Sanguina nivaloides and Sanguina aurantia gen. et spp. nov. (Chlorophyta): the taxonomy, phylogeny, biogeography and ecology of two newly recognised algae causing red and orange snow
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31074825
PubMed Central
PMC6545352
DOI
10.1093/femsec/fiz064
PII: 5487888
Knihovny.cz E-zdroje
- Klíčová slova
- Chlamydomonas nivalis, haplotype network, red snow, snow algae,
- MeSH
- Chlorophyta klasifikace genetika fyziologie MeSH
- ekosystém MeSH
- fylogeneze MeSH
- fylogeografie MeSH
- mezerníky ribozomální DNA MeSH
- Rhodophyta MeSH
- sníh mikrobiologie MeSH
- zmrazování MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH
- Jižní Amerika MeSH
- Severní Amerika MeSH
- Názvy látek
- mezerníky ribozomální DNA MeSH
Melting snowfields in polar and alpine regions often exhibit a red and orange colouration caused by microalgae. The diversity of these organisms is still poorly understood. We applied a polyphasic approach using three molecular markers and light and electron microscopy to investigate spherical cysts sampled from alpine mountains in Europe, North America and South America as well as from both polar regions. Molecular analyses revealed the presence of a single independent lineage within the Chlamydomonadales. The genus Sanguina is described, with Sanguina nivaloides as its type. It is distinguishable from other red cysts forming alga by the number of cell wall layers, cell size, cell surface morphology and habitat preference. Sanguina nivaloides is a diverse species containing a total of 18 haplotypes according to nuclear ribosomal DNA internal transcribed spacer 2, with low nucleotide divergence (≤3.5%). Based on molecular data we demonstrate that it has a cosmopolitan distribution with an absence of geographical structuring, indicating an effective dispersal strategy with the cysts being transported all around the globe, including trans-equatorially. Additionally, Sanguina aurantia is described, with small spherical orange cysts often clustered by means of mucilaginous sheaths, and causing orange blooms in snow in subarctic and Arctic regions.
Charles University Faculty of Science Department of Ecology Viničná 7 128 44 Prague 2 Czech Republic
The Czech Academy of Sciences Institute of Botany Dukelská 135 Třeboň 379 82 Czech Republic
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Agardh CA. Systema Algarum. Lundae. 1824;XI-XXI:13–4.
Agardh CA. Icones Algarum Europaerum. Leipzig: Leopold Voss, 1828–35.
anagreh L, Pegg C, Harikumar A et al. .. Assessing intragenomic variation of the internal transcribed spacer two: Adapting the Illumina metagenomics protocol. PLoS One. 2017;12:e0181491. PubMed PMC
Allewaert CC, Vanormelingen P, Pröschold T et al. .. Species diversity in European Haematococcus pluvialis (Chlorophyceae, Volvocales). Phycologia. 2015;54:583–98.
Andersen RA. Report of the nomenclature committee for algae: 19. Taxon. 2018;67:1029–30.
Bauer F. Microscopical observation on the red snow. Quart J Sci Arts. 1819;7:222–9.(incl. plate VI).
Bauer F. Red snow of Baffin's Bay. Amer J Sci Arts. 1820;2:356.
Bidigare RR, Ondrusek ME, Kennicutt MC II et al. .. Evidence for a photoprotective function for secondary carotenoids of snow algae. J Phycol. 1993;29:427–34.
Brown RM, Larson DA, Bold HC. Airborne algae: Their abundance and heterogenity. Science. 1964;143:583–4. PubMed
Brown SP, Jumpponen A. Microbial ecology of snow reveals taxa-specific biogeographical structure. Microb Ecol. 2019;77:946–58. PubMed
Brown SP, Olson BJSC, Jumpponen A. Fungi and algae co-occur in snow: An issue of shared habitat or algal facilitation of heterotrophs?. Arctic, Antarctic, and Alpine Research. 2015;47:729–49.
Brown SP, Ungerer MC, Jumpponen A. A community of clones: Snow algae are diverse communities of spatially structured clones. Int J Plant Sci. 2016;177:432–9.
