Skip to main content
Log in

Chilling out: the evolution and diversification of psychrophilic algae with a focus on Chlamydomonadales

  • Review
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The Earth is a cold place. Most of it exists at or below the freezing point of water. Although seemingly inhospitable, such extreme environments can harbour a variety of organisms, including psychrophiles, which can withstand intense cold and by definition cannot survive at more moderate temperatures. Eukaryotic algae often dominate and form the base of the food web in cold environments. Consequently, they are ideal systems for investigating the evolution, physiology, and biochemistry of photosynthesis under frigid conditions, which has implications for the origins of life, exobiology, and climate change. Here, we explore the evolution and diversification of photosynthetic eukaryotes in permanently cold climates. We highlight the known diversity of psychrophilic algae and the unique qualities that allow them to thrive in severe ecosystems where life exists at the edge. We focus on psychrophilic green algae from the Chlamydomonadales, discussing recent discoveries and directions for future research, and argue that they are among the best available models for studying psychrophily and life at the edge in photosynthetic eukaryotes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aletsee L, Jahnke J (1992) Growth and productivity of the psychrophilic marine diatoms Thalassiosira antarctica Comber and Nitzschia frigida Grunow in batch cultures at temperatures below the freezing point of sea water. Polar Biol 11:643–647

    Article  Google Scholar 

  • An M, Mou S, Zhang X, Ye N, Zheng Z, Cao S, Xu D, Fan X, Wang Y, Miao J (2013a) Temperature regulates fatty acid desaturases at a transcriptional level and modulates the fatty acid profile in the Antarctic microalga Chlamydomonas sp. ICE-L. Bioresour Technol 134:151–157

    Article  CAS  PubMed  Google Scholar 

  • An M, Mou S, Zhang X, Zheng Z, Ye N, Wang D, Zhang W, Miao J (2013b) Expression of fatty acid desaturase genes and fatty acid accumulation in Chlamydomonas sp. ICE-L under salt stress. Bioresour Technol 149:77–83

    Article  CAS  PubMed  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  CAS  PubMed  Google Scholar 

  • Baldisserotto C, Ferroni L, Moro I, Fasulo MP, Pancaldi S (2005) Modulations of the thylakoid system in snow xanthophycean alga cultured in the dark for two months: comparison between microspectrofluorimetric responses and morphological aspects. Protoplasma 226:125–135

    Article  CAS  PubMed  Google Scholar 

  • Becker S, Quartino ML, Campana GL, Bucolo P, Wiencke C, Bischof K (2011) The biology of an Antarctic rhodophyte, Palmaria decipiens: recent advances. Antarct Sci 23:419–430

    Article  Google Scholar 

  • Bidigare RR, Ondrusek ME, Kennicutt MC, Iturriaga R, Harvey HR, Hoham RW, Macko SA (1993) Evidence for a photoprotective function for secondary carotenoids of snow algae. J Psychol 29:427–434

    CAS  Google Scholar 

  • Bielewicz S, Bell E, Kong W, Friedberg I, Priscu JC, Morgan-Kiss RM (2011) Protist diversity in a permanently ice-covered Antarctic lake during the polar night transition. ISME J 5:1559–1564

    Article  PubMed  PubMed Central  Google Scholar 

  • Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Kuo A, Lindquist E, Lucas S, Pangilinan J, Polle J et al (2010) The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22:2943–2955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A, Dunigan DD, Gurnon J, Ladunga I, Lindquist E, Lucas S et al (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13:1–12

    Article  CAS  Google Scholar 

  • Bligh J, Johnson KG (1973) Glossary of terms for thermal physiology. J Appl Physiol 35:941–961

    CAS  PubMed  Google Scholar 

  • Bravo L, Saavedra-Mella FA, Vera F, Guerra A, Cavieres LA, Ivanov AG, Hüner NP, Corcuera LJ (2007) Effect of cold acclimation on the photosynthetic performance of two ecotypes of Colobanthus quitensis (Kunth) Bartl. J Exp Bot 58:3581–3590

