Polar Biology

, Volume 41, Issue 5, pp 909–923 | Cite as

Genus richness of microalgae and Cyanobacteria in biological soil crusts from Svalbard and Livingston Island: morphological versus molecular approaches

  • Martin RippinEmail author
  • Nadine Borchhardt
  • Laura Williams
  • Claudia Colesie
  • Patrick Jung
  • Burkhard Büdel
  • Ulf Karsten
  • Burkhard Becker
Original Paper


Biological soil crusts (BSCs) are key components of polar ecosystems. These complex communities are important for terrestrial polar habitats as they include major primary producers that fix nitrogen, prevent soil erosion and can be regarded as indicators for climate change. To study the genus richness of microalgae and Cyanobacteria in BSCs, two different methodologies were employed and the outcomes were compared: morphological identification using light microscopy and the annotation of ribosomal sequences taken from metatranscriptomes. The analyzed samples were collected from Ny-Ålesund, Svalbard, Norway, and the Juan Carlos I Antarctic Base, Livingston Island, Antarctica. This study focused on the following taxonomic groups: Klebsormidiophyceae, Chlorophyceae, Trebouxiophyceae, Xanthophyceae and Cyanobacteria. In total, combining both approaches, 143 and 103 genera were identified in the Arctic and Antarctic samples, respectively. Furthermore, both techniques concordantly determined 15 taxa in the Arctic and 7 taxa in the Antarctic BSC. In general, the molecular analysis indicated a higher microalgal and cyanobacterial genus richness (about 11 times higher) than the morphological approach. In terms of eukaryotic algae, the two sampling sites displayed comparable genus counts while the cyanobacterial genus richness was much higher in the BSC from Ny-Ålesund. For the first time, the presence of the genera Chloroidium, Ankistrodesmus and Dunaliella in polar regions was determined by the metatranscriptomic analysis. Overall, these findings illustrate that only the combination of morphological and molecular techniques, in contrast to one single approach, reveals higher genus richness for complex communities such as polar BSCs.


Biological soil crust Eukaryotic algae Cyanobacteria Morphological identification Metatranscriptomics 



This study was funded by the Deutsche Forschungsgemeinschaft (DFG) within the project ‘Polarcrust’ (BE1779/18-1, KA899/23-1, BU666/17-1) which is part of the Priority Program 1158 ‘Antarctic Research’. We also thank the AWIPEW station, the Instituto Antártico Chileno, the Spanish Antarctic Committee and the Juan Carlos I Antarctic Base for their logistic support. Sampling and research activities were approved by the German authorities (Umwelt Bundesamt: Biological soil crust algae from the polar regions; 24.09.2014).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

300_2018_2252_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 12 kb)
300_2018_2252_MOESM2_ESM.xlsx (44 kb)
Supplementary material 2 (XLSX 43 kb)


  1. Albrecht M, Pröschold T, Schumann R (2017) Identification of Cyanobacteria in a eutrophic coastal lagoon on the Southern Baltic coast. Front Microbiol 8:923. PubMedPubMedCentralCrossRefGoogle Scholar
  2. An SS, Friedel T, Hegewald E (1999) Phylogenetic relationships of Scenedesmus and Scenedesmus-like coccoid green algae as inferred from ITS-2 rDNA sequence comparison. Plant Biol 1:418–428. CrossRefGoogle Scholar
  3. Andreyeva V, Kurbatova L (2014) Terrestrial and aerophilic nonmotile green microalgae (Chlorophyta) from regions of investigation of Russian Antarctic expedition. Nov Sist Nizsh Rast 46:12–26Google Scholar
