Abstract
Microbial communities at cryosphere are the cosmopolitan buffers of important biogeochemical processes stationed at extreme archaic and frigid conditions. In the present study microbial diversity analysis from accumulation zone of two glaciers of North Sikkim, India has been carried by two culture independent methods. The phospholipid fatty acids analysis of Changme Khang and Changme Khangpu glacier showed that both of these were dominated by Gram-positive bacteria followed by Gram-negative bacteria. Among the two glaciers, Changme Khang (54.04%) had higher percentage of Gram-positive bacteria than Changme Khangpu (24.84%), while Gram-negative bacteria were higher in Changme Khangpu (22.65%) than Changme Khang (4.41%). The metagenomic analysis shows the dominance of Proteobacteria followed by Firmicutes and Actinobacteria. Betaproteobacteria were the dominant class among Proteobacteria. Similar kind of bacterial diversity was also observed from other polar and non-polar glaciers.
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Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(2):403–410
Auman AJ, Breezee JL, Gosink JJ, Kampfer P, Staley JT (2006) Psychromonas ingrahamii sp. nov., a novel gas vacuolate, psychrophilic bacterium isolated from Arctic polar sea ice. Int J Syst Evol Microbiol 56:1001–1007
Bahuguna IM, Kulkarni AV, Arrawatia ML et al. (2001) Glacier Atlas of Tista Basin (Sikkim Himalaya), SAC/RESA/MWRG-GLI/SN/16/2001
Bajracharya SR, Shrestha B (2011) The status of glaciers in the Hindu Kush-Himalayan region. ICIMOD, Kathmandu
Bajracharya SR, Mool PK, Shrestha BR (2007) Impact of climate change on Himalayan Glaciers and glacial Lakes: case studies on GLOFs and associated hazards in Nepal and Bhutan. ICIMOD, Kathmandu
Bhutiyani MR, Kale VS, Pawar NJ (2008) Changing streamflow patterns in the rivers of northwestern Himalaya: implications of global warming in the 20th century. Curr Sci 95(5):618–626
Byers A (2012) Committee on Himalayan Glaciers, hydrology, climate change, and implications for water security. The National Academies Press, Washington, pp 78–103
Cameron KA, Hodson AJ, Osborn AM (2012) Structure and diversity of bacterial, eukaryotic and archaeal communities in glacial cryoconite holes from the Arctic and the Antarctic. FEMS Microbial Ecol 82:254–267
Cavicchioli R, Siddiqui KS, Andrews D, Sowers KR (2002) Low-temperature extremophiles and their applications. Curr Opin Biotechnol 13:253-161
Cheng SM, Foght JM (2007) Cultivation-independent and dependent characterization of bacteria resident beneath John Evans Glacier. FEMS Microbial Ecol 59:318–330
Choudhari S (2015) Insights into glacial metagenome and sequence biases in comparative metagenomics. Rutgers, The State University of New Jersey. PhD Thesis
Choudhari S, Lohia R, Grigoriev A (2014) Comparative metagenome analysis of an Alaskan glacier. J Bioinf Comput Biol 12(2):1441003
Committee on Himalayan glacier and hydrology (CHGH) Report (2012) Himalayan glaciers: climate change, water resources, and water security. The National Academies Press, Washington, DC
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173
Edwards A (2015) Coming in from the cold: potential microbial threats from the terrestrial cryosphere. Front Earth Sci 3:12. https://doi.org/10.3389/feart.2015.00012
Edwards A, Pachebat JA, Swain M, Hegarty M, Hodson AJ, Irvine-Fynn TDL, Rasser SME, Sattler B (2013) A metagenomic snapshot of taxonomic and functional diversity in an alpine glacier cryoconite ecosystem. Environ Res Lett 8:035003
Ewa P, Bosnak CP (2012) The Analysis of Drinking Waters by U.S. EPA Method 200.8 Using the NexION 300D/350D ICP-MS in Standard, Collision and Reaction Modes. PerkinElmer, Inc. 940 Winter Street Waltham, MA 02451 USA, 1–9
Fan F, Zhang B, Morrill PL (2017) Phospholipid fatty acid (PLFA) analysis for profiling microbial communities in offshore produced water. Mar Pollut Bull 122(1–2):194–206