    Article  CAS  PubMed  Google Scholar 

  • Brown SP, Olson BJSC, Jumpponen A (2015) Fungi and algae co-occur in snow: an issue of shared habitat or algal facilitation of heterotrophs. Arct Antarct Alp Res 47:429–749

    Article  Google Scholar 

  • Burki F (2014) The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb Perspect Biol 6:a016147. doi:10.1101/cshperspect.a016147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chaux F, Peltier G, Johnson X (2015) A security network in PSI photoprotection: regulation of photosynthetic control, NPQ and O2 photoreduction by cyclic electron flow. Front Plant Sci 6:875. doi:10.3389/fpls.2015.00875

    Article  PubMed  PubMed Central  Google Scholar 

  • Christmas NAM, Anesio AM, Sánchez-Baracaldo P (2015) Multiple adaptations to polar and alpine environments within cyanobacteria: a phylogenomic and Bayesian approach. Front Microbiol 6:1070. doi:10.3389/fmicb.2015.01070

    Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93

    Article  CAS  PubMed  Google Scholar 

  • Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Maruyama A, Arias MC, Ball SG, Gile GH, Hirakawa Y et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65

    Article  CAS  PubMed  Google Scholar 

  • Dahal K, Knowles VL, Plaxton WC, Hüner NPA (2014) Enhancement of photosynthetic performance, water use efficiency and grain yield during long-term growth under elevated CO2 in wheat and rye is growth temperature and cultivar dependant. Environ Exp Bot 106:207–220

    Article  CAS  Google Scholar 

  • Daugbjerg N, Marchant HJ, Thomsen HA (2000) Life history stages of Pyramimonas tychotreta (Prasinophyceae, Chlorophyta), a marine flagellate from the Ross Sea, Antarctica. Phycol Res 48:199–209

    Article  Google Scholar 

  • Delmont TO, Hammar KM, Ducklow HW, Yager PL, Post AF (2014) Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya. Front Microbiol 5:646. doi:10.3389/fmicb.2014.00646

    Article  PubMed  PubMed Central  Google Scholar 

  • Deming JW (2002) Psychrophiles and polar regions. Curr Opin Microbiol 5:301–309

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470

    Article  CAS  Google Scholar 

  • Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim Biophys Acta 1847:468–485

    Article  CAS  PubMed  Google Scholar 

  • Dietz K-J (2015) Efficient high light acclimation involves rapid processes at multiple mechanistic levels. J Exp Bot 66:2401–2414

    Article  CAS  PubMed  Google Scholar 

  • Dolhi JM, Maxwell DP, Morgan-Kiss RM (2013) Review: the Antarctic Chlamydomonas raudensis: an emerging model for cold adaptation of photosynthesis. Extremophiles 17:711–722

    Article  CAS  PubMed  Google Scholar 

  • Dolhi JM, Teufel AG, Kong W, Morgan-Kiss RM (2015) Diversity and spatial distribution of autotrophic communities within and between ice-covered Antarctic lakes (McMurdo Dry Valleys). Limnol Oceanogr 60:977–991

    Article  Google Scholar 

  • Eddie B, Krembs C, Neuer S (2008) Characterization and growth response to temperature and salinity of psychrophilic, halotolerant Chlamydomonas sp. ARC isolated from Chukchi sea ice. Mar Ecol Prog Ser 354:107–117

    Article  CAS  Google Scholar 

  • Feller G, Gerday C (2003) Psychrophilic enzymes: hot topic in cold adaptation. Nat Rev Microbiol 1:200–208

    Article  CAS  PubMed  Google Scholar 

  • Figueroa-Martinez F, Nedelcu AM, Smith DR, Reyes-Prieto A (2015) When the lights go out: the evolutionary fate of free-living colorless green algae. New Phytol 206:972–982

