Microbial Ecology

, Volume 71, Issue 1, pp 113–123 | Cite as

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

  • Kateřina ČapkováEmail author
  • Tomáš Hauer
  • Klára Řeháková
  • Jiří Doležal
Environmental Microbiology


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.


Soil crusts Cyanobacterial diversity Western Himalayas High-elevation Desert Phosphorus 



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.


  1. 1.
    Kubečková K, Johansen JR, Warren SD, Sparks RL (2003) Development of immobilized cyanobacterial amendments for reclamation of microbiotic soil crusts. Algol Stud 109:341–362CrossRefGoogle Scholar
  2. 2.
    Tirkey J, Adhikary SP (2005) Cyanobacteria in biological soil crusts of India. Curr Sci 89:515–521Google Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 9:107–115CrossRefGoogle Scholar
  6. 6.
    Belnap J, Lange O (2001) Biological soil crusts: structure, function and management. Springer Verlag, BerlinGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefPubMedGoogle Scholar
  10. 10.
    Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62. doi: 10.1126/science.1133258 CrossRefPubMedGoogle Scholar
  11. 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 CrossRefPubMedGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 14.
    Phillips RJ (2008) Geological map of the Karakoram fault zone, Eastern Karakoram, Ladakh, NW Himalaya. Journal of Maps: 21-37Google Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. 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 CrossRefPubMedGoogle Scholar
  21. 21.
    Zbíral J, Honsa I, Malý S (1997) Analýza půd III—jednotné pracovní postupy. ÚKZÚZ, BrnoGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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. 24.
    Rowel LD (1994) Soil science: methods and applications. Longman Scientific & Technical, Burnt Mill, HarlowGoogle Scholar
  25. 25.
    Bischoff HW, Bold H (1963) Some soil algae from enchanted rock and related algal species. Univ Texas Publ, Phycological studies IVGoogle Scholar
  26. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  27. 27.
    Nubel U, GarciaPichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332PubMedCentralPubMedGoogle Scholar
  28. 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 CrossRefPubMedGoogle Scholar
  29. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  30. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  31. 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 CrossRefPubMedGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  34. 34.
    ter Braak CJF, Smilauer P (2012) CANOCO reference manual and user’s guide to CANOCO for windows. Centre for Biometry, WageningenGoogle Scholar
  35. 35.
    Jan L, Petr Š (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, CambridgeGoogle Scholar
  36. 36.
    Team RDC (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  37. 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 57:289–300Google Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  41. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  42. 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: 317-339Google Scholar
  43. 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 1130Google Scholar
  44. 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 44:846–849CrossRefGoogle Scholar
  45. 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)Google Scholar
  46. 46.
    Evans RD, Johansen JR (1999) Microbiotic crusts and ecosystem processes. Crit Rev Plant Sci 18:183–225. doi: 10.1080/07352689991309199 CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 373–397CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Kateřina Čapková
    • 1
    • 2
    Email author
  • Tomáš Hauer
    • 1
    • 2
  • Klára Řeháková
    • 2
    • 3
  • Jiří Doležal
    • 1
    • 2
  1. 1.Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  2. 2.Institute of BotanyAcademy of Sciences of the Czech RepublicTřeboňCzech Republic
  3. 3.Institute of HydrobiologyBiology Centre of AS CRČeské BudějoviceCzech Republic

Personalised recommendations