Caisová L, Marin B, Melkonian M. A close-up view on ITS2 evolution and speciation - a case study in the Ulvophyceae (Chlorophyta, Viridiplantae). BMC Evol Biol. 2011;11:262. PubMed PMC
Caisová L, Marin B, Melkonian M. A consensus secondary structure of ITS2 in the Chlorophyta identified by phylogenetic reconstruction. Protist. 2013;164:482–96. PubMed
Clement M, Posada D, Crandall K. TCS: A computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–9. PubMed
Cohn F, Chlamydococcus nivalis (F.A.Bauer) A. Braun. Rabenhorst: Algae Exsiccatae, 1861, 1141.
Coleman AW. The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. Protist. 2000;151:1–9. PubMed
Coleman AW. Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Res. 2007;35:3322–9. PubMed PMC
Czygan F-C. Blutregen und Blutschnee: Stickstoffmangel-Zellen von Haematococcus pluvialis und Chlamydomonas nivalis. Arch Mikrobiol. 1970;74:69–76. PubMed
Darty K, Denise A, Ponty Y. VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics. 2009;25:1974–5. PubMed PMC
Demchenko E. Morphology, ecophysiology and molecular phylogeny of marine and psychrophilic green flagellates belonging to Microglena and their adaptation to changing ecological conditions. DAAD Reports. 2013;322:1–15.
Demchenko E, Mikhailyuk T, Coleman AW et al. .. Generic and species concepts in Microglena (previously the Chlamydomonas monadina group) revised using an integrative approach. Eur J Phycol. 2012;47:264–90.
Di Mauro B, Garzonio R, Rossini M et al. .. Saharan dust events in the European Alps: Role in snowmelt and geochemical characterization. The Cryosphere. 2019; 13:1147–65.
Ehrenberg CG. Dritter Beitrag zur Erkenntnis großer Organisation in der Richtung des kleinsten Raumes. Physikalische Abhandlungen der Koeniglichen Akademie der Wissenschaften zu Berlin. 1834;1833:145–336.
Ehrenberg CG, König. Preuss. Akad. Wiss. Berlin; Über eine frische Probe der die Crimson Cliffs scharlachroth färbenden Substanz aus der Baffins Bai und das sie begleitende kleinste Leben. Bericht über die zur Bekanntmachung geeigneten Verhandl. 1851:741–4.
Ettl H, Gärtner G. Syllabus der Boden-, Luft- und Flechtenalgen. Springer, 2014.
Farr ER, Zijlstra G. Index nominum genericorum (Plantarum), 1996+. http://botany.si.edu/ing/(18 March 2019, date last accessed).
Fjerdingstad E, Kemp K, Fjerdingstad E et al. .. Chemical analyses of red “snow” from East-Greenland with remarks on Chlamydomonas nivalis (Bau.) Wille. Arch Hydrobiol. 1974;73:70–83.
Flotow J. Über Haematococcus pluvialis. Nov Act Leop Carol. 1844;20:413–606.
Fučíková K, Lewis LA. Intersection of Chlorella, Muriella and Bracteacoccus: Resurrecting the genus Chromochloris Kol et Chodat (Chlorophyceae, Chlorophyta). Fottea. 2012;12:83–93.
Gillespie RG, Baldwin BG, Waters JM et al. .. Long-distance dispersal: A framework for hypothesis testing. Trends Ecol Evol. 2012;27:47–56. PubMed
Gradinger R, Nürnberg D. Snow algal communities on arctic pack ice floes dominated by Chlamydomonas nivalis (Bauer) Wille. Proc NIPR Symp Polar Biol. 1996;9:35–43.
Guiry MD, Guiry GM. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway, 2018. http://www.algaebase.org (14 June 2018, date last accessed).
Hepperle D, Nozaki H, Hohenberger S et al. .. Phylogenetic position of the Phacotaceae within the Chlamydophyceae as revealed by analysis of 18s rDNA and rbcL sequences. J Mol Evol. 1998;47:420–30. PubMed
Hodač L, Hallmann C, Spitzer K et al. .. Widespread green algae Chlorella and Stichococcus exhibit polar-temperate and tropical-temperate biogeography. FEMS Microbiol Ecol. 2016;92:fiw122. PubMed
Hoham RW. New findings in the life history of the snow alga, Chlainomonas rubra (Stein et Brooke) comb. nov. (Chlorophyta, Volvocales). Syesis. 1974;7:239–47.
Hoham RW, Roemer SC, Mullet JE. The life history and ecology of the snow alga Chloromonas brevispina comb. nov. (Chlorophyta, Volvocales). Phycologia. 1979;18:55–70.