    Article  PubMed  PubMed Central  Google Scholar 

  • Flaim G, Rott E, Frassanito R, Guella G, Obertegger U (2010) Eco-fingerprinting of the dinoflagellate Borghiella dodgei: experimental evidence of a specific environmental niche. Hydrobiologia 639:85–98

    Article  CAS  Google Scholar 

  • Gao Z, Li D, Meng C, Xu D, Zhang X, Ye N (2013) Survival and proliferation characteristics of the microalga Chlamydomonas sp. ICE-L after hypergravitational stress pretreatment. Icarus 226:971–979

    Article  Google Scholar 

  • Gómez I, Wulff A, Roleda MY, Huovinen P, Karsten U, Quartino ML, Dunton K, Wiencke C (2009) Light and temperature demands of marine benthic macroalgae and seaweeds in polar regions. Bot Mar 52:593–608

    Article  Google Scholar 

  • Gudynaite-Savitch L, Gretes M, Morgan-Kiss R, Savitch L, Simmonds J, Kohalmi S, Hüner NPA (2006) Cytochrome f from the Antarctic psychrophile, Chlamydomonas raudensis UWO241: structure, sequence, and complementation in the mesophile, Chlamydomonas reinhardtii. Mol Gen Genomics 275:387–398

    Article  CAS  Google Scholar 

  • Guiry MD, Guiry GM (2016) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. http://www.algaebase.org

  • Hanschen ER, Marriage TN, Ferris PJ, Hamaji T, Toyoda A, Fujiyama A, Neme R, Noguchi H et al (2016) The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity. Nat Commun 7:11370. doi:10.1038/ncomms11370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffman PF, Schrag DP (2002) The snowball Earth hypothesis: testing the limits of global change. Terra Nova 14:129–155

    Article  CAS  Google Scholar 

  • Hoham RW, Duval B (2001) Microbial ecology of snow and freshwater ice with emphasis on snow algae. In: Johns HG, Pomeroy JW, Walker DA, Hoham RS (eds) Snow ecology. Cambridge University Press, Cambridge, pp 186–203

    Google Scholar 

  • Hüner NPA, Grodzinski B (2011) Photosynthesis and photoautotrophy. In: Moo-Young M (ed) Comprehensive biotechnology, 2nd edn. Elsevier, Amsterdam, pp 315–322

    Chapter  Google Scholar 

  • Hüner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Article  Google Scholar 

  • Hüner NPA, Bode R, Dahal K, Busch FA, Possmayer M, Szyszka B, Rosso D, Ensminger I, Krol M, Ivanov AG, Maxwell DP (2013) Shedding some light on cold acclimation, cold adaptation, and phenotypic plasticity. Botany 91:127–136

    Article  CAS  Google Scholar 

  • Hyde WT, Crowley TJ, Baum SK, Peltier RW (2000) Neoproterozoic ‘snowball Earth’ simulations with a coupled climate/ice-sheet model. Nature 405:425–429

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2007) Climate change 2007: The physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

  • Jungblut AD, Vincent WF, Lovejoy C (2012) Eukaryotes in Arctic and Antarctic cyanobacterial mats. FEMS Microbiol Ecol 82:416–428

    Article  CAS  PubMed  Google Scholar 

  • Kaczmarska I, Mather L, Luddington IA, Muise F, Ehrman JM (2014) Cryptic diversity in a cosmopolitan diatom known as Asterionellopsis glacialis (Flagilariaceae): implications for ecology, biogeography and taxonomy. Am J Bot 101:267–286

    Article  PubMed  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657

    Article  CAS  PubMed  Google Scholar 

  • Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607

    Article  CAS  PubMed  Google Scholar 

  • Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, Armbrust EV, Archibald JM, Bharti AK, Bell CJ et al (2014) The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol 12:e1001889. doi:10.1371/journal.pbio.1001889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kennicutt MC II, Chown SL (2014) Polar research: six priorities for Antarctic science. Nature 512:23–25

