Skip to main content

Advertisement

SpringerLink
Log in

Shifts in Bacterial Community Composition and Functional Traits at Different Time Periods Post-deglaciation of Gangotri Glacier, Himalaya

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Climate change causes an unprecedented increase in glacial retreats. The melting ice exposes land for colonization and diversification of bacterial communities leading to soil development, changes in plant community composition, and ecosystem functioning. Although a few studies have focused on macro-level deglaciation impacts, little is known about such effects on the bacterial community succession. Here, we provide meta-barcoding-based insight into the ecological attributes of bacterial community across different retreating periods of the Gangotri glacier, western Himalaya. We selected three sites along a terminal moraine representing recent (~ 20 yrs), intermediate (~ 100 yrs), and late (~ 300 yrs) deglaciation periods. Results showed that the genus Mycobacterium belonging to phylum Actinobacteria dominated recently deglaciated land. Relative abundance of these pioneer bacterial taxa decreased by 20–50% in the later stages with the emergence of new and rising of the less abundant members of the phyla Proteobacteria, Firmicutes, Planctomycetes, Acidobacteria, Verrucomicrobia, Candidatus TM6, and Chloroflexi. The community in the recent stage was less rich and harbored competitive interactions, while the later stages experienced a surge in bacterial diversity with cooperative interactions. The shift in α-diversity and composition was strongly influenced by soil organic carbon, carbon to nitrogen ratio, and soil moisture content. The functional analyses revealed a progression from a metabolism focused to a functionally progressive community required for bacterial co-existence and succession in plant communities. Overall, the findings indicate that the bacterial communities inhabit, diversify, and develop specialized functions post-deglaciation leading to nutrient inputs to soil and vegetation development, which may provide feedback to climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The DNA sequence dataset has been deposited to the National Centre for Biotechnology Information (NCBI) Short Read Archive (https://www.ncbi.nlm.nih.gov/sra). The BioProject accession number is PRJNA754406.

Code Availability

Not applicable.

References

  1. Cramer W, Bondeau A, Woodward FI et al (2001) Global response of terrestrial ecosystem structure and function to CO 2 and climate change: results from six dynamic global vegetation models: ecosystem dynamics, CO 2 and climate change. Glob Change Biol 7:357–373. https://doi.org/10.1046/j.1365-2486.2001.00383.x

    Article  Google Scholar 

  2. Venkatachalam S, Kannan VM, Saritha VN et al (2021) Bacterial diversity and community structure along the glacier foreland of Midtre Lovénbreen, Svalbard. Arct Ecol Indic 126:107704. https://doi.org/10.1016/j.ecolind.2021.107704

    Article  CAS  Google Scholar 

  3. Wu X, Zhang W, Liu G et al (2012) Bacterial diversity in the foreland of the Tianshan No. 1 glacier China. Environ Res Lett 7:014038. https://doi.org/10.1088/1748-9326/7/1/014038

    Article  Google Scholar 

  4. 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. https://doi.org/10.1111/1462-2920.13766

    Article  PubMed  Google Scholar 

  5. Alfaro FD, Salazar-Burrows A, Bañales-Seguel C et al (2020) Soil microbial abundance and activity across forefield glacier chronosequence in the northern Patagonian Ice Field, Chile. Arct Antarct Alp Res 52:553–562. https://doi.org/10.1080/15230430.2020.1820124

    Article  Google Scholar 

  6. Frkova Z, Pistocchi C, Vystavna Y, et al (2021) Phosphorus dynamics during early soil development in extreme environment. Soils and biogeochemical cycling. Preprint.

  7. Bradley JA, Anesio AM, Arndt S (2017) Microbial and biogeochemical dynamics in glacier forefields are sensitive to century-scale climate and anthropogenic change. Front Earth Sci. https://doi.org/10.3389/feart.2017.00026

    Article  Google Scholar 

  8. Gilbert JA, Dupont CL (2011) Microbial metagenomics: beyond the genome. Annu Rev Mar Sci 3:347–371. https://doi.org/10.1146/annurev-marine-120709-142811

    Article  Google Scholar 

  9. Feng W, Zhang Y, Yan R et al (2020) Dominant soil bacteria and their ecological attributes across the deserts in northern China. Eur J Soil Sci 71:524–535. https://doi.org/10.1111/ejss.12866

    Article  CAS  Google Scholar 

  10. Ortiz-Estrada ÁM, Gollas-Galván T, Martínez-Córdova LR, Martínez-Porchas M (2019) Predictive functional profiles using metagenomic 16S rRNA data: a novel approach to understanding the microbial ecology of aquaculture systems. Rev Aquac 11:234–245. https://doi.org/10.1111/raq.12237

