaciers, snow, lakes, or sediments from the barren lands, unique sites with high temperatures (Manikaran, Soldhar, and Ringigad hot springs) have also been located in the Himalayas [67]. Even in the presence of very high temperatures (>40 °C), the complexity of microbial communities is maintained. These hot springs have been reported to possess a high diversity of hyperthermophiles and thermophilic bacteria [68,69,70,71,72,73]. The microbial interactions and the flow of flux was also assessed through metagenome analysis [74,75]. However, advanced investigations on these thermophilic microbial communities with respect to their role in biogeochemical cycles and adaptations are awaited.
Apart from the extensive molecular studies of microbial communities, there are some studies available that provide the status of the microbial biomass in the soil affected by the climatic conditions/anthropogenic activities [76,77]. Forest fires are one of the main anthropogenic activities that exerts a negative effect to the beneficial microbiota [78].
Although a plethora of information on the microbial communities associated with the colder environments is available, understanding the ecological processes and the interactions among the microbial communities is still in its infancy. As per the records, bacterial groups are frequently targeted, whereas information of the fungal component remains scarce. Further, apart from high-throughput methods used in ecological studies, environmental factors still restrict the understanding on microbial interactions effectively. More investigations are required targeting functional attributes that can help us to understand the complex network of the energy flow in such microbial communities. It is widely known that the microbial communities of the low-temperature environments are highly sensitive to temperature changes; therefore, they can serve as indicators of climate change. Out of all these important issues, the cold-adapted microbial communities require more investigation regarding their isolation, characterization, preservation, and careful utilization for various industries.

3. Bioprospection of Cold-Tolerant Microbes: Versatile and Promising Candidates for Various Applications

The cold-adaptive microorganisms are recognized as potential source of cold-active enzymes and bioactive compounds [7]. In the present scenario, the industries are diverting towards green chemistry to use enzyme-based reactions rather than involve chemicals such as in the textile industries [79]. Working with enzymes has several advantages, such as less interference on byproducts, reduced energy consumption with negligible pollution, and no compromise of product quality. The cold-active enzymes have shown low activation enthalpy and flexibility in structures. Such thermodynamic parameters help these cold-active enzymes to perform catalytic actions under the low kinetic energy of cold environments [80]. Lipase, cellulase, amylase, invertase, protease, and lignin-degrading enzymes, produced by cold-adaptive microorganisms, have various applications in detergent, food, the pharmaceutical industry, and so forth [81]. Antifreeze proteins from cold-adaptive organisms have also been recognized for their important physiological and biotechnological contributions. They are the group of proteins that control the shape and size of ice crystals and allow the biochemical activities below freezing temperatures. The production of AFPs from different organisms is the result of convergent evolution through the pressure of extreme cold temperature. The AFPs are reported for other industrial applications too [82,83].
The microorganisms colonizing the extreme colder regions are adapted to cope with various stress conditions (limited nutrient availability, radiations, desiccation, etc.) and produce novel metabolites that are absent in the mesophiles. These metabolites have significant importance in various industries such as food, textiles, therapeutics, and so forth [84,85]. Bioactive compounds related to antimicrobial and immunosuppressive activities, for example, have also been isolated from the cold environment microorganisms [86].
The low-temperature environments of Himalaya are seen as a promising source for novel products, bioactive compounds, and other industrially relevant substances/compounds [22,27,87]. Metagenomic investigations reveal the functional potential of the inhabiting soil microbial communities and allow to study the metabolic pathways and interactions associated with the uncultured biological components also [88]. For example, cold-active enzymes (amylases, endocellulases) were obtained from the clone library and are highly active at low temperatures [89,90]. These low-temperature active products can be used in industries to reduce energy consumption. Apart from this, the multicopper enzymes, well known as versatile and efficient tools against a range of complex compounds, are highly distributed in the region. Potential to produce laccase enzyme from the cold-adapted microorganisms of glacial sites and the hot springs of Himalaya have been reported through culture-dependent and culture-independent methods [91,92]. The cold-adapted microorganisms of Himalayan soils have also been reported as an abundant source of diverse cold-active lipases [93,94] that have importance in bioremediation, food industries, and cleaning industries [95]. The Himalayan soils are found to possess high diversity of bacteria that produce carbonic anhydrase, which is an important candidate for investigations related to carbon sequestration [96]. Among the microorganisms, cold-adapted yeasts are recognized as an important group for their survival strategies and biotechnological benefits [97]. There are some records available on these single-cell eukaryotes from Himalaya; however, more investigations are awaited for their ecological contributions [98].
Not only the biotechnological benefits but also the inhabiting cold loving microorganisms contribute to several ecological processes in different ecosystems located in Himalaya (Figure 3). In the environmental importance, biodegradation and agriculture (such as plant growth promoting activities and biocontrol) under the colder regions are well supported by the inhabiting microbes [99,100]. These microorganisms have the capability to degrade a range of compounds that have been identified as strong agents in bioremediation. They are also involved in the carbon cycle and contribute in the energy flux in the environment. Pseudomonas, Acinetobacter, Rhodococcus, Bacillus, and Sphingobium have been found to contribute significantly to the degradation of complex hydrocarbons (such as petroleum products) under low-temperature environments [101,102,103,104]. The presence of a particular hydrocarbon compound also affects the environment on the ecological ground. For example, a colder area (China–Russia) contaminated with petroleum revealed the microbial shifts and the abundance of efficient degraders (endemic communities) [105].
The biodegradation process in low-temperature environments is very slow and restricted. Organic carbon is sequestered and accumulates in these environments (in the form of lignocellulosic material). These cold-adapted bacteria were also found to possess different hydrolytic enzymatic activities indicating their contribution in the cycling of nutrients including carbon [34,40,106]. Studies from Indian Himalaya have proved that the associated psychrotolerant spp. (bacteria and fungi) have the potential to produce lignin-degrading enzymes at a wide range of temperature and pH [91,107] (Figure 4).
Apart from degradation, the inhabiting microbial communities have shown their immense contribution to improve the agriculture in low to extreme low temperature environments of Himalaya. These psychrotrophic/psychrophilic microorganisms have been reported for their potential in plant growth promotion activities. They are found to possess activities, such as phosphate solubilization, indole acetic acid production, and siderophore secretion, that are useful in agriculture under low-temperature environments [52,108]. In the recent two decades, several researchers have published the potential utilization of microbial strains from Indian Himalaya. Rhodococcus, Pseudomonas, Bacillus, Serratia, and Ascomycetous fungi (Trichoderma, Aspergillus, Penicillium) have been recognized as promising candidates in agriculture and forestry [100,109,110,111,112], but they need further attention for obtaining a form of valuable product. Recently, a strain of Stenotrophomonas with multiple plant growth promoting activities and possibilities to utilize as biofertilizer has been reported [113]. In last few years, a range of endophytes have been isolated and screened for their importance in agriculture under the low-temperature environments of Himalaya [114,115]; except for this, they have also been recognized as a good source of antimicrobial compounds [116]. Towards ecological aspects, the specific dark septate endophytes have been also investigated from the high altitude of Himalaya, and they await their recognition for their role as indicators of the changing climate under the mountain ecosystem [117]. By considering the ecological and biotechnological importance of the endophytes, it is important to investigate this group effectively because they are likely to be the important players that help in the nutrient flux between soil and plants (especially in the nutrient-poor soils of high altitudes of Himalaya).
Additional information on the taxonomic and functional aspects of microbial communities of Himalayan regions is provided in Table 1.

