Skip to main content

Advertisement

SpringerLink
Log in

The eurythermal adaptivity and temperature tolerance of a newly isolated psychrotolerant Arctic Chlorella sp.

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

A new strain of Chlorella sp. (Chlorella-Arc), isolated from Arctic glacier melt water, was found to have high specific growth rates (μ) between 3 and 27 °C, with a maximum specific growth rate of 0.85 day−1 at 15 °C, indicating that this strain was a eurythermal strain with a broad temperature tolerance range. To understand its acclimation strategies to low and high temperatures, the physiological and biochemical responses of the Chlorella-Arc to temperature were studied and compared with those of a temperate Chlorella pyrenoidosa strain (Chlorella-Temp). As indicated by declining F v/F m, photoinhibition occurred in Chlorella-Arc at low temperature. However, Chlorella-Arc reduced the size of the light-harvesting complex (LHC) to alleviate photoinhibition, as indicated by an increasing Chl a/b ratio with decreasing temperatures. Interestingly, Chlorella-Arc tended to secrete soluble sugar into the culture medium with increasing temperature, while its intracellular soluble sugar content did not vary with temperature changes, indicating that the algal cells might suffer from osmotic stress at high temperature, which could be adjusted by excretion of soluble sugar. Chlorella-Arc accumulated protein and lipids under lower temperatures (<15 °C), and its metabolism switched to synthesis of soluble sugar as temperatures rose. This reflects a flexible ability of Chlorella-Arc to regulate carbon and energy distribution when exposed to wide temperature shifts. More saturated fatty acids (SFA) in Chlorella-Arc than Chlorella-Temp also might serve as the energy source for growth in the cold and contribute to its cold tolerance.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ahn JW, Hwangbo K, Lee SY, Choi HG, Park YI, Liu JR, Jeong WJ (2012) A new Arctic Chlorella species for biodiesel production. Bioresour Technol 125:340–343

    Article  CAS  PubMed  Google Scholar 

  • An M, Mou S, Zhang X, Ye N, Zheng Z, Cao S, Xu D, Fan X, Wang Y, Miao J (2013) 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 

  • Anning T, Harris G, Geider RJ (2001) Thermal acclimation in the marine diatom Chaetoceros calcitrans (Bacillariophyceae). Eur J Phycol 36:233–241

    Article  Google Scholar 

  • Araujo SD, Garcia VMT (2005) Growth and biochemical composition of the diatom Chaetoceros cf. wighamii brightwell under different temperature, salinity and carbon dioxide levels. I. Protein, carbohydrates and lipids. Aquaculture 246:405–412

    Article  Google Scholar 

  • Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66

    Article  CAS  PubMed  Google Scholar 

  • Buchwal A, Rachlewicz G, Fonti P, Cherubini P, Gartner H (2013) Temperature modulates intra-plant growth of Salix polaris from a high Arctic site (Svalbard). Polar Biol 36:1305–1318

    Article  Google Scholar 

  • Chen D, Liu P, Shi J, Liu Y (2009) Microalgal polysaccharide and its application. Modern Chem Ind 29(S2):224–226, 228

    Google Scholar 

  • Chen Z, He C, Hu HH (2012) Temperature responses of growth, photosynthesis, fatty acid and nitrate reductase in Antarctic and temperate Stichococcus. Extremophiles 16:127–133

    Article  CAS  PubMed  Google Scholar 

  • Chong GL, Chu WL, Othman RY, Phang SM (2011) Differential gene expression of an Antarctic Chlorella in response to temperature stress. Polar Biol 34:637–645

    Article  Google Scholar 

  • Converti A, Casazza AA, Ortiz EY, Perego P, Del Borghi M (2009) Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem Eng Process 48:1146–1151

    Article  CAS  Google Scholar 

  • Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prásil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–17

    Google Scholar 

  • Dere S, Günes T, Sivaci R (1998) Spectrophotometric determination of chlorophyll-a, b and carotenoid contents of some algae species using different solvents. Turk J Bot 22:13–17

    Google Scholar 

  • Dias DP, Marenco RA (2006) Photoinhibition of photosynthesis in Minquartia guianensis and Swietenia macrophylla inferred by monitoring the initial fluorescence. Photosynthetica 44:235–240

    Article  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 

  • Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Eilers P, Peeters J (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42:199–215

    Article  Google Scholar 

  • Førland EJ, Benestad R, Hanssen-Bauer I, Haugen JE and Skaugen TE (2012). Temperature and precipitation development at Svalbard 1900–2100. Adv Meteorol. 2011:1–14. doi:10.1155/2011/893790

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta Gen Subj 990:87–92

    Article  CAS  Google Scholar 

  • Greene RM, Geider RJ, Kolber Z, Falkowski PG (1992) Iron-induced changes in light harvesting and photochemical energy-conversion processes in eukaryotic marine-algae. Plant Physiol 100:565–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han Y, Fan S, Zhang Q, Wang Y (2013) Effect of heat stress on the MDA, proline and soluble sugar content in leaf lettuce seedlings. Agric Sci 4:112–115