    Article  Google Scholar 

  11. Langille MGI, Zaneveld J, Caporaso JG et al (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Sun S, Jones RB, Fodor AA (2020) Inference-based accuracy of metagenome prediction tools varies across sample types and functional categories. Microbiome 8:46. https://doi.org/10.1186/s40168-020-00815-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Shrestha UB, Gautam S, Bawa KS (2012) Widespread climate change in the Himalayas and associated changes in local ecosystems. PLoS ONE 7:e36741. https://doi.org/10.1371/journal.pone.0036741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Singh RK (2018) Impact of Climate Change on the Retreat of Himalayan Glaciers and Its Impact on Major River Hydrology: Himalayan Glacier Hydrology. In Climate Change and Environmental Concerns: Breakthroughs in Research and Practice, IGI Global, pp. 681–694

  15. Pusalkar PK, Singh DK (2012) Flora of Gangotri national park, western Himalaya. Botanical Survey of India, India

    Google Scholar 

  16. Tiwari P, Bhattacharya P, Rawat GS, Talukdar G (2021) Equilibrium in soil respiration across a climosequence indicates its resilience to climate change in a glaciated valley, western Himalaya. Sci Rep. https://doi.org/10.1038/s41598-021-02199-x

    Article  PubMed  PubMed Central  Google Scholar 

  17. Sanyal AK, Uniyal VP, Chandra K, Bhardwaj M (2013) Diversity, distribution pattern and seasonal variation in moth assemblages along altitudinal gradient in Gangotri landscape area, Western Himalaya, Uttarakhand, India. J Threat Taxa 5:3646–3653. https://doi.org/10.11609/JoTT.o2597.3646-53

    Article  Google Scholar 

  18. Tiwari P, Bhattacharya P, Rawat GS et al (2021) Experimental warming increases ecosystem respiration by increasing above-ground respiration in alpine meadows of Western Himalaya. Sci Rep. https://doi.org/10.1038/s41598-021-82065-y

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lanzén A, Epelde L, Blanco F et al (2016) Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient. Sci Rep. https://doi.org/10.1038/srep28257

    Article  PubMed  PubMed Central  Google Scholar 

  20. Rayment GE, Lyons DJ (2011) Soil chemical methods: Australasia. CSIRO Publishing, Collingwood, Vic

    Google Scholar 

  21. Blakemore LC, Searle PL, Daly BK (1987) Methods for chemical analysis of soils. NZ Soil Bureau, Dept. of Scientific and Industrial Research, Lower Hutt, N.Z.

    Google Scholar 

  22. Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38. https://doi.org/10.1097/00010694-193401000-00003

    Article  CAS  Google Scholar 

  23. Bremner JM (2018) Nitrogen-Total. In: Sparks DL, Page AL, Helmke PA et al (eds) SSSA book series. Soil Science Society of America, American Society of Agronomy, Madison, WI, USA, pp 1085–1121

    Google Scholar 

  24. Luo Z, Liu J, Zhao P et al (2019) Biogeographic patterns and assembly mechanisms of bacterial communities differ between habitat generalists and specialists across elevational gradients. Front Microbiol. https://doi.org/10.3389/fmicb.2019.00169

    Article  PubMed  PubMed Central  Google Scholar 

  25. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Pedrós-Alió C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14:257–263. https://doi.org/10.1016/j.tim.2006.04.007

    Article  CAS  PubMed  Google Scholar 

  28. Deng Y, Jiang Y-H, Yang Y et al (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113. https://doi.org/10.1186/1471-2105-13-113

    Article  PubMed  PubMed Central  Google Scholar 

  29. Shannon P, Markiel A, Ozier O et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Spellerberg IF, Fedor PJ (2003) A tribute to Claude Shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the ‘Shannon-Wiener’ Index: on species richness and diversity. Glob Ecol Biogeogr 12:177–179. https://doi.org/10.1046/j.1466-822X.2003.00015.x

    Article  Google Scholar 

  31. Oksanen J, Guillaume Blanchet F, Friendly M Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens M, Szoecs E, Wagner H (2020) Vegan: community ecology package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan.