4. Knowledge Gaps and Future Prospects

So far, we have discussed the importance of Himalaya as a fraction of the cryosphere, which contributes significantly to the global ecology. Although the microbial diversity of Himalaya has been explored by various research groups, still the information related to the microbial ecology of this unique region is scarce. Most researchers have focused on the taxonomic aspects, while the microbial interactions and functional ecology remain neglected. Further, the diversity or the composition of the most important micro-eukaryotes in the Himalayan region is not targeted well, neither with culture-dependent nor with culture-independent methods. Since Himalaya shares climatic similarities with the polar regions, information on the microbial composition and the metabolic activities needs to be investigated so that it can be compared to the extreme colder regions to identify microbial resources (e.g., Antarctic and Arctic investigated for novel antibiotics, degraders, etc.). The gene pool of several unique sites of Himalaya (most of the glaciers, rock-associated microbial communities) is still untouched. The gene pool is precious because of its wide tolerance against a range of environmental conditions, such as high-temperature fluctuation and precipitation in lush green forests to barren cold deserts.
Majority of these studies report high abundance of extremotolerant species that might be due to a broad fluctuation in temperature (extreme low to normal 30–40 °C) of various regions of Himalaya. This broad range of temperature change allows the mesophiles and the tolerants to grow actively in the environment. This could be one the reasons for the distinct metabolic ability of Himalayan microorganisms from the microbial communities of the Antarctic region [31].
Besides, in the present scenario of global warming, these cold environments are being recognized as highly affected regions because of their sensitivity towards temperature change. While most of the studies provide information on the shifts in microbial communities in various environments of the polar regions, the ecology of the Himalayas still needs focused attention. Very rare or negligible information is on record about the transformation of the microbial activities under the changing environmental conditions. The change in green cover and glacier retreat are documented for Arctic and Antarctic, but no such authentic information is provided in the context of Himalaya.
It will be important to explore the extreme cold regions of Himalaya to enhance our understanding on the metabolic activities in the low-temperature environments. This would help us to identify ecological problems associated with the mountain system, leading to the efficient use of natural resources along with the preservation of the unique biodiversity, the microbial diversity in particular, of Himalaya.

Funding

No external funding was received for writing this review paper.

