Journal of Applied Phycology

, Volume 25, Issue 1, pp 285–297 | Cite as

Response of Antarctic, temperate, and tropical microalgae to temperature stress

Article

Abstract

The global temperature increase has significant implications on the survival of microalgae which form the basis of all aquatic food webs. The aim of this study was to compare the response of similar taxa of microalgae from the Antarctic (Chlamydomonas UMACC 229, Chlorella UMACC 237, and Navicula glaciei UMACC 231), temperate (Chlamydomonas augustae UMACC 247, Chlorella vulgaris UMACC 248, and Navicula incerta UMACC 249), and tropical (C. augustae UMACC 246, C. vulgaris UMACC 001, and Amphiprora UMACC 239) regions to changing temperature. The Antarctic, temperate, and tropical strains were grown over specific temperature ranges of 4 °C to 30 °C, 4 °C to 32 °C, and 13 °C to 38 °C, respectively. The three Antarctic strains survived at temperatures much higher than their ambient regime. In comparison, the tropical strains are already growing at their upper temperature limits. The three Chlorella strains from different regions are eurythermal, with a large overlap on tolerance ranging from 4 °C to 38 °C. The specific growth rate (μ) of the Antarctic Navicula decreased (<0.34 day−1) at temperatures above 4 °C, showing it to be sensitive to temperature increase. If further warming of Earth occurs, N. glaciei UMACC 231 is likely to have the most deleterious consequences than the other two Antarctic microalgae studied. The percentage of polyunsaturated fatty acids (PUFA) decreased with increasing temperature in the Antarctic Navicula. As temperature increases, the growth and nutritional value of this commonly occurring diatom in the Antarctic may decrease, with consequences for the aquatic food web. Of the three Chlamydomonas strains, only the Antarctic strain produced predominantly PUFA, especially 16:3 (48.4–57.2 % total fatty acids).