  32. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108. https://doi.org/10.1016/j.tree.2003.10.013

    Article  PubMed  Google Scholar 

  33. Li J, Ma Y-B, Hu H-W et al (2015) Field-based evidence for consistent responses of bacterial communities to copper contamination in two contrasting agricultural soils. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00031

    Article  PubMed  PubMed Central  Google Scholar 

  34. Grace JB (2007) Structural equation modeling and natural systems. Biometrics 63:977–977. https://doi.org/10.1111/j.1541-0420.2007.00856_13.x

    Article  Google Scholar 

  35. R Core Team (2020) R: A language and environment for statistical computing. R Found Stat Comput, Vienna, Austria

    Google Scholar 

  36. Ciccazzo S, Esposito A, Borruso L, Brusetti L (2016) Microbial communities and primary succession in high altitude mountain environments. Ann Microbiol 66:43–60. https://doi.org/10.1007/s13213-015-1130-1

    Article  Google Scholar 

  37. Ji M, Greening C, Vanwonterghem I et al (2017) Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature 552:400–403. https://doi.org/10.1038/nature25014

    Article  CAS  PubMed  Google Scholar 

  38. Jangid K, Whitman WB, Condron LM et al (2013) Soil bacterial community succession during long-term ecosystem development. Mol Ecol 22:3415–3424. https://doi.org/10.1111/mec.12325

    Article  PubMed  Google Scholar 

  39. Bhattacharya P, Tiwari P, Rai ID et al (2022) Edaphic factors override temperature in shaping soil bacterial diversity across an elevation-vegetation gradient in Himalaya. Appl Soil Ecol 170:104306. https://doi.org/10.1016/j.apsoil.2021.104306

    Article  Google Scholar 

  40. Brady NC, Weil RR (2002) The nature and properties of soils, 13th edn. Prentice Hall, New Jersey, p 249

    Google Scholar 

  41. Qiang W, He L, Zhang Y et al (2021) Aboveground vegetation and soil physicochemical properties jointly drive the shift of soil microbial community during subalpine secondary succession in southwest China. CATENA 202:105251. https://doi.org/10.1016/j.catena.2021.105251

    Article  Google Scholar 

  42. Zhu B, Li C, Wang J et al (2020) Elevation rather than season determines the assembly and co-occurrence patterns of soil bacterial communities in forest ecosystems of Mount Gongga. Appl Microbiol Biotechnol 104:7589–7602. https://doi.org/10.1007/s00253-020-10783-w

    Article  CAS  PubMed  Google Scholar 

  43. Santos R, de Carvalho CCCR, Stevenson A et al (2015) Extraordinary solute-stress tolerance contributes to the environmental tenacity of mycobacteria: extraordinary stress-tolerance of mycobacteria. Environ Microbiol Rep 7:746–764. https://doi.org/10.1111/1758-2229.12306

    Article  CAS  PubMed  Google Scholar 

  44. Miteva VI, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep greenland glacier ice core. Appl Environ Microbiol 70:202–213. https://doi.org/10.1128/AEM.70.1.202-213.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Johnson SS, Hebsgaard MB, Christensen TR et al (2007) Ancient bacteria show evidence of DNA repair. Proc Natl Acad Sci 104:14401–14405. https://doi.org/10.1073/pnas.0706787104

    Article  PubMed  PubMed Central  Google Scholar 

  46. 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. https://doi.org/10.1007/s00203-015-1121-4

    Article  CAS  PubMed  Google Scholar 

  47. Shao K, Bai C, Cai J et al (2019) Illumina sequencing revealed soil microbial communities in a Chinese alpine grassland. Geomicrobiol J 36:204–211. https://doi.org/10.1080/01490451.2018.1534902

    Article  CAS  Google Scholar 

  48. Edwards A, Pachebat JA, Swain M et al (2013) A metagenomic snapshot of taxonomic and functional diversity in an alpine glacier cryoconite ecosystem. Environ Res Lett 8:035003. https://doi.org/10.1088/1748-9326/8/3/035003

    Article  Google Scholar 

  49. Ahmad T, Gupta G, Sharma A et al (2021) Metagenomic analysis exploring taxonomic and functional diversity of bacterial communities of a Himalayan urban fresh water lake. PloS One 16:e0248116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Dube JP, Valverde A, Steyn JM et al (2019) Differences in bacterial diversity, composition and function due to long-term agriculture in soils in the eastern free state of South Africa. Diversity 11:61. https://doi.org/10.3390/d11040061

    Article  CAS  Google Scholar 

  51. Kazemi S, Hatam I, Lanoil B (2016) Bacterial community succession in a high-altitude subarctic glacier foreland is a three-stage process. Mol Ecol 25:5557–5567. https://doi.org/10.1111/mec.13835

