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Molecular, morphological and ultrastructural characteristics of Prasiola crispa (Lightfoot) Kützing (Chlorophyta) from Spitsbergen (Arctic)

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Abstract

It is commonly known that seabirds, along with cyanobacteria, play a key role in the enrichment of nutrient-poor polar terrestrial ecosystems. In habitats particularly enriched with nitrogen and phosphate ions, ornithogenic vegetation with Prasiola crispa and unique species composition develops. However, no studies have examined the potentially different impacts associated with seabirds on the morphological, ultrastructural and molecular diversity of P. crispa. For that purpose, the present study analyzed four populations from the Hornsund Fjord area (West Spitsbergen) collected in the vicinity of planktivorous or piscivorous colonies and individual nests of seabirds. The morphological variability of P. crispa was studied using fresh samples, and it was documented with light microscopy as well as transmission and scanning electron microscopy. Populations were investigated by molecular analyses based on rbcL and 18S rRNA sequences. The differences in features measured were subjected to statistical analysis. This study provides new data concerning the macro- and submicroscopic structure and molecular diversity of P. crispa with regard to differences in humidity and the quantity of biogenic nutrients deposited by seabirds. Molecular research provided the first data about P. crispa from Spitsbergen. Birds’ diet is relevant for the quantity and quality of the provided nutrients, especially nitrogen compounds (planktivorous species) and phosphorus (piscivorous birds). Climate changes influence the quantitative structure of the colony, clearly favoring piscivorous birds. This, in turn, causes changes in the environment and vegetation. The obtained data on the P. crispa population may be compared with potential changes in the future.

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References

  • Adams NM (1994) Seaweeds of New Zealand. An illustrated guide. Canterbury University Press, Christchurch, pp 1–360

    Google Scholar 

  • Bock C, Jacob A, Kirst GO, Leibfritz D, Mayer A (1996) Metabolic changes of the Antarctic green algae Prasiola crispa subjected to water stress investigated by in vivo 31P NMR. J Exp Bot 47(295):241–249

    Article  CAS  Google Scholar 

  • Boraso A, Zaixso JM (2011) Atlas de sensibilidad ambiental de la costa y el Mar Argentino. Algas marinas bentónicas 1–28

  • Broady PA, Flint EA, Nelson WA, Cassie Coope V, De Winton MD, Novis PM (2012) Phylum chlorophyta and charophyta: green algae. In: Gordon DP (ed) New Zealand inventory of biodiversity. Kingdoms bacteria, protozoa, chromista, plantae, fungi. Canterbury University Press, Christchurch, pp 347–381

    Google Scholar 

  • Brodie J, Maggs CA, John DM (2007) Green Seaweeds of Britain and Ireland. British Phycological Society, London, pp 1–242

    Google Scholar 

  • Burrows EM (1991) Seaweeds of the British Isles. Chlorophyta. Natural History Museum Publications, London, pp 1–238

    Google Scholar 

  • Caram B, Jónsson S (1972) Nouvelle inventaire des algues marines de l’Islande. Acta Botanica Islandica 1:5–31

    Google Scholar 

  • Cărăuş I (2012) Algae of Romania. A distributional checklist of actual algae. Stud Cerc Biol Univ Bacău 7:1–809

    Google Scholar 

  • Clayton MN, Wiencke C (1986) Techniques and equipment for culturing Antarctic benthic marine algae, and for preparing specimens for electron microscopy. Serie Cientifica Instituto Antarctico Chileno. Chile 34:93–97

    Google Scholar 

  • Graeve M, Kattner G, Wiencke C, Karsten U (2002) Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogenetic and trophic relationships. Mar Ecol Prog Ser 231:67–74

    Article  CAS  Google Scholar 

  • Gustavs L, Görs M, Karsten U (2011) Polyol patterns in biofilm-forming aeroterrestrial green algae (Trebouxiophyceae, Chlorophyta). J Phycol 47:533–537

    Article  PubMed  Google Scholar 

  • Hoek C, Mann DG, Johns HM (1995) Algae: an introduction to phycology. Printed in Great Britain at University Press, Cambridge, pp 1–623