    Article  CAS  PubMed  Google Scholar 

  • Kirchhoff H (2013) Architectural switches in plant thylakoid membranes. Photosynth Res 116:481–487

    Article  CAS  PubMed  Google Scholar 

  • Klochkova TA, Kwak MS, Han JW, Motomura T, Nagasato C, Kim GH (2013) Cold-tolerant strain of Haematococcus pluvialis (Haematococcaceae, Chlorophyta) from Blomstrandhalvoya (Svalbard). Algae 28:185–192

    Article  CAS  Google Scholar 

  • Koch F, Marcoval MA, Panzeca C, Bruland KW, Sanudo-Wilhelmy SA, Gobler CJ (2011) The effect of vitamin B12 on phytoplankton growth and community structure in the Gulf of Alaska. Limnol Oceanogr 56:1023–1034

    Article  CAS  Google Scholar 

  • Komárek J, Nedbalová L (2007) Green cryosestic algae. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Dordrecht, pp 323–342

    Google Scholar 

  • Kvíderová J (2011) Research on cryosestic communities in Svalbard: the snow alga of temporary snowfields in Petuniabukta, Central Svalbard. Czech Polar Rep 2:8–19

    Article  Google Scholar 

  • Laybourne-Parry J, Pearce DA (2007) The biodiversity and ecology of Antarctic lakes: models for evolution. Philos Trans R Soc Lond B 362:2273–2289

    Article  CAS  Google Scholar 

  • Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31:1–46

    Article  Google Scholar 

  • Lemoine Y, Schoefs B (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177

    Article  CAS  PubMed  Google Scholar 

  • Li W, Podar M, Morgan-Kiss RM (2016) Ultrastructural and single-cell-level characterization reveals metabolic diversity in microbial eukaryote community from an ice-covered Antarctic lake. Appl Environ Microbiol 82:3659–3670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Libby E, Ratcliff WC (2014) Ratcheting the evolution of multicellularity. Science 346:426–427

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Huang XH, Wang XL, Zhang XC, Li GY (2006a) Phylogenetic studies on two strains of Antarctic ice algae based on morphological and molecular characteristics. Phycologia 45:190–198

    Article  Google Scholar 

  • Liu S, Liu C, Huang X, Chai Y, Cong B (2006b) Optimization of parameters for isolation of protoplasts from the antarctic sea ice alga Chlamydomonas sp. ICE-L. J Appl Phycol 18:783–786

    Article  CAS  Google Scholar 

  • Liu Y, Ding Y, Jian J-C, Wu Z-H, Miao J-L (2011) Prokaryotic expression and its conditional optimization of glutathione reductase gene of antarctic Chlamydomonas sp. ICE-L. Oceanol Limnol Sin 42:817–821

    CAS  Google Scholar 

  • Liu C, Wu G, Huang X, Liu S, Cong B (2012) Validation of housekeeping genes for gene expression studies in an ice alga Chlamydomonas during freezing acclimation. Extremophiles 16:419–425

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Wang X, Wang X, Sun X (2016) Acclimation of Antarctic Chlamydomonas to the sea-ice environment: a transcriptomic analysis. Extremophiles 20:437–450

    Article  CAS  PubMed  Google Scholar 

  • Lukeš M, Procházková L, Shmidt V, Nedbalová L, Kaftan D (2014) Temperature dependence of photosynthesis and thylakoid lipid composition in the red snow alga Chlamydomonas cf. nivalis (Chlorophyceae). FEMS Microbiol Ecol 89:303–315

    Article  PubMed  CAS  Google Scholar 

  • Lynch M (2007) The frailty of adaptive hypotheses for the origins of organismal complexity. PNAS USA 104:8597–8604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyon BR, Mock T (2014) Polar microalgae: new approaches towards understanding adaptations to an extreme and changing environment. Biology 3:56–80

    Article  PubMed  PubMed Central  Google Scholar 

  • Margesin R, Schinner F, Marx J-C, Gerday C (2007) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin

    Google Scholar 

  • Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima S, Mori T, Nishida K, Yagisawa F et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  CAS  PubMed  Google Scholar 

  • Matsuzaki R, Kawai-Toyooka H, Hara Y, Nozaki H (2015) Revisiting the taxonomic significance of aplanozygote morphologies of two cosmopolitan snow species of the genus Chloromonas (Volvocales, Chlorophyceae). Phycologia 54:491–502

    Article  Google Scholar 

  • McKay CP (2000) Thickness of tropical ice and photosynthesis on a snowball Earth. Geophys Res Lett 27:2153–2156

    Article  CAS  PubMed  Google Scholar 

  • McKie-Krisberg ZM, Gast RJ, Sanders RW (2015) Physiological responses of three species of Antarctic mixotrophic phytoflagellates to changes in light and dissolved nutrients. Microb Ecol 70:21–29

    Article  CAS  PubMed  Google Scholar 

  • Melis A (1998) Photostasis in plants. In: Williams TP, Thistle AB (eds) Photostasis and related phenomena. Plenum Press, New York, pp 207–220

    Chapter  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mock T, Hoch N (2005) Long-term temperature acclimation of photosynthesis in steady-state cultures of the polar diatom Fragilariopsis cylindrus. Photosynth Res 85:307–317

    Article  CAS  PubMed  Google Scholar 

  • Morgan-Kiss RM, Ivanov AG, Hüner NPA (2002a) The Antarctic psychrophile, Chlamydomonas subcaudata, is deficient in state I–state II transitions. Planta 214:435–445

    Article  CAS  PubMed  Google Scholar 

  • Morgan-Kiss R, Ivanov AG, Williams J, Mobashsher K, Hüner NPA (2002b) Differential thermal effects on the energy distribution between photosystem II and photosystem I in thylakoid membranes of a psychrophilic and a mesophilic alga. Biochim Biophys Acta 1561:251–265

    Article  CAS  PubMed  Google Scholar 

  • Morgan-Kiss RM, Priscu JS, Pocock T, Gudynaite-Savitch L, Hüner NPA (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70:222–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan-Kiss RM, Ivanov AG, Modla S, Czymmek K, Hüner NPA, Priscu JC, Lisle JT, Hanson TE (2008) Identity and physiology of new psychrophilic eukaryotic green alga, Chlorella sp., strain BI, isolated from a transitory pond near Bratina Island, Antarctica. Extremophiles 12:701–711

    Article  CAS  PubMed  Google Scholar 

  • Morgan-Kiss RM, Lizzote MP, Kong W, Priscu JC (2016) Photoadaptation to the polar night by phytoplankton in a permanently ice-covered Antarctic lake. Limnol Oceanogr 61:3–13

    Article  CAS  Google Scholar 

  • Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144–167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mou S, Xu D, Ye N, Zhang X, Liang C, Liang Q, Zhen Z, Zhuang Z, Miao J (2012) Rapid estimation of lipid content in an Antarctic ice alga (Chlamydomonas sp.) using the lipophilic fluorescent dye BODIPY505/515. J Appl Phycol 24:1169–1176

    Article  CAS  Google Scholar 

  • Mou S, Zhang X, Ye N, Miao J, Cao S, Xu D, Fan X, An M (2013) Analysis of Delta pH and the xanthophyll cycle in NPQ of the Antarctic sea ice alga Chlamydomonas sp. ICE-L. Extremophiles 17:477–484

    Article  CAS  PubMed  Google Scholar 

  • Mou S, Zhang X, Miao J, Zheng Z, Xu D, Ye N (2015) Reference genes for gene expression normalization in Chlamydomonas sp. ICE-L by quantitative real-time RT-PCR. J Plant Biochem Biotechnol 24:276–282

    Article  CAS  Google Scholar 

  • Müller T, Bleiβ W, Martin CD, Rogaschewski S, Fuhr G (1998) Snow algae from northwest Svalbard: their identification, distribution, pigment and nutrient content. Polar Biol 20:14–32