  4. Bañón M, Justel A, Velázquez D, Quesada A (2013) Regional weather survey on Byers Peninsula, Livingston Island, South Shetland Islands, Antarctica. Antarct Sci 25:146–156. CrossRefGoogle Scholar
  5. Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178. CrossRefGoogle Scholar
  6. Belnap J, Büdel B, Lange OL (2001a) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 3–30CrossRefGoogle Scholar
  7. Belnap J, Rosentreter R, Leonard S et al (2001b) Biological soil crusts: Ecology and management. US Department of the Interior, Bureau of Land Management, National Science and Technology Center, DenverGoogle Scholar
  8. Bentley DR, Balasubramanian S, Swerdlow HP et al (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456:53–59. PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bischoff H, Bold H (1963) Some soil algae from enchanted rock and related algal species. Univiversity of Texas Publications, AustinGoogle Scholar
  10. Bock C, Krienitz L, Pröschold T (2011) Taxonomic reassessment of the genus Chlorella (Trebouxiophyceae) using molecular signatures (barcodes), including description of seven new species. Fottea 11:293–312. CrossRefGoogle Scholar
  11. Bold HC (1942) The cultivation of algae. Bot Rev 8:69–138CrossRefGoogle Scholar
  12. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. PubMedPubMedCentralCrossRefGoogle Scholar
  13. Borchhardt N, Baum C, Mikhailyuk T, Karsten U (2017a) Biological soil crusts of Arctic Svalbard—Water availability as potential controlling factor for microalgal biodiversity. Front Microbiol 8:1485. PubMedPubMedCentralCrossRefGoogle Scholar
  14. Borchhardt N, Schiefelbein U, Abarca N et al (2017b) Diversity of algae and lichens in biological soil crusts of Ardley and King George Island, Antarctica. Antarct Sci 29:229–237CrossRefGoogle Scholar
  15. Borie I, Ibraheem M (2003) Preliminary survey of microalgal soil crusts in a xeric habitats (Wadi-Araba, eastern desert, Egypt). Egypt J Phycol 4:17–33Google Scholar
  16. Breen K, Lévesque E (2008) The influence of biological soil crusts on soil characteristics along a high Arctic glacier foreland, Nunavut, Canada. Arctic Antarct Alp Res 40:287–297. CrossRefGoogle Scholar
  17. Broady PA (1976) Six new species of terrestrial algae from Signy Island, South Orkney Islands, Antarctica. Br Phycol J 11:387–405. CrossRefGoogle Scholar
  18. Broady P (1986) Ecology and taxonomy of the terrestrial algae of the Vestfold Hills. In: Pickard J (ed) Antarctic oasis: terrestrial environments and history of the Vestfold Hills. Academic Press, North Ryde, pp 165–202Google Scholar
  19. Buchheim MA, Chapman RL (1991) Phylogeny of the colonial green flagellates: a study of 18S and 26S rRNA sequence data. BioSystems 25:85–100. PubMedCrossRefGoogle Scholar
  20. Büdel B (2001) Synopsis: comparative biogeography of soil-crust biota. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 141–152CrossRefGoogle Scholar
  21. Büdel B, Darienko T, Deutschewitz K et al (2009) Southern African biological soil crusts are ubiquitous and highly diverse in drylands, being restricted by rainfall frequency. Microb Ecol 57:229–247. PubMedCrossRefGoogle Scholar
  22. Büdel B, Dulic T, Darienko T et al (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, Switzerland, pp 55–80CrossRefGoogle Scholar
  23. Casamatta DA, Johansen JR, Vis ML, Broadwater ST (2005) Molecular and morphological characterization of ten polar and near-polar strains within the Oscillatoriales (Cyanobacteria). J Phycol 41:421–438. CrossRefGoogle Scholar