Acknowledgments

ICIMOD (International Centre for Integrated Mountain Development), Nepal is gratefully acknowledged for providing the map of Himalaya. AP thanks the Editors of the special issue “Microbial Diversity in Extreme Environments” for the invitation.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Khan, A.A.; Pant, N.C.; Sarkar, A.; Tandon, S.K.; Thamban, M.; Mahalinganathan, K. The Himalayan cryosphere: A critical assessment and evaluation of glacial melt fraction in the Bhagirathi basin. Geo. Front. 2017, 8, 107–115. [Google Scholar] [CrossRef] [Green Version]
  2. Singh, J.S. Sustainable development of the Indian Himalayan region: Linking ecological and economic concerns. Curr. Sci. 2006, 90, 784–788. [Google Scholar]
  3. Joshi, D.; Kumar, S.; Suyal, D.C.; Goel, R. The Microbiome of the Himalayan ecosystem. In Mining of Microbial Wealth and Meta Genomics; Kalia, V., Shouche, Y., Purohit, H., Rahi, P., Eds.; Springer: Singapore, 2017; pp. 110–116. [Google Scholar]
  4. Margesin, R.; Miteva, V. Diversity and ecology of psychrophilic microorganisms. Res. Microbiol. 2011, 162, 346–361. [Google Scholar] [CrossRef] [PubMed]
  5. Hassan, N.; Rafiq, M.; Hayat, M.; Shah, A.A.; Hasan, F. Psychrophilic and psychrotrophic fungi: A comprehensive review. Rev. Env. Sci. Biotechnol. 2016, 15, 147–172. [Google Scholar] [CrossRef]
  6. Dhaulaniya, A.S.; Balan, B.; Kumar, M.; Agarwal, P.K.; Singh, D.K. Cold survival strategies for bacteria, recent advancement and potential industrial applications. Arch. Microbiol. 2019, 201, 1–16. [Google Scholar] [CrossRef]
  7. Margesin, R.; Feller, G. Biotechnological applications of psychrophiles. Environ. Technol. 2010, 31, 835–844. [Google Scholar] [CrossRef]
  8. Margesin, R.; Collins, T. Microbial ecology of the cryosphere (glacial and permafrost habitats): Current knowledge. Appl. Microbiol. Biotechnol. 2019, 103, 2537–2549. [Google Scholar] [CrossRef] [Green Version]
  9. Mukherji, A.; Sinisalo, A.; Nusser, M.; Garrard, R.; Eriksson, M. Contributions of the cryosphere to mountain communities in the Hindu Kush Himalaya: A review. Reg. Env. Chang. 2019, 19, 1311–1326. [Google Scholar] [CrossRef] [Green Version]
  10. Collins, T.; Margesin, R. Psychrophilic lifestyles: Mechanisms of adaptation and biotechnological tools. Appl. Microbiol. Biotechnol. 2019, 103, 2857–2871. [Google Scholar] [CrossRef]
  11. Bore, E.k.; Halicki, S.; Kuzyakov, Y.; Dippold, M.A. Structural and physiological adaptations of soil microorganisms to freezing revealed by position-specific labeling and compound-specific 13C analysis. Biogeochemistry 2019, 143, 207–219. [Google Scholar] [CrossRef]
  12. Robinson, C.H. Cold adaptation in Arctic and Antarctic fungi. New Phytol. 2001, 151, 341–353. [Google Scholar] [CrossRef]
  13. Cavicchioli, R.; Siddiqui, K.S.; Andrews, D.; Sowers, K.R. Low-temperature extremophiles and their applications. Curr. Opi. Biotechnol. 2002, 13, 253–261. [Google Scholar] [CrossRef]
  14. Chattopadhyay, M.K.; Raghu, G.; Sharma, Y.V.R.K.; Biju, A.R.; Rajasekharan, M.V.; Shivaji, S. Increase in oxidative stress at low temperature in an Antarctic bacterium. Curr. Microbiol. 2011, 62, 544–546. [Google Scholar] [CrossRef]
  15. Siddiqui, K.S.; Williams, T.J.; Wilkins, D.; Yau, S.; Allen, M.A.; Brown, M.V.; Lauro, F.M.; Cavicchioli, R. Pyshcrophiles. Annu. Rev. Earth Planet Sci. 2013, 41, 87–115. [Google Scholar] [CrossRef]
  16. Yu, T.; Keto-Timonen, R.; Jiang, X.; Virtanen, J.-P.; Korkeala, H. Insights into the phylogeny and evolution of cold shock proteins: From Enteropathogenic Yersinia and Escherichia coli to Eubacteria. Int. J. Mol. Sci. 2019, 20, 4059. [Google Scholar] [CrossRef] [Green Version]
  17. Arai, T.; Fukami, D.; Hoshino, T.; Kondo, H.; Tsuda, S. Ice-binding proteins from the fungus Antarctomyces psychrotrophicus possibly originate from two different bacteria through horizontal gene transfer. Febs J. 2019, 286, 946–962. [Google Scholar] [CrossRef] [Green Version]
  18. Singh, P.; Hanada, Y.; Singh, S.M.; Tsuda, S. Antifreeze protein activity in Arctic cryoconite bacteria. Fems Microbiol. Lett. 2011, 351, 14–22. [Google Scholar] [CrossRef] [Green Version]
  19. Marco, M.; Brocca, S.; Orlando, M.; Lott, M. The “cold revolution”. Present and future applications of cold-active enzymes and ice-binding proteins. New Biotechnol. 2019, 55, 5–11. [Google Scholar]
  20. Dhakar, K.; Pandey, A. Wide pH range tolerance in extremophiles: Towards understanding an important phenomenon for future biotechnology. Appl. Microbiol. Biotechnol. 2016, 100, 2499–2510. [Google Scholar] [CrossRef]
  21. Marizcurrena, J.J.; Cerdá, M.F.; Alem, D.; Castro-Sowinski, S. Living with Pigments: The Colour Palette of Antarctic Life. In The Ecological Role of Micro-organisms in the Antarctic Environment; Castro-Sowinski, S., Ed.; Springer Polar Sciences: Cham, Switzerland, 2019; pp. 65–82. [Google Scholar]
  22. Rehakova, K.; Capkova, K.; Hrouzek, P.; Koblizek, M.; Dolezal, J. Microbial photosynthetic and photoprotective pigments in Himalayan soils originating from different elevations and successional stages. Soil Biol. Biochem. 2019, 132, 153–164. [Google Scholar] [CrossRef]
  23. Stres, B.; Sul, W.J.; Murovec, B.; Tiedje, J.M. Recently deglaciated high-altitude soils of the Himalaya: Diverse environments, heterogenous bacterial communities and long-range dust inputs from the upper troposphere. PLoS ONE 2013, 8, e76440. [Google Scholar] [CrossRef]
  24. Miteva, V. Bacteria in snow and glacier ice. In Psychrophiles: From Biodiversity to Biotechnology; Margesin, R., Schinner, F., Marx, J.-C., Gerday, C., Eds.; Springer-Verlag: Berlin/Heidelberg, Germany, 2008; pp. 31–50. [Google Scholar]
  25. Kerfahi, D.; Tripathi, B.M.; Dong, K.; Kim, M.; Kim, H.; Ferry Slik, J.W.; Go, R.; Adams, J.M. From the High Arctic to the Equator: Do Soil Metagenomes Differ According to Our Expectations? Microb. Ecol 2019, 77, 168–185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Fierer, N.; Leff, J.W.; Adams, B.J.; Nielsen, U.N.; Bates, S.T.; Lauber, C.L.; Owens, S.; Gilbert, J.A.; Wall, D.H.; Caporaso, J.G. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. PNAS 2012, 109, 21390–21395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Pandey, A.; Dhakar, K.; Jain, R.; Pandey, N.; Gupta, V.K.; Kooliyottil, R.; Dhyani, A.; Malviya, M.K.; Adhikari, P. Cold Adapted Fungi from Indian Himalaya: Untapped Source for Bioprospecting. Proc. Natl. Acad. Sci. India. Sect. B Biol. Sci. 2018, 89, 1125–1132. [Google Scholar] [CrossRef]
  28. Adhikari, N.P.; Liu, Y.; Liu, K.; Zhang, F.; Adhikari, S.; Chen, Y.; Liu, X. Bacterial community composition and diversity in Koshi River, the largest river of Nepal. Ecol. Indic. 2019, 104, 501–511. [Google Scholar] [CrossRef]
