[en] The Arctic region undergoes rapid climate change resulting in soil warming with
consequent changes in microbial community structure. Therefore, it is important to gain
more knowledge on the pioneer photosynthetic microorganisms and their relations to
environmental factors. Here we provide a description of the community composition
of microbial phototrophs in three different types of soils in the High Arctic (Svalbard):
vegetated soil at a raised marine terrace, biological soil crust (BSC) at high elevation,
and poorly-developed BSC in a glacier foreland. The studied sites differed from each
other in microclimatic conditions (soil temperature and soil water content), soil chemistry
and altitude. Combining morphological (cell biovolume) and molecular methods (NGS
amplicon sequencing of cyanobacterial 16S rRNA and eukaryotic 18S rRNA sequences
of isolates), we studied the diversity and biovolume of cyanobacteria and eukaryotic
microalgae. The results showed that cyanobacteria prevailed in the high altitude BSC
as well as in pioneering BSC samples in glacier foreland though with lower biomass.
More specifically, filamentous cyanobacteria, mainly Leptolyngbya spp., dominated the
BSCs from these two localities. In contrast, coccoid microalgae (green and yellow-green
algae) had higher biovolume in low altitude vegetated soils. Thus, the results of this study
contribute to a better understanding of microphototrophic communities in different types
of Arctic soil environments.
Wilmotte, Annick ; Université de Liège - ULiège > Département des sciences de la vie > Physiologie et génétique bactériennes
Laska, Kamil
Elster, Josef
Language :
English
Title :
Comparison of Microphototrophic Communities Living in Different Soil Environments in the High Arctic
Alternative titles :
[fr] Comparaison des communautés microbiennes phototrophes vivant dans différents environnements en Arctique
Publication date :
October 2019
Journal title :
Frontiers in Ecology and Evolution
eISSN :
2296-701X
Publisher :
Frontiers Media S.A., Switzerland
Volume :
7
Pages :
393
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
CCAMBIO, MICROBIAN, BIPOLES, PYROCYANO
Funders :
BELSPO - SPP Politique scientifique - Service Public Fédéral de Programmation Politique scientifique F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
ACIA (2005). Arctic Climate Impact Assessment. Cambridge: Cambridge University Press.
Ambrožová K., Láska K., (2017). Air temperature variability in the vertical profile over the coastal area of Petuniabukta, central Spitsbergen. 38, 41–60. 10.1515/popore-2017-0004
Belnap J., Lange O. L., (2003). Biological Soil Crusts: Structure, Function, and Management. Springer-Verlag. 10.1007/978-3-642-56475-8
Belnap J., Rosentreter R., Leonard S., Kaltenecker J. H., Williams J., Eldridge D., (2001). Biological Soil Crust: Ecology and Manangement. Ecology and Manangement of Microbiotic Soil Crusts. Denver, CO: United States Department of the Interior Bureau of Land Management National Science and Technology Center Information and Communications Group.