Hooker JD. 36. Red snow. Edinb J Sci. 1825;2:184.
Ji M, Greening C, Vanwonterghem I et al. .. Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature. 2017;552:400–3. PubMed
Jombart T. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–5. PubMed
Jombart T, Pontier D, Dufour AB. Genetic markers in the playground of multivariate analysis. Heredity. 2009;102:330–41. PubMed
Jombart T, Devillard S, Dufour AB et al. .. Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity. 2008;101:92–103. PubMed
Jones HG, Pomeroy JW, Walker DA et al. .(eds.) Snow ecology. An interdisciplinary examination of snow-covered ecosystems. Cambridge: Cambridge University Press, 2001; 378.
Kawecka B. Biology and ecology of snow algae 2. Formation of aplanospores in Chlamydomonas nivalis (Bauer) Wille (Chlorophyta, Volvocales). Acta Hydrobiol. 1981;23:211–5.
Kobayashi Y, Fukushima H. On the red and green snow newly found in Japan II. Bot Mag Tokyo. 1952;65:128–36.
Koetschan C, Förster F, Keller A et al. .. The ITS2 Database III-sequences and structures for phylogeny. Nucleic Acids Res. 2010;38:D275–9. PubMed PMC
Kol E. The snow and ice algae of Alaska. Smithsonian Miscellaneous Collection. 1942;101:1–36.
Kol E. Kryobiologie: Biologie und Limnologie des Schnees und Eises, I. Kryovegetation. Die Binnengewässer Einzeldarstellungen aus der Limnologie und ihren Nachbargebieten Volume XXIV volume 24. Stuttgart: E. Schweizerbart'sche Verlagsbuchhandlung (Nägele u. Obermiller), 1968.
Ley R, Williams MW, Schmidt SK. Microbial population dynamics in an extreme environment: controlling factors in talus soils at 3750 m in the Colorado Rocky Mountains. Biogeochemistry. 2004;68:313–35.
Leya T. Feldstudien und genetische Untersuchungen zur Kryophilie der Schneealgen Nordwestspitzbergens. Berichte aus der Biologie. Aachen: Shaker, 2004.
Leya T. Die „Ross-Proben“ von den Crimson Cliffs: Probe „MB_ES_1781c“ aus der Ehrenberg Sammlung des Naturkundemuseums Berlin. Berlin: Fraunhofer IBMT, 2008, 6.
Leya T, Müller T, Ling HU et al. .. Snow algae from north-western Spitsbergen (Svalbard). Reports on Polar and Marine Research. 2004;492:46–54.
Leya T, Rahn A, Lütz C et al. .. Response of arctic snow and permafrost algae to high light and nitrogen stress by changes in pigment composition and applied aspects for biotechnology. FEMS Microbiol Ecol. 2009;67:432–43. PubMed
Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2. PubMed
Ling HU. Snow algae of the Windmill Islands, continental Antarctica: Chlorosarcina antarctica comb. nov. (Chlorophyceae, Chlorophyta) from pink snow, with discussion of Chlorosarcina and allied genera. Phycologia. 2002;41:1–9.
Ling HU, Seppelt RD. Snow algae of the Windmill Islands, continental Antarctica. 2. Chloromonas rubroleosa sp. nov. (Volvocales, Chlorophyta), an alga of red snow. Eur J Phycol. 1993;28:77–84.
Link DHF. 45./2. Coccophysium nivale. Handbuch zur Erkennung der nutzbarsten und am häufigsten vorkommenden Gewächse Drittel Teil. Berlin: Haude und Spenersche Buchhandlung; (S.J. Joseephy), 1833, 341–2.
Lu N, Wei D, Chen F et al. .. Lipidomic profiling reveals lipid regulation in the snow alga Chlamydomonas nivalis in response to nitrate or phosphate deprivation. Process Biochem. 2012a;48:605–13.
Lu N, Wei D, Jiang X-L et al. .. Regulation of lipid metabolism in the snow alga Chlamydomonas nivalis in response to NaCl stress: An integrated analysis by cytomic and lipidomic approaches. Process Biochem. 2012b;47:1163–70.