  24. Champenois J, Marfaing H, Pierre R (2015) Review of the taxonomic revision of Chlorella and consequences for its food uses in Europe. J Appl Phycol 27:1845–1851. CrossRefGoogle Scholar
  25. Chi W, Zheng L, He C et al (2017) Quorum sensing of microalgae associated marine Ponticoccus sp. PD-2 and its algicidal function regulation. AMB Express 7:59. PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chown S, Huiskes A, Gremmen N et al (2012) Continent-wide risk assessment for the establishment of nonindigenous species in Antarctica. PNAS 109:4938–4943PubMedPubMedCentralCrossRefGoogle Scholar
  27. Colesie C, Gommeaux M, Green TGA, Büdel B (2014a) Biological soil crusts in continental Antarctica: garwood Valley, southern Victoria Land, and Diamond Hill, Darwin Mountains region. Antarct Sci 26:115–123. CrossRefGoogle Scholar
  28. Colesie C, Green TGA, Türk R et al (2014b) Terrestrial biodiversity along the Ross Sea coastline, Antarctica: lack of a latitudinal gradient and potential limits of bioclimatic modeling. Polar Biol 37:1197–1208. CrossRefGoogle Scholar
  29. Concostrina-Zubiri L, Huber-Sannwald E, Martínez I et al (2013) Biological soil crusts greatly contribute to small-scale soil heterogeneity along a grazing gradient. Soil Biol Biochem 64:28–36. CrossRefGoogle Scholar
  30. Cooper E, Wookey P (2001) Field measurements of the growth rates of forage lichens, and the implications of grazing by Svalbard reindeer. Symbiosis 31:173–186Google Scholar
  31. Cox EJ (1996) Identification of freshwater diatoms from live material. Chapman & Hall, LondonGoogle Scholar
  32. Cumbers J, Rothschild LJ (2014) Salt tolerance and polyphyly in the cyanobacterium Chroococcidiopsis (Pleurocapsales). J Phycol 50:472–482. PubMedCrossRefGoogle Scholar
  33. Czerwik-Marcinkowska J, Massalski A, Olech M, Wojciechowska A (2015) Morphology, ultrastructure and ecology of Muriella decolor (Chlorophyta) from subaerial habitats in Poland and the Antarctic. Polish Polar Res 36:163–174. CrossRefGoogle Scholar
  34. Darienko T, Gustavs L, Eggert A et al (2015) Evaluating the species boundaries of green microalgae (Coccomyxa, Trebouxiophyceae, Chlorophyta) using integrative taxonomy and DNA barcoding with further implications for the species identification in environmental samples. PLoS ONE 10:e0127838. PubMedPubMedCentralCrossRefGoogle Scholar
  35. de Wever A, Leliaert F, Verleyen E et al (2009) Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proc R Soc B Biol Sci 276:3591–3599. CrossRefGoogle Scholar
  36. Dojani S, Kauff F, Weber B, Büdel B (2014) Genotypic and phenotypic diversity of Cyanobacteria in biological soil crusts of the succulent Karoo and Nama Karoo of Southern Africa. Microb Ecol 67:286–301. PubMedCrossRefGoogle Scholar
  37. Doyle JJ, Doyle JL, Ballenger JA et al (1997) A phylogeny of the chloroplast gene rbcL in the Leguminosae: taxonomic correlations and insights into the evolution of nodulation. Am J Bot 84:541–554. PubMedCrossRefGoogle Scholar
  38. Elferink S, Neuhaus S, Wohlrab S et al (2017) Molecular diversity patterns among various phytoplankton size-fractions in West Greenland in late summer. Deep Res Part I Oceanogr Res Pap 121:54–69. CrossRefGoogle Scholar
  39. Elster J, Lukesova A, Svoboda J et al (1999) Diversity and abundance of soil algae in the polar desert, Sverdrup Pass, central Ellesmere Island. Polar Rec 35:231–254 (Gr Brit) CrossRefGoogle Scholar
