Abstract
The Western Himalayas offer diverse environments for investigating the diversity and distribution of microbial communities and their response to both the abiotic and biotic factors across the entire altitudinal gradient. Such investigations contribute significantly to our understanding of the complex ecological processes that shape microbial diversity. The proposed study focuses on the investigation of the bacterial and fungal communities in the forest and alpine grasslands of the Western Himalayan region, as well as their relationship with the physicochemical parameters of soil. A total of 185 isolates were obtained using the culture-based technique belonging to Bacillus (37%), Micrococcus (16%), and Staphylococcus (7%). Targeted metagenomics revealed the abundance of bacterial phyla Pseudomonadota (23%) followed by Acidobacteriota (20.2%), Chloroflexota (15%), and Bacillota (11.3%). At the genera level, CandidatusUdaeobacter (6%), Subgroup_2 (5.5%) of phylum Acidobacteriota, and uncultured Ktedonobacterales HSB_OF53-F07 (5.2%) of Choloroflexota phylum were found to be preponderant. Mycobiome predominantly comprised of phyla Ascomycota (54.1%), Basidiomycota (24%), and Mortierellomycota (19.1%) with Archaeorhizomyces (19.1%), Mortierella (19.1%), and Russula (5.4%) being the most abundant genera. Spearman’s correlation revealed that the bacterial community was most influenced by total nitrogen in the soil followed by soil organic carbon as compared to other soil physicochemical factors. The study establishes a fundamental relationship between microbial communities and the physicochemical properties of soil. Furthermore, the study provides valuable insights into the complex interplay between biotic and abiotic factors that influence the microbial community composition of this unique region across various elevations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The sequences obtained from the high throughput sequencing effort were submitted to the NCBI database using the Sequence Read Archive (SRA) submission with the project number PRJNA931940.
References
Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285. https://doi.org/10.1111/j.1469-8137.2009.03160.x
Adhikari P, Jain R, Sharma A, Pandey A (2021) Plant growth promotion at low temperature by phosphate-solubilizing Pseudomonas spp. Isolated from high-altitude Himalayan soil. Microb Ecol 82(3):677–687. https://doi.org/10.1007/s00248-021-01702-1
Baldrian P (2017) Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol Rev 41(2):109–130. https://doi.org/10.1093/femsre/fuw040
Bhattacharya P, Mondol S, Talukdar G, Rawat GS (2020) Soil bacterial community diversity and composition vary more with elevation than seasons in alpine habitats of Western Himalaya. bioRxiv 2020:2020-11. https://doi.org/10.1101/2020.11.05.370114
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37(8):852–857. https://doi.org/10.1038/s41587-019-0209-9
Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008) Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci 105(supplement_1):11505–11511. https://doi.org/10.1073/pnas.0801920105
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13(7):581–583. https://doi.org/10.1038/nmeth.3869
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108(supplement_1):4516–4522. https://doi.org/10.1073/pnas.1000080107
Chopra VL (2018) Climate change and its ecological implications for the Western Himalaya. Scientific publishers, p 289
Dar GH, Sofi S, Padder SA, Kabli A (2018) Molecular characterization of rhizobacteria isolated from walnut (Juglans regia) rhizosphere in Western Himalayas and assessment of their plant growth promoting activities. Biodiversitas J Biol Divers 19(2):662–669. https://doi.org/10.13057/biodiv/d190245
Devi SP, Jani K, Sharma A, Jha DK (2022) Bacterial communities and their bioremediation capabilities in oil-contaminated agricultural soils. Environ Monit Assess 194:1–3. https://doi.org/10.1007/s10661-021-09669-9
Dhakar K, Pandey A (2020) Microbial ecology from the Himalayan cryosphere perspective. Microorganisms 8(2):1–17. https://doi.org/10.3390/microorganisms8020257
Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MG (2020) PICRUSt2 for prediction of metagenome functions. NatBiotechnol 38(6):685–688. https://doi.org/10.1038/s41587-020-0548-6