  29. Kumar, S.; Suyal, D.C.; Yadav, A.; Shouche, Y.; Goel, R. Microbial diversity and soil physiochemical characteristic of higher altitude. PLoS ONE 2019, 14, e0213844. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Sherpa, M.T.; Najar, I.N.; Das, S.; Thakur, N. Culture independent bacterial diversity of Changme Khang and Changme Khangpu glaciers of North Sikkim, India. Environ. Sustain. 2019, 2, 241–253. [Google Scholar] [CrossRef]
  31. Sanyal, A.; Antony, R.; Samui, G.; Thamban, M. Microbial communities and their potential for degradation of dissolved organic carbon in cryoconite hole environments of Himalaya and Antarctica. Microbiol. Res. 2018, 208, 32–42. [Google Scholar] [CrossRef]
  32. Xiang, S.R.; Yao, T.D.; An, L.Z.; Xu, B.Q.; Li, Z.; Wu, G.J.; Wang, Y.Q.; Ma, S.; Chen, X.R. Bacterial diversity in Malan ice core from the Tibetan Plateau. Folia Microbiol. 2004, 49, 269–275. [Google Scholar] [CrossRef]
  33. Thakur, V.; Kumar, V.; Kumar, S.; Singh, D. Diverse culturable bacterial communities with cellulolytic potential revealed from pristine habitat in Indian trans-Himalaya. Can. J. Microbiol. 2018, 64, 798–808. [Google Scholar] [CrossRef]
  34. Venkatachalam, S.; Gowdaman, V.; Prabagaran, S.R. Culturable and culture-independent bacterial diversity and the prevalence of cold-adapted enzymes from the Himalayan mountain ranges of India and Nepal. Microb. Ecol. 2015, 69, 472–491. [Google Scholar] [CrossRef] [PubMed]
  35. Kasana, R.C. Bacterial Diversity in Cold Environments of Indian Himalayas. In Mining of Microbial Wealth and Meta Genomics; Kalia, V., Shouche, Y., Purohit, H., Rahi, P., Eds.; Springer: Singapore, 2017; pp. 83–99. [Google Scholar]
  36. Dhakar, K.; Sharma, A.; Pandey, A. Cold, pH and salt tolerant Penicillium spp. inhabit the high-altitude soils in Himalaya, India. World J. Microbiol. Biotechnol. 2014, 30, 1315–1324. [Google Scholar] [CrossRef] [PubMed]
  37. Devi, L.S.; Khaund, P.; Nongkhlaw, F.M.W.; Joshi, S.R. Diversity of Culturable Soil Micro-fungi along Altitudinal Gradients of Eastern Himalayas. Mycobiology 2012, 40, 151–158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Sharma, D.; Gosai, K.; Dutta, J.; Arunachalam, A.; Shukla, A.K. Fungal diversity of twelve major vegetational zones of Arunachal Himalaya, India. Curr. Res. Env. Appl. Mycol. 2015, 5, 101–119. [Google Scholar] [CrossRef]
  39. Luo, B.; Sun, H.; Zhang, Y.; Yan, W.; Zhang, R.; Ni, Y. Habitat-specificity and diversity of culturable cold-adapted yeasts of a cold-based glacier in the Tianshan Mountains, northwestern China. Appl. Microbiol. Biotechnol. 2019, 103, 2311–2327. [Google Scholar] [CrossRef] [PubMed]
  40. Gangwar, P.; Alam, S.I.; Bansod, S.; Singh, L. Bacterial diversity of soil samples from the western Himalayas, India. Can. J. Microbiol. 2009, 55, 564–577. [Google Scholar] [CrossRef]
  41. Soni, R.; Saluja, B.; Goel, R. Bacterial community analysis using temporal temperature gradient gel electrophoresis (TTGE) of 16S rDNA PCR products of soil metagenome. Ekologija 2010, 56, 94–98. [Google Scholar] [CrossRef]
  42. Liu, Y.; Yao, T.; Jiao, N.; Kang, S.; Huang, S.; Li, Q.; Wang, K.; Liu, X. Culturable bacteria in glacial meltwater at 6,350 m on the East Rongbuk Glacier, Mount Everest. Extremophiles 2009, 13, 89–99. [Google Scholar] [CrossRef]
  43. Pradhan, S.; Srinivas, T.N.R.; Pindi, P.K.; Kishore, K.H.; Begum, Z.; Singh, P.K.; Singh, A.K.; Pratibha, M.S.; Yasal, A.K.; Reddy, G.S.N.; et al. Bacterial biodiversity from Roopkund Glacier, Himalayan mountain ranges, India. Extremophiles 2010, 14, 377–395. [Google Scholar] [CrossRef]
  44. Sherpa, M.T.; Najar, I.N.; Das, S.; Thakur, N. Bacterial diversity in an alpine debris-free and debris-cover accumulation zone glacier ice, North Sikkim, India. Indian J. Microbiol. 2018, 58, 470–478. [Google Scholar] [CrossRef]
  45. Shivaji, S.; Kumari, K.; Kishore, K.H.; Pindi, P.K.; Rao, P.S.; Radha Srinivas, T.N.; Asthana, R.; Ravindra, R. Vertical distribution of bacteria in a lake sediment from Antarctic by culture independent and culture-dependent approaches. Res. Microbiol. 2011, 162, 191–203. [Google Scholar] [CrossRef] [PubMed]
  46. Srinivas, T.N.; Singh, S.M.; Pradhan, S.; Prathibha, M.S.; Kishore, K.H.; Singh, A.K.; Begum, Z.; Prabagaran, S.R.; Reddy, G.S.; Shivaji, S. Comparison of bacterial diversity in proglacial soil from Kafni Glacier, Himalayan Mountain ranges, India, with the bacterial diversity of other glaciers in the world. Extremophiles 2011, 15, 673–690. [Google Scholar] [CrossRef] [PubMed]
  47. Chaturvedi, P.; Reddy, G.S.N.; Shivaji, S. Dyadobacter hamtensis sp. nov. from Hamta glacier, located in the Himalayas, India. Int. J. Syst. Evol. Microbiol. 2005, 55, 2113–2117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Mayilraj, S.; Prasad, G.S.; Suresh, K.; Saini, H.S.; Shivaji, S.; Chakrabarti, T. Planococcus stackebrandtii sp. nov. isolated from a cold desert of the Himalayas, India. Int. J. Syst. Evol. Microbiol. 2005, 55, 91–94. [Google Scholar] [CrossRef] [Green Version]
  49. Najar, I.N.; Sherpa, M.T.; Das, S.; Thakur, N. Geobacillus yumthangensis sp. nov., a thermophilic bacterium isolated from a north-east Indian hot spring. Int. J. Syst. Evol. Microbiol. 2018, 68, 3430–3434. [Google Scholar] [CrossRef] [PubMed]
  50. Rehakova, K.; Chlumska, Z.; Dolezal, J. Soil Cyanobacterial and Microalgal Diversity in Dry Mountains of Ladakh, NW Himalaya, as Related to Site, Altitude, and Vegetation. Microb. Ecol. 2011, 62, 337–346. [Google Scholar] [CrossRef] [PubMed]
  51. Yadav, A.N.; Sachan, S.G.; Verma, P.; Tyagi, S.P.; Kaushik, R.; Saxena, A.K. Culturable diversity and functional annotation of psychrotrophic bacteria from cold desert of Leh Ladakh (India). World J. Microbiol. Biotechnol. 2015, 31, 95–108. [Google Scholar] [CrossRef] [PubMed]
  52. Yadav, A.N.; Sachan, S.G.; Verma, P.; Saxena, A.K. Prospecting cold deserts of north western Himalayas for microbial diversity and plant growth promoting attributes. J. Biosci. Bioengg. 2015, 119, 683–693. [Google Scholar] [CrossRef]
  53. Rathour, R.; Gupta, J.; Kumar, M.; Hiloidhari, M.; Mehrotra, A.K.; Thakur, I.S. Metagenomic sequencing of microbial communities from brackish water of Pangong lake of the Northwest Indian Himalayas. Genome Announc. 2017, 5, e01029-17. [Google Scholar] [CrossRef] [Green Version]
  54. Pandey, A.; Jain, R.; Sharma, A.; Dhakar, K.; Kaira, G.S.; Rahi, P.; Dhyani, A.; Pandey, N.; Adhikari, P.; Shouche, Y.S. 16S rRNA gene sequencing and MALDI-TOF mass spectrometry based comparative assessment and bioprospection of psychrotolerant bacteria isolated from high altitudes under mountain ecosystem. SN Appl. Sci. 2019, 1, 278. [Google Scholar] [CrossRef] [Green Version]