    CAS  Google Scholar 

  • Hawes I (1990) Effects of freezing and thawing on a species of Zygnema(Chlorophyta) from the Antarctic. Phycologia 29:326–331

    Article  Google Scholar 

  • He J, Wang G, Li S, K TL, Zheng S (2005) Community structure and biomasss of ice algae and phytoplankton in the Laptev Sea (Arctic) in spring. Chin J Polar Res 17:1–5

    Google Scholar 

  • Horn G, Hofweber R, Kremer W, Kalbitzer HR (2007) Structure and function of bacterial cold shock proteins. Cell Mol Life Sci 64:1457–1470

    Article  CAS  PubMed  Google Scholar 

  • Hu H, Li H, Xu X (2008) Alternative cold response modes in Chlorella (Chlorophyta, Trebouxiophyceae) from Antarctica. Phycologia 47:28–34

    Article  CAS  Google Scholar 

  • Huner NPA, Maxwell DP, Gray GR, Savitch LV, Laudenbach DE, Falk S (1995) Photosynthetic response do light and temperature—PSII excitation pressure and redox signaling. Acta Physiol Plant 17:167–176

    CAS  Google Scholar 

  • Jeong H, Lim JM, Park J, Sim YM, Choi HG, Lee J, Jeong WJ (2014) Plastid and mitochondrion genomic sequences from Arctic Chlorella sp. ArM0029B. BMC Genomics 15:286

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Laverty KS, Brown J, Nunez M, Brown L, Chagoya J, Burow M, Quigg A (2014) Effects of fluctuating temperature and silicate supply on the growth, biochemical composition and lipid accumulation of Nitzschia sp. Bioresour Technol 154:336–344

    Article  CAS  PubMed  Google Scholar 

  • Juneau P, Green BR, Harrison PJ (2005) Simulation of Pulse-Amplitude-Modulated (PAM) fluorescence: limitations of some PAM-parameters in studying environmental stress effects. Photosynthetica 43:75–83

    Article  CAS  Google Scholar 

  • Krembs C, Eicken H, Deming JW (2011) Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc Natl Acad Sci U S A 108:3653–3658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwak KJ, Park SJ, Han JH, Kim MK, Oh SH, Han YS, Kang H (2011) Structural determinants crucial to the RNA chaperone activity of glycine-rich RNA-binding proteins 4 and 7 in Arabidopsis thaliana during the cold adaptation process. J Exp Bot 62:4003–4011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Los DA, Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1:221–230

    CAS  PubMed  Google Scholar 

  • Melis A (1985) Functional properties of photosystem II in spinach chloroplasts. Biochim Biophys Acta 808:334–342

    Article  CAS  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 

  • Mock T, Valentin K (2004) Photosynthesis and cold acclimation: molecular evidence from a polar diatom. J Phycol 40:732–741

    Article  CAS  Google Scholar 

  • Morgan-Kiss R, Ivanov AG, Williams J, Khan M, Huner NPA (2002) 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 Biomembr 1561:251–265

    Article  CAS  Google Scholar 

  • Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner 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, Huner NPA, Priscu JC, Lisle JT, Hanson TE (2008) Identity and physiology of a 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 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Osipova S, Dudareva L, Bondarenko N, Nasarova A, Sokolova N, Obolkina L, Glyzina O, Timoshkin O (2009) Temporal variation in fatty acid composition of Ulothrix zonata (Chlorophyta) from ice and benthic communities of Lake Baikal. Phycologia 48:130–135

    Article  CAS  Google Scholar 

  • Pirt SJ (1975) Principles of microbe and cell cultivation. Blackwell, Oxford

    Google Scholar 

  • Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237

    Article  CAS  Google Scholar 

  • Renaud SM, Parry DL, Thinh LV (1994) Microalgae for use in tropical aquaculture I: Gross chemical and fatty acid composition of 12 species of microalgae from the Northern Territory, Australia. J Appl Phycol 6:337–345

    Article  CAS  Google Scholar 

  • Renaud SM, Zhou HC, Parry DL, Thinh LV, Woo KC (1995) Effect of temperature on the growth, total lipid content and fatty acid composition of recently isolated tropical microalgae Isochrysis sp., Nitzschia closterium, Nitzschia paleacea, and commercial species Isochrysis sp. (clone T ISO). J Appl Phycol 7:595–602

    Article  CAS  Google Scholar 

  • Renaud SM, Thinh L-V, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211:195–214

    Article  CAS  Google Scholar 

  • Rigor IG, Colony RL, Martin S (2000) Variations in surface air temperature observations in the Arctic, 1979–97. J Clim 13:896–914