Egidi E, Delgado-Baquerizo M, Plett JM, Wang J, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK (2019) A few Ascomycota taxa dominate soil fungal communities worldwide. Nat Commun 10(1):2369. https://doi.org/10.1038/s41467-019-10373-z
Ewels P, Magnusson M, Lundin S, Kaller M (2016) MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinform 32(19):3047–3048. https://doi.org/10.1093/bioinformatics/btw354
Jaggi V, Brindhaa NT, Sahgal M (2020) Microbial diversity in north western Himalayan agroecosystems: functions and applications. In: Microbiological Advancements for Higher Altitude Agro-Ecosystems & Sustainability, pp 135–161. https://doi.org/10.1007/978-981-15-1902-4_8
Jani K, Mahajan A, Kajale S, Ashar A, Sharma A (2022) Soil bacterial community structure, metabolic adaptations and their functional interactions to abiotic factors in Antarctica. Pol Polar Res:21–36. https://doi.org/10.24425/ppr.2021.138588
Kajale S, Deshpande N, Shouche Y, Sharma A (2020) Cultivation of diverse microorganisms from hypersaline lake and impact of delay in sample processing on cell viability. Curr Microbiol 77(5):716–721. https://doi.org/10.1007/s00284-019-01857-8
Kotas P, Santruckova H, Elster J, Kastovska E (2018) Soil microbial biomass, activity and community composition along altitudinal gradients in the High Arctic (Billefjorden, Svalbard). Biogeosciences 15(6):1879–1894. https://doi.org/10.5194/bg-15-1879-2018
Looby CI, Martin PH (2020) Diversity and function of soil microbes on montane gradients: the state of knowledge in a changing world. FEMS Microbiol Ecol 96(9):fiaa122. https://doi.org/10.1093/femsec/fiaa122
Nilsson RH, Larsson KH, Taylor AF, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47(D1):D259–D264. https://doi.org/10.1093/nar/gky1022
Nottingham AT, Turner BL, Whitaker J, Ostle NJ, McNamara NP, Bardgett RD, Salinas N, Meir P (2015) Soil microbial nutrient constraints along a tropical forest elevation gradient: a belowground test of a biogeochemical paradigm. Biogeosciences 12(20):6071–6083. https://doi.org/10.5194/bg-12-6071-2015
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Oksanen MJ (2013) Package ‘vegan’. Community Ecol Package Version 2(9):1–295
Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate (No. 939). US Department of Agriculture
Pandey A, Jain R, Sharma A, Dhakar K, Kaira GS, Rahi P, Dhyani A, Pandey N, Adhikari P, Shouche YS (2019) 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 1:1–12. https://doi.org/10.1007/s42452-019-0273-2
Pandey N, Jain R, Dhakar K, Sharma A, Pandey A (2023) A reduction in temperature induces bioactive red pigment production in a psychrotolerant Penicillium sp. GEU_37 isolated from Himalayan soil. Fungal Biol 127(3):927–937. https://doi.org/10.1016/j.funbio.2023.01.008
Parkinson JA, Allen SE (1975) A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6(1):1–11. https://doi.org/10.1080/00103627509366539
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596. https://doi.org/10.1093/nar/gks1219
Rana KL, Kour D, Kaur T, Devi R, Yadav A, Yadav AN (2021) Bioprospecting of endophytic bacteria from the Indian Himalayas and their role in plant growth promotion of maize (Zea mays L.). JAppl Biol Biotechnol 9(3):41–50. https://doi.org/10.7324/JABB.2021.9306
Rognes T, Flouri T, Nichols B, Quince C, Mahe F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
Sharma A, Jani K, Shouche YS, Pandey A (2015) Microbial diversity of the Soldhar hot spring, India, assessed by analyzing 16S rRNA and protein-coding genes. AnnMicrobiol 65:1323–1332. https://doi.org/10.1007/s13213-014-0970-4
Sharma A, Pandey A, Shouche YS, Kumar B, Kulkarni G (2009) Characterization and identification of Geobacillus spp. isolated from Soldhar hot spring site of Garhwal Himalaya, India. J Basic Microbiol 49(2):187–194. https://doi.org/10.1002/jobm.200800194
Sharma UC, Datta M, Sharma V (2022) Soils in the Hindu Kush Himalayas: management for agricultural land use. Springer, pp 117–144. https://doi.org/10.1007/978-3-031-11458-8_6
Shen C, Xiong J, Zhang H, Feng Y, Lin X, Li X, Liang W, Chu H (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211. https://doi.org/10.1016/j.soilbio.2012.07.013