  55. Gupta, P.; Sangwan, N.; Lal, R.; Vakhlu, J. Bacterial diversity of Drass, cold desert in Western Himalaya, and its comparison with Antarctic and Arctic. Arch. Microbiol. 2015, 197, 851–860. [Google Scholar] [CrossRef] [PubMed]
  56. Janatková, K.; Reháková, K.; Doležal, J.; Simek, M.; Chlumska, Z.; Dvorsky, M.; Kopecky, M. Community structure of soil phototrophs along environmental gradients in arid Himalaya. Environ. Microbiol. 2013, 15, 2505–2516. [Google Scholar]
  57. Schmidt, S.; Lynchi, R.; King, A.; Karki, D.; Robeson, M.S.; Nagy, L.; Williams, M.W.; Mitter, M.S.; Freeman, K.R. Phylogeography of microbial phototrophs in the dry valleys of the high Himalayas and Antarctic. Proc. Roy Soc. B Biol. Sci. 2011, 278, 702–708. [Google Scholar] [CrossRef] [PubMed]
  58. King, A.J.; Freeman, K.R.; McCormick, K.F.; Lynch, R.C.; Lozupone, C.; Knight, R.; Schmidt, S.K. Biogeography and habitat modeling of high-alpine bacteria. Nat. Comm. 2010, 1, 53. [Google Scholar] [CrossRef] [Green Version]
  59. Schmidt, S.K.; Reed, S.C.; Nemergut, D.R.; Grandy, A.S.; Cleveland, C.C.; Weintraub, M.N.; Hill, A.W.; Costello, E.K.; Meyer, A.F.; Neff, J.C.; et al. The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc. Biol. Sci. 2008, 275, 2793–2802. [Google Scholar] [CrossRef] [Green Version]
  60. Franzetti, A.; Tatangelo, V.; Gandolfi, I.; Bertolini, V.; Bestetti, G.; Diolaiuti, G.; D’Agata, C.; Mihalcea, C.; Smiraglia, C.; Ambrosini, R. Bacterial community structure on two alpine debris-covered glaciers and biogeography of Polaromonas phylotypes. ISME J. 2013, 7, 1483–1492. [Google Scholar] [CrossRef] [Green Version]
  61. Freeman, K.R.; Martin, A.P.; Karki, D.; Lynch, R.C.; Mitter, M.S.; Meyer, A.F.; Longcore, J.E.; Simmons, D.R.; Schmidt, S.K. Evidence that chytrids dominate fungal communities in high-elevation soils. Proc. Nat. Acad. Sci. USA 2009, 106, 18315–18320. [Google Scholar] [CrossRef] [Green Version]
  62. Schmidt, S.K.; Naff, C.S.; Lynch, R.C. Fungal communities at the edge: Ecological lessons from high alpine fungi. Fun. Ecol. 2012, 5, 443–452. [Google Scholar] [CrossRef]
  63. Liu, Y.; Yao, T.; Jiao, N.; Kang, S.; Xu, B.; Zeng, Y.; Huang, S.; Liu, X. Bacterial diversity in the snow over Tibetan Plateau Glaciers. Extremophiles 2009, 13, 411–423. [Google Scholar] [CrossRef] [Green Version]
  64. Zhang, S.; Hou, S.; Wu, Y.; Qin, D. Bacteria in Himalayan glacial ice and its relationship to dust. Biogeosciences 2008, 5, 1741–1750. [Google Scholar] [CrossRef] [Green Version]
  65. Guo, G.; Kong, W.; Liu, J.; Zhao, J.; Du, H.; Zhang, X.; Xia, P. Diversity and distribution of autotrophic microbial community along environmental gradients in grassland soils on the Tibetan Plateau. Appl. Microbiol. Biotechnol. 2015, 99, 8765–8776. [Google Scholar] [CrossRef] [PubMed]
  66. Deng, Y.; Cui, X.; Herna´ndez, M.; Dumont, M.G. Microbial diversity in hummock and hollow soils of three wetlands on the Qinghai-Tibetan plateau revealed by 16S rRNA pyrosequencing. PLoS ONE 2014, 9, e103115. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Rao, M.P.N.; Liu, L.; Jiao, J.-Y.; Xiao, M.; Li, W.-J. Hot Springs of India: Occurrence and Microbial Diversity. In Extremophiles in Eurasian Ecosystems: Ecology, Diversity, and Applications. Microorganisms for Sustainability; Egamberdieva, D., Birkeland, N.K., Panosyan, H., Li, W.J., Eds.; Springer: Singapore, 2018; pp. 29–55. [Google Scholar]
  68. Kumar, M.; Yadav, A.N.; Tiwari, R.; Prasanna, R.; Saxena, A.K. Deciphering the diversity of culturable thermotolerant bacteria from Manikaran hot springs. Ann. Microbiol. 2014, 64, 741–751. [Google Scholar] [CrossRef]
  69. Najar, I.N.; Sherpa, M.T.; Das, S.; Thakur, N. Microbial ecology of two hot springs of Sikkim: Predominate population and geochemistry. Sci. Total Environ. 2018, 637, 730–745. [Google Scholar] [CrossRef]
  70. Pandey, A.; Dhakar, K.; Sharma, A.; Priti, P.; Sati, P.; Kumar, B. Thermophilic bacteria that tolerate a wide temperature and pH range colonize the Soldhar (95 °C) and Ringigad (80 °C) hot springs of Uttarakhand, India. Ann. Microbiol. 2015, 65, 809–816. [Google Scholar] [CrossRef]
  71. Rawat, N.; Joshi, G.K. Bacterial community structure analysis of a hot spring soil by next generation sequencing of ribosomal RNA. Genomics 2018, 111, 1053–1058. [Google Scholar] [CrossRef]
  72. Sahay, H.; Yadav, A.N.; Singh, A.K.; Singh, S. Hot springs of Indian Himalayas: Potential sources of microbial diversity and thermostable hydrolytic enzymes. 3 Biotech 2017, 7, 118. [Google Scholar] [CrossRef] [Green Version]
  73. Sharma, A.; Paul, D.; Dhotre, D.; Jani, K.; Pandey, A.; Shouche, Y.S. Deep sequencing analysis of bacterial community structure of Soldhar hot spring, India. Microbiology 2017, 86, 136–142. [Google Scholar] [CrossRef]
  74. Sharma, A.; Schmidt, M.; Kiesel, B.; Mahato, N.K.; Cralle, L.; Singh, Y.; Richnow, H.H.; Gilbert, J.A.; Arnold, W.; Lal, R. Bacterial and archaeal viruses of Himalayan hot springs at manikaran modulate host genomes. Front. Microbiol. 2018, 9, 3095. [Google Scholar] [CrossRef]
  75. Mahato, N.K.; Sharma, A.; Singh, Y.; Lal, R. Comparative metagenomic analyses of a high-altitude Himalayan geothermal spring revealed temperature-constrained habitat-specific microbial community and metabolic dynamics. Arch. Microbiol. 2019, 201, 377–388. [Google Scholar] [CrossRef]
  76. Bargali, K.; Manral, V.; Padalia, K.; Bargali, S.S.; Upadhyay, V.P. Effect of vegetation type and season on microbial biomass carbon in Central Himalayan forest soils, India. Catena 2018, 171, 125–135. [Google Scholar] [CrossRef]
  77. Lungmuana; Singh, S.B.; Choudhury, B.U.; Vanthawmliana; Saha, S.; Hnamte, V. Transforming jhum to plantations: Effect on soil microbiological and biochemical properties in the foot hills of North Eastern Himalayas, India. Catena 2019, 177, 84–91. [Google Scholar] [CrossRef]
  78. Mittal, D.; Shukla, R.; Verma, S.; Sagar, A.; Verma, K.S.; Pandey, A.; Negi, Y.S.; Saini, R.V.; Saini, A.K. Fire in pine grown regions of Himalayas depletes cultivable plant growth promoting beneficial microbes in the soil. Appl. Soil Ecol. 2019, 139, 117–124. [Google Scholar] [CrossRef]
  79. Razzaq, A.; Shamsi, S.; Ali, A.; Ali, Q.; Sajjad, M.; Malik, A.; Ashraf, M. Microbial Proteases Applications. Front. Bioeng. Biotechnol. 2019, 7, 110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  80. Cavicchioli, R.; Charlton, T.; Ertan, H.; Mohd Omar, S.; Siddiqui, K.S.; Williams, T.J. Biotechnological uses of enzymes from psychrophiles. Microb. Biotechnol. 2011, 4, 449–460. [Google Scholar] [CrossRef] [Green Version]
