Microbial Ecology

, Volume 77, Issue 1, pp 136–147 | Cite as

Marked Succession of Cyanobacterial Communities Following Glacier Retreat in the High Arctic

  • Igor S. PessiEmail author
  • Ekaterina Pushkareva
  • Yannick Lara
  • Fabien Borderie
  • Annick Wilmotte
  • Josef Elster
Soil Microbiology


Cyanobacteria are important colonizers of recently deglaciated proglacial soil but an in-depth investigation of cyanobacterial succession following glacier retreat has not yet been carried out. Here, we report on the successional trajectories of cyanobacterial communities in biological soil crusts (BSCs) along a 100-year deglaciation gradient in three glacier forefields in central Svalbard, High Arctic. Distance from the glacier terminus was used as a proxy for soil age (years since deglaciation), and cyanobacterial abundance and community composition were evaluated by epifluorescence microscopy and pyrosequencing of partial 16S rRNA gene sequences, respectively. Succession was characterized by a decrease in phylotype richness and a marked shift in community structure, resulting in a clear separation between early (10–20 years since deglaciation), mid (30–50 years), and late (80–100 years) communities. Changes in cyanobacterial community structure were mainly connected with soil age and associated shifts in soil chemical composition (mainly moisture, SOC, SMN, K, and Na concentrations). Phylotypes associated with early communities were related either to potentially novel lineages (< 97.5% similar to sequences currently available in GenBank) or lineages predominantly restricted to polar and alpine biotopes, suggesting that the initial colonization of proglacial soil is accomplished by cyanobacteria transported from nearby glacial environments. Late communities, on the other hand, included more widely distributed genotypes, which appear to establish only after the microenvironment has been modified by the pioneering taxa.


Cyanobacteria Glacier forefield High Arctic High-throughput sequencing Primary succession Proglacial soil 



IS Pessi is a PhD FRIA fellow and A Wilmotte is a Research Associate of the FRS-FNRS. The authors would like to thank J Kavan for the help setting up the sampling strategy and L Cappelatti, HD Laughinghouse IV, PB Costa, E Verleyen, A Corato, T Gerards, and F Franck for the valuable suggestions and discussion.

Funding information

This work was supported by the Ministry of Education, Youth, and Sports of the Czech Republic (grants LM2010009 and RVO67985939) and the Belgian National Fund for Scientific Research (FRS-FNRS) under the projects PYROCYANO (grant CRCH1011-1513911) and BIPOLES (grant FRFC2457009).

Supplementary material

248_2018_1203_MOESM1_ESM.docx (2.2 mb)
ESM 1 (DOCX 2.19 mb)


