Abstract
Glacial and kettle lakes in the high-altitude Himalayas are unique habitats with significant scope for microbial ecology. The present study provides insights into bacterial community structure and function of the sediments of two high-altitude lakes using 16S amplicon and whole-genome shotgun (WGS) metagenomics. Microbial communities in the sediments of Parvati kund (glacial lake) and Bhoot ground (kettle lake) majorly consist of bacteria and a small fraction of archaea and eukaryota. The bacterial population has an abundance of phyla Proteobacteria, Bacteroidetes, Acidobacteria, Actinobacteria, Firmicutes, and Verrucomicrobia. Despite the common phyla, the sediments from each lake have a distinct distribution of bacterial and archaeal taxa. The analysis of the WGS metagenomes at the functional level provides a broad picture of microbial community metabolism of key elements and suggested chemotrophs as the major primary producers. In addition, the findings also revealed that polyhydroxyalkanoates (PHA) are a crucial stress adaptation molecule. The abundance of PHA metabolism in Alpha- and Betaproteobacteria and less representation in other bacterial and archaeal classes in both metagenomes was disclosed. The metagenomic insights provided an incisive view of the microbiome from Himalayan lake's sediments. It has also opened the scope for further bioprospection from virgin Himalayan niches.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bolch T, Kulkarni A, Kääb A et al (2012) The state and fate of Himalayan glaciers. Science 336:310–314
Bradley JA, Singarayer JS, Anesio AM (2014) Microbial community dynamics in the forefield of glaciers. Proc R Soc B 281:20140882
Brumfield KD, Huq A, Colwell RR et al (2020) Microbial resolution of whole genome shotgun and 16S amplicon metagenomic sequencing using publicly available NEON data. PLoS ONE 15:e0228899
Dhakar K, Pandey A (2020) Microbial ecology from the Himalayan cryosphere perspective. Microorganisms 8:257
Dutta H, Dutta A (2016) The microbial aspect of climate change. Energ Ecol Environ 1:209–232
Gupta P, Sangwan N, Lal R, Vakhlu J (2015) Bacterial diversity of Drass, cold desert in Western Himalaya, and its comparison with Antarctic and Arctic. Arch Microbiol 197:851–860
Hotaling S, Hood E, Hamilton TL (2017) Microbial ecology of mountain glacier ecosystems: biodiversity, ecological connections and implications of a warming climate. Environ Microbiol 19:2935–2948
Jung MY, Park SJ, Kim SJ et al (2014) A mesophilic, autotrophic, ammonia-oxidizing archaeon of Thaumarchaeal group I. 1a cultivated from a deep oligotrophic soil horizon. Appl Environ Microbiol 80:3645–3655
Kasana RC (2017) Bacterial diversity in cold environments of Indian Himalayas. In: Kalia V, Shouche Y, Purohit H, Rahi P (eds) Mining of Microbial Wealth and MetaGenomics. Springer, Singapore. https://doi.org/10.1007/978-981-10-5708-3_5
Keegan KP, Glass EM, Meyer F (2016) MG-RAST, a Metagenomics service for analysis of microbial community structure and function. Methods Mol Biol 1399:207–333
Khadka N, Zhang G, Thakuri S (2018) Glacial lakes in the Nepal Himalaya: Inventory and decadal dynamics (1977–2017). Remote Sens 10:1913
Koo H, Hakim JA, Fisher PR et al (2016) Distribution of cold adaptation proteins in microbial mats in Lake Joyce, Antarctica: analysis of metagenomic data by using two bioinformatics tools. J Microbiol Methods 120:23–28
Koo H, Hakim JA, Morrow CD et al (2018) Metagenomic analysis of microbial community compositions and cold-responsive stress genes in selected Antarctic lacustrine and soil ecosystems. Life (basel) 8:29
Korzhenkov AA, Toshchakov SV, Bargiela R et al (2019) Archaea dominate the microbial community in an ecosystem with low-to-moderate temperature and extreme acidity. Microbiome 7:11
Kulkarni AV, Karyakarte Y (2014) Observed changes in Himalaya glaciers. Curr Sci 106:237–244
Kumar V, Thakur V, Ambika, et al (2018) Bioplastic reservoir of diverse bacterial communities revealed along altitude gradient of Pangi-Chamba trans-Himalayan region. FEMS Microbiol Lett 365:fny144
Kumar R, Acharya V, Mukhia S et al (2019a) Complete genome sequence of Pseudomonas frederiksbergensis ERDD5:01 revealed genetic bases for survivability at high altitude ecosystem and bioprospection potential. Genomics 111:492–499
Kumar V, Kumar S, Darnal S et al (2019b) Optimized chromogenic dyes-based identification and quantitative evaluation of bacterial l-asparaginase with low/no glutaminase activity bioprospected from pristine niches in Indian trans-Himalaya. 3 Biotech 9:275
Kumar V, Kumar S, Singh D (2020b) Microbial polyhydroxyalkanoates from extreme niches: bioprospection status, opportunities and challenges. Int J Biol Macromol 147:1255–1267
Kumar V, Thakur V, Ambika, et al (2020a) Genomic insights revealed physiological diversity and industrial potential for Glaciimonas sp. PCH181 isolated from Satrundi glacier in Pangi-Chamba Himalaya. Genomics 112:637–646
Kumar V, Darnal S, Kumar S et al (2021) Bioprocess for co-production of polyhydroxybutyrate and violacein using Himalayan bacterium Iodobacter sp PCH194. Bioresour Technol 319:124235
Liao B, Yan X, Zhang J et al (2019) Microbial community composition in alpine lake sediments from the Hengduan Mountains. Microbiol Open 8:e832