  40. Ettl H, Gärtner G (2014) Syllabus der Boden-, Luft- und FlechtenalgenGoogle Scholar
  41. Evans RD, Johansen JR (1999) Microbiotic crusts and ecosystem processes. CRC Crit Rev Plant Sci 18:183–225. CrossRefGoogle Scholar
  42. Evans KM, Wortley AH, Mann DG (2007) An assessment of potential diatom “barcode” genes (cox1, rbcL, 18S and ITS rDNA) and their effectiveness in determining relationships in Sellaphora (Bacillariophyta). Protist 158:349–364. PubMedCrossRefGoogle Scholar
  43. Førland EJ, Benestad R, Hanssen-Bauer I et al (2011) Temperature and precipitation development at Svalbard 1900–2100. Adv Meteorol. CrossRefGoogle Scholar
  44. Frenot Y, Chown SL, Whinam J et al (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biol Rev 80:45–72. PubMedCrossRefGoogle Scholar
  45. Geisen S, Tveit AT, Clark IM et al (2015) Metatranscriptomic census of active protists in soils. ISME J 9:2178–2190. PubMedPubMedCentralCrossRefGoogle Scholar
  46. Geitler L (1932) Cyanophyceae. Akadademische Verlagsgesellschaft M.B.H, LeipzigGoogle Scholar
  47. Giełwanowska I, Olech M (2012) New ultrastructural and physiological features of the thallus in Antarctic lichens. Acta Biol Cracoviensia Ser Bot 54:40–52. CrossRefGoogle Scholar
  48. Greaves MP, Wilson MJ (1970) The degradation of nucleic acids and montmorillonite-nucleic-acid complexes by soil microorganisms. Soil Biol Biochem 2:257–268CrossRefGoogle Scholar
  49. Hall JD, Fucikova K, Lo C et al (2010) An assessment of proposed DNA barcodes in freshwater green algae. Cryptogam Algol 31:529–555Google Scholar
  50. Hodač L, Hallmann C, Spitzer K et al (2016) Widespread green algae Chlorella and Stichococcus exhibit polar-temperate and tropical-temperate biogeography. FEMS Microbiol Ecol 92:1–16. CrossRefGoogle Scholar
  51. Hoham R (1975) Optimum temperatures and temperature ranges for growth of snow algae. Arct Alp Res 7:13–24CrossRefGoogle Scholar
  52. Holzinger A, Karsten U (2013) Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological, and molecular mechanisms. Front Plant Sci 4:327. PubMedPubMedCentralCrossRefGoogle Scholar
  53. John DM, Whitton BA, Brook AJ (2002) The freshwater algal flora of the British Isles: an identification guide to freshwater and terrestrial algae. Cambridge University Press, New YorkGoogle Scholar
  54. Jones AK, Rhodes ME, Evans SC (1973) The use of antibiotics to obtain axenic cultures of algae. Br Phycol J 8:185–196. CrossRefGoogle Scholar
  55. Kastovská K, Elster J, Stibal M, Santrůcková H (2005) Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (High Arctic). Microb Ecol 50:396–407. PubMedCrossRefGoogle Scholar
  56. Kawasaki Y, Nakada T, Tomita M (2015) Taxonomic revision of oil-producing green algae, Chlorococcum oleofaciens (Volvocales, Chlorophyceae), and its relatives. J Phycol 51:1000–1016. PubMedCrossRefGoogle Scholar
  57. Kawecka B (1986) Ecology of snow algae. Polish Polar Res 7:407–415Google Scholar
  58. Kim M, Cho A, Lim HS et al (2015) Highly heterogeneous soil bacterial communities around Terra Nova Bay of Northern Victoria Land, Antarctica. PLoS ONE 10:e0119966. PubMedPubMedCentralCrossRefGoogle Scholar
  59. Klimke W, O’Donovan C, White O et al (2011) Solving the problem: genome annotation standards before the data deluge. Stand Genom Sci 5:168–193. CrossRefGoogle Scholar
  60. Komárek J (2016) Review of the cyanobacterial genera implying planktic species after recent taxonomic revisions according to polyphasic methods: state as of 2014. Hydrobiologia 764:259–270. CrossRefGoogle Scholar