Siles JA, Margesin R (2016) Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: what are the driving factors? Microb Ecol 72:207–220
Srinivas TN, Singh SM, Pradhan S, Pratibha MS, Kishore KH, Singh AK, Begum Z, Prabagaran SR, Reddy GS, Shivaji S (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. https://doi.org/10.1007/s00792-011-0398-8
Suyal DC, Joshi D, Kumar S, Bhatt P, Narayan A, Giri K, Singh M, Soni R, Kumar R, Yadav A, Devi R (2022) Himalayan microbiomes for agro-environmental sustainability: current perspectives and future challenges. MicrobEcol 13:1–33. https://doi.org/10.1007/s00248-021-01849-x
Tonjer LR, Thoen E, Morgado L, Botnen S, Mundra S, Nybakken L, Bryn A, Kauserud H (2021) Fungal community dynamics across a forest-alpine ecotone. Mol Ecol 30(19):4926–4938. https://doi.org/10.1111/mec.16095
Walkeley A (1947) A critical examination of a rapid method for determination of organic carbon in soils: effect of variation in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–257
Wang Y, Osman JR, DuBow MS (2020) Bacterial communities on the surface of the mineral sandy soil from the Desert of Maine (USA). CurrMicrobiol 77:1429–1437. https://doi.org/10.1007/s00284-020-01946-z
Whitaker J, Ostle N, Nottingham AT, Ccahuana A, Salinas N, Bardgett RD, Meir P, McNamara NP (2014) Microbial community composition explains soil respiration responses to changing carbon inputs along an Andes-to-Amazon elevation gradient. JEcol 102(4):1058–1071. https://doi.org/10.1111/1365-2745.12247
White TJ, Bruns T, Lee SJ, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenies. In: PCR Protocols: a Guide to Methods and Applications (eds MA Innis, DH Gelfand, JJ Sninsky, TJ White)18(1):315– 322. Academic Press, San Diego, California
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York ([Internet], Available from: https://ggplot2.tidyverse.org). Accessed 15 Apr 2023
Wu H, Gu Q, Xie Y, Lou Z, Xue P, Fang L, Yu C, Jia D, Huang G, Zhu B, Schneider A (2019) Cold-adapted Bacilli isolated from the Qinghai–Tibetan Plateau are able to promote plant growth in extreme environments. EnvironMicrobiol 21(9):3505–3526. https://doi.org/10.1111/1462-2920.14722
Yadav AN (2021) Beneficial plant-microbe interactions for agricultural sustainability. J Appl Biol Biotechnol 9(1):i–iv. https://doi.org/10.7324/JABB.2021.91ed
Yadav AN, Sachan SG, Verma P, Kaushik R, Saxena AK (2016) Cold active hydrolytic enzymes production by psychrotrophic Bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. J Basic Microbiol 56(3):294–307. https://doi.org/10.1002/jobm.201500230
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67(5):1613. https://doi.org/10.1099/ijsem.0.001755
Zhou Y, Clark M, Su J, Xiao C (2015) Litter decomposition and soil microbial community composition in three Korean pine (Pinus koraiensis) forests along an altitudinal gradient. Plant Soil 386:171–183. https://doi.org/10.1007/s11104-014-2254-y
Acknowledgements
We are thankful to Namrata Jiya and Mrunal Karande for managing sample transportation.
Funding
This work was supported by the Department of Biotechnology (DBT), Government of India (by Grant No. BT/Coord.II/01/03/2016), under the project Establishment of Centre for Excellence, National Centre for Microbial Resource (NCMR).
Author information
Authors and Affiliations
Contributions
AR: MS writing, data analysis. CV: isolation and identification of isolates. JMR, BSR, and SP: sample collection, soil analysis, MS writing. MJ: community DNA extraction and sequencing. CR: MS writing and data validation. KDP: sequence analysis of bacterial isolates and MS writing. AS: conceptualization, project administration, funding acquisition, supervision, MS writing.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
All authors approved the manuscript.
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 2023 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Rambia, A., Veluchamy, C., Rawat, J.M. et al. Revealing bacterial and fungal communities of the untapped forest and alpine grassland zones of the Western-Himalayan region. Int Microbiol (2023). https://doi.org/10.1007/s10123-023-00430-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10123-023-00430-5