  81. Gomes, J.; Steiner, W. Extremophiles and Extremozymes. Food Technol. Biotechnol. 2004, 42, 223–235. [Google Scholar]
  82. Kim, H.J.; Lee, J.H.; Hur, Y.B.; Lee, C.W.; Park, S.-H.; Koo, B.-W. Marine antifreeze proteins: Structure, function, and application to cryopreservation as a potential cryoprotectant. Marine Drugs 2017, 15. [Google Scholar] [CrossRef] [Green Version]
  83. Venkatesh, S.; Dayananda, C. Properties, potentials, and prospects of antifreeze proteins. Crit. Rev. Biotechnol. 2008, 28, 57–82. [Google Scholar] [CrossRef]
  84. Bratchkova, A.; Ivanova, V. Bioactive metabolites produced by microorganisms collected in Antarctic and the Arctic. Biotechnol. Biotechnol. Equip 2011, 25, 1–7. [Google Scholar] [CrossRef]
  85. Giudice, A.L.; Fani, R. Antimicrobial potential of cold-adapted bacteria and fungi from Polar Regions. In Biotechnology of Extremophiles; Rampelotto, P.H., Ed.; Springer International Publishing: New York, NY, USA, 2016. [Google Scholar]
  86. Tian, Y.; Li, Y.-L.; Zhao, F.-C. Secondary metabolites from Polar organisms. Marine Drugs 2017, 15, 28. [Google Scholar] [CrossRef] [Green Version]
  87. Panwar, S.; Molpa, D.; Joshi, G.K. Biotechnological Potential of Some Cold-Adapted Bacteria Isolated from North-Western Himalaya. Microbiol 2019, 88, 343–352. [Google Scholar] [CrossRef]
  88. Vester, J.K.; Glaring, M.A.; Stougaard, P. Improved cultivation and metagenomics as new tools for bioprospecting in cold environments. Extremophiles 2015, 19, 17–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Bhat, A.; Riyaz-Ul-Hassan, S.; Ahmad, N.; Srivastava, N.; Johri, S. Isolation of cold-active, acidic endocellulase from Ladakh soil by functional metagenomics. Extremophiles 2013, 17, 229–239. [Google Scholar] [CrossRef] [PubMed]
  90. Sharma, S.; Khan, F.G.; Qazi, G.N. Molecular cloning and characterization of amylase from soil metagenomic library derived from Northwestern Himalayas. Appl. Microbiol. Biotechnol. 2010, 86, 1821–1828. [Google Scholar] [CrossRef] [PubMed]
  91. Kaira, G.S.; Dhakar, K.; Pandey, A. A psychrotolerant strain of Serratia marcescens (MTCC 4822) produces laccase at wide temperature and pH range. AMB Express 2015, 5, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Gupta, V.; Gupta, N.; Capalash, N.; Sharma, P. Bio-prospecting Bacterial Diversity of Hot Springs in Northern Himalayan Region of India for Laccases. Indian J. Microbiol. 2017, 57, 285–291. [Google Scholar] [CrossRef] [PubMed]
  93. Joseph, B.; Shrivastava, N.; Ramteke, P.W. Extracellular cold-active lipase of Microbacterium luteolum isolated from Gangotri glacier, western Himalaya: Isolation, partial purification and characterization. J. Genet. Eng. Biotechnol. 2012, 10, 137–144. [Google Scholar] [CrossRef] [Green Version]
  94. Jain, R.; Pandey, A.; Pasupuleti, M.; Pande, V. Prolonged Production and Aggregation Complexity of Cold Active Lipase from Pseudomonas proteolytica (GBPI_Hb61) Isolated from Cold Desert Himalaya. Mol. Biotechnol. 2017, 59, 34–45. [Google Scholar] [CrossRef]
  95. Kavitha, M. Cold active lipases—An update. Front Life Sci. 2016, 9, 226–238. [Google Scholar] [CrossRef] [Green Version]
  96. Giri, A.; Pant, D. CO2 management using carbonic anhydrase producing microbes from western Indian Himalaya. Biores. Technol. Rep. 2019, 8, 100320. [Google Scholar] [CrossRef]
  97. Buzzini, P.; Margesin, R. Cold-Adapted Yeasts: A Lesson from the Cold and a Challenge for the XXI Century. In Cold-adapted Yeasts; Buzzini, P., Margesin, R., Eds.; Springer: Berlin/Heidelberg, Germany, 2014; pp. 3–22. [Google Scholar]
  98. Wang, M.; Tian, J.; Xiang, M.; Liu, X. Living strategy of cold-adapted fungi with the reference to several representative species. Mycology 2017, 8, 178–188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  99. Tribelli, P.M.; Lopez, N.I. Reporting Key Features in Cold-Adapted Bacteria. Life 2018, 13, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  100. Pandey, A.; Yarzabal, L.A. Bioprospecting cold-adapted plant growth promoting microorganisms from mountain environments. Appl. Microbiol. Biotechnol. 2019, 103, 643–657. [Google Scholar] [CrossRef] [PubMed]
  101. Bisht, S.; Pandey, P.; Kaur, G.; Aggarwal, H.; Sood, A.; Sharma, S.; Kumar, V.; Bisht, N.S. Utilization of endophytic strain Bacillus sp. SBER3 for biodegradation of polyaromatic hydrocarbons (PAH) in soil model system. Eur. J. Soil. Biol. 2014, 60, 67–76. [Google Scholar] [CrossRef]
  102. Mahajan, R.; Verma, S.; Kushwaha, M.; Singh, D.; Akhter, Y.; Chatterjee, S. Biodegradation of di-n-butyl phthalate by psychrotolerant Sphingobium yanoikuyae strain P4 and protein structural analysis of carboxylesterase involved in the pathway. Int. J. Biol. Macromol. 2019, 122, 806–816. [Google Scholar] [CrossRef]
  103. Margesin, R. Alpine Microorganisms: Useful Tools for Low-Temperature Bioremediation. J. Microbiol. 2007, 45, 281–285. [Google Scholar]
  104. Margesin, R.; Schinner, F. Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl. Microbiol. Biotechnol. 2001, 56, 650–663. [Google Scholar] [CrossRef]
  105. Yang, G.L.; Hou, S.G.; Le Baoge, R.; Li, Z.G.; Xu, H.; Liu, Y.P.; Du, W.T.; Liu, Y.Q. Differences in bacterial diversity and communities between glacial snow and glacial soil on the Chongce Ice Cap, West Kunlun Mountains. Sci. Rep. 2016, 6, 36548. [Google Scholar] [CrossRef] [Green Version]
  106. Jiménez, D.J.; Montaña, J.S.; Alvarez, D.; Baena, S. A novel cold active esterase derived from Colombian high Andean forest soil metagenome. World J. Microbiol. Biotechnol. 2012, 1, 361–370. [Google Scholar] [CrossRef]
  107. Dhakar, K.; Pandey, A. Laccase Production from a temperature and pH tolerant fungal strain of Trametes hirsuta (MTCC 11397). Enzyme Res. 2013, 2013, 869062. [Google Scholar] [CrossRef] [Green Version]
  108. Jain, R.; Pandey, A. A phenazine-1-carboxylic acid producing polyextremophilic Pseudomonas chlororaphis (MCC2693) strain, isolated from mountain ecosystem, possesses biocontrol and plant growth promotion abilities. Microbiol. Res. 2016, 190, 63–71. [Google Scholar] [CrossRef] [PubMed]
  109. Trivedi, P.; Pandey, P.; Sa, T. Chromate reducing and plant growth promoting activities of psychrotrophic Rhodococcus erythropolis MTCC 7905. J. Basic Microbiol. 2007, 47, 513–517. [Google Scholar] [CrossRef] [PubMed]
  110. Selvakumar, G.; Mohan, M.; Kundu, S.; Gupta, A.D.; Joshi, P.; Nazim, S.; Gupta, H.S. Cold tolerance and plant growth promotion potential of Serratia marcescens strain SRM (MTCC 8708) isolated from flowers of summer squash (Cucurbita pepo). Lett. Appl. Microbiol. 2008, 46, 171–175. [Google Scholar] [CrossRef] [PubMed]