  1. 1.
    Dowdeswell JA, Hagen JO, Björnsson H, Glazovsky AF, Harrison WD, Holmlund P, Jania J, Koerner RM, Lefauconnier B, Ommanney CSL, Thomas RH (1997) The mass balance of circum-Arctic glaciers and recent climate change. Quat Res 48:1–14. CrossRefGoogle Scholar
  2. 2.
    Matthews JA (1992) The ecology of recently-deglaciated terrain: a geoecological approach to glacier forelands and primary succession. Cambridge University Press, CambridgeGoogle Scholar
  3. 3.
    Bradley JA, Singarayer JS, Anesio AM (2014) Microbial community dynamics in the forefield of glaciers. Proc R Soc B 281:20140882. CrossRefPubMedGoogle Scholar
  4. 4.
    Elster J (2002) Ecological classification of terrestrial algal communities in polar environments. In: Beyer L, Bölter M (eds) Geoecology of Antarctic ice-free coastal landscapes. Springer-Verlag, Berlin, pp 303–326CrossRefGoogle Scholar
  5. 5.
    Hodkinson ID, Coulson SJ, Webb NR (2003) Community assembly along proglacial chronosequences in the high Arctic: vegetation and soil development in north-west Svalbard. J Ecol 91:651–663. CrossRefGoogle Scholar
  6. 6.
    Kaštovská K, Elster J, Stibal M, Šantrůčková H (2005) Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (High Arctic). Microb Ecol 50:396–407. CrossRefPubMedGoogle Scholar
  7. 7.
    Büdel B, Dulić T, Darienko T, Rybalka N, Friedl T (2016) Cyanobacteria and algae of biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer International Publishing, Cham, pp 55–80CrossRefGoogle Scholar
  8. 8.
    Pushkareva E, Johansen JR, Elster J (2016) A review of the ecology, ecophysiology and biodiversity of microalgae in Arctic soil crusts. Polar Biol 39:2227–2240. CrossRefGoogle Scholar
  9. 9.
    Hu C, Gao K, Whitton BA (2002) Semi-arid regions and deserts. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer, Dordrecht, pp 345–369Google Scholar
  10. 10.
    Knowles EJ, Castenholz RW (2008) Effect of exogenous extracellular polysaccharides on the desiccation and freezing tolerance of rock-inhabiting phototrophic microorganisms. FEMS Microbiol Ecol 66:261–270. CrossRefPubMedGoogle Scholar
  11. 11.
    Castenholz RW, Garcia-Pichel F (2002) Cyanobacterial responses to UV radiation. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer, Dordrecht, pp 481–499Google Scholar
  12. 12.
    Yoshitake S, Uchida M, Koizumi H, Kanda H, Nakatsubo T (2010) Production of biological soil crusts in the early stage of primary succession on a High Arctic glacier foreland. New Phytol 186:451–460. CrossRefPubMedGoogle Scholar
  13. 13.
    Breen K, Lévesque E (2006) Proglacial succession of biological soil crusts and vascular plants: biotic interactions in the High Arctic. Can J Bot 84:1714–1731. CrossRefGoogle Scholar
  14. 14.
    Kwon HY, Jung JY, Kim O, Laffly D, Lim HS, Lee YK (2015) Soil development and bacterial community shifts along the chronosequence of the Midtre Lovénbreen glacier foreland in Svalbard. Ecol Environ 38:461–476. CrossRefGoogle Scholar
  15. 15.
    Bajerski F, Wagner D (2013) Bacterial succession in Antarctic soils of two glacier forefields on Larsemann Hills, East Antarctica. FEMS Microbiol Ecol 85:128–142. CrossRefPubMedGoogle Scholar
  16. 16.
    Zumsteg A, Luster J, Göransson H, Smittenberg RH, Brunner I, Bernasconi SM, Zeyer J, Frey B (2012) Bacterial, archaeal and fungal succession in the forefield of a receding glacier. Microb Ecol 63:552–564. CrossRefPubMedGoogle Scholar
  17. 17.
    Rime T, Hartmann M, Brunner I, Widmer F, Zeyer J, Frey B (2015) Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Mol Ecol 24:1091–1108. CrossRefPubMedGoogle Scholar
  18. 18.
    Rime T, Hartmann M, Frey B (2016) Potential sources of microbial colonizers in an initial soil ecosystem after retreat of an alpine glacier. ISME J 10:1625–1641. CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microb Ecol 53:110–122. CrossRefPubMedGoogle Scholar
  20. 20.
    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 275:2793–2802. CrossRefPubMedGoogle Scholar
  21. 21.
    Turicchia S, Ventura S, Schütte U, Soldati E, Zielke M, Solheim B (2005) Biodiversity of the cyanobacterial community in the foreland of the retreating glacier Midtre Lovènbreen, Spitsbergen, Svalbard. Algol Stud 117:427–440. CrossRefGoogle Scholar
  22. 22.
    Frey B, Bühler L, Schmutz S, Zumsteg A, Furrer G (2013) Molecular characterization of phototrophic microorganisms in the forefield of a receding glacier in the Swiss Alps. Environ Res Lett 8:15033. CrossRefGoogle Scholar
  23. 23.
    Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, FAO C, Farmerie GW, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1. CrossRefPubMedGoogle Scholar
  25. 25.
    Pushkareva E, Pessi IS, Wilmotte A, Elster J (2015) Cyanobacterial community composition in Arctic soil crusts at different stages of development. FEMS Microbiol Ecol 91:fiv143. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Pessi IS, Maalouf PC, Laughinghouse IV HD, Baurain D, Wilmotte A (2016) On the use of high-throughput sequencing for the study of cyanobacterial diversity in Antarctic aquatic mats. J Phycol 52:356–368. CrossRefPubMedGoogle Scholar
  27. 27.
    Pessi IS, Lara Y, Durieu B, Maalouf PC, Verleyen E, Wilmotte A (2018) Community structure and distribution of benthic cyanobacteria in Antarctic lacustrine microbial mats. FEMS Microbiol Ecol 94:fiy042. CrossRefGoogle Scholar
  28. 28.
    Pushkareva E, Pessi IS, Namsaraev Z, Mano M-J, Elster J, Wilmotte A (2018) Cyanobacteria inhabiting biological soil crusts of a polar desert: Sør Rondane Mountains, Antarctica. Syst Appl Microbiol
  29. 29.
    ACIA (2005) Arctic climate impact assessment. Cambridge University Press, CambridgeGoogle Scholar
  30. 30.
    Láska K, Witoszová D, Prošek P (2012) Weather patterns of the coastal zone of Petuniabukta, central Spitsbergen in the period 2008–2010. Pol Polar Res 33:297–318. CrossRefGoogle Scholar
  31. 31.
    Szczuciński W, Rachlewicz G (2007) Geological setting of the Petuniabukta region. Landf Anal 5:212–215Google Scholar
  32. 32.
    Rachlewicz G, Szczuciński W, Ewertowski M (2007) Post-‘Little Ice Age’ retreat rates of glaciers around Billefjorden in central Spitsbergen, Svalbard. Pol Polar Res 28:159–186Google Scholar
  33. 33.
    Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424. CrossRefGoogle Scholar
  34. 34.
    Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332PubMedPubMedCentralGoogle Scholar
  35. 35.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. CrossRefPubMedGoogle Scholar
  36. 36.
    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. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Lanzén A, Jørgensen SL, Huson DH, Gorfer M, Grindhaug SH, Jonassen I, Øvreås L, Urich T (2012) CREST—classification resources for environmental sequence tags. PLoS One 7:e49334. CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618. CrossRefPubMedGoogle Scholar
  39. 39.
    Hoffmann L, Komárek J, Kaštovský (2005) System of cyanoprokaryotes (cyanobacteria)—state in 2004. Algol Stud 117:95–115. CrossRefGoogle Scholar
  40. 40.
    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. CrossRefGoogle Scholar
  43. 43.
    Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525.[0511:CAOPCA]2.0.CO;2CrossRefGoogle Scholar
  44. 44.
    Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625.[2614:VPOSDM]2.0.CO;2CrossRefPubMedGoogle Scholar
  45. 45.
    Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. CrossRefGoogle Scholar
  47. 47.
    Taton A, Grubisic S, Ertz D, Hodgson DA, Piccardi R, Biondi N, Tredici MR, Mainini M, Losi D, Marinelli F, Wilmotte A (2006) Polyphasic study of Antarctic cyanobacterial strains. J Phycol 42:1257–1270. CrossRefGoogle Scholar
  48. 48.
    Martineau E, Wood SA, Miller MR, Jungblut AD, Hawes I, Webster-Brown J, Packer MA (2013) Characterisation of Antarctic cyanobacteria and comparison with New Zealand strains. Hydrobiologia 711:139–154. CrossRefGoogle Scholar
  49. 49.
    Bosak T, Liang B, Sim MS, Petroff AP (2009) Morphological record of oxygenic photosynthesis in conical stromatolites. Proc Natl Acad Sci U S A 106:10939–10943. CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Lopes VR, Ramos V, Martins A, Sousa M, Welker M, Antunes A, Vasconcelos VM (2012) Phylogenetic, chemical and morphological diversity of cyanobacteria from Portuguese temperate estuaries. Mar Environ Res 73:7–16. CrossRefPubMedGoogle Scholar
  51. 51.
    Saw JHW, Schatz M, Brown MV, Kunkel DD, Foster JS, Shick H, Christensen S, Hou S, Wan X, Donachie SP (2013) Cultivation and complete genome sequencing of Gloeobacter kilaueensis sp. nov., from a lava cave in Kīlauea Caldera, Hawai'i. PLoS One 8:e76376. CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506. CrossRefPubMedGoogle Scholar
  53. 53.
    Schulz S, Brankatschk R, Dümig A, Kögel-Knabner I, Schloter M, Zeyer J (2013) The role of microorganisms at different stages of ecosystem development for soil formation. Biogeosciences 10:3983–3996. CrossRefGoogle Scholar
  54. 54.
    Gaget V, Keulen A, Lau M, Monis P, Brookes JD (2016) DNA extraction from benthic cyanobacteria: comparative assessment and optimization. J Appl Microbiol 122:294–304. CrossRefPubMedGoogle Scholar
  55. 55.
    Wilmotte A, Golubić S (1991) Morphological and genetic criteria in the taxonomy of Cyanophyta/cyanobacteria. Algol Stud 64:1–24Google Scholar
  56. 56.
    Fierer N, Nemergut DR, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642. CrossRefPubMedGoogle Scholar
  57. 57.
    Chrismas NAM, Barker G, Anesio AM, Sánchez-Baracaldo P (2016) Genomic mechanisms for cold tolerance and production of exopolysaccharides in the Arctic cyanobacterium Phormidesmis priestleyi BC1401. BMC Genomics 17:533. CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Lara Y, Durieu B, Cornet L, Verlaine O, Rippka R, Pessi IS, Misztak A, Joris B, Javaux EJ, Baurain D, Wilmotte A (2017) Draft genome sequence of the axenic strain Phormidesmis priestleyi ULC007, a cyanobacterium isolated from Lake Bruehwiler (Larsemann Hills, Antarctica). Genome Announc 5:e01546–e01516. CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Edwards A, Anesio AM, Rassner SM, Sattler B, Hubbard B, Perkins WT, Young M, Griffith GW (2011) Possible interactions between bacterial diversity, microbial activity and supraglacial hydrology of cryoconite holes in Svalbard. ISME J 5:150–160. CrossRefPubMedGoogle Scholar
  60. 60.
    Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol Evol 27:219–225. CrossRefPubMedGoogle Scholar
  61. 61.
    Vonnahme TR, Devetter M, Žárský JD, Šabacká M, Elster J (2016) Controls on microalgal community structures in cryoconite holes upon high-Arctic glaciers, Svalbard. Biogeosciences 13:659–674. CrossRefGoogle Scholar
  62. 62.
    Hodson A, Anesio AM, Tranter M, Fountain A, Mark O, Priscu J, Laybourn-Parry J, Sattler B (2008) Glacial ecosystems. Ecol Monogr 78:41–67. CrossRefGoogle Scholar
  63. 63.
    Freedman Z, Zak DR (2015) Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long-term chronosequence. Environ Microbiol 17:3208–3218. CrossRefPubMedGoogle Scholar
  64. 64.
    Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175. CrossRefGoogle Scholar
  65. 65.
    Crocker RL, Major J (1955) Soil development in relation to vegetation and surface age at Glacier Bay, Alaska. J Ecol 43:427–448CrossRefGoogle Scholar
  66. 66.
    Sigler WV, Crivii S, Zeyer J (2002) Bacterial succession in glacial forefield soils characterized by community structure, activity and opportunistic growth dynamics. Microb Ecol 44:306–316. CrossRefPubMedGoogle Scholar
  67. 67.
    Sigler WV, Zeyer J (2004) Colony-forming analysis of bacterial community succession in deglaciated soils indicates pioneer stress-tolerant opportunists. Microb Ecol 48:316–323. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Igor S. Pessi
    • 1
    • 2
    Email author
  • Ekaterina Pushkareva
    • 3
  • Yannick Lara
    • 1
    • 4
  • Fabien Borderie
    • 1
    • 5
  • Annick Wilmotte
    • 1
  • Josef Elster
    • 3
    • 6
  1. 1.InBioS – Centre for Protein EngineeringUniversity of LiègeLiègeBelgium
  2. 2.Department of MicrobiologyUniversity of HelsinkiHelsinkiFinland
  3. 3.Centre for Polar EcologyUniversity of South BohemiaČeské BudějoviceCzech Republic
  4. 4.UR Geology – Palaeobiogeology-Palaeobotany-PalaeopalynologyUniversity of LiègeLiègeBelgium
  5. 5.Laboratoire Chrono-environnement, UMR 6249 CNRS Université Bourgogne Franche-Comté UsC INRABesançonFrance
  6. 6.Institute of Botany, Academy of Sciences of the Czech RepublicTřeboňCzech Republic

Personalised recommendations