Skip to main content

Advertisement

SpringerLink
Log in

Some Like it High! Phylogenetic Diversity of High-Elevation Cyanobacterial Community from Biological Soil Crusts of Western Himalaya

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The environment of high-altitudinal cold deserts of Western Himalaya is characterized by extensive development of biological soil crusts, with cyanobacteria as dominant component. The knowledge of their taxonomic composition and dependency on soil chemistry and elevation is still fragmentary. We studied the abundance and the phylogenetic diversity of the culturable cyanobacteria and eukaryotic microalgae in soil crusts along altitudinal gradients (4600–5900 m) at two sites in the dry mountains of Ladakh (SW Tibetan Plateau and Eastern Karakoram), using both microscopic and molecular approaches. The effects of environmental factors (altitude, mountain range, and soil physico-chemical parameters) on the composition and biovolume of phototrophs were tested by multivariate redundancy analysis and variance partitioning. Both phylogenetic diversity and composition of morphotypes were similar between Karakorum and Tibetan Plateau. Phylogenetic analysis of 16S rRNA gene revealed strains belonging to at least five genera. Besides clusters of common soil genera, e.g., Microcoleus, Nodosilinea, or Nostoc, two distinct clades of simple trichal taxa were newly discovered. The most abundant cyanobacterial orders were Oscillatoriales and Nostacales, whose biovolume increased with increasing elevation, while that of Chroococales decreased. Cyanobacterial species richness was low in that only 15 morphotypes were detected. The environmental factors accounted for 52 % of the total variability in microbial data, 38.7 % of which was explained solely by soil chemical properties, 14.5 % by altitude, and 8.4 % by mountain range. The elevation, soil phosphate, and magnesium were the most important predictors of soil phototrophic communities in both mountain ranges despite their different bedrocks and origin. The present investigation represents a first record on phylogenetic diversity of the cyanobacterial community of biological soil crusts from Western Himalayas and first record from altitudes over 5000 m.

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

References

  1. Kubečková K, Johansen JR, Warren SD, Sparks RL (2003) Development of immobilized cyanobacterial amendments for reclamation of microbiotic soil crusts. Algol Stud 109:341–362

    Article  Google Scholar 

  2. Tirkey J, Adhikary SP (2005) Cyanobacteria in biological soil crusts of India. Curr Sci 89:515–521

    Google Scholar 

  3. Johansen JR (1993) Cryptogamic crusts of semiarid and arid lands of North America. J Phycol 29:140–147. doi:10.1111/j.0022-3646.1993.00140.x

    Article  Google Scholar 

  4. Heckman KA, Anderson WB, Wait DA (2006) Distribution and activity of hypolithic soil crusts in a hyperarid desert (Baja California, Mexico). Biol Fertil Soils 43:263–266. doi:10.1007/s00374-006-0104-7

    Article  Google Scholar 

  5. Belnap J, Harper KT (1995) Influence of cryptobitic soil crusts on lemental content of tissue of 2 desert seed plants. Arid Soil Res Rehabil 9:107–115

    Article  CAS  Google Scholar 

  6. Belnap J, Lange O (2001) Biological soil crusts: structure, function and management. Springer Verlag, Berlin

    Google Scholar 

  7. Schmidt SK, Reed SC, Nemergut DR, Grandy AS, Cleveland CC, Weintraub MN, Hill AW, Costello EK, Meyer AF, Neff JC, Martin AM (2008) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc R Soc B Biol Sci 275:2793–2802. doi:10.1098/rspb.2008.0808

    Article  CAS  Google Scholar 

  8. Lamb EG, Han S, Lanoil BD, Henry GHR, Brummell ME, Banerjee S, Siciliano SD (2011) A high arctic soil ecosystem resists long-term environmental manipulations. Glob Chang Biol 17:3187–3194. doi:10.1111/j.1365-2486.2011.02431.x

    Article  Google Scholar 

  9. Ives AR, Cardinale BJ (2004) Food-web interactions govern the resistance of communities after non-random extinctions. Nature 429:174–177. doi:10.1038/nature02515

    Article  PubMed  CAS  Google Scholar 

  10. Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62. doi:10.1126/science.1133258

    Article  PubMed  CAS  Google Scholar 

  11. Janatkova K, Rehakova K, Dolezal J, Simek M, Chlumska Z, Dvorsky M, Kopecky M (2013) Community structure of soil phototrophs along environmental gradients in arid Himalaya. Environ Microbiol 15:2505–2516. doi:10.1111/1462-2920.12132

    Article  PubMed  CAS  Google Scholar 

  12. Bhattacharyya A (1989) Vegetation and climate during the last 30,000 years in Ladakh. Palaeogeogr Palaeoclimatol Palaeoecol 73:25–38. doi:10.1016/0031-0182(89)90042-4

