Bacterial Communities Associated with the Biofilms Formed in High-Altitude Brackish Water Pangong Tso Located in the Himalayan Plateau

Abstract

Pangong Tso is a long and narrow lake situated at an altitude of ~ 4266 m amsl in the Himalayan Plateau on the side of the India/China border. Biofilm has been observed in a small area near the shore of Pangong Tso. Bacterial communities of the lake sediment, water and biofilms were studied using amplicon sequencing of V3-V4 region of the 16S rRNA gene. The standard QIIME pipeline was used for analysis. The metabolic potential of the community was predicted using functional prediction tool Tax4Fun. Bacterial phyla Proteobacteria, followed by Bacteroidetes, Acidobacteria, Planctomycetes, Actinobacteria, and Firmicutes, were found to be dominant across these samples. Shannon’s and Simpson’s alpha diversity analysis revealed that sediment communities are the most diverse, and water communities are the least diverse. Principal Coordinates based beta diversity analysis showed significant variation in the bacterial communities of the water, sediment and biofilm samples. Bacterial phyla Verrucomicrobia, Deinococcus-Thermus and Cyanobacteria were explicitly enriched in the biofilm samples. Predictive functional profiling of these bacterial communities showed a higher abundance of genes involved in photosynthesis, biosynthesis of secondary metabolites, carbon fixation in photosynthetic organisms and glyoxylate and dicarboxylate metabolism in the biofilm sample. In conclusion, the Pangong Tso bacterial communities are quite similar to other saline and low-temperature lakes in the Tibetan Plateau. Bacterial community structure of the biofilm samples was significantly different from that of the water and sediment samples and enrichment of saprophytic communities was observed in the biofilm samples, indicating an important succession event in this high-altitude lake.

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Data Availability

The sequence data is made available at NCBI SRA submission with Bioproject ID PRJNA496310 for the microbial mat, sediment and the water bacterial community.

References

  1. 1.

    Mao D, Wang Z, Yang H, Li H, Thompson J, Li L, Song K, Chen B, Gao H, Wu J (2018) Impacts of climate change on tibetan lakes: patterns and processes. Remote Sens 10:358

    Article  Google Scholar 

  2. 2.

    Adrian R, O’Reilly CM, Zagarese H et al (2009) Lakes as sentinels of climate change. Limnol Oceanogr 54:2283–2297

    Article  Google Scholar 

  3. 3.

    Mladenov N, Sommaruga R, Morales-Baquero R et al (2011) Dust inputs and bacteria influence dissolved organic matter in clear alpine lakes. Nat Commun. https://doi.org/10.1038/ncomms1411

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Hou D, Huang Z, Zeng S, Liu J, Wei D, Deng X, Weng S, He Z, He J (2017) Environmental factors shape water microbial community structure and function in shrimp cultural enclosure ecosystems. Front Microbiol. https://doi.org/10.3389/fmicb.2017.02359

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Bartrons M, Catalan J, Casamayor EO (2012) High bacterial diversity in epilithic biofilms of oligotrophic mountain lakes. Microb Ecol 64:860–869

    Article  Google Scholar 

  6. 6.

    Battin TJ, Kaplan LA, Denis Newbold J, Hansen CME (2003) Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426:439–442

    CAS  Article  Google Scholar 

  7. 7.

    Bhat FA, Yousuf AR, Aftab A, Arshid J, Mahdi MD, Balkhi MH (2011) Ecology and biodiversity in Pangong Tso (lake) and its inlet stream in Ladakh, India. Int J Biodivers Conserv 3:501–511

    Google Scholar 

  8. 8.

    Srivastava P, Kumar A, Singh R et al (2020) Rapid lake level fall in Pangong Tso (lake) in Ladakh, NW Himalaya: a response of late Holocene aridity. Curr Sci 119:219–231

    CAS  Google Scholar 

  9. 9.

    Drew F (1875) The Jummoo and Kashmir territories: a geographical account, Part 73. Nineteenth century collections online: mapping the world: maps and travel literature. E. Stanford. https://books.google.co.in/books?id=t9gMAAAAIAAJ

  10. 10.