Lu N, Chen JH, Wei D et al. .. Global metabolic regulation of the snow alga Chlamydomonas nivalis in response to nitrate or phosphate deprivation by a metabolome profile analysis. Int J Mol Sci. 2016;17:19. PubMed PMC
Lutz S, Anesio AM, Raiswell R et al. .. The biogeography of red snow microbiomes and their role in melting arctic glaciers. Nat Commun. 2016;7:11968. PubMed PMC
Lütz-Meindl U, Lütz C. Analysis of element accumulation in cell wall attached and intracellular particles of snow algae by EELS and ESI. Micron. 2006;37:452–8. PubMed
Marchant HJ. Snow algae from the Australian Snowy Mountains. Phycologia. 1982;21:178–84.
Marshall WA. Biological particles over Antarctica. Nature. 1996;383:680.
Mataloni G, Tesolín G. A preliminary survey of cryobiontic algal communities from Cierva Point (Antarctic Peninsula). Antarct Sci. 1997;9:250–8.
Matsuzaki R, Hara Y, Nozaki H. A taxonomic revision of Chloromonas reticulata (Volvocales, Chlorophyceae), the type species of the genus Chloromonas, based on multigene phylogeny and comparative light and electron microscopy. Phycologia. 2012;51:74–85.
Matsuzaki R, Nozaki H, Kawachi M. Taxonomic revision of Chloromonas nivalis (Volvocales, Chlorophyceae) strains, with the new description of two snow-inhabiting Chloromonas species. PLoS One. 2018;13:e0193603. PubMed PMC
Matsuzaki R, Nozaki H, Takeuchi N et al. .. Taxonomic re-examination of “Chloromonas nivalis (Volvocales, Chlorophyceae) zygotes” from Japan and description of C. muramotoi sp. nov. PLoS One. 2019;14:e0210986. PubMed PMC
Mazumdar N, Gopalakrishnan KK, Visnovsky G et al. .. A novel alpine species of Haematococcus (Chlamydomonadales: Chlorophyta) from New Zealand. N Z J Bot. 2018;56:216–26.
Muramoto K, Nakada T, Shitara T et al. .. Re-examination of the snow algal species Chloromonas miwae (Fukushima) Muramoto et al., comb. nov. (Volvocales, Chlorophyceae) from Japan, based on molecular phylogeny and cultured material. Eur J Phycol. 2010;45:27–37.
Meneghini G. Monographia Nostochinearum italicarum addito specimine de Rivulariis. Memorie della Reale Accademia delle Scienze di Torino, ser 2. 1843;5:1–143 pls I-XVII.
Mosser JL, Mosser AG, Brock TD. Photosynthesis in the snow: The alga Chlamydomonas nivalis (Chlorophyceae). J Phycol. 1977;13:22–7.
Müller T, Leya T, Fuhr G. Persistent snow algal fields in Spitsbergen: Field observations and a hypothesis about the annual cell circulation. Arct Antarct Alp Res. 2001;33:42–51.
Müller T, Bleiß W, Martin C-D et al. .. Snow algae from northwest Svalbard: their identification, distribution, pigment and nutrient content. Polar Biol. 1998;20:14–32.
Nagai S, Lian C, Yamaguchi S et al. .. Microsatellite markers reveal population genetic structure of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) in Japanese coastal waters. J Phycol. 2007;43:43–54.
N.N Captain Sir John Ross has brought from Baffin's Bay a Quantity of Red Snow. London: London Times, 1818.
Nakada T, Ota S. What is the correct name for the type of Haematococcus Flot. (Volvocales, Chlorophyceae)?. Taxon. 2016;65:343–8.
Nedbalová L, Mihál M, Kvíderová J et al. .. Identity, ecology and ecophysiology of planktic green algae dominating in ice-covered lakes on James Ross Island (northeastern Antarctic Peninsula). Extremophiles. 2017;21:187–200. PubMed
Novakovskaya IV, Patova EN, Boldina ON et al. .. Molecular phylogenetic analyses, ecology and morphological characteristics of Chloromonas reticulata (Goroschankin) Gobi which causes red blooming of snow in the subpolar Urals. Cryptogam, Algol. 2018;39:199–213.
Novis PM. Ecology of the snow alga Chlainomonas kolii (Chlamydomonadales, Chlorophyta) in New Zealand. Phycologia. 2002;41:280–92.
Novis PM, Visnovsky G. Novel alpine algae from New Zealand: Chlorophyta. Phytotaxa. 2012;39:1–30.