    Article  Google Scholar 

  • Nakada T, Misawa K, Nozaki H (2008) Molecular systematics of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18s rRNA phylogenetic analyses. Mol Phylogenet Evol 49:281–291

    Article  CAS  Google Scholar 

  • Neale PJ, Priscu JC (1995) The photosynthetic apparatus of phytoplankton from a perennially ice-covered Antarctic lake: acclimation to an extreme shade environment. Plant Cell Physiol 36:253–263

    Article  CAS  Google Scholar 

  • Newsted WJ, Hüner NPA (1987) Major sclerotial polypeptides of psychrophilic fungi: temperature regulation of in vivo synthesis in vegetative hyphae. Can J Bot 66:1755–1761

    Google Scholar 

  • Newsted WJ, Hüner NPA, Insell JP, Griffith M, van Huystee RB (1985) The effects of temperature on the growth and polypeptide composition of several snow mold species. Can J Bot 63:2311–2318

    Article  CAS  Google Scholar 

  • Nisbet EG, Fowler CMR (1999) Archaean metabolic evolution in microbial mats. Proc R Soc Lond B Biol 226:2375–2382

    Article  Google Scholar 

  • Panikov NS, Sizova MV (2006) Growth kinetics of microorganisms isolated from Alaskan soil and permafrost in solid media frozen down to −35 °C. FEMS Microbiol Ecol 59:500–512

    Article  PubMed  CAS  Google Scholar 

  • Pocock TH, Lachance M-A, Pröschold T, Priscu JC, Kim SS, Hüner NPA (2004) Identification of psychrophilic green alga from lake Bonney, Antarctica: Chlamydomonas raudensis Ettl. (UWO 241) Chlorophyceae. J Phycol 40:1138–1148

    Article  Google Scholar 

  • Pocock TH, Koziak A, Rosso D, Falk S, Hüner NPA (2007) Chlamydomonas raudensis (UWO241), Chlorophyceae, exhibits the capacity for rapid D1 repair in response to chronic photoinhibition at low temperature. J Phycol 43:924–936

    Article  CAS  Google Scholar 

  • Possmayer M, Gupta RK, Szyszka-Mroz B, Maxwell DP, Lachance M-A, Hüner NPA, Smith DR (2016) Resolving the phylogenetic relationship between Chlamydomonas sp. UWO241 and Chlamydomonas raudensis SAG 49.72 (Chlorophyceae) with nuclear and plastid DNA sequences. J Phycol 52:305–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK et al (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quartino ML, Zaixso HE, Boraso de Zaixso AL (2005) Biological and environmental characterization of marine macroalgal assemblages in Potter Cove, South Shetland Islands, Antarctica. Bot Mar 48:187–197

    Article  Google Scholar 

  • Quesada A, Vincent WF (2012) Cyanobacteria in the cryosphere: snow, ice and extreme cold. In: Whitton BA (ed) Ecology of cyanobacteria II. Springer, Amsterdam, pp 387–399

    Chapter  Google Scholar 

  • Raven JA (1997) Phagotrophy in phototrophs. Limnol Oceanogr 42:198–205

    Article  CAS  Google Scholar 

  • Raymond JA (2014) The ice-binding proteins of a snow alga, Chloromonas brevispina: probable acquisition by horizontal gene transfer. Extremophiles 18:987–994

    Article  CAS  PubMed  Google Scholar 

  • Raymond JA, Kim HJ (2012) Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLoS ONE 7:e35968. doi:10.1371/journal.pone.0035968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond JA, Morgan-Kiss R (2013) Separate origins of ice-binding proteins in Antarctic Chlamydomonas species. PLoS ONE 8:e59186. doi:10.1371/journal.pone.0059186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Remias D, Lutz-Meindl U, Lutz C (2005) Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. Eur J Phycol 40:259–268