    Huntington E (1906) Pangong: a glacial lake in the tibetan plateau. J Geol 14:599–617

    Article  Google Scholar 

  11. 11.

    APHA (American Public Health Association), American Water Works Association (AWWA) and Water Environment Federation (WEF) 2005 Standard methods for the examination of water and wastewater (Washington: DC)

  12. 12.

    Sinclair L, Osman OA, Bertilsson S, Eiler A (2015) Microbial community composition and diversity via 16S rRNA gene amplicons: evaluating the illumina platform. PLoS ONE 10:e0116955

    Article  Google Scholar 

  13. 13.

    Zhang J, Kobert K, Flouri T, Stamatakis A (2013) PEAR: a fast and accurate illumina paired-End reAd mergeR. Bioinformatics 30:614–620

    Article  Google Scholar 

  14. 14.

    Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  Article  Google Scholar 

  15. 15.

    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  Article  Google Scholar 

  16. 16.

    Zakrzewski M, Proietti C, Ellis JJ et al (2016) Calypso: a user-friendly web-server for mining and visualizing microbiome–environment interactions. Bioinformatics. https://doi.org/10.1093/bioinformatics/btw725

    Article  PubMed Central  Google Scholar 

  17. 17.

    Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124

    CAS  Article  Google Scholar 

  18. 18.

    Heberle H, Meirelles GV, da Silva FR, Telles GP, Minghim R (2015) InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics. https://doi.org/10.1186/s12859-015-0611-3

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Aßhauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data: Fig. 1. Bioinformatics 31:2882–2884. https://doi.org/10.1093/bioinformatics/btv287

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2015) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462

    Article  Google Scholar 

  21. 21.

    Morris EK, Caruso T, Buscot F et al (2014) Choosing and using diversity indices: insights for ecological applications from the German biodiversity exploratories. Ecol Evol 4:3514–3524

    Article  Google Scholar 

  22. 22.

    Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an Athalassohaline Lake in Northwestern China. Appl Environ Microbiol 72:3832–3845

    CAS  Article  Google Scholar 

  23. 23.

    Braga RM, Dourado MN, Araújo WL (2016) Microbial interactions: ecology in a molecular perspective. Brazil J Microbiol 47:86–98

    CAS  Article  Google Scholar 

  24. 24.

    Boutaiba S, Hacene H, Bidle KA, Maupin-Furlow JA (2011) Microbial diversity of the hypersaline Sidi Ameur and Himalatt salt lakes of the Algerian Sahara. J Arid Environ 75:909–916

    Article  Google Scholar 

  25. 25.

    Last WM, Ginn FM (2005) Saline systems of the Great Plains of western Canada: an overview of the limnogeology and paleolimnology. Saline Syst 1:10

    Article  Google Scholar 

  26. 26.

    Wong HL, Smith D-L, Visscher PT, Burns BP (2015) Niche differentiation of bacterial communities at a millimeter scale in Shark Bay microbial mats. Sci Rep. https://doi.org/10.1038/srep15607

    Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Jiang H, Dong H, Yu B, Lv G, Deng S, Wu Y, Dai M, Jiao N (2009) Abundance and diversity of aerobic anoxygenic phototrophic bacteria in saline lakes on the Tibetan plateau. FEMS Microbiol Ecol 67:268–278

    CAS  Article  Google Scholar 

  28. 28.

    Piwosz K, Shabarova T, Pernthaler J et al (2020) Bacterial and eukaryotic small-subunit amplicon data do not provide a quantitative picture of microbial communities, but they are reliable in the context of ecological interpretations. mSphere. https://doi.org/10.1128/msphere.00052-20

    Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Yang J, Ma L, Jiang H, Wu G, Dong H (2016) Salinity shapes microbial diversity and community structure in surface sediments of the Qinghai-Tibetan Lakes. Sci Rep. https://doi.org/10.1038/srep25078

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Koblížek M (2015) Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol Rev 39:854–870. https://doi.org/10.1093/femsre/fuv032

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I, Ulbrich M, Klenk H-P, Schomburg D, Petersen J, Göker M (2017) Phylogenomics of rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME J 11:1483–1499

    Article  Google Scholar 

  32. 32.