Novis PM, Hoham RW, Beer T et al. .. Two snow species of the quadriflagellate green alga Chlainomonas (Chlorophyta, Volvocales): Ultrastructure and phylogenetic position within the Chloromonas clade. J Phycol. 2008;44:1001–12. PubMed
Nozaki H, Onishi K, Morita E. Differences in pyrenoid morphology are correlated with differences in the rbcL genes of members of the Chloromonas lineage (Volvocales, Chlorophyceae). J Mol Evol. 2002;55:414–30. PubMed
Persoon CH, Göttingen; Synopsis Methodica Fungorum. 1801;1:214.
Perty M. Zur Kenntnis kleinster Lebensformen. Bern. 1852:1–228.
Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25:1253–6. PubMed
Procházková L, Remias D, Řezanka T et al. .. Chloromonas nivalis subsp. tatrae, subsp. nov. (Chlamydomonadales, Chlorophyta): re-examination of a snow alga from the High Tatra Mountains (Slovakia). Fottea. 2018a;18:1–18. PubMed PMC
Procházková L, Remias D, Holzinger A et al. .. Ecophysiological and morphological comparison of two populations of Chlainomonas sp. (Chlorophyta) causing red snow on ice-covered lakes in the High Tatras and Austrian Alps. Eur J Phycol. 2018b;53:230–43. PubMed PMC
Pröschold T, Marin B, Schlösser UG et al. .. Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist. 2001;152:265–300. PubMed
Remias D. Cell Structure and Physiology of Alpine Snow and Ice Algae. In: Lütz C.(ed.) Plants in Alpine Regions: Cell Physiology of Adaptation and Survival Strategies. Wien: Springer, 2012, 175–85.
Remias D, Lütz-Meindl U, Lütz C. Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. Eur J Phycol. 2005;40:259–68.
Remias D, Karsten U, Lütz C et al. .. Physiological and morphological processes in the Alpine snow alga Chloromonas nivalis (Chlorophyceae) during cyst formation. Protoplasma. 2010;243:73–86. PubMed
Remias D, Wastian H, Lütz C et al. .. Insights into the biology and phylogeny of Chloromonas polyptera (Chlorophyta), an alga causing orange snow in Maritime Antarctica. Antarct Sci. 2013;25:648–56.
Remias D, Pichrtová M, Pangratz M et al. .. Ecophysiology, secondary pigments and ultrastructure of Chlainomonas sp. (Chlorophyta) from the European Alps compared with Chlamydomonas nivalis forming red snow. FEMS Microbiol Ecol. 2016;92:fiw030. PubMed PMC
Ross J. A Voyage of Discovery, Made Under the order of the Admirality, in His Majesty's Ships Isabella and Alexander for the Purpose of Exploring Baffin's Bay, and Inquiring into the Probability of a North-West Passage. London: John Murray, 1819.
Ross J.(ed.) Entdeckungsreise unter den Befehlen der Britischen Admiraltät mit den Königlichen Schiffen Isabella und Alexander um Baffins-Bay auszuforschen und die Möglichkeit einer nordwestlichen Durchfahrt zu Untersuchen. Leipzig: Friedrich Fleischer, 1820.
Sattler B, Remias D, Lütz C et al. .. Leben auf Schnee und Eis. In: Erschbamer B, Koch EM.(eds.) Glaziale und periglaziale Lebensräume im Raum Obergurgl. Innsbruck: Innsbruck University Press iup, 2010.
Schlichting HE., Jr The importance of airborne algae and Protozoa. J Air Pollut Control Assoc. 1969;19:946–51. PubMed
Schultz J, Wolf M. ITS2 sequence-structure analysis in phylogenetics: A how-to manual for molecular systematics. Mol Phylogen Evol. 2009;52:520–3. PubMed
Segawa T, Matsuzaki R, Takeuchi N et al. .. Bipolar dispersal of red-snow algae. Nat Commun. 2018;9:3094. PubMed PMC
Seibel PN, Müller T, Dandekar T et al. .. Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE. BMC Res Notes. 2008;1:91. PubMed PMC
Seibel PN, Müller T, Dandekar T et al. .. 4SALE - A tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinformatics. 2006;7:498. PubMed PMC
Shuttleworth RJ. Upon the colouring matter of red snow. The Edinburgh New Philosophical Journal. 1840a;29:54–64. (with 1 coloured plate).