    Article  CAS  PubMed  Google Scholar 

  52. Koch AL (2001) Oligotrophs versus copiotrophs. BioEssays 23:657–661

    Article  CAS  PubMed  Google Scholar 

  53. Ortiz-Álvarez R, FiererRíos NA et al (2018) Consistent changes in the taxonomic structure and functional attributes of bacterial communities during primary succession. ISME J 12:1658–1667. https://doi.org/10.1038/s41396-018-0076-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Drake HL, Gößner AS, Daniel SL (2008) Old acetogens, new light. Ann N Y Acad Sci 1125:100–128. https://doi.org/10.1196/annals.1419.016

    Article  CAS  PubMed  Google Scholar 

  55. Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276. https://doi.org/10.1038/nrmicro.2018.9

    Article  CAS  PubMed  Google Scholar 

  56. Wang J, Wu Y, Li J et al (2021) Energetic supply regulates heterotrophic nitrogen fixation along a glacial chronosequence. Soil Biol Biochem 154:108150. https://doi.org/10.1016/j.soilbio.2021.108150

    Article  CAS  Google Scholar 

  57. Tiwari P, Singh JS (2017) A plant growth promoting rhizospheric Pseudomonas aeruginosa strain inhibits seed germination in Triticum aestivum (L) and Zea mays (L). Microbiol Res. https://doi.org/10.4081/mr.2017.7233

    Article  PubMed  Google Scholar 

  58. Florentino AP, Weijma J, Stams AJM, Sánchez-Andrea I (2016) Ecophysiology and application of acidophilic sulfur-reducing microorganisms. In: Rampelotto PH (ed) Biotechnology of extremophiles. Springer International Publishing, Cham, pp 141–175

    Chapter  Google Scholar 

Download references

Acknowledgements

Forest Department of Uttarakhand provided necessary permits to research in Gangotri National Park. We acknowledge help from Dr. Devendra Kumar and Umed S Rana (field assistance), Arun Kumar (laboratory work), Dr. Punyasloke Bhadury (DNA sequencing), Dr. Awadhesh Pandit and Tejali Naik (NGS work), Sitendu Goswami, and Dr. Raman Kumar (Data analysis). We thank Dr. Samrat Mondol, Dr. Sathyakumar (Nodal Scientist, NMSHE), Dr. Dhananjay Mohan (Director), Dr. Y.V. Jhala (Dean), Dr. Bitapi Sinha (Research Coordinator), and Nodal Officer of Wildlife Forensics and Conservation Genetics Cell of Wildlife Institute of India for facilitating this work.

Funding

This research is part of the project National Mission for Sustaining the Himalayan Ecosystem (NMSHE) funded by the Department of Science and Technology, Government of India (Grant No. DST/SPLICE/CCP/NMSHE/TF-2/WII/2014[G]). Partial funding for the bacterial Next Generation Sequencing was provided by the United Nations Development Programme and the Ministry of Environment, Forest and Climate Change Government of India through the Third National Communication project (Grant No. 7/2/2015-CC). Pamela Bhattacharya was supported by the Council of Scientific and Industrial Research, Government of India (Award no. 09/668(0012)/2019– EMR–I).

Author information

Authors and Affiliations

  1. Wildlife Institute of India, Chandrabani, Dehradun, 248001, India

    Pamela Bhattacharya, Pankaj Tiwari, Gautam Talukdar & Gopal S. Rawat

Authors
  1. Pamela Bhattacharya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pankaj Tiwari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gautam Talukdar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gopal S. Rawat
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: PT and PB; Funding acquisition: GSR, GT, and PB; Resources: GSR and GT; Supervision: GSR and GT; Methodology: PT and PB; Data curation: PB; Formal analysis and investigation: PB and PT; Writing—original draft preparation: PB and PT; Writing—review and editing: GSR, GT, PB, and PT.

Corresponding author

Correspondence to Gopal S. Rawat.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical Approval

Not applicable.

Consent to Participate

All authors gave consent to participate and publish all information provided in the manuscript.

Consent to Publish

All authors gave consent to participate and publish all information provided in the manuscript.

Additional information

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.

Supplementary file1 (DOCX 14292 KB)

Supplementary file2 (XLSX 25782 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhattacharya, P., Tiwari, P., Talukdar, G. et al. Shifts in Bacterial Community Composition and Functional Traits at Different Time Periods Post-deglaciation of Gangotri Glacier, Himalaya. Curr Microbiol 79, 91 (2022). https://doi.org/10.1007/s00284-022-02779-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-022-02779-8

Search

Navigation