Liu Y, Yao T, Jiao N et al (2011) Microbial diversity in the snow, a moraine lake and a stream in Himalayan glacier. Extremophiles 15:411–421
Madsen EL (2011) Microorganisms and their roles in fundamental biogeochemical cycles. Curr Opin Biotechnol 22:456–464
Mahato NK, Sharma A, Singh Y, Lal R (2019) Comparative metagenomic analyses of a high-altitude Himalayan geothermal spring revealed temperature-constrained habitat-specific microbial community and metabolic dynamics. Arch Microbiol 201:377–388
Margesin R, Collins T (2019) Microbial ecology of the cryosphere (glacial and permafrost habitats): current knowledge. Appl Microbiol Biotechnol 103:2537–2549
Maurer M, Schaefer JM, Rupper S, Corley A (2019) Acceleration of ice loss across the Himalayas over the past 40 years. Sci Adv 5:eaav7266
Meyer F, Paarmann D, D’Souza M et al (2008) The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9:386
Obruca S, Sedlacek P, Koller M et al (2018) Involvement of polyhydroxyalkanoates in stress resistance of microbial cells: biotechnological consequences and applications. Biotechnol Adv 36:856–870
Pradhan S, Srinivas TNR, Pindi PK et al (2010) Bacterial biodiversity from roopkund glacier, himalayan mountain ranges, India. Extremophiles 14:377–395
Rampelotto PH (2013) Extremophiles and extreme environments. Life (basel) 3:482–485
Reverey F, Grossart HP, Premke K, Lischeid G (2016) Carbon and nutrient cycling in kettle hole sediments depending on hydrological dynamics: a review. Hydrobiologia 775:1–20
Reverey F, Ganzert L, Lischeid G et al (2018) Dry-wet cycles of kettle hole sediments leave a microbial and biogeochemical legacy. Sci Total Environ 627:985–996
Roy C, Rameez MJ, Haldar PK et al (2020) Microbiome and ecology of a hot spring-microbialite system on the Trans-Himalayan plateau. Sci Rep 10:5917
Ruuskanen MO, St Pierre KA, St Louis VL et al (2018) Physicochemical drivers of microbial community structure in sediments of lake Hazen, Nunavut. Canada. Front Microbiol 9:1138
Santoro AL, Bastviken D, Gudasz C et al (2013) Dark carbon fixation: an important process in lake sediments. PLoS ONE 8:e65813
Santoro AL, Enrich-Prast A, Bastviken D et al (2021) Spatial and vertical distribution of aerobic and anaerobic dark inorganic carbon fixation in coastal tropical lake sediments. Aquat Sci 83:43
Sharma N, Kumar J, Abedin MM et al (2020) Metagenomics revealing molecular profiling of community structure and metabolic pathways in natural hot springs of the Sikkim Himalaya. BMC Microbiol 20:246
Shivaji S, Pratibha MS, Sailaja B et al (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 15:1–22
Srinivas TN, Singh SM, Pradhan S et al (2011) 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 15:673–690
Sruamsiri D, Thayanukul P, Suwannasilp BB (2020) In situ identification of polyhydroxyalkanoate (PHA)-accumulating microorganisms in mixed microbial cultures under feast/famine conditions. Sci Rep 10:3752
Stres B, Sul WJ, Murovec B, Tiedje JM (2014) Recently deglaciated high-altitude soils of the Himalaya: Diverse environments, heterogenous bacterial communities and long-range dust inputs from the upper troposphere. PLoS ONE 8:e76440
Thakur V, Kumar V, Kumar S, Singh D (2018) Diverse culturable bacterial communities with cellulolytic potential revealed from pristine habitat in Indian trans-Himalaya. Can J Microbiol 28:1–11
Varin T, Lovejoy C, Jungblut AD et al (2012) Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the high Arctic. Appl Environ Microbiol 78:549–559
Vasquez-Cardenas D, Meysman FJR, Boschker HTS (2020) A cross-system comparison of dark carbon fixation in coastal sediments. Global Biogeochem Cyc 34:e2019GB006298
Venkatachalam S, Gowdaman V, Prabagaran SR (2015) Culturable and culture-independent bacterial diversity and the prevalence of cold-adapted enzymes from the Himalayan mountain ranges of India and Nepal. Microb Ecol 69:472–491
Zhang W, Bahadur A, Sajjad W et al (2021) Bacterial diversity and community composition distribution in cold-desert habitats of Qinghai-Tibet plateau, China. Microorganisms 9:262
Acknowledgements
DS acknowledges the Council of Scientific and Industrial Research (CSIR), Govt. of India for funds under Niche Creating Project (NCP) number MLP0143. The authors are thankful to the Director, CSIR-Institute of Himalayan Bioresource Technology (CSIR-IHBT), for providing the necessary facilities to carry out the work. Authors duly acknowledge the Next Generation Genomic Facility, Biox Centre, IIT, Mandi, Himachal Pradesh, India, for providing the facility for illumina MiSeq sequencing. Special thanks to Dr. Tulika P. Shrivastava and her lab for their kind help and coordination during Illumina sequencing run. Technical assistance by Mr. Mohit Sawarnkar for library preparation is also duly acknowledged. SK acknowledges Indian Council of Medical Research (ICMR), New Delhi, India, for providing a Research Fellowship. The manuscript represents CSIR-IHBT publication number 4875.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Communicated by A. Oren.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kumar, V., Kumar, S. & Singh, D. Metagenomic insights into Himalayan glacial and kettle lake sediments revealed microbial community structure, function, and stress adaptation strategies. Extremophiles 26, 3 (2022). https://doi.org/10.1007/s00792-021-01252-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00792-021-01252-x