Shuttleworth RJ. Nouvelles observations sur la matière colorant de la neige rouge. 1840b;25, Geneva.
Škaloud P, Rindi F. Ecological differentiation of cryptic species within an asexual protist morphospecies: a case study of filamentous green alga Klebsormidium (Streptophyta). J Eukaryot Microbiol. 2013;60:350–62. PubMed
Škaloud P, Steinová J, Řídká T et al. .. Assembling the challenging puzzle of algal biodiversity: species delimitation within the genus Asterochloris (Trebouxiophyceae, Chlorophyta). J Phycol. 2015;51:507–27. PubMed
Sommerfelt SC. Om den røde Sne, eller Sphærella nivalis Sommerf., Uredo nivalis Auct. Mag Nat videnskab. 1824;4:249–53.
Spijkerman E, Wacker A, Weithoff G et al. .. Elemental and fatty acid composition of snow algae in Arctic habitats. Front Microbiol. 2012;3:380. PubMed PMC
Sprengel C. Coccochloris nivalis Spreng. Syst Veg. 1827;4:373.
Stein JR, Amundsen CC. Studies on snow algae and fungi from the front range of Colorado. Can J Bot. 1967;45:2033–45.
Stibal M, Elster J, Šabacká M et al. .. Seasonal and diel changes in photosynthetic activity of the snow alga Chlamydomonas nivalis (Chlorophyceae) from Svalbard determined by pulse amplitude modulation fluorometry. FEMS Microbiol Ecol. 2007;59:265–73. PubMed
Sutton EA. The physiology and life histories of selected cryophytes of the Pacific Northwest Department of Oceanography volume PhD. Corvallis, OR: Oregon State University, 1970, 98.
Terashima M, Umezawa K, Mori S et al. .. Microbial community analysis of colored snow from an alpine snowfield in northern Japan reveals the prevalence of betaproteobacteria with snow algae. Front Microbiol. 2017;8:1481. PubMed PMC
Thomas WH, Broady PA. Distribution of coloured snow and associated algal genera in New Zealand. N Z J Bot. 1997;35:113–7.
VanWinkle‐Swift KP, Rickoll WL. The zygospore wall of Chlamydomonas monoica (Chlorophyceae): morphogenesis and evidence for the presence of sporopollenin. J Phycol. 2008;33:655–65.
Vogt C. Neige rouge. In: Desor E.(ed.) Excursions et séjours dans les glaciers et les hautes régions des Alpes, de M Agassiz et de ses compagnons de voyage. Neuchatel and Paris, 1844, 215–24.(16; pl. 1: fig. 1-5 (as 'Discerea nivalis‘).
Vukić J, Ulqini D, Šanda R. Occurrence of Knipowitschia goerneri Ahnelt, 1991 (Gobiidae) in southern Albania confirmed with molecular tools. J Appl Ichthyol. 2017;33:284–90.
Wayama M, Ota S, Matsuura H et al. .. Three-dimensional ultrastructural study of oil and astaxanthin accumulation during encystment in the green alga Haematococcus pluvialis. PLoS One. 2013;8:e53618. PubMed PMC
Wilkinson DM, Koumoutsaris S, Mitchell EAD et al. .. Modelling the effect of size on the aerial dispersal of microorganism. J Biogeogr. 2012;39:89–97.
Wille N. Algologische Notizen IX-XIV. Nyt Magazin for Naturvidenskaberne. 1903;41:89–185.
Wrangel FA. Microscopiska och Physiologiska Undersökningar rörande utvecklingen af Lepraria Kermesina och dess likhet med den sa kallade röda Snön. Tilläg till Anmärkningarne rörande Byssus Jolithus Linn. Kongl Vetenskaps-Akademiens Handlingar för år 1823, Stockholm. 1823;1:71–95.
Žárský V, Kalina T, Sulek J. Notes on the sexual reproduction of Chlamydomonas geitleri Ettl. Arch Protistenkd. 1985;130:343–53.
Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003;31:3406–15. PubMed PMC
Phylogeny and lipid profiles of snow-algae isolated from Norwegian red-snow microbiomes
Two New Kremastochrysopsis species, K. austriaca sp. nov. and K. americana sp. nov. (Chrysophyceae)1