  61. Komárek J, Anagnostidis K (1998) Freshwater flora of Central Europe—Cyanoprokaryota, vol 1. Chroococcales. Springer, BerlinGoogle Scholar
  62. Komárek J, Anagnostidis K (2005) Freshwater flora of Central Europe—Cyanoprokaryota, vol 2. Oscillatorialles. Springer, BerlinGoogle Scholar
  63. Kopylova E, Noé L, Touzet H (2012) SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28:3211–3217. PubMedCrossRefGoogle Scholar
  64. Lee K, Eisterhold ML, Rindi F et al (2014) Isolation and screening of microalgae from natural habitats in the midwestern United States of America for biomass and biodiesel sources. J Nat Sci Biol Med 5:333. PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lee JR, Raymond B, Bracegirdle TJ et al (2017) Climate change drives expansion of Antarctic ice-free habitat. Nature 547:49–54. PubMedCrossRefGoogle Scholar
  66. Li Z, Shin HH, Lee T, Han M-S (2015) Resting stages of freshwater algae from surface sediments in Paldang Dam Lake, Korea. Nov Hedwigia 101:475–500. CrossRefGoogle Scholar
  67. Lind EM, Brook AJ (1980) A key to the commoner desmids of the English Lake District. Freshwater Biological AssociationGoogle Scholar
  68. Lukešová A, Kociánová M, Váňa J et al (2010) Mud boils of the Giant Mts and Abisko Mts tundra—preliminary comparative study. Opera Corcon 47:55–82Google Scholar
  69. Lürling M (2003) Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Ann Limnol 39:85–101. CrossRefGoogle Scholar
  70. Manoylov KM (2014) Taxonomic identification of algae (Morphological and molecular): species concepts, methodologies, and their implications for ecological bioassessment. J Phycol 50:409–424. PubMedCrossRefGoogle Scholar
  71. Margulies M, Egholm M, Altman WE et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–381. PubMedPubMedCentralCrossRefGoogle Scholar
  72. Margulis L, Hinkle G, McKhann H, Moynihan B (1988) Mychonastes desiccatus Brown sp. nova (Chlorococcales, Chlorophyta)—an intertidal alga forming achlorophyllous desiccation-resistant cysts. Arch Hydrobiol Suppl Algol Stud 78:425–446PubMedGoogle Scholar
  73. Massalski A, Mrozinska T, Olech M (1994) Ultrastructure of Lobosphaera reniformis (Watanabe) Komárek et fott (= Chlorellales) from King George Island, South Shetland Islands, Antarctica. Acta Soc Bot Pol 63:205–210CrossRefGoogle Scholar
  74. Massana R, del Campo J, Sieracki ME et al (2014) Exploring the uncultured microeukaryote majority in the oceans: reevaluation of ribogroups within stramenopiles. ISME J 8:854–866. PubMedCrossRefGoogle Scholar
  75. Matuła J, Pietryka M, Richter D, Wojtuń B (2007) Cyanoprokaryota and algae of Arctic terrestrial ecosystems in the Hornsund area, Spitsbergen. Polish Polar Res 28:283–315Google Scholar
  76. Maturilli M, Herber A, König-Langlo G (2013) Climatology and time series of surface meteorology in Ny-Ålesund, Svalbard. Earth Syst Sci Data 5:155–163. CrossRefGoogle Scholar
  77. Michel RFM, Schaefer CEGR, Simas FMB et al (2014) Active-layer thermal monitoring on the Fildes Peninsula, King George Island, maritime Antarctica. Solid Earth 5:1361–1374. CrossRefGoogle Scholar
  78. Miller CS, Baker BJ, Thomas BC et al (2011) EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol 12:R44. PubMedPubMedCentralCrossRefGoogle Scholar
  79. Misawa S (1999) Rapid diagnosis of infectious diseases; features and limitations of the microscopic examination of clinical specimens. J Assoc Rapid Method Autom Microbiol 10:121–131Google Scholar