    Thomas FA, Sinha RK, Krishnan KP (2020) Bacterial community structure of a glacio-marine system in the Arctic (Ny-Ålesund, Svalbard). Sci Total Environ 718:135264. https://doi.org/10.1016/j.scitotenv.2019.135264

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Sorensen KB, Canfield DE, Teske AP, Oren A (2005) Community composition of a hypersaline endoevaporitic microbial mat. Appl Environ Microbiol 71:7352–7365

    CAS  Article  Google Scholar 

  34. 34.

    Lindh MV, Sjöstedt J, Andersson AF et al (2015) Disentangling seasonal bacterioplankton population dynamics by high-frequency sampling. Environ Microbiol 17:2459–2476. https://doi.org/10.1111/1462-2920.12720

    Article  PubMed  Google Scholar 

  35. 35.

    Theodorakopoulos N, Bachar D, Christen R et al (2013) Exploration of Deinococcus-Thermusmolecular diversity by novel group-specific PCR primers. MicrobiologyOpen. https://doi.org/10.1002/mbo3.119

    Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Lavrentyeva EV, Erdyneeva EB, Banzaraktsaeva TG et al (2020) Prokaryotic diversity in the biotopes of the gudzhirganskoe Saline Lake (Barguzin Valley, Russia). Microbiology 89:359–368. https://doi.org/10.1134/s0026261720030157

    CAS  Article  Google Scholar 

  37. 37.

    Diez B, Bauer K, Bergman B (2007) Epilithic cyanobacterial communities of a marine tropical beach rock (Heron Island, Great Barrier Reef): diversity and diazotrophy. Appl Environ Microbiol 73:3656–3668

    CAS  Article  Google Scholar 

  38. 38.

    Pontefract A, Zhu TF, Walker VK, Hepburn H, Lui C, Zuber MT, Ruvkun G, Carr CE (2017) Microbial diversity in a hypersaline sulfate lake: a terrestrial analog of ancient mars. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01819

    Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Zhong Z-P, Liu Y, Wang F et al (2016) Planktosalinus lacus gen. nov., sp. nov., a member of the family Flavobacteriaceae isolated from a salt lake. Int J Syst Evol Microbiol 66:2084–2089. https://doi.org/10.1099/ijsem.0.000997

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Dong H, Zhang G, Jiang H, Yu B, Chapman LR, Lucas CR, Fields MW (2006) Microbial diversity in sediments of saline Qinghai Lake, China: linking geochemical controls to microbial ecology. Microb Ecol 51:65–82

    CAS  Article  Google Scholar 

  41. 41.

    Rawat SR, Männistö MK, Bromberg Y, Häggblom MM (2012) Comparative genomic and physiological analysis provides insights into the role of Acidobacteriain organic carbon utilization in Arctic tundra soils. FEMS Microbiol Ecol 82:341–355

    CAS  Article  Google Scholar 

  42. 42.

    Mosier AC, Murray AE, Fritsen CH (2007) Microbiota within the perennial ice cover of Lake Vida, Antarctica. FEMS Microbiol Ecol 59:274–288

    CAS  Article  Google Scholar 

  43. 43.

    Guseva NV, Nalivayko NG, Kopylova YG, Khvaschevskaya AA, Vaishlya OB (2014) Chemical and microbial composition of Khakassia Saline Lakes with regard to their ecological state. IERI Procedia 8:130–135

    Article  Google Scholar 

  44. 44.