Borchhardt N., Baum C., Mikhailyuk T., Karsten U., (2017). Biological soil crusts of arctic svalbard-water availability as potential controlling factor for microalgal biodiversity. Front. Microbiol. 8:1485. 10.3389/fmicb.2017.0148528848507
Boutte C., Grubisic S., Balthasart P., Wilmotte A., (2006). Testing of primers for the study of cyanobacterial molecular diversity by DGGE. J. Microbiol. Methods 65, 542–550. 10.1016/j.mimet.2005.09.01716290299
Bowker M. A., Maestre F. T., Escolar C., (2010). Biological crusts as a model system for examining the biodiversity-ecosystem function relationship in soils. Soil Biol. Biochem. 42, 405–417. 10.1016/j.soilbio.2009.10.025
Büdel B., Colesie C., (2014). Biological soil crusts, in Antarctic Terrestrial Microbiology: Physical and Biological Properties of Antarctic Soil Habitats, ed Cowan D, (Berlin: Springer-Verlag), 131–161. 10.1007/978-3-642-45213-0_8
Büdel B., Dulić T., Darienko T., Rybalka N., Friedl T., (2016). Cyanobacteria and Algae of Biological Soil Crusts, in Biological Soil Crusts: An Organizing Principle in Drylands. Ecological Studies (Analysis and Synthesis), Vol. 226, eds Weber B., Büdel B., Belnap J., (Cham: Springer), 55–80. 10.1007/978-3-319-30214-0_4
Čapková K., Hauer T., Řeháková K., Doležal J., (2016). Some like it high! Phylogenetic diversity of high-elevation cyanobacterial community from biological soil crusts of western himalaya. Microb. Ecol. 71, 113–123. 10.1007/s00248-015-0694-426552394
Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K.. (2010). QIIME allows analysis of high- throughput community sequencing data. Nat. Publ. Gr. 7, 335–336. 10.1038/nmeth.f.30320383131
Cole J. R., Wang Q., Fish J. A., Chai B., McGarrell D. M., Sun Y.. (2014). Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, 633–642. 10.1093/nar/gkt124424288368
Colesie C., Green T. G. A., Türk R., Hogg I. D., Sancho L. G., Büdel B., (2014). Terrestrial biodiversity along the Ross Sea coastline, Antarctica: lack of a latitudinal gradient and potential limits of bioclimatic modeling. Polar Biol. 37, 1197–1208. 10.1007/s00300-014-1513-y
Edgar R. C., (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998. 10.1038/nmeth.260423955772
Elster J., (2002). Elster J., (2002). Ecological classification of terrestrial algal communities of polar environment, in Geoecology of Antarctic Ice-Free Coastal Landscapes, eds Beyer L., Bolter M., (Berlin; Heidelberg: Springer-Verlag), 303–326. 10.1007/978-3-642-56318-8_17
Elster J., Benson E., (2004). Life in polar terrestrial environmentawith a focus on algae and cyanobacteria, in Life in the Frozen State, eds Fuller B. J., Lane N., Benson E. E., (Florida, FL: CRC Press), 111–150. 10.1201/9780203647073.ch3
Elster J., Lukešová A., Svoboda J., Kopecký J., Kanda H., (1999). Diversity and abundance of soil algae in the polar desert, Sverdrup Pass, central Ellesmere Island. Polar Rec. 35:231. 10.1017/S0032247400015515
French H. M., (2007). The Periglacial Environment. 3d ed. Chichester: Wiley & Sons. 10.1002/9781118684931
Hall T. A., (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.
Hanáček M., Nývlt D., Flašar J., Stacke V., Mida P., Lehejček J.. (2013). New methods to reconstruct clast transport history in different glacial sedimentary environments: Case study for Old Red sandstone clasts from polythermal Hørbyebreen and Bertilbreen valley glaciers, Central Svalbard. Czech Polar Rep. 3, 107–129. 10.5817/CPR2013-2-13
Hillebrand H., Dürselen C. D., Kirschtel D., Pollingher U., Zohary T., (1999). Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 35, 403–424. 10.1046/j.1529-8817.1999.3520403.x
Housman D. C., Powers H. H., Collins A. D., Belnap J., (2006). Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan Desert. J. Arid Environ. 66, 620–634. 10.1016/j.jaridenv.2005.11.014
Hrbáček F., Láska K., Engel Z., (2016). Effect of snow cover on the active-layer thermal regime – a case study from James Ross Island, Antarctic Peninsula. Permafr. Periglac. Process. 27, 307–315. 10.1002/ppp.1871
Hu C., Gao K., Whitton B. A., (2012). Semi-arid regions and deserts, in Ecology of Cyanobacteria II: Their Diversity in Space and Time, ed Whitton B. A., (Springer Science+Business Media B.V.), 345–369. 10.1007/978-94-007-3855-3_12
Huang L., Zhang Z., Li X., (2014). Carbon fixation and its influence factors of biological soil crusts in a revegetated area of the Tengger Desert, northern China. J. Arid Land 6, 725–734. 10.1007/s40333-014-0027-3
Janatková K., Řeháková K., DoleŽal J., Šimek M., Chlumská Z., Dvorský M.. (2013). Community structure of soil phototrophs along environmental gradients in arid Himalaya. Environ. Microbiol. 15, 2505–2516. 10.1111/1462-2920.1213223647963
Kaštovská K., Elster J., Stibal M., Šantručková H., (2005). Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (high arctic). Microb. Ecol. 50, 396–407. 10.1007/s00248-005-0246-416328651
Kaštovská K., Stibal M., Šabacká M., Černá B., Šantručková H., Elster J., (2007). Microbial community structure and ecology of subglacial sediments in two polythermal Svalbard glaciers characterized by epifluorescence microscopy and PLFA. Polar Biol. 30, 277–287. 10.1007/s00300-006-0181-y
Katoh K., Standley D. M., (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. 10.1093/molbev/mst01023329690
Kipp V., (2004). Biodiversität und phylogenetische Stellung eukaryotischer Algen in kalzifizierenden Biofilmen (Diploma thesis). Universität Göttingen.