    Article  CAS  Google Scholar 

  • Remias D, Albert A, Luetz C (2010a) Effects of realistically simulated, elevated UV irradiation on photosynthesis and pigment composition of the alpine snow alga Chlamydomonas nivalis and the arctic soil alga Tetracystis sp. (Chlorophyceae). Photosynthetica 48:269–277

    Article  CAS  Google Scholar 

  • Remias D, Karsten U, Luetz C, Leya T (2010b) Physiological and morphological processes in the Alpine snow alga Chloromonas nivalis (Chlorophyceae) during cyst formation. Protoplasma 243:73–86

    Article  PubMed  Google Scholar 

  • Remias D, Pichrtova M, Pangratz M, Luetz C, Holzinger A (2016) Ecophysiology, secondary pigments and ultrastructure of Chlainomonas sp. (Chlorophyta) from the European Alps compared with Chlamydomonas nivalis forming red snow. FEMS Microbiol Ecol 92:fiw030. doi:10.1093/femsec/fiw030

    Article  PubMed  PubMed Central  Google Scholar 

  • Řezanka T, Nedbalová L, Kolouchova I, Sigler K (2013) LC-MS/APCI identification of glucoside esters and diesters of astaxanthin from the snow alga Chlamydomonas nivalis including their optical stereoisomers. Phytochemistry 88:34–42

    Article  PubMed  CAS  Google Scholar 

  • Rochaix J-D (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65:287–309

    Article  CAS  PubMed  Google Scholar 

  • Rothschild LJ (2008) The evolution of photosynthesis…again? Philos Trans R Soc Lond B 363:2787–2801

    Article  CAS  Google Scholar 

  • Schlichting CD (2008) Hidden reaction norms, cryptic genetic variation and evolvability. Ann N Y Acad Sci 1133:187–203

    Article  PubMed  Google Scholar 

  • Schönknecht G, Weber APM, Lercher MJ (2014) Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. BioEssays 36:9–20

    Article  PubMed  CAS  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui KS, Williams TJ, Wilkins D, Yau S, Allen MA, Brown MV, Lauro FM, Cavicchioli R (2013) Psychrophiles. Annu Rev Earth Planet Sci 41:87–115

    Article  CAS  Google Scholar 

  • Szyszka-Mroz B, Pittock PP, Ivanov AG, Hüner NPA (2015) The Antarctic psychrophile Chlamydomonas sp. UWO241 preferentially phosphorylates a photosystem I–cytochrome b6/f supercomplex. Plant Physiol 169:717–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thingstad TF, Havskum H, Garde K, Riemann B (1996) On the strategy of “eating your competitor”: a mathematical analysis of algal mixotrophy. Ecology 77:2108–2118

    Article  Google Scholar 

  • Tikkanen M, Aro AM (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci 19:10–17

    Article  CAS  PubMed  Google Scholar 

  • Umen JG, Olson BJSC (2012) Genomics of volvocine algae. Adv Bot Res 64:185–243

    Article  PubMed  PubMed Central  Google Scholar 

  • Varshney P, Mikulic P, Vonshak A, Beardall J, Wangikar PP (2015) Extremophilic micro-algae and their potential contribution to biotechnology. Bioresour Technol 184:363–382

    Article  CAS  PubMed  Google Scholar 

  • Vincent WF, Mueller D, van Hove P, Howard-Williams P (2004) Glacial periods on early Earth and implications for the evolution of life. In: Seckbach J (ed) Cellular origin, life in extreme habitats and astrobiology. Springer, Dordrecht, pp 481–501

    Google Scholar 

  • Wang DS, Xu D, Wang YT, Fan X, Ye NH, Wang WQ, Zhang XW, Mou SL, Guan Z (2015) Adaptation involved in nitrogen metabolism in sea ice alga Chlamydomonas sp. ICE-L to Antarctic extreme environments. J Appl Phycol 27:787–796

    Article  CAS  Google Scholar 

  • West NJ, Obernosterer I, Zemb O, Lebaron P (2008) Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. Environ Microbiol 10:738–756

