Abstract
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.
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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. https://doi.org/10.1006/qres.1997.1900
Matthews JA (1992) The ecology of recently-deglaciated terrain: a geoecological approach to glacier forelands and primary succession. Cambridge University Press, Cambridge
Bradley JA, Singarayer JS, Anesio AM (2014) Microbial community dynamics in the forefield of glaciers. Proc R Soc B 281:20140882. https://doi.org/10.1098/rspb.2014.0882
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 303–326
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. https://doi.org/10.1046/j.1365-2745.2003.00786.x
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. https://doi.org/10.1007/s00248-005-0246-4
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 55–80
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. https://doi.org/10.1007/s00300-016-1902-5
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 345–369
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. https://doi.org/10.1111/j.1574-6941.2008.00568.x
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 481–499
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. https://doi.org/10.1111/j.1469-8137.2010.03180.x
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. https://doi.org/10.1139/b06-131
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. https://doi.org/10.5141/ecoenv.2015.049
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. https://doi.org/10.1111/1574-6941.12105
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. https://doi.org/10.1007/s00248-011-9991-8
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. https://doi.org/10.1111/mec.13051
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. https://doi.org/10.1038/ismej.2015.238
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. https://doi.org/10.1007/s00248-006-9144-7
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 275:2793–2802. https://doi.org/10.1098/rspb.2008.0808
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. https://doi.org/10.1127/1864-1318/2005/0117-0427
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. https://doi.org/10.1088/1748-9326/8/1/015033
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. https://doi.org/10.1038/ismej.2007.53
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. https://doi.org/10.1093/nar/gks808
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. https://doi.org/10.1093/femsec/fiv143
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. https://doi.org/10.1111/jpy.12399
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.https://doi.org/10.1093/femsec/fiy042
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
ACIA (2005) Arctic climate impact assessment. Cambridge University Press, Cambridge
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. https://doi.org/10.2478/v10183-012-0025-0
Szczuciński W, Rachlewicz G (2007) Geological setting of the Petuniabukta region. Landf Anal 5:212–215
Rachlewicz G, Szczuciński W, Ewertowski M (2007) Post-‘Little Ice Age’ retreat rates of glaciers around Billefjorden in central Spitsbergen, Svalbard. Pol Polar Res 28:159–186
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
Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
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
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. https://doi.org/10.1371/journal.pone.0049334
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
Hoffmann L, Komárek J, Kaštovský (2005) System of cyanoprokaryotes (cyanobacteria)—state in 2004. Algol Stud 117:95–115. https://doi.org/10.1127/1864-1318/2005/0117-0095
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/aem.71.12.8228-8235.2005
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
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
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525. https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2
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. https://doi.org/10.1890/0012-9658(2006)87[2614:VPOSDM]2.0.CO;2
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
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. https://doi.org/10.1111/j.1529-8817.2006.00278.x
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. https://doi.org/10.1007/s10750-013-1473-1
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. https://doi.org/10.1073/pnas.0900885106
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. https://doi.org/10.1016/j.marenvres.2011.10.005
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
Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506. https://doi.org/10.1038/nrmicro2795
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. https://doi.org/10.5194/bg-10-3983-2013
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. https://doi.org/10.1111/jam.13332
Wilmotte A, Golubić S (1991) Morphological and genetic criteria in the taxonomy of Cyanophyta/cyanobacteria. Algol Stud 64:1–24
Fierer N, Nemergut DR, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642. https://doi.org/10.1016/j.resmic.2010.06.002
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
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
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
Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol Evol 27:219–225. https://doi.org/10.1016/j.tree.2011.09.012
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. https://doi.org/10.5194/bg-13-659-2016
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. https://doi.org/10.1890/07-0187.1
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. https://doi.org/10.1111/1462-2920.12762
Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175. https://doi.org/10.2307/2937039
Crocker RL, Major J (1955) Soil development in relation to vegetation and surface age at Glacier Bay, Alaska. J Ecol 43:427–448
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. https://doi.org/10.1007/s00248-002-2025-9
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. https://doi.org/10.1007/s00248-003-0189-6
Acknowledgements
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
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).
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Pessi, I.S., Pushkareva, E., Lara, Y. et al. Marked Succession of Cyanobacterial Communities Following Glacier Retreat in the High Arctic. Microb Ecol 77, 136–147 (2019). https://doi.org/10.1007/s00248-018-1203-3
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DOI: https://doi.org/10.1007/s00248-018-1203-3