Langhans T. M., Storm C., Schwabe A., (2009). Biological soil crusts and their microenvironment: impact on emergence, survival and establishment of seedlings. Flora Morphol. Distrib. Funct. Ecol. Plants 204, 157–168. 10.1016/j.flora.2008.01.001
Langhans T. M., Storm C., Schwabe A., (2010). Regeneration processes of biological soil crusts, macro-cryptogams and vascular plant species after fine-scale disturbance in a temperate region: recolonization or successional replacement? Flora Morphol. Distrib. Funct. Ecol. Plants 205, 46–60. 10.1016/j.flora.2008.12.001
Láska K., Witoszová D., Prošek P., (2012). Weather patterns of the coastal zone of Petuniabukta, central Spitsbergen in the period 2008-2010. Polish Polar Res. 33, 297–318. 10.2478/v10183-012-0025-0
Leung A. K., Garg A., Ng C. W. W., (2015). Effects of plant roots on soil-water retention and induced suction in vegetated soil. Eng. Geol. 193, 183–197. 10.1016/j.enggeo.2015.04.017
Lozupone C., Knight R., (2005). UniFrac: a new phylogenetic method for comparing microbial communities unifrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235. 10.1128/AEM.71.12.8228-8235.200516332807
Martineau E., Wood S. A., Miller M. R., Jungblut A. D., Hawes I., Webster-Brown J.. (2013). Characterisation of Antarctic cyanobacteria and comparison with New Zealand strains. Hydrobiologia 711, 139–154. 10.1007/s10750-013-1473-1
McDonald D., Price M. N., Goodrich J., Nawrocki E. P., DeSantis T. Z., Probst A.. (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610–618. 10.1038/ismej.2011.13922134646
Nayak S., Prasanna R., (2007). Soil pH and its role in cyanobacterial abundance and diversity in rice field soils. Appl. Ecol. Environ. Res. 5, 103–113. 10.15666/aeer/0502_103113
Newsham K. K., Pearce D. A., Bridge P. D., (2010). Minimal influence of water and nutrient content on the bacterial community composition of a maritime Antarctic soil. Microbiol. Res. 165, 523–530. 10.1016/j.micres.2009.11.00520006478
Pessi I. S., Maalouf P., de C., Laughinghouse I. V. H. D, 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. 10.1111/jpy.1239927273529
Pessi I. S., Pushkareva E., Lara Y., Borderie F., Wilmotte A., Elster J., (2018). Marked succession of cyanobacterial communities following glacier retreat in the high Arctic. Microb. Ecol. 77, 136–147. 10.1007/s00248-018-1203-329796758
Philippot L., Raaijmakers J. M., Lemanceau P., Van Der Putten W. H., (2013). Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799. 10.1038/nrmicro310924056930
Pietrasiak N., Regus J. U., Johansen J. R., Lam D., Sachs J. L., Santiago L. S., (2013). Biological soil crust community types differ in key ecological functions. Soil Biol. Biochem. 65, 168–171. 10.1016/j.soilbio.2013.05.011
Prach K., Klimešová J., Košnar J., Redčenko O., Hais M., (2012). Variability of contemporary vegetation around Petuniabukta, central Spitsbergen. Polish Polar Res. 33, 383–394. 10.2478/v10183-012-0026-z
Pushkareva E., Elster J., (2013). Biodiversity and ecological classification of cryptogamic soil crusts in the vicinity of Petunia Bay, Svalbard. Czech Polar Rep. 3, 7–18. 10.5817/CPR2013-1-3
Pushkareva E., Johansen J. R., Elster J., (2016). A review of the ecology, ecophysiology and biodiversity of microalgae in Arctic soil crusts. Polar Biol. 39, 2227–2240. 10.1007/s00300-016-1902-5