  80. Nagao M, Arakawa K, Takezawa D et al (1999) Akinete formation in Tribonema bombycinum Derbes et Solier (Xanthophyceae) in relation to freezing tolerance. J Plant Res 112:163–174CrossRefGoogle Scholar
  81. Oren A (2005) A hundred years of Dunaliella research: 1905-2005. Saline Syst 1:2. PubMedPubMedCentralCrossRefGoogle Scholar
  82. Patova E, Davydov D, Vera A (2015) Cyanoprokaryotes and algae. In: Matveyeva M (ed) Plants and fungi of the polar deserts in the northern hemisphere. MAPAФOH, pp 133–164Google Scholar
  83. Pawlowski J, Christen R, Lecroq B et al (2011) Eukaryotic richness in the abyss: insights from pyrotag sequencing. PLoS ONE 6:e18169. PubMedPubMedCentralCrossRefGoogle Scholar
  84. Peel MC, Finlayson BL, McMahon TA (2007) World map of the Köppen-Geiger climate classification updated. Hydrol Earth Syst Sci 11:1633–1644. CrossRefGoogle Scholar
  85. Pereira EB, Evangelista H, Pereira KCD et al (2006) Apportionment of black carbon in the South Shetland Islands, Antartic Peninsula. J Geophys Res 111:D03303. CrossRefGoogle Scholar
  86. Peveling E, Galun M (1976) Electron-microscopical studies on the phycobiont Coccomyxa Schmidle. New Phytol 77:713–718. CrossRefGoogle Scholar
  87. Pfaff S, Borchardt N, Boy J et al (2016) Desiccation tolerance and growth-temperature requirements of Coccomyxa (Trebouxiophyceae, Chlorophyta) strains from Antarctic biological soil crusts. Arch Hydrobiol Suppl Algol Stud 151:3–19. CrossRefGoogle Scholar
  88. Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562. PubMedCrossRefGoogle Scholar
  89. Pointing SB, Büdel B, Convey P et al (2015) Biogeography of photoautotrophs in the high polar biome. Front Plant Sci 6:692. PubMedPubMedCentralCrossRefGoogle Scholar
  90. Poonguzhali S, Madhaiyan M, Sa T (2007) Quorum-sensing signals produced by plant-growth promoting Burkholderia strains under in vitro and in planta conditions. Res Microbiol 158:287–294. PubMedCrossRefGoogle Scholar
  91. Prescott GW (1964) How to know the fresh-water algae. Plenum Press, New YorkGoogle Scholar
  92. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  93. Pushkareva E, Johansen JR, Elster J (2016) A review of the ecology, ecophysiology and biodiversity of microalgae in Arctic soil crusts. Polar Biol. CrossRefGoogle Scholar
  94. Rippin M, Komsic-Buchmann K, Becker B (2016) RNA isolation from biological soil crusts: methodological aspects. Arch Hydrobiol Suppl Algol Stud 151:21–37. CrossRefGoogle Scholar
  95. Rippka R, Deruelles J, Waterbury JB et al (1979) Generic assignments, strain histories and properties of pure cultures of Cyanobacteria. J Gen Microbiol 111:1–61. CrossRefGoogle Scholar
  96. Rivasseau C, Farhi E, Compagnon E et al (2016) Coccomyxa actinabiotis sp. nov. (Trebouxiophyceae, Chlorophyta), a new green microalga living in the spent fuel cooling pool of a nuclear reactor. J Phycol 52:689–703. PubMedCrossRefGoogle Scholar
  97. Sanders RW, Caron DA, Davidson JM et al (2001) Nutrient acquisition and population growth of a mixotrophic alga in axenic and bacterized cultures. Microb Ecol 42:513–523. PubMedCrossRefGoogle Scholar
  98. Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol 6:229. PubMedPubMedCentralCrossRefGoogle Scholar
  99. Schmidle W (1901) Ueber drei Algengenera. Berichte der Dtsch Bot Gessellschaft 19:10–24Google Scholar
  100. Schulz K, Mikhailyuk T, Dreßler M et al (2016) Biological soil crusts from coastal dunes at the Baltic Sea: Cyanobacterial and algal biodiversity and related soil properties. Microb Ecol 71:178–193. PubMedCrossRefGoogle Scholar
