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Snow and Glacial Algae: a Review1 J. Phycol. 56, 264–282 (2020) © 2019 The Authors. Journal of Phycology published by Wiley Periodicals, Inc. on behalf of Phycological Society of America This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. DOI: 10.1111/jpy.12952 P UBLICATION R EVIEW SNOW AND GLACIAL ALGAE: A REVIEW1 Ronald W. Hoham2 Department of Biology, Colgate University, Hamilton, New York 13346, USA and Daniel Remias2 School of Engineering, University of Applied Sciences Upper Austria, Wels 4600, Austria Snow or glacial algae are found on all continents, Key index words: albedo; community structure; and most species are in the Chlamydomonadales cryophilic; environmental parameters; genomics; gla- (Chlorophyta) and Zygnematales (Streptophyta). cial algae; life cycles; primary productivity; sec- Other algal groups include euglenoids, cryptomonads, ondary metabolites; snow algae chrysophytes, dinoflagellates, and cyanobacteria. They Abbreviations: Cr, Chloromonas; Cd, Chlamydomonas; may live under extreme conditions of temperatures Ch Chlainomonas ° , ; DIC, dissolved inorganic carbon; near 0 C, high irradiance levels in open exposures, DOC, dissolved organic carbon; DON, dissolved low irradiance levels under tree canopies or deep in organic nitrogen; HTS, high-throughput sequencing; snow, acidic pH, low conductivity, and desiccation IBPs, ice binding proteins; MAAs, mycosporine-like after snow melt. These primary producers may color amino acids; OTUs, operational taxonomic units; snow green, golden-brown, red, pink, orange, or PUFAs, polyunsaturated fatty acids; TXT, triple purple-grey, and they are part of communities that crossover triangle include other eukaryotes, bacteria, archaea, viruses, and fungi. They are an important component of the global biosphere and carbon and water cycles. Life Snow may cover up to 32% of the Earth’s land cycles in the Chlamydomonas–Chloromonas–Chlaino- surface and ice up to 11% (Allison et al. 2018). This monas complex include migration of flagellates in review on algae that live in these habitats is an liquid water and formation of resistant cysts, many of update since Hoham and Duval (2001) in the com- which were identified previously as other algae. prehensive reference on snow ecology (Jones et al. Species differentiation has been updated through the 2001), and we use the original taxonomic names use of metagenomics, lipidomics, high-throughput used by authors in their papers even though sequencing (HTS), multi-gene analysis, and ITS. changes have been made since then. Previous over- Secondary metabolites (astaxanthin in snow algae and views in this area of phycology include those of Kol purpurogallin in glacial algae) protect chloroplasts (1968), Hoham (1980), and Hoham and Ling and nuclei from damaging PAR and UV, and ice (2000). Additional reports on cell structure and binding proteins (IBPs) and polyunsaturated fatty physiology (Remias 2012), adaptation strategies acids (PUFAs) reduce cell damage in subfreezing (Leya 2013), ecology, systematics, and life cycles temperatures. Molecular phylogenies reveal that snow (Komarek and Nedbalova 2007), glacial ice algae algae in the Chlamydomonas–Chloromonas complex (Williamson et al. 2019), glacial ecosystems (Hod- have invaded the snow habitat at least twice, and some son et al. 2008), and cold alpine regions (Sattler species are polyphyletic. Snow and glacial algae et al. 2012) have further contributed to our under- reduce albedo, accelerate the melt of snowpacks and standing of these algae. Organisms regarded as true glaciers, and are used to monitor climate change. snow and glacial algae thrive in a liquid water film Selected strains of these algae have potential for between melting snow and ice crystals, and usually producing food or fuel products. do not propagate outside of this habitat. Otherwise, 1Received 23 August 2019. Accepted 20 November 2019. First microalgae of different origins such as bare soils Published Online 11 December 2019. Published Online 29 February and from lichen fragments may be passively trans- 2020, Wiley Online Library (wileyonlinelibrary.com). ported onto snow and ice surfaces by meltwater 2Authors for correspondence: e-mails: [email protected]; rho- inflow or wind. Under certain conditions, they may [email protected]. even cause a snow discoloration, but are not Editorial Responsibility: S. Krueger-Hadfield (Associate Editor) The copyright line for this article was changed on 08 May 2020 regarded as true snow or glacial algae in the strict after original online publication. sense. Microbial communities that inhabit snow and 264 SNOW ALGAE/GLACIAL ALGAE 265 glacial ice are not only abundant and taxonomically growth (Hoham et al. 2008b), and