    Article  Google Scholar 

  13. Epard J-L, Steck A (2008) Structural development of the Tso Morari ultra-high pressure nappe of the Ladakh Himalaya. Tectonophysics 451:242–264. doi:10.1016/j.tecto.2007.11.050

    Article  Google Scholar 

  14. Phillips RJ (2008) Geological map of the Karakoram fault zone, Eastern Karakoram, Ladakh, NW Himalaya. Journal of Maps: 21-37

  15. Klimes L (2003) Life-forms and clonality of vascular plants along an altitudinal gradient in E ladakh (NW Himalayas). Basic Appl Ecol 4:317–328. doi:10.1078/1439-1791-00163

    Article  Google Scholar 

  16. Klimes L, Dolezal J (2010) An experimental assessment of the upper elevational limit of flowering plants in the western Himalayas. Ecography 33:590–596. doi:10.1111/j.1600-0587.2009.05967.x

    Google Scholar 

  17. Dvorsky M, Dolezal J, de Bello F, Klimesova J, Klimes L (2011) Vegetation types of East Ladakh: species and growth form composition along main environmental gradients. Appl Veg Sci 14:132–147. doi:10.1111/j.1654-109X.2010.01103.x

    Article  Google Scholar 

  18. Klimesova J, Dolezal J, Dvorsky M, de Bello F, Klimes L (2011) Clonal growth forms in Eastern Ladakh, Western Himalayas: classification and habitat preferences. Folia Geobotanica 46:191–217. doi:10.1007/s12224-010-9076-3

    Article  Google Scholar 

  19. Campbell BJ, Polson SW, Hanson TE, Mack MC, Schuur EAG (2010) The effect of nutrient deposition on bacterial communities in arctic tundra soil. Environ Microbiol 12:1842–1854. doi:10.1111/j.1462-2920.2010.02189.x

    Article  PubMed  CAS  Google Scholar 

  20. Kastovska K, Elster J, Stibal M, Santruckova H (2005) Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (high arctic). Microb Ecol 50:396–407. doi:10.1007/s00248-005-0246-4

    Article  PubMed  Google Scholar 

  21. Zbíral J, Honsa I, Malý S (1997) Analýza půd III—jednotné pracovní postupy. ÚKZÚZ, Brno

    Google Scholar 

  22. Mehlich A (1978) New extraction for soil test evaluation of phosphorus, potassium, magnesium, sodium, manganese and zinc. Commun Soil Sci Plant Anal 9:477–492. doi:10.1080/00103627809366824

    Article  CAS  Google Scholar 

  23. Kimbrough DE, Wakakuwa J (1991) Report of an interlaboratory study comparing EPA SW-846 method 3050(1) and an alternative method from the California Department of Health Services. queryWaste Testing and Quality Assurance : Third Volume 1075:231–244. doi:10.1520/stp25480s

    Google Scholar 

  24. Rowel LD (1994) Soil science: methods and applications. Longman Scientific & Technical, Burnt Mill, Harlow

    Google Scholar 

  25. Bischoff HW, Bold H (1963) Some soil algae from enchanted rock and related algal species. Univ Texas Publ, Phycological studies IV

  26. Taton A, Grubisic S, Brambilla E, De Wit R, Wilmotte A (2003) Cyanobacterial diversity in natural and artificial microbial mats of lake fryxell (McMurdo dry valleys, antarctica): a morphological and molecular approach. Appl Environ Microbiol 69:5157–5169. doi:10.1128/aem.69.9.5157-5169.2003

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  27. Nubel U, GarciaPichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332

    PubMed Central  PubMed  CAS  Google Scholar 

  28. Wilmotte A, Vanderauwera G, Dewachter R (1993) Structure of the 16-S ribosomal-RNA of the thermophilic cyanobacterium chlorogleopsis (mastigocladus-laminosus HTF) strain PCC7518, and phylogenetic analyses. FEBS Lett 317:96–100. doi:10.1016/0014-5793(93)81499-p

    Article  PubMed  CAS  Google Scholar 

  29. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi:10.1093/molbev/mst010

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  30. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    Article  PubMed Central  PubMed  Google Scholar 

  31. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010

    Article  PubMed  CAS  Google Scholar 

  32. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. doi:10.1093/molbev/msp259

    Article  PubMed  CAS  Google Scholar 

  33. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi:10.1038/nmeth.2109

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  34. ter Braak CJF, Smilauer P (2012) CANOCO reference manual and user’s guide to CANOCO for windows. Centre for Biometry, Wageningen

    Google Scholar 

  35. Jan L, Petr Š (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge

    Google Scholar 

  36. Team RDC (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  37. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

    Google Scholar 

  38. Rehakova K, Chlumska Z, Dolezal J (2011) Soil cyanobacterial and microalgal diversity in Dry mountains of ladakh, NW Himalaya, as related to site, altitude, and vegetation. Microb Ecol 62:337–346. doi:10.1007/s00248-011-9878-8