Foght J, Aislabie J, Turner S, Brown CE, Ryburn J, Saul DJ, Lawson W (2004) Culturable bacteria in subglacial sediments and ice from two southern hemisphere glaciers. Microb Ecol 47:329–340
Franzetti A, Navarra F, Tagliaferri I, Gandolfi I, Bestetti G, Minora U, Azzoni RS, Diolaiuti G, Smiraglia C, Ambrosini R (2017) Potential sources of bacteria colonizing the cryoconite of an alpine glacier. PLoS One 12(3):e0174786
Garcia-Lopez E, Cid C (2017) Glaciers and ice sheets as analog environments of potentially habitable icy worlds. Front Microbiol 8:1407
Griffiths GW (2012) Do we need a global strategy for microbial conservation? Trends Ecol Evol 27(1):1–2
Grzesiak J, Zdanowski MK, Górniak D, Swiatecki A, Piekarczyk TA, Szatraj K, Kurowska JS, Nieckarz M (2015) Microbial community changes along the ecology glacier ablation zone (King George Island, Antarctica). Polar Biol 38(12):2069–2083
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinf Oxford Engl 29(2):1072–1075
Hagen SB, Ims RA, Yoccoz NG (2003) Density dependent melanism in sub-arctic populations of winter moth larvae (Operophtera brumata). Ecol Entomol 28:659–665
Hell K, Edwards A, Zarsky J, Podmirseg SM, Girdwood S, Pachebat JA, Insam H, Sattler B (2013) The dynamic bacterial communities of a melting High Arctic glacier snowpack. ISME J 7:1814–1826
Himanshu Swarnkar MK, Singh D, Kumar R (2016) First complete genome sequence of a species in the genus Microterricola, an extremophilic cold active enzyme producing bacterial strain ERGS5:02 isolated from Sikkim Himalaya. J Biotechnol 222:17–18
Huston AL, Krieger-Brockett BB, Deming JW (2000) Remarkably low temperature optima for extracellular enzyme activity from Arctic bacteria and sea ice. Environ Microbiol 2:383–388
Jianchu X, Eriksson M, Vaidya R, Shrestha A, Hewitt K (2007) The melting Himalayas: regional challenges and local impacts of climate change on mountain ecosystem and livelihoods. ICIMOD Technical paper, Kathmandu, pp 1–14
Junge K, Christner B, Staley J (2011) Diversity of psychrophilic bacteria from sea ice and glacial ice communities. Extrem Handbook 11(2):793–815 (Springer)
Kayani MR, Doyle SM, Sangwan N, Wang G, Gilbert JA, Christner BC, Zhu TF (2018) Metagenomic analysis of basal ice from an Alaskan glacier. Microbiome Announc 6(1):123. https://doi.org/10.1186/s40168-018-0505-5
Kumar R, Singh D, Swarnkar MK, Singh AK, Kumar S (2015a) Genome assembly of Chryseobacterium polytrichastri ERMR1:04, a psychrotolerant bacterium with cold active proteases, isolated from east Rathong glacier in India. Genome Announc 3(6):e01305–e01315
Kumar R, Singh D, Swarnkar MK, Singh AK, Kumar S (2015b) Complete genome sequence of Arthrobacter sp. ERGS1:01, a putative novel bacterium with prospective cold active industrial enzymes, isolated from east Rathong glacier in India. J Biotechnol 214:139–140
Kumar R, Singh D, Swarnkar MK, Singh AK, Kumar S (2016) Complete genome sequence of Arthrobacter alpinus ERGS4:06, a yellow pigmented bacterium tolerant to cold and radiations isolated from Sikkim Himalaya. J Biotechnol 220:86–87
Lanekoff I, Karlsson R (2010) Analysis of intact ladderane phospholipids, originating from viable anammox bacteria, using RP-LC-ESI-MS. Anal Bioanal Chem 397(8):3543–3551
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie2. Nat Methods 9(2):357–359
Liu J, Zhang Z, Liu Z, Zhu H, Dang H, Lu J, Cui Z (2011) Production of cold adapted amylase by marine bacterium Wangia sp. C52: optimization, modeling, and partial characterization. Mar Biotechnol 13(5):837–844
Margesin R, Neuner G, Storey KB (2007) Cold-loving microbes, plants, and animals-fundamental and applied aspects. Naturwissenschaften 94(2):77–99