    Google Scholar 

  • Holzinger A, Karsten U, Lütz C, Wiencke C (2006) Ultrastructure and photosynthesis in the supralittoral green macroalga Prasiola crispa from Spitsbergen (Norway) under UV exposure. Phycologia 45:168–177

    Article  Google Scholar 

  • Hoyer K, Karsten U, Sawall T, Wiencke C (2001) Photoprotective substances in Antarctic macroalgae and their variation with respect to depth distribution, different tissues and developmental stages. Mar Ecol Prog Ser 211:117–129

    Article  CAS  Google Scholar 

  • Hu H, Wei Y (2006) The freshwater algae of China. Systematics, Taxonomy and Ecology, pp 1–1023

    Google Scholar 

  • Jackson AE, Seppelt RD (1995) The accumulation of proline in Prasiola crispa during winter in Antarctica. Physiol Plant 94(1):25–30. doi:10.1111/j.1399-3054.1995.tb00779.x

    Article  CAS  Google Scholar 

  • Jacob A, Wiencke C, Lehmann H, Kirst GO (1992) Physiology and ultrastructure of desiccation in the green alga Prasiola crispa from Antarctica. Bot Mar 35(4):297–303

    Article  Google Scholar 

  • Jacobs A, Kirst GO (1995) Zur Biologie der Supralitoralalge Prasiola crispa ssp. Antarctica. In: Wiencke C, Arntz W (eds) Benthos in polaren Gewässern, vol 155. Ber Polarforsch, Bremerhaven, pp 24–25

  • John DM, Whitton BA, Brook AJ (2011) The freshwater algal flora of the British Isles. An identification guide to freshwater and terrestrial algae. Cambridge University Press, Cambridge, pp 567–572

    Google Scholar 

  • Karsten U, Escoubeyrou Charles F (2009) The effect of re-dissolution solvents and HPLC columns on the analysis of mycosporine-like amino acids in the eulittoral macroalgae Prasiola crispa and Porphyra umbilicalis. Helgol Mar Res 63:231–238. doi:10.1007/s10152-009-0152-0

    Article  Google Scholar 

  • Knebel G (1936) Monographye der Algenreihe der Prasiolases, insbesondere von Prasiola crispa. Hedwigia 75:1–120

    Google Scholar 

  • Komárek O, Komárek J (1999) Diversity of freshwater and terrestrial habitats and their oxyphototroph microflora in the Arctowski Station region, South Shetland Islands. Polish Polar Research 20(3):259–282

    Google Scholar 

  • Kosugi M, Katashima Y, Aikawa S, Tanabe Y, Kudoh S, Kashino Y, Koike H, Satoh K (2010) Comparative study on the photosynthetic properties of Prasiola (Chlorophyceae) and Nostoc (Cyanophyceae) from Antarctic and non-Antarctic sites. J Phycol 46(3):466–476. doi:10.1111/j.1529-8817.2010.00831.x

    Article  Google Scholar 

  • Kováčik L, Pereira AB (2001) Green alga Prasiola crispa and its lichenized form Mastodia tesselata in Antarctic environment: general aspects. Nova Hedwig Beih 123:465–478

    Google Scholar 

  • Kützing FT (1843) Phycologia generalis oder Anatomie, Physiologie und Systemkunde der Tange. F.A. Brockhaus, Leipzig, pp 1–458

    Google Scholar 

  • Lightfoot J (1777) Flora scotica, vol 2, 1st edn. B White, London, pp 531–1151

    Google Scholar 

  • Lindstrom SC (1977) An annotated bibliography of the benthic marine algae of Alaska. Alaska Dept Fish Game Tech Data Rep 31:1–172

    Google Scholar 

  • Lud D, Buma AGJ, van de Poll W, Moerdijk TCW, Huiskes AHL (2001) DNA damage and photosynthetic performance in the Antarctic terrestrial alga Prasiola crispa spp. antarctica (Chlorophyta) under manipulated UV-B radiation. J Phycol 37:459–467