    Article  CAS  PubMed  Google Scholar 

  • West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. PNAS USA 102:6543–6549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiencke C (1990) Seasonality of red and green macroalgae from Antarctica—a long-term culture study under fluctuating Antarctic daylengths. Polar Biol 10:601–607

    Article  Google Scholar 

  • Wiencke C, Bartsch I, Bischoff B, Peters AF, Breeman AM (1994) Temperature requirements and biogeography of Antarctic, Arctic and amphiequatorial seaweeds. Bot Mar 37:247–259

    Article  Google Scholar 

  • Wu G, Liu C, Liu S, Cong B, Huang X (2010) High-quality RNA preparation for cDNA library construction of the Antarctic sea-ice alga Chlamydomonas sp. ICE-L. J Appl Phycol 22:779–783

    Article  CAS  Google Scholar 

  • Xavier JC, Brandt A, Ropert-Coudert Y, Badhe R, Gutt J, Havermans C, Jones C, Costa ES, Lochte K, Schloss IR, Kinnicutt MC II, Sutherland WJ (2016) Future challenges in Southern Ocean ecology research. Front Mar Sci 3:94. doi:10.3389/fmars.2016.00094

    Article  Google Scholar 

  • Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693

    Article  CAS  PubMed  Google Scholar 

  • Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG et al (2014) Three keys to the radiation of angiosperms to frozen environments. Nature 506:89–92

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Liu S, Cong B, Wu G, Liu C, Lin X, Shen J, Huang X (2011) A novel omega-3 fatty acid desaturase involved in acclimation processes of polar condition from Antarctic ice algae Chlamydomonas sp. ICE-L. Mar Biotechnol 13:393–401

    Article  CAS  PubMed  Google Scholar 

  • Zubkov MV, Tarran GA (2008) High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455:224–226

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

MC is supported by a postdoctoral fellowship from the Natural Sciences and Engineering Research Council (NSERC) of Canada. NPAH and DRS are each funded by a Discovery Grant from NSERC. NPAH is grateful for support through the Canadian Foundation for Innovation and the Canada Research Chairs Programme.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Norman P. A. Hüner.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online resource 1

Biodiversity and distribution of confirmed psychrophilic algae to date. Only algae with temperature survival limits confirmed in laboratory-grown culture experiments are included in this analysis. Species that have been isolated from cold environments but their growth rates have not been tested in laboratory experiment are not included in this table, since such species could be psychrotrophs. Similarly, efforts are being made to describe the distribution and diversity of phototrophs in cold environments using nucleic acid sequencing of environmental samples (Dolhi et al. 2015; Bielewicz et al. 2011); however, such findings are not included in this table since the psychrophilic nature of the organisms cannot be confirmed. Algae culture collections, such as the Bigelow National Center for Marine Algae and Microbiota, contain a number of organisms isolated from permanently cold environments (https://ncma.bigelow.org/products/algae/cold-water); however, most of these organisms have not been characterized in terms of their psychrophilic traits and, thus, were not included in this table. Note that some species have an uncertain taxonomy and could represent a polyphyletic clade instead of a single species (indicated by *). In certain cases, the growth of the organisms depends not only on cold temperatures, but also on a different environmental factor (salinity or interactions with other organisms; indicated by **). Some species have been isolated from multiple cold environments; however, the habitats in the table correspond to the original specie description (indicated by ***) (XLSX 20 kb)

Online resource 2

A summary of permanent environmental stresses faced by UWO241 in its natural habitat and the adaptations developed in response to these conditions. Shaded boxes correspond to work that is planned or currently in progress (PDF 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cvetkovska, M., Hüner, N.P.A. & Smith, D.R. Chilling out: the evolution and diversification of psychrophilic algae with a focus on Chlamydomonadales. Polar Biol 40, 1169–1184 (2017). https://doi.org/10.1007/s00300-016-2045-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-016-2045-4

Keywords

Navigation