  101. Shen S (2008) Genetic diversity analysis with ISSR PCR on green algae Chlorella vulgaris and Chlorella pyrenoidosa. Chin J Oceanol Limnol 26:380–384. CrossRefGoogle Scholar
  102. Sherwood AR, Vis ML, Entwisle TJ et al (2008) Contrasting intra versus interspecies DNA sequence variation for representatives of the Batrachospermales (Rhodophyta): insights from a DNA barcoding approach. Phycol Res 56:269–279. CrossRefGoogle Scholar
  103. Shi XL, Marie D, Jardillier L et al (2009) Groups without cultured representatives dominate eukaryotic picophytoplankton in the oligotrophic South East Pacific Ocean. PLoS ONE 4:e7657. PubMedPubMedCentralCrossRefGoogle Scholar
  104. Singh SP, Singh P (2015) Effect of temperature and light on the growth of algae species: a review. Renew Sustain Energy Rev 50:431–444. CrossRefGoogle Scholar
  105. Škaloud P, Friedl T, Hallmann C et al (2016) Taxonomic revision and species delimitation of coccoid green algae currently assigned to the genus Dictyochloropsis (Trebouxiophyceae, Chlorophyta). J Phycol 52:599–617. PubMedCrossRefGoogle Scholar
  106. Skinner CE (1932) Isolation in pure culture of green algae from soil by a simple technique. Plant Physiol 7:533–537. PubMedPubMedCentralCrossRefGoogle Scholar
  107. Solden L, Lloyd K, Wrighton K (2016) The bright side of microbial dark matter: lessons learned from the uncultivated majority. Curr Opin Microbiol 31:217–226. PubMedCrossRefGoogle Scholar
  108. Starr RC, Jeffrey AZ (1993) UTEX—the culture collection of algae at the University of Texas at Austin 1993 list of cultures. J Phycol 29:1–106CrossRefGoogle Scholar
  109. Stoyanov P, Moten D, Mladenov R et al (2014) Phylogenetic relationships of some filamentous cyanoprokaryotic species. Evol Bioinform 10:39–49. CrossRefGoogle Scholar
  110. Stoyneva M (2000) Soil algae in museum samples from some Southwest Asia sites I. Hist Nat Bulg 12:129–146Google Scholar
  111. Taberlet P, Coissac E, Pompanon F et al (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050. PubMedCrossRefGoogle Scholar
  112. Takeuchi N (2001) Seasonal and altitudinal variations in snow algal communities on an Alaskan glacier (Gulkana glacier in the Alaska range). Hydrol Process 15:3447–3459. CrossRefGoogle Scholar
  113. Thomas DN, Fogg T, Convey P et al (2008a) Introduction to the polar regions. In: Thomas DN (ed) The biology of polar regions. University Press, Oxford, pp 1–27CrossRefGoogle Scholar
  114. Thomas DN, Fogg T, Convey P et al (2008b) Periglacial and terrestrial habitats in polar regions. In: Thomas DN (ed) The biology of polar regions. University Press, Oxford, pp 53–100CrossRefGoogle Scholar
  115. Thompson AW, Foster RA, Krupke A et al (2012) Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337:1546–1550PubMedCrossRefGoogle Scholar
  116. Thorn R, Lynch M (2007) Fungi and eukaryotic algae. In: Paul EA (ed) Soil microbiology, ecology, and biochemistry. Elsevier, Oxford, pp 145–162CrossRefGoogle Scholar
  117. Tschaikner A, Ingolic E, Gärtner G (2007) Observations in a new isolate of Coelastrella terrestris (Reisigl) Hegewald & Hanagata (Chlorophyta, Scenedesmaceae) from Alpine Soil (Tyrol, Austria). Phyton (B Aires) 46:237–245Google Scholar
  118. Urich T, Lanzén A, Qi J et al (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 3:e2527. PubMedPubMedCentralCrossRefGoogle Scholar
  119. Urich T, Lanzén A, Stokke R et al (2014) Microbial community structure and functioning in marine sediments associated with diffuse hydrothermal venting assessed by integrated meta-omics. Environ Microbiol 16:2699–2710. PubMedCrossRefGoogle Scholar