    Article  Google Scholar 

  • Matuła J, Pietryka M, Richter D, Wojtuń B (2007) Cyanoprokaryota and algae of Arctic terrestrial ecosystems in the Hornsund area, Spitsbergen. Pol Polar Res 28(4):283–315

    Google Scholar 

  • Miotti C, Curiel D, Rismondo A, Bellemo G, Dri C, Checchin E, Marzocchi M (2005) First report of a species of Prasiola (Chlorophyta: Prasiolaceae) from the Mediterranean Sea (Lagoon of Venice). Sci Mar 69(3):242–346

    Google Scholar 

  • Moniz MBJ, Rindi F, Novis PM, Broady PA, Guiry MD (2012) Molecular phylogeny of Antarctic Prasiola (Prasiolales, Trebouxiophyceae) reveals extensive cryptic diversity. J Phycol 48:940–955. doi:10.1111/j.1529-8817.2012.01172.x

    Article  PubMed  Google Scholar 

  • Naw MWD, Hara Y (2002) Morphology and molecular phylogeny of Prasiola sp. (Prasiolales, Chlorophyta) from Myanmar. Phycol Res 50:175–182. doi:10.1046/j1440-1835.2002.00271.x

    Article  CAS  Google Scholar 

  • Neustupa J (1998) Prasiola crispa (Lightfoot) Meneghini in Královská obora in Prague. Novit Bot Univ Carol 12:35–39

    Google Scholar 

  • Ohtani S, Suyama K, Yamamoto H, Aridomi Y, Itoh R, Fukuoka Y (2000) Distribution of soil algae at the monitoring sites in the vicinity of Syowa Station between austral summers of 1992/1993 and 1997/1998. Polar Biosci 13:113–132

    Google Scholar 

  • Okamura K (1936) Nippon kaisô shi. Descriptions of Japanese algae. Uchida Rokakuho, Tokyo, pp 1–427

    Google Scholar 

  • Olech M (1990) Preliminary studies on ornithocoprophilous lichens of the Arctic and Antarctic regions. Proc NIPR Symp Polar Biol 3:218–223

    Google Scholar 

  • Pažoutovà M, Moniz BJ, Rindi F (2012) Diversity and distribution of Prasiola (Prasiolales, Chlorophyta) in Spitsbergen (Svalbard Islands). In: Bernardowá et al (eds) Polar ecology conference. Abstracts and contact list, České Budějovice, Czech Republic, 99

  • Pizarro H, Izaguirre I, Tell G (1996) Epilithic algae from a freshwater stream at Hope Bay, Antarctica. Antarct Sci 8(2):161–167

    Article  Google Scholar 

  • Raven JA, Taylor R (2003) Macroalgal growth in nutrient-enriched estuaries: a biogeochemical and evolutionary perspective. Water Air Soil Pollut 3:7–26

    Article  CAS  Google Scholar 

  • Reynolds E (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17(1):208–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richter D, Matuła J, Pietryka M (2009) Cyanobacteria and algae of selected habitats in tundra around Hornsund fjord (West Spitsbergen). Oceanol Hydrobiol Stud 38:1–6

    Google Scholar 

  • Richter D, Pietryka M, Matuła J (2015) Relationship of cyanobacterial and algal assemblages with vegetation in the high Arctic tundra (West Spitsbergen, Svalbard Archipelago). Pol Polar Res 36(3):239–260

    Google Scholar 

  • Rindi F, Guiry MD (2003) Composition and distribution of subaerial algal assemblages in Galway City, western Ireland. Cryptog Algol 24:245–267

    Google Scholar 

  • Rindi F, Guiry MD (2004) Composition and spatial variability of terrestrial algal assemblages occurring at the bases of urban walls in Europe. Phycologia 43:225–235

    Article  Google Scholar 

  • Rindi F, Guiry MD, Barbiero RP, Cinelli F (1999) The marine and terrestrial Prasiolales (Chlorophyta) of Galway City, Ireland: a morphological and ecological study. J Phycol 35:469–482