  111. Suyal, D.C.; Shukla, A.; Goel, R. Growth promotory potential of the cold adapted diazotroph Pseudomonas migulae S10724 against native green gram (Vigna radiata (L.) Wilczek). 3 Biotech 2014, 4, 665–668. [Google Scholar] [CrossRef] [Green Version]
  112. Rinu, K.; Malviya, M.K.; Sati, P.; Tiwari, S.C.; Pandey, A. Response of cold-tolerant Aspergillus spp. to solubilization of Fe and Al phosphate in presence of different nutritional sources. ISRN Soil Science 2013, 2013, 598541. [Google Scholar] [CrossRef] [Green Version]
  113. Kumar, A.; Soni, R.; Kanwar, S.S.; Pabbi, S. Stenotrophomonas: A versatile diazotrophic bacteria from the rhizospheric soils of Western Himalayas and development of its liquid biofertilizer formulation. Vegetos 2019, 32, 103–109. [Google Scholar]
  114. Barman, D.; Dkhar, M.S. Plant Growth-Promoting potential of endophytic bacteria isolated from Costus speciosus in tropical deciduous forest of eastern Himalaya. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci. 2019, 89, 841–852. [Google Scholar] [CrossRef]
  115. Adhikari, P.; Pandey, A. Phosphate solubilization potential of endophytic fungi isolated from Taxus wallichiana Zucc. Roots. Rhizosphere 2019, 9, 2–9. [Google Scholar] [CrossRef]
  116. Arora, P.; Wani, Z.A.; Ahmad, T.; Sultan, P.; Gupta, S.; Hassan, S.R.U. Community structure, spatial distribution, diversity and functional characterization of culturable endophytic fungi associated with Glycyrrhiza glabra L. Fungal Biol. 2019, 123, 373–383. [Google Scholar] [CrossRef]
  117. Pandey, A. Are dark septate endophytes bioindicators of climate in mountain ecosystems? Rhizosphere 2019, 9, 110–111. [Google Scholar] [CrossRef]
  118. Pandey, A.; Das, N.; Kumar, B.; Rinu, K.; Trivedi, P. Phosphate solubilization by Penicillium spp. isolated from soil samples of Indian Himalayan region. World J. Microbiol. Biotechnol. 2008, 24, 97–102. [Google Scholar] [CrossRef]
  119. Selvakumar, G.; Joshi, P.; Nazim, S.; Mishra, P.K.; Kundu, S.; Gupta, H.S. Exiguobacterium acetylicum strain 1P (MTCC 8707) a novel bacterial antagonist from the North Western Indian Himalayas. World J. Microbiol. Biotechnol. 2009, 25, 131–137. [Google Scholar] [CrossRef]
  120. Sharma, A.; Pandey, A.; Shouche, Y.S.; Kumar, B.; Kulkarni, G. Research paper characterization and identification of Geobacillus spp. isolated from soldhar hot spring site of Garhwal Himalaya, India. J. Basic Microbiol. 2009, 49, 187–194. [Google Scholar] [CrossRef] [PubMed]
  121. Joshi, P.; Bhatt, A.B. Diversity and function of plant growth promoting rhizobacteria associated with wheat rhizosphere in North Himalayan Region. Int. J. Environ. Sci. 2010, 1, 1135–1143. [Google Scholar]
  122. King, A.J.; Karki, D.; Nagy, L.; Racoviteanu, A.; Schmidt, S.K. Microbial biomass and activity in high elevation (>5100 m) soils from the Annapurna and Sagarmatha regions of the Nepalese Himalayas. Himalayan J. Sci. 2010, 6, 11–18. [Google Scholar] [CrossRef] [Green Version]
  123. Liu, Y.; Yao, T.; Jiao, N.; Tian, L.; Hu, A.; Yu, W.; Li, S. Microbial diversity in the snow, a moraine lake and a stream in Himalayan glacier. Extremophiles 2011, 15, 411–421. [Google Scholar] [CrossRef]
  124. Tayung, K.; Barik, B.P.; Jha, D.K.; Deka, D.C. Identification and characterization of antimicrobial metabolite from an endophytic fungus, Fusarium solani isolated from bark of Himalayan yew. Mycosphere 2011, 2, 203–213. [Google Scholar]
  125. Lyngwi, N.A.; Koijam, K.; Sharma, D.; Joshi, S.R. Cultivable bacterial diversity along the altitudinal zonation and vegetation range of tropical Eastern Himalaya. Rev. Biol. Trop. 2013, 61, 467–490. [Google Scholar] [CrossRef] [Green Version]
  126. Arunkumar, K.; Singh, R.D.; Patra, A.K.; Sahu, S.K. Probing of microbial community structure, dehydrogenase and soil carbon in-relation to different land uses in soils of Ranichauri (Garhwal Himalayas). Int. J. Curr. Microbiol. App. Sci. 2013, 2, 325–338. [Google Scholar]
  127. Bisht, S.C.; Mishra, P.K.; Joshi, G.K. Genetic and functional diversity among root-associated psychrotrophic Pseudomonad’s isolated from the Himalayan plants. Arch. Microbiol. 2013, 195, 605–615. [Google Scholar] [CrossRef]
  128. Kammerlander, B.; Breiner, H.-W.; Filker, S.; Sommaruga, R.; Sonntag, B.; Stoeck, T. High diversity of protistan plankton communities in remote high mountain lakes in the European Alps and the Himalayan mountains. FEMS Microbiol. Ecol. 2015, 91, fiv010. [Google Scholar] [CrossRef] [Green Version]
  129. Capkova, K.; Hauer, T.; Rehakova, K.; Dolezal, J. Some Like it High! Phylogenetic diversity of high-elevation cyanobacterial community from biological soil crusts of western Himalaya. Microb. Ecol. 2016, 71, 113–123. [Google Scholar] [CrossRef] [PubMed]
  130. Soni, R.; Suyal, D.C.; Sai, S.; Goel, R. Exploration of nifH gene through soil metagenomes of the western Indian Himalayas. 3 Biotech 2016, 6, 25. [Google Scholar] [CrossRef] [Green Version]
  131. Azzoni, R.S.; Tagliaferri, I.; Franzetti, A.; Mayer, C.; Lambrecht, A.; Compostella, C. Bacterial diversity in snow from mid-latitude mountain areas: Alps, Eastern Anatolia, Karakoram and Himalaya. Ann. Glaciol. 2018, 59, 10–20. [Google Scholar] [CrossRef] [Green Version]
  132. Bisht, G.; Sourirajan, A.; Baumler, D.J.; Dev, K. 16S rRNA Gene Amplicon Data Set-Based Bacterial Diversity in a Water-Soil Sample from Pangong Tso Lake, a High-Altitude Grassland Lake of the Northwest Himalayas. Microbiol Resour. Announc. 2018, 7, e01192-18. [Google Scholar] [CrossRef] [Green Version]
  133. Kumar, V.; Thakur, V.; Ambika; Kumar, S.; Singh, D. Bioplastic reservoir of diverse bacterial communities revealed along altitude gradient of Pangi-Chamba trans-Himalayan region. FEMS Microbiol. Lett. 2018, 365. [Google Scholar] [CrossRef] [Green Version]
  134. Najar, I.N.; Sherpa, M.T.; Das, S.; Thakur, N. Draft genome sequence of Geobacillus yumthangensis AYN2 sp. nov., a denitrifying and sulfur reducing thermophilic bacterium isolated from the hot springs of Sikkim. Gene Rep. 2018, 10, 162–166. [Google Scholar] [CrossRef]
  135. Yadvinder, S.; Gulati, A.; Singh, D.P.; Khattar, J.I.S. Cyanobacterial community structure in hot water springs of Indian North Western Himalayas: A morphological, molecular and ecological approach. Algal Res. 2018, 29, 179–192. [Google Scholar]
  136. Verma, R.; Bhalla, A.; Kumar, S. Valorization of lignocellulosic residues for cost-effective production of thermo-alkali-stable xylanase by Geobacillus thermodenitrificans X1 of Indian Himalayan hot spring. Waste Bio Valori 2018, 1–11. [Google Scholar] [CrossRef]