Mc Cammon SA, Bowman JP (2000) Antarctic Flavobacterium species: description of Flavobacterium gillisiae sp. nov., Flavobacterium tegetincola sp. nov. and Flavobacterium xanthum sp. nov., nom. rev. and reclassification of (Flavobacterium) salegens as Salegentibacter salegens gen. nov., comb. nov. Int J Syst Evolut Microbiol 3(3):1055–1063
Miteva VI, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microbiol 70(1):202–213
Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144–167
Mosier AC, Murray AE, Fritsen C (2007) Microbiota within the perennial ice cover of Lake Vida, Antarctica. FEMS Microbiol Ecol 59(2):274–288
Munoz PA, Marquez SL, Nilo FDG, Miranda VM, Blamey JM (2017) Structure and application of antifreeze proteins from Antarctic bacteria. Microb Cell Fact 16:1–13
Najar IN, Sherpa MT, Das S, Das S, Thakur N (2018) Microbial ecology of two hot springs of Sikkim: predominate population and geochemistry. Sci Total Environ 637–638:730–745
Nowak A, Hodson A (2014) Changes in meltwater chemistry over a 20-year period following a termal regime switch from polythermal to cold-based glaciation at Austre Broggerbreen, Svalbard. Polar Res 33:22779
Nurk S, Meleshko D, Korobeynikov A, Pevzner PA (2017) metaSPAdes: a new versatile metagenomic assembler. Genome Res 27(5):824–834
Piper AM (1944) A graphical procedure in the geochemical interpretation of water analysis. Trans Am Geophys Union 25:914–923
Powl AM, East JM, Lee AG (2007) Different effects of lipid chain length on the two sides of a membrane and the lipid annulus of MscL. Biophys J 93:113–122
Priscu JC, Christner BC (2004) Earth’s icy biosphere. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM Press, Washington, DC, pp 130–145. https://doi.org/10.1128/9781555817770.ch13
Quideau SA, McIntosh ACS, Norris CE, Lloret E, Swallow MJB, Hannam K (2016) Extraction and analysis of microbial phospholipid fatty acids in soils. J Vis Exp 114:e54360
Ramana KV, Singh L, Dhaked RK (2002) Biotechnological application of psychrophiles and their habitat to low temperature. J Sci Ind Res 59(2):87–101
Rogers SO, Starmer WT, Castello JD (2004) Recycling of pathogenic microbes through survival in ice. Med Hypotheses 63:773–777
Rondon J, Gomez W, Ball MM (2016) Diversity of culturable bacteria recovered from Pico Bolívar’s glacial and subglacial environments, at 4,950 m, in Venezuelan tropical andes. Can J Microbiol 62(11):1–14
Schutte U, Abdo Z, Foster J, Ravel J, Bunge J, Solheim B, Forney LJ (2010) Bacterial diversity in a glacier foreland of the high Arctic. Mol Ecol 19(1):55–66
Segawa T, Miyamoto K, Ushida K, Agata K, Okada N, Kohshima S (2005) Seasonal change in bacterial flora and biomass in mountain snow from the Tateyama Mountains, Japan, analyzed by 16S rRNA gene sequencing and real-time PCR. Appl Environ Microbiol 71(1):123–130
Segawa T, Ushida K, Narita H, Kanda H, Kohshima S (2010) Bacterial communities in two Antarctic ice cores analyzed by 16S rRNA gene sequencing analysis. Polar Sci 4:215–227
Shen L, Yao T, Xu B, Wang H, Jiao N, Kang S, Liu X, Liu Y (2012) Variation of culturable bacteria along depth in the East Rongbuk ice core, Mt. Everest. Geosci Front 3:327–334
Sherpa MT, Najar IN, Das S, Thakur N (2018a) Bacterial diversity in an alpine debris-free and debris-cover accumulation zone Glacier Ice, North Sikkim, India. Indian J Microbiol 58(4):470–478
Sherpa MT, Najar IN, Das S, Thakur N (2018b) Diversity of bacillus species from chumbu glacier. Res J Life Sci, Bioinf, Pharm Chem Sci 4(3):164–174
Sherpa MT, Najar IN, Das S, Thakur N (2019) The diversity of Pseudomonas species from the accumulation Zone of Kanchengayao Glacier, North Sikkim, India. J Pure Appl Microbiol 13(1):339–348
Shivaji S, Pratibha MS, Sailaja B, Hara Kishore K, Singh AK, Begum Z, Anarasi U, Prabagaran SR, Reddy GS, Srinivas TN (2011) Bacterial diversity of soil in the vicinity of Pindari glacier, Himalayan mountain ranges, India, using culturable bacteria and soil 16S rRNA gene clones. Extremophiles 15(1):1–22