  120. Uzunov BA, Stoyneva MP, Gärtner G, Koefler W (2008) First record of Coelastrella species (Chlorophyta: Scenedesmaceae) in Bulgaria. Berichte des naturwissenschaftlichen-medizinischen Verein Innsbruck 95:27–34Google Scholar
  121. Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of “unculturable” bacteria. FEMS Microbiol Lett 309:1–7. PubMedCrossRefGoogle Scholar
  122. Vieira HH, Bagatini IL, Guinart CM, Vieira AAH (2016) tufA gene as molecular marker for freshwater Chlorophyceae. Algae 31:155–165. CrossRefGoogle Scholar
  123. Vishnivetskaya TA (2009) Viable Cyanobacteria and green algae from the permafrost darkness. Permafrost soils. Springer, Heidelberg, pp 73–84CrossRefGoogle Scholar
  124. Vogel S (1955) Niedere “Fensterpflanzen” in der Südafrikanischen Wüste: Eine ökologische Schilderung. Duncker & HumblotGoogle Scholar
  125. Vogel S, Eckerstorfer M, Christiansen HH (2012) Cornice dynamics and meteorological control at Gruvefjellet, Central Svalbard. Cryosph 6:157–171. CrossRefGoogle Scholar
  126. Wang NF, Zhang T, Zhang F et al (2015) Diversity and structure of soil bacterial communities in the Fildes Region (maritime Antarctica) as revealed by 454 pyrosequencing. Front Microbiol 6:1188. PubMedPubMedCentralCrossRefGoogle Scholar
  127. Ward DM, Weller R, Bateson MM (1990) 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345:63–65. PubMedCrossRefGoogle Scholar
  128. Waterbury JB, Stanier RY (1978) Patterns of growth and development in pleurocapsalean Cyanobacteria. Microbiol Rev 42:2–44PubMedPubMedCentralGoogle Scholar
  129. Williams P (2007) Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153:3923–3938. PubMedCrossRefGoogle Scholar
  130. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  131. Williams L, Borchhardt N, Colesie C et al (2017) Biological soil crusts of Arctic Svalbard and of Livingston Island, Antarctica. Polar Biol 40:399–411. CrossRefGoogle Scholar
  132. Wilmotte A (1994) Molecular evolution and taxonomy of the Cyanobacteria. In: Bryant D (ed) The molecular biology of cyanobacteria. Springer, Dordrecht, pp 1–25Google Scholar
  133. Wu HL, Hseu RS, Lin LP (2001) Identification of Chlorella spp. isolates using ribosomal DNA sequences. Bot Bull Acad Sin 42:115–121Google Scholar
  134. Wu Z, Duangmanee P, Zhao P et al (2016) The effects of light, temperature, and nutrition on growth and pigment accumulation of three Dunaliella salina strains isolated from saline soil. Jundishapur J Microbiol 9:e26732. PubMedPubMedCentralCrossRefGoogle Scholar
  135. Yoon T-H, Kang H-E, Kang C-K et al (2016) Development of a cost-effective metabarcoding strategy for analysis of the marine phytoplankton community. PeerJ 4:e2115. PubMedPubMedCentralCrossRefGoogle Scholar
  136. Yoshitake S, Uchida M, Koizumi H et al (2010) Production of biological soil crusts in the early stage of primary succession on a high Arctic glacier foreland. New Phytol 186:451–460. PubMedCrossRefGoogle Scholar
  137. Zidarova R (2008) Algae from Livingston Island (S Shetland Islands): a checklist. Phytol Balc 14:19–35Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.University of Cologne, Botanical InstituteCologneGermany
  2. 2.Department of Applied Ecology & PhycologyUniversity of RostockRostockGermany
  3. 3.Department of Plant Ecology & SystematicsUniversity of KaiserslauternKaiserslauternGermany
  4. 4.Department of Forest Genetics and Plant PhysiologySwedish University of Agricultural SciencesUmeåSweden

Personalised recommendations