Keywords

Antarctic microalgae Temperature stress Chlamydomonas Chlorella Diatoms 

References

  1. Beardall J, Stojkovic S, Larsen S (2009) Living in a high CO2 world: Impacts of global climate change on marine phytoplankton. Plant Ecol Divers 2:191–205CrossRefGoogle Scholar
  2. Bidigare RR, Ondrusek ME, Kennicutt MC II, Ituurriaga R, Harvey HR, Hoham RW, Macko SA (1993) Evidence for a photoprotective function for secondary carotenoids of snow algae. J Phycol 29:427–434CrossRefGoogle Scholar
  3. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedCrossRefGoogle Scholar
  4. Bonilla S, Rautio M, Vincent WF (2009) Phytoplankton and phytobenthos pigment strategies: implications for algal survival in the changing Arctic. Polar Biol 32:1293–1303CrossRefGoogle Scholar
  5. Chinnasamy S, Ramakrishnan B, Bhatnagar A, Das KC (2009) Biomass production potential of a wastewater alga Chlorella vulgaris ARC 1 under elevated levels of CO2 and temperature. Int J Mol Sci 10:518–532PubMedCrossRefGoogle Scholar
  6. Chong GL, Chu WL, Othman RY, Phang SM (2010) Differential gene expression of an Antarctic Chlorella in response to temperature stress. Polar Biol 34:637–645CrossRefGoogle Scholar
  7. Chu WL, Phang SM, Goh SH (1994) Studies on the production of useful chemicals, especially fatty acids in the marine diatom Nitzschia inconspicua Grunow. Hydrobiologia 285:33–40CrossRefGoogle Scholar
  8. Chu WL, Yuen YY, Wong CY, Teoh ML, Phang SM (2002) Isolation and culture of microalgae from the Windmill Islands Region, Antarctica. In: Proceedings of the Malaysian International Seminar on Antarctica: opportunities for research, 5–6 August 2002. Kuala Lumpur, pp 53–59Google Scholar
  9. Chu WL, See YC, Phang SM (2009) Use of immobilised Chlorella vulgaris for the removal of colour from textile dyes. J Appl Phycol 21:641–648CrossRefGoogle Scholar
  10. Clarke A, Murphy EJ, Meredith MP, King JC, Peck LS, Barnes DKA, Smith RC (2007) Climate change and the marine ecosystem of the western Antarctic Peninsula. Philos Trans R Soc Lond B Biol Sci 362:149–166PubMedCrossRefGoogle Scholar
  11. 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 48:1146–1151CrossRefGoogle Scholar
  12. de-Bashan LE, Trejo A, Huss VAR, Hernandez JP, Bashan Y (2008) Chlorella sorokiniana UTEX 2805, a heat and intense, sunlight-tolerant microalga with potential for removing ammonium from wastewater. Bioresour Technol 99:4980–4989PubMedCrossRefGoogle Scholar
  13. De Boer MK, Koolmees EM, Vrieling EG, Breeman AK, Van Rijsel M (2005) Temperature responses of three Fibrocapsa japonica strains (Raphidophyceae) from different climate regions. J Plankton Res 27:47–60CrossRefGoogle Scholar
  14. de Castro Araujo S, Garcia VMT (2005) Growth and biochemical composition of the diatom Chaetoceros cf. wighamii brightwell under different temperature, salinity and carbon dioxide levels. I. Protein, carbohydrate and lipids. Aquaculture 246:405–412CrossRefGoogle Scholar
  15. 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 354:107–117CrossRefGoogle Scholar
  16. Eggert A, Visser RJW, van Hasselt PR, Breeman AM (2006) Differences in acclimation potential of photosynthesis in seven isolates of the tropical to warm temperate macrophyte Valonia utricularis (Chlorophyta). Phycologia 45:546–556CrossRefGoogle Scholar
  17. Fu FX, Zhang YH, Warner ME, Feng YY, Sun J, Hutchins DA (2008) A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae 7:76–90CrossRefGoogle Scholar
  18. Gao KS, Li P, Watanabe T, Helbling EW (2008) Combined effects of ultraviolet radiation and temperature on morphology, photosynthesis, and DNA of Arthrospira (Spirulina) platensis (Cyanophyta). J Phycol 44:777–786CrossRefGoogle Scholar
  19. Gomez F, Souissi S (2008) The impact of the 2003 summer heat wave and the 2005 late cold wave on the phytoplankton in the north-eastern English Channel. C R Biol 331:678–685PubMedCrossRefGoogle Scholar
  20. Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241PubMedCrossRefGoogle Scholar
  21. Henderson RJ, Hegseth EN, Park MT (1998) Seasonal variation in lipid and fatty acid composition of ice algae from the Barents Sea. Polar Biol 20:48–55CrossRefGoogle Scholar
  22. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  23. Hu HH, Gao KS (2006) Response of growth and fatty acid compositions of Nannochloropsis sp. to environmental factors under elevated CO2 concentration. Biotechnol Lett 28:987–992PubMedCrossRefGoogle Scholar
  24. Hu HH, Li HY, Xu XD (2008) Alternative cold response modes in Chlorella (Chlorophyta, Trebouxiophyceae) from Antarctica. Phycologia 47:28–34CrossRefGoogle Scholar
  25. Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE, Alvarez Perez HJ, Garland T Jr (2009) Why tropical forest lizards are vulnerable to climate warming. Proc R Soc B 276:1939–1948PubMedCrossRefGoogle Scholar
  26. Huiskes AHL, Convey P, Bergstrom DM (2006) Trends in Antarctic terrestrial and limnetic ecosystems: Antarctica as a global indicator. In: Bergstrom DM, Convey P, Huiskes AHL (eds) Trends in Antarctic terrestrial and limnetic ecosystems: Antarctic as a global indicator, 1st edn. Springer, Dordrecht, pp 1–13CrossRefGoogle Scholar
  27. IPCC (2007) Climate Change 2007. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) The physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  28. Jiang H, Gao K (2004) Effects of lowering temperature during culture on the production of polyunsaturated fatty acids in the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). J Phycol 40:651–654CrossRefGoogle Scholar
  29. Kitaya Y, Xiao L, Masuda A, Ozawa T, Tsuda M, Omasa K (2008) Effects of temperature, photosynthesis photon flux