Singh P, Bengtsson L (2004) Hydrological sensitivity of a large Himalayan basin to climate change. Hydrol Process 18(13):2363–2385
Singh P, Hanada Y, Singh SM, Tsuda S (2014) Antifreeze protein activity in Arctic cryoconite bacteria. FEMS Microbiol Lett 351(1):14–22
Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G, Pasolli E, Tett A, Huttenhower C, Segata N (2015) MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods 12(2):902–903
Turchetti B, Buzzini JP, Goretti M, Branda E, Diolaiuti G, Agata CD, Smiraglia C, Martini AV (2008) Psychrophilic yeasts in glacial environments of Alpine glaciers. FEMS Microbial Ecol 63(1):73–83
Ueda M, Goto T, Nakazawa M, Miyatake K, Sakaguchi M, Inouye K (2010) A novel cold-adapted cellulase complex from Eisenia foetida: characterization of a multienzyme complex with carboxymethyl cellulase, beta-glucosidase, beta-1,3 glucanase, and beta-xylosidase. Comp Biochem Physiol Part B: Biochem Mol Biol 157(1):26–32
Willerslev E, Hansen AJ, Poinar HN (2004) Isolation of nucleic acids and cultures from fossil ice and permafrost. Trends Ecol Evol 19(3):141–147
Wu X, Zhang W, Liu G, Yang X, Hu P, Chen T, Zhang G, Li Z (2012) Bacterial diversity in the foreland of the Tianshan No. 1 glacier, China. Environ Res Lett 7:014038
Yao T, Xiang S, Zhang X, Wang N, Wang Y (2006) Microorganisms in the Malan ice core and their relation to climatic and environmental changes. Global Biogeochem Cycles 20:GB1004. https://doi.org/10.1029/2004gb002424
Yoon JH, Kang SS, Lee KC, Lee ES, Kho YH, Kang KH, Park YH (2001) Planomicrobium koreense gen. nov., sp. nov., a bacterium isolated from the Korean traditional fermented seafood jeotgal, and transfer of Planococcus okeanokoites (Nakagawa et al. 1996) and Planococcus mcmeekinii (Junge et al. 1998) to the genus Planomicrobium. Int J Syst Evolut Microbiol 51:1511–1520
Zdanowski MK, Bogdanowicz A, Gawor J, Gromadka R, Wolicka D, Grzesiak J (2017) Enrichment of cryoconite hole anaerobes: implications for the subglacial microbiome. Microb Ecol 73:532–538
Zhang S, Hou S, Ma X, Qin D, Chen T (2007) Culturable bacteria in Himalayan glacial ice in response to atmospheric circulation. Biogeoscience 4:1–9
Zhang SH, Hou SG, Yang GL, Wang JH (2010) Bacterial community in the East Rongbuk Glacier, Mt. Qomolangma (Everest) by culture and culture-independent methods. Microbiol Res 165(4):336–345
Zhang S, Hou S, Qin X, Du W (2015) Preliminary study on effects of glacial retreat on the dominant glacial snow bacteria in Laohugou glacier No. 12. Geomicrobiology 32(2):113–118
Zhang B, Wu X, Zhang G, Li S, Zhang W, Chen X, Sun L, Zhang B, Liu G, Chen T (2016) The diversity and biogeography of the communities of Actinobacteria in the forelands of glaciers at a continental scale. Environ Res Lett 11(11):054012
Acnowledgement
This study has been funded by the Department of Science and Technology, Govt. of India (IUCCC) and Department of Biotechnology (BT/20/NE/2011). We are grateful to Forest Department, Govt. of Sikkim for providing research permit and access to the sampling sites. Authors are thankful to Dr. Uttam Lal, Dr. Rakesh Ranjan and Dr. Smriti Basnet for their support during the field study. The authors would like to thank Department of Microbiology for all the laboratory facilities.
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MTS performed sample collection, did the field study, experimental works, analysis and prepared the manuscript, NT designed the study, reviewed and edited manuscript, INN and SD helped in some experimental work.
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Sherpa, M.T., Najar, I.N., Das, S. et al. Culture independent bacterial diversity of Changme Khang and Changme Khangpu glaciers of North Sikkim, India. Environmental Sustainability 2, 241–253 (2019). https://doi.org/10.1007/s42398-019-00067-z
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DOI: https://doi.org/10.1007/s42398-019-00067-z