    Article  Google Scholar 

  • Sang M, Wang M, Liu JH, Zhang CW, Li AF (2012) Effects of temperature, salinity, light intensity, and pH on the eicosapentaenoic acid production of Pinguiococcus pyrenoidosus. J Ocean Univ China 11:181–186

    Article  CAS  Google Scholar 

  • Seaburg KG, Parked BC, Wharton RA, Simmons GM (1981) Temperature-growth responses of algal isolates from Antarctic oases. J Phycol 17:353–360

    Article  Google Scholar 

  • Serodio J, Vieira S, Cruz S, Coelho H (2006) Rapid light-response curves of chlorophyll fluorescence in microalgae: relationship to steady-state light curves and non-photochemical quenching in benthic diatom-dominated assemblages. Photosynth Res 90:29–43

    Article  CAS  PubMed  Google Scholar 

  • Shukla SP, Kviderova J, Triska J, Elster J (2013) Chlorella mirabilis as a potential species for biomass production in low-temperature environment. Front Microbiol 4:97. doi:10.3389/fmicb.2013.00097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh SM, Elster J (2007) Cyanobacteria in Antarctic lake environments. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Netherlands, pp 303–320

    Chapter  Google Scholar 

  • Srivastava A, Guisse B, Greppin H, Strasser RJ (1997) Regulation of antenna structure and electron transport in Photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochim Biophys Acta Bioenerg 1320:95–106

    Article  CAS  Google Scholar 

  • Strain HH, Cope BT, Svec WA (1971) Analytical procedures for the isolation, identification, estimation, and investigation of the chlorophylls. Methods Enzymol 23:452–476

    Article  Google Scholar 

  • Teoh ML, Chu WL, Marchant H, Phang SM (2004) Influence of culture temperature on the growth, biochemical composition and fatty acid profiles of six Antarctic microalgae. J Appl Phycol 16:421–430

    Article  CAS  Google Scholar 

  • Teoh ML, Phang SM, Chu WL (2013) Response of Antarctic, temperate, and tropical microalgae to temperature stress. J Appl Phycol 25:285–297

    Article  CAS  Google Scholar 

  • Thompson PA, Guo MX, Harrison PJ, Whyte JN (1992) Effects of variation in temperature. II On the fatty acid composition of eight species of marine phytoplankton. J Phycol 28:488–497

    Article  CAS  Google Scholar 

  • Underwood GJ, Fietz S, Papadimitriou S, Thomas DN, Dieckmann G (2010) Distribution and composition of dissolved extracellular polymeric substances (EPS) in Antarctic sea ice. Mar Ecol Prog Ser 404:1–19

    Article  CAS  Google Scholar 

  • Walker JM (1994) The bicinchoninic acid (BCA) assay for protein quantitation. Methods Mol Biol 32:5–8

    CAS  PubMed  Google Scholar 

  • Wen XG, Gong HM, Lu CM (2005) Heat stress induces a reversible inhibition of electron transport at the acceptor side of photosystem II in a cyanobacterium Spirulina platensis. Plant Sci 168:1471–1476

    Article  CAS  Google Scholar 

  • White S, Anandraj A, Bux F (2011) PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. Bioresour Technol 102:1675–1682

    Article  CAS  PubMed  Google Scholar 

  • Wozniak B, Dera J, Ficek D, Ostrowska M, Majchrowski R (2002) Dependence of the photosynthesis quantum yield in oceans on environmental factors. Oceanologia 44:439–459

    Google Scholar 

Download references

Acknowledgments

The financial support from Hi-Tech Research and Development Program of China (No. 2012AA021706) and China Postdoctoral Science Foundation Funded Project (Nos. 2013M531370, 2014T70532, and 2014M561661) for this research is gratefully acknowledged.

Author information

Author notes

    Authors and Affiliations

    1. Jiangsu Provincial Key Laboratory of Marine Biology, College of Resources and Environmental Science, Nanjing Agricultural University, 1 Tongwei Road, Nanjing, 210095, Jiangsu, People’s Republic of China

      Kewei Cao, Meilin He, Weinan Yang, Shanmei Zou & Changhai Wang

    2. Key Laboratory for Polar Science of State Oceanic Administration, Polar Research Institute of China, Shanghai, 200136, People’s Republic of China

      Bo Chen & Wei Luo

    Authors
    1. Kewei Cao
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Meilin He
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Weinan Yang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Bo Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Wei Luo
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Shanmei Zou
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Changhai Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Changhai Wang.

    Additional information

    Kewei Cao and Meilin He contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary Fig. 1

    (JPEG 1314 kb)

    Supplementary Fig. 2

    (GIF 134 kb)

    High Resolution image (TIFF 6113 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Cao, K., He, M., Yang, W. et al. The eurythermal adaptivity and temperature tolerance of a newly isolated psychrotolerant Arctic Chlorella sp.. J Appl Phycol 28, 877–888 (2016). https://doi.org/10.1007/s10811-015-0627-0

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10811-015-0627-0

    Keywords

    Search

    Navigation