    Vavourakis CD, Ghai R, Rodriguez-Valera F, Sorokin DY, Tringe SG, Hugenholtz P, Muyzer G (2016) Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake Brines. Front Microbiol. https://doi.org/10.3389/fmicb.2016.00211

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Máthé I, Tóth E, Mentes A, Szabó A, Márialigeti K, Schumann P, Felföldi T (2018) A new Rhizobium species isolated from the water of a crater lake, description of Rhizobium aquaticum sp. nov. Antonie Van Leeuwenhoek 111:2175–2183

    Article  Google Scholar 

  46. 46.

    Kaiser K, Benner R (2008) Major bacterial contribution to the ocean reservoir of detrital organic carbon and nitrogen. Limnol Oceanogr 53:99–112

    CAS  Article  Google Scholar 

  47. 47.

    Cole JK, Hutchison JR, Renslow RS et al (2014) Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotroph-heterotroph interactions. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00109

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Michaud L, Caruso C, Mangano S, Interdonato F, Bruni V, Lo Giudice A (2012) Predominance of Flavobacterium, Pseudomonas, and Polaromonas within the prokaryotic community of freshwater shallow lakes in the northern Victoria Land, East Antarctica. FEMS Microbiol Ecol 82:391–404

    CAS  Article  Google Scholar 

  49. 49.

    Baatar B, Chiang P-W, Rogozin DY, Wu Y-T, Tseng C-H, Yang C-Y, Chiu H-H, Oyuntsetseg B, Degermendzhy AG, Tang S-L (2016) Bacterial communities of three saline meromictic Lakes in Central Asia. PLoS ONE 11:e0150847

    Article  Google Scholar 

  50. 50.

    Yurkov VV, Gorlenko VM (1990) Erythrobacter sibiricus sp. nov. a new freshwater aerobic species containing bacteriochlorophyll a. Mikrobiologiya 59:120

    CAS  Google Scholar 

  51. 51.

    Paul Antony C, Kumaresan D, Hunger S, Drake HL, Murrell JC, Shouche YS (2012) Microbiology of Lonar Lake and other soda lakes. ISME J 7:468–476

    Article  Google Scholar 

  52. 52.

    Qurashi AW, Sabri AN (2012) Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 43:1183–1191. https://doi.org/10.1590/s1517-83822012000300046

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Odeyemi OA, Ahmad A (2017) Population dynamics, antibiotics resistance and biofilm formation of Aeromonas and Vibrio species isolated from aquatic sources in Northern Malaysia. Microb Pathog 103:178–185. https://doi.org/10.1016/j.micpath.2017.01.007

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Rose SJ, Babrak LM, Bermudez LE (2015) Mycobacterium avium possesses extracellular DNA that contributes to biofilm formation, structural integrity, and tolerance to antibiotics. PLoS ONE 10:e0128772. https://doi.org/10.1371/journal.pone.0128772

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. 55.

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

    Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Ren Z, Wang F, Qu X, Elser JJ, Liu Y, Chu L (2017) Taxonomic and functional differences between microbial communities in Qinghai Lake and its input streams. Front Microbiol. https://doi.org/10.3389/fmicb.2017.02319

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Authors acknowledge the Director, NCCS, Pune for extending necessary facilities for this study. The authors also acknowledge the financial support of the SERB-DST (YSS/2015/000149) and DBT (BT/Coor. II/01/03/2016).

Funding

The SERB-DST (YSS/2015/000149) and DBT (BT/Coord. II/01/03/2016) provided funds this research.

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PR designed the study and collected the samples. KJ and AS helped in the molecular work. DC performed the bioinformatics and statistical analyses. DD guided in the analysis. PR and DC drafted the manuscript. PR supervised the data analysis and revised the manuscript. YS analyzed physicochemical properties of the Pangong Lake water. All authors have read and approved the final version of the manuscript.

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Correspondence to Praveen Rahi.

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Chaudhari, D.S., Dhotre, D.P., Jani, K. et al. Bacterial Communities Associated with the Biofilms Formed in High-Altitude Brackish Water Pangong Tso Located in the Himalayan Plateau. Curr Microbiol 77, 4072–4084 (2020). https://doi.org/10.1007/s00284-020-02244-4

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