interactions of diverse and complex in terms of their interactions, light on growth and life cycle development (Hoham but their role in global biogeochemical cycles has et al. 2000a,b, 2009). Snow and glacial algae are been underestimated (Maccario et al. 2015, Havig examples of how life can adapt to harsh environmen- and Hamilton 2019, Williamson et al. 2019). Algal tal conditions in terms of solar irradiance, low tem- blooms typically occur from one to several weeks peratures or nutrients, and show that phototroph during spring and summer when air temperatures extremophiles perform well in putative extreme habi- P remain above 0°C in semi-permanent snowfields tats such as melting snowpacks or glacial surfaces. As UBLICATION and glaciers in temperate, mountainous, and polar a result, these microbes have been considered as regions (Hoham and Duval 2001). The most promi- Earth analogs for life outside our planet (Havig and nent snow algae belong to the Chlamydomonadales Hamilton 2019, Vimercati et al. 2019b). (Chlorophyta) and glacial algae to the Zygnematales Diversity and community structure. Snow algae have (Streptophyta). Yet, other groups of algae may color been found on every continent and are a global phe- snow including euglenoids, cryptomonads, chryso- nomenon. Their distributions are limited to suitable phytes, and dinoflagellates (Hoham and Duval habitats depending on snow or permanent ice, eco- R 2001). When the concentration of cells reaches a logical, and climatic conditions. Since 2000, they have EVIEW À population in several thousands of cells mL 1,a been recorded from all continents and geographic snow or ice discoloration takes place. The color and regions (Table 1) except Australia where they were its intensity depend on the pigment composition reported previously from the Snowy Mountains and population density. When chlorophylls domi- (Marchant 1982). Communities of snow algae are nate, green snow appears (Chlamydomonadales; diverse and taxonomically broad, comprised of clones Figs. 1a and 2a). If primary carotenoids like fucox- with discrete patches, and are heterogeneous (Brown anthin dominate, golden-brown snow appears et al. 2016). Even though they color the snow red, (Chrysophyceae; Figs. 1b and 2b). In many cases, green, orange, or golden-brown, they still may be an the pigment composition can vary depending on important component of snow even in the absence of the stage of the life cycle. Most prominent are sec- these colors (Brown and Jumpponen 2019). Green ondary carotenoids like astaxanthin of certain snow in the Laurentian Mountains, Quebec, was À chlamydomonadalean green algae, which dominate defined as having more than 4,000 cells Á mL 1, over chlorophylls to cause orange (Figs. 1c and 2c), whereas white snow had populations below that level pink (Figs. 1d and 2d), and red snow (Figs. 1e and (Hoham and Duval 2001). 2e). Purple to brown phenols abundantly present in When using HTS to evaluate snowfields such as glacial streptophytic algae (Zygnematales) cause those dominated by green algae, HTS outputs need grey snow or purple ice (Figs. 1f and 2f); however, to be thoroughly checked when organisms are this color is frequently masked by dark cryoconite poorly represented in databases, which is the case particles which are common at surfaces of old ice. for cryoflora (Lutz et al. 2019). An optimized work- Molecular phylogenies have enhanced our under- flow was recommended to include a consistent sam- standing of the evolutionary history of snow species pling, a two-molecular marker approach, light in the Chlamydomonas–Chloromonas–Chlainomonas microscopy-based guidance, generations of appro- complex (Hoham et al. 2002, 2006, Novis et al. 2008, priate reference sequences, and final manual verifi- Muramoto et al. 2010, Remias et al. 2013b, 2016, cation of taxonomic assignments. HTS and 2018, Matsuzaki et al. 2014, 2015, 2018, 2019, subsequent oligotyping on the Greenland Ice Sheet Prochazkova et al. 2019a,b). Metagenomics (Hisa- showed an extremely low algal diversity of the strep- kawa et al. 2015, Lutz et al. 2015a, Raymond 2016, tophytes, Ancylonema nordenskioldii€ and Mesotaenium Maccario et al. 2019), lipidomics (Rezanka et al. berggrenii that dominated at all sites (Lutz et al. 2014), and HTS (Lutz et al. 2015a, 2018, 2019, 2018). Green snow represented a wet, carbon, and Segawa et al. 2018) have significantly contributed nutrient-rich environment dominated by Microglena, new information. Samples from difficult inaccessible whereas red snow was dry, nutrient poor, and colo- regions and satellite imaging of large ice sheets show- nized by Chloromonas (Lutz et al. 2015b). Population ing algal abundance or melting processes has densities
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