  137. Shrivastava, N.; Nandi, I.; Ibeyaima, A.; Gupta, S.; Sarethy, I.P. Microbial diversity of a Himalayan forest and characterization of rare actinomycetes for antimicrobial compounds. 3 Biotech 2019, 9, 27. [Google Scholar] [CrossRef]
Microorganisms 08 00257 g001 550
Figure 1. Geographical distribution of Himalayan ranges (Source: ICIMOD (International Centre for Integrated Mountain Development), Nepal).
Figure 1. Geographical distribution of Himalayan ranges (Source: ICIMOD (International Centre for Integrated Mountain Development), Nepal).
Microorganisms 08 00257 g001
Microorganisms 08 00257 g002 550
Figure 2. To maintain cellular integrity and functionality, cold-loving microbial cells possess some extraordinary features—a: increase in unsaturated fatty acids against desiccation, b: RNA binding proteins (RBP) help to retain the RNA primary structure to support expression, c, d: Accumulation of cryoprotectants and functioning of cold-active enzymes support homeostasis and growth in stressed environments, e: inhibition of ice crystal formation protects the cell from damage at low temperatures.
Figure 2. To maintain cellular integrity and functionality, cold-loving microbial cells possess some extraordinary features—a: increase in unsaturated fatty acids against desiccation, b: RNA binding proteins (RBP) help to retain the RNA primary structure to support expression, c, d: Accumulation of cryoprotectants and functioning of cold-active enzymes support homeostasis and growth in stressed environments, e: inhibition of ice crystal formation protects the cell from damage at low temperatures.
Microorganisms 08 00257 g002
Microorganisms 08 00257 g003 550
Figure 3. Ecological processes regulated by cold-adapted microorganisms in different ecosystems. (a) Biogeochemical cycles in the barren lands of glacial regions (>3500 m asl). (b) Nutrient cycles/energy flow in the high-altitude forests. (c) Agriculture system under the low-temperature regions of mountains (Photo credit: Khashti Dasila).
Figure 3. Ecological processes regulated by cold-adapted microorganisms in different ecosystems. (a) Biogeochemical cycles in the barren lands of glacial regions (>3500 m asl). (b) Nutrient cycles/energy flow in the high-altitude forests. (c) Agriculture system under the low-temperature regions of mountains (Photo credit: Khashti Dasila).
Microorganisms 08 00257 g003
Microorganisms 08 00257 g004 550
Figure 4. Conversion of different forms of carbon through microbial activities under the biodegradation process.
Figure 4. Conversion of different forms of carbon through microbial activities under the biodegradation process.
Microorganisms 08 00257 g004
Table
Table 1. Taxonomic and functional information associated with the microbial communities of Himalayan region.
Table 1. Taxonomic and functional information associated with the microbial communities of Himalayan region.
Serial. No.LocationMicroorganismsReportReferences
1Northwestern Himalaya, IndiaFungiPlant growth promoting activities of Penicillium spp.[118]
2Uttarakhand, IndiaBacteriaAntagonistic activity[119]
3Uttarakhand, IndiaBacteriaThermophiles from hot springs[120]
4Uttarakhand, IndiaBacteriaPlant growth promoting activities[121]
5Kargil, IndiaBacteriaCold-active amylases (culture independent)[90]
6Annapurna and Sagarmatha region, NepalMicrobial communitiesMicrobial biomass and associated ecological processes[122]
7Langtang Valley, NepalBacteriaBacterial diversity of glaciers (culture independent)[123]
8North-Central NepalPhototrophsDiversity of cyanobacteria and Chlorophyceae (culture independent)[57]
9Arunachal Pradesh, IndiaFungiAntimicrobial activity[124]
10Northeast IndiaBacteriaBacterial diversity (culture dependent)[125]
11Uttarakhand, IndiaMicrobial communitiesComparative study of soil microbial communities by PLFA (culture independent)[126]
12Northwestern Himalayas, IndiaBacteriaPlant growth promoting activities of Pseudomonas[127]
13Khumbu Valley, NepalMicro-eukaryotesPlanktonic diversity (culture independent)[128]
14Uttarakhand, IndiaBacteriaPlant growth promoting activities[111]
15Himachal Pradesh, IndiaBacteriaPlant growth promoting activities (culture dependent)[52]
16Ladakh, IndiaBacteriaCyanobacterial communities[129]
17Uttarakhand, IndiaFunctional aspect of bacterial communitiesDistribution of nifH gene through metagenomics[130]
18Ladakh, IndiaMicrobial communitiesMetagenomics based study of Pangong lake water[53]
19Indian Himalaya (Himachal Pradesh and Sikkim)BacteriaPotential of hot spring inhabiting bacteria to produce thermostable enzymes (culture dependent)[72]
20Khumbu Valley, NepalBacteriaBacterial diversity associated to snow (culture independent)[131]
21Uttarakhand, IndiaMicrobial communitiesMicrobial biomass associated to the forests and their relation to ecological processes[76]
22Ladakh, IndiaBacteriaMetagenomics[132]
23Himachal Pradesh, IndiaBacteriaBioplastic-producing bacterial communities (culture independent)[133]
24Sikkim, IndiaBacteriaContribution of thermophiles in nitrogen and sulfur cycle[134]
25Indian HimalayaBacteria and fungi Degradation potential of cryoconites inhabiting microbial communities (culture dependent)[31]
26Himachal Pradesh, IndiaBacterial and Archaeal virusesAbundance of viruses in the Manikaran hot spring through metagenomics[74]
27Sikkim, IndiaBacteriaCulture-dependent diversity[44]
28Northwestern Himalaya, IndiaCyanobacteriaDiversity of cyanobacteria in hot spring (culture dependent)[135]
29Himachal Pradesh, IndiaBacteriaCellulolytic potential[33]
30Himachal Pradesh, IndiaBacteriaPotential to degrade enzymes from bacteria colonizing hot spring[136]
31Himachal Pradesh and Uttarakhand, IndiaBacteriaCO2 mineralization through carbonic anhydrase[96]
32Uttarakhand, IndiaBacteriaPotential of cold-tolerant bacteria in hill agriculture (culture independent)[29]
33Himachal Pradesh, IndiaBacteria and ArchaeaTaxonomic and functional potential of hyperthermophiles through metagenomics[75]
34Sikkim, IndiaBacteriaCulture-independent diversity[30]
35Uttarakhand, IndiaActinomycetesAntimicrobial activity[137]

Share and Cite

MDPI and ACS Style

Dhakar, K.; Pandey, A. Microbial Ecology from the Himalayan Cryosphere Perspective. Microorganisms 2020, 8, 257. https://doi.org/10.3390/microorganisms8020257

AMA Style

Dhakar K, Pandey A. Microbial Ecology from the Himalayan Cryosphere Perspective. Microorganisms. 2020; 8(2):257. https://doi.org/10.3390/microorganisms8020257

Chicago/Turabian Style

Dhakar, Kusum, and Anita Pandey. 2020. "Microbial Ecology from the Himalayan Cryosphere Perspective" Microorganisms 8, no. 2: 257. https://doi.org/10.3390/microorganisms8020257

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop