Marked Succession of Cyanobacterial Communities Following Glacier Retreat in the High Arctic
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.
KeywordsCyanobacteria 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.
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).
- 2.Matthews JA (1992) The ecology of recently-deglaciated terrain: a geoecological approach to glacier forelands and primary succession. Cambridge University Press, CambridgeGoogle Scholar
- 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
- 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
- 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. https://doi.org/10.1098/rspb.2008.0808 CrossRefPubMedGoogle Scholar
- 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 https://doi.org/10.1016/j.syapm.2018.01.006
- 29.ACIA (2005) Arctic climate impact assessment. Cambridge University Press, CambridgeGoogle Scholar
- 31.Szczuciński W, Rachlewicz G (2007) Geological setting of the Petuniabukta region. Landf Anal 5:212–215Google Scholar
- 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.Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424. https://doi.org/10.1046/j.1529-8817.1999.3520403.x CrossRefGoogle Scholar
- 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. https://doi.org/10.1128/AEM.69.9.5157-5169.2003 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1038/ismej.2011.139 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
- 42.Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x CrossRefGoogle Scholar
- 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. https://doi.org/10.1371/journal.pone.0076376 CrossRefPubMedPubMedCentralGoogle Scholar
- 55.Wilmotte A, Golubić S (1991) Morphological and genetic criteria in the taxonomy of Cyanophyta/cyanobacteria. Algol Stud 64:1–24Google Scholar
- 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. https://doi.org/10.1186/s12864-016-2846-4 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1128/genomea.01546-16 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1038/ismej.2010.100 CrossRefPubMedGoogle Scholar