Pushkareva E., Kvíderová J., Šimek M., Elster J., (2017). Nitrogen fixation and diurnal changes of photosynthetic activity in Arctic soil crusts at different development stage. Eur. J. Soil Biol. 79, 21–30. 10.1016/j.ejsobi.2017.02.002
Pushkareva E., Pessi I. S., Wilmotte A., Elster J., (2015). Cyanobacterial community composition in Arctic soil crusts at different stages of development. FEMS Microbiol. Ecol. 91:fiv143. 10.1093/femsec/fiv14326564957
Řeháková K., Chlumská Z., Doležal 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. 10.1007/s00248-011-9878-821643700
Richardson A. E., Simpson R. J., (2011). Soil microorganisms mediating phosphorus availability. Plant Physiol. 156, 989–996. 10.1104/pp.111.17544821606316
Rippin M., Borchhardt N., Williams L., Colesie C., Jung P., Büdel B.. (2018). Genus richness of microalgae and Cyanobacteria in biological soil crusts from Svalbard and Livingston Island: morphological versus molecular approaches. Polar Biol. 41, 909–923. 10.1007/s00300-018-2252-2
Stanier R. Y., Deruelles J., Rippka R., Herdman M., Waterbury J. B., (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111, 1–61. 10.1099/00221287-111-1-1
Stewart K. J., Grogan P., Coxson D. S., Siciliano S. D., (2014). Topography as a key factor driving atmospheric nitrogen exchanges in arctic terrestrial ecosystems. Soil Biol. Biochem. 70, 96–112. 10.1016/j.soilbio.2013.12.005
Szczucinski W., Rachlewicz G., (2007). Geological setting of the Petuniabukta Region. Landf. Anal. 5, 212–215.
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S., (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729. 10.1093/molbev/mst19724132122
Tashyreva D., Elster J., (2012). Production of dormant stages and stress resistance of polar cyanobacteria, in Life on Earth and Other Planetary Bodies, Cellular Origin, Life in Extreme Habitats and Astrobiology, eds Hanslmeier A., Kempe S., Seckbach J., (Dordrecht: Springer Science+Business Media Dordrecht), 367–386. 10.1007/978-94-007-4966-5_21
Taton A., Grubisic S., Ertz D., Hodgson D. A., Piccardi R., Biondi N.. (2006). Polyphasic study of antarctic cyanobacterial strains. J. Phycol. 42, 1257–1270. 10.1111/j.1529-8817.2006.00278.x
Tillett D., Neilan B. A., (2000). Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. J. Phycol. 36, 251–258. 10.1046/j.1529-8817.2000.99079.x
Westermann S., Lüers J., Langer M., Piel K., Boike J., (2009). The annual surface energy budget of a high-arctic permafrost site on Svalbard, Norway. Cryosph 3, 245–263. 10.5194/tc-3-245-2009
White T. J., Bruns T., Lee S., Taylor J., (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in PCR Protocols, eds Innis M. A., Gelfand D. H., Sninsky J. J., White T. J., (Academic Press), 315-322. 10.1016/B978-0-12-372180-8.50042-1
Williams L., Loewen-Schneider K., Maier S., Büdel B., (2016). Cyanobacterial diversity of western European biological soil crusts along a latitudinal gradient. FEMS Microbiol. Ecol. 92:fiw157. 10.1093/femsec/fiw15727411981
Yilmaz M., Phlips E. J., Tillett D., (2009). Improved methods for the isolation of cyanobacterial dna from environmental samples. J. Phycol. 45, 517–521. 10.1111/j.1529-8817.2009.00651.x27033829
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. N. Phytol. 186, 451–460. 10.1111/j.1469-8137.2010.03180.x20136719