    Article  PubMed  CAS  Google Scholar 

  39. Mitchell RJ, Campbell CD, Chapman SJ, Cameron CM (2010) The ecological engineering impact of a single tree species on the soil microbial community. J Ecol 98:50–61. doi:10.1111/j.1365-2745.2009.01601.x

    Article  CAS  Google Scholar 

  40. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631. doi:10.1073/pnas.0507535103

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  41. Dvorsky M, Dolezal J, Kopecky M, Chlumska Z, Janatkova K, Altman J, de Bello F, Rehakova K (2013) Testing the stress-gradient hypothesis at the roof of the world: effects of the cushion plant thylacospermum caespitosum on species assemblages. Plos One 8(1):e53514. doi:10.1371/journal.pone.0053514

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  42. Dor I, Danin A (2001) Life strategies of Microcoleus vaginatus: A crust-forming cyanophyte on desert soils. Nova Hedwigia Beiheft Nova Hedwigia Beiheft Algae and extreme environments Ecology and Physiology Proceedings of the International Conference 11-16 September, Trebon, Czech Republic 123: 317-339

  43. Komárek J (2013) Cyanoprokaryota 3: Heterocytous genera. In: Budel B, Gartner G, Krienitz L, Schagerl M (eds), Süßwasserflora von Mitteleuropa (vol 19/3). Spektrum Akademischer Verlag, pp 1130

  44. Stackebrandt E, Goebel BM (1994) A place for DNA-DNA reassociation and 16S ribosomal-RNA-sequence analyses in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  45. Berrendero GE, Johansen J, Kaštovský J,Bohunická M, Čapková K, (2015) Macrochaete gen. nov. (Cyanobacteria): The first step in solving the extensively polyphyletic genus Calothrix. J Phycol (under review)

  46. Evans RD, Johansen JR (1999) Microbiotic crusts and ecosystem processes. Crit Rev Plant Sci 18:183–225. doi:10.1080/07352689991309199

    Article  Google Scholar 

  47. Ma XJ, Chen T, Zhang GS, Wang R (2004) Microbial community structure along an altitude gradient in three different localities. Folia Microbiol 49:105–111. doi:10.1007/bf02931382

    Article  CAS  Google Scholar 

  48. Balser TC, Gutknecht JLM, Liang C (2010) How will climate change impact soil microbial communities? In: Dixon GR, Emma T (eds) Soil microbiology and sustainable crop production. University of Reading Press, Reading, pp 373–397

    Chapter  Google Scholar 

  49. Zelikova TJ, Housman DC, Grote EE, Neher DA, Belnap J (2012) Warming and increased precipitation frequency on the Colorado plateau: implications for biological soil crusts and soil processes. Plant Soil 355:265–282. doi:10.1007/s11104-011-1097-z

    Article  CAS  Google Scholar 

  50. Lynch RC, King AJ, Farias ME, Sowell P, Vitry C, Schmidt SK (2012) The potential for microbial life in the highest-elevation (>6000 m.a.s.l.) mineral soils of the Atacama region. J Geophys Res Biogeosci 117. doi: 10.1029/2012jg001961

Download references

Acknowledgments

This study was funded by the national project 13-13368S of Grant Agency of CR and by the Institute of Botany, Academy of Sciences of the CR long-term research development project no. RVO67985939 and by grant of the Faculty of Science, University of South Bohemia (GAJU 145-2013P). Field assistance by M. Dvorský, J. Altman Z. Chlumská, help with laboratory analyses by our technicians, and Martin Kopecky’s help with graphs are gratefully acknowledged. Access to computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum, provided under the programme “Projects of Large Infrastructure for Research, Development, and Innovations” (LM2010005), is greatly appreciated.

Author information

Authors and Affiliations

  1. Faculty of Science, University of South Bohemia, Branišovská 31, České Budějovice, 37005, Czech Republic

    Kateřina Čapková, Tomáš Hauer & Jiří Doležal

  2. Institute of Botany, Academy of Sciences of the Czech Republic, Dukelská 135, Třeboň, 379 82, Czech Republic

    Kateřina Čapková, Tomáš Hauer, Klára Řeháková & Jiří Doležal

  3. Institute of Hydrobiology, Biology Centre of AS CR, Na Sádkách 7, České Budějovice, 37005, Czech Republic

    Klára Řeháková

Authors
  1. Kateřina Čapková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomáš Hauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Klára Řeháková
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiří Doležal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kateřina Čapková.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Čapková, K., Hauer, T., Řeháková, K. et al. Some Like it High! Phylogenetic Diversity of High-Elevation Cyanobacterial Community from Biological Soil Crusts of Western Himalaya. Microb Ecol 71, 113–123 (2016). https://doi.org/10.1007/s00248-015-0694-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-015-0694-4

Keywords

Search

Navigation