    Article  Google Scholar 

  • Rindi F, McIvor L, Guiry MD (2004) The Prasiolales (Chlorophyta) of Atlantic Europe: an assessment based on morphological, molecular, and ecological data, including the characterization of Rosenvingiella radicans (Kützing) comb. nov. J Phycol 40:977–997. doi:10.1111/j.1529-8817.2004.04012x

    Article  Google Scholar 

  • Rindi F, McIvor L, Sherwoodd AR, Friedl T, Guiry MD, Sheath RG (2007) Molecular phylogeny of the green algal order Prasiolales (Trebouxiophyceae, Chlorophyta). J Phycol 43:811–822

    Article  CAS  Google Scholar 

  • Scagel RF, Gabrielson PW, Garbary DJ, Golden L, Hawkes MW, Lindstrom SC, Oliveira JC, Widdowson TB (1989) A synopsis of the bentic marine algae of British Columbia, southeast Alaska, Washington and Oregon. Phycol Contrib Univ Brit Columbia 3:1–532

    Google Scholar 

  • Sfriso A (2011) Chlorophyta multicellulari e fanerogame acquatiche. Ambiente di transizione italiani e litorali adiacenti. Arpa Emilia-Romagna, Bologna, pp 1–318

    Google Scholar 

  • Silva PC, Basson PW, Moe RL (1996) Catalogue of the benthic marine algae of the Indian Ocean. Univ Calif Publ Bot 79:1–1259

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastructure Res. 26(1):31–43

    Article  CAS  Google Scholar 

  • Starmach K (1972) Chlorophyta III Zielenice nitkowate w: flora Słodkowodna Polski. PWN Warszawa-Kraków 10:1–751

  • StatSoft, Inc. (2014) STATISTICA (data analysis software system), version 12. www.statsoft.com

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2012) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony method. Mol Biol Evol 28:2731–2739

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ, Clustal W (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Widdowson TB (1989) A synopsis of the benthic marine algae of British Columbia, southeast Alaska, Washington and Oregon. Phycol Contrib Univ Br Columbia 3:532

    Google Scholar 

  • Wiencke C (1996) Recent advances in the investigation of Antarctic macroalgae. Polar Biol 16:231–240

    Article  Google Scholar 

  • Wojtuń B, Samecka-Cymerman A, Kolon K, Kempers AJ, Skrzypek G (2013) Metals in some dominant vascular plants, mosses, lichens, algae, and the biological soil crust in various types of terrestrial tundra, SW Spitsbergen, Norway. Polar Biol 36:1799–1809. doi:10.1007/s00300-013-1399-0

    Article  Google Scholar 

  • Womersley HBS (1984) The marine benthic flora of southern Australia. Part I. Adelaide: South Australian. Government Printer, Washington, p 329

    Google Scholar 

  • Zemolin APP, Cruz LC, Paula MT, Pereira BK, Albuquerque MP, Victoria FC, Pereira AB, Posser T, Franco JL (2014) Toxicity induced by Prasiola crispa to fruit fly Drosophila melanogaster and cockroach Nauphoeta cinerea: evidence for bioinsecticide action. J Toxicol Environ Health Part A 77:115–124

    Article  CAS  PubMed  Google Scholar 

  • Zwolnicki A, Zmudczyńska-Skarbek KM, Iliszko L, Stempniewicz L (2013) Guano deposition and nutrient enrichment in the vicinity of planktivorous and piscivorous seabird colonies in Spitsbergen. Polar Biol 36:363–372

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank Richard Ashcroft for language revision. The authors thank the Chief Editor and the anonymous reviewers for valuable remarks on the manuscript.

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Correspondence to Dorota Richter.

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Richter, D., Matuła, J., Urbaniak, J. et al. Molecular, morphological and ultrastructural characteristics of Prasiola crispa (Lightfoot) Kützing (Chlorophyta) from Spitsbergen (Arctic). Polar Biol 40, 379–397 (2017). https://doi.org/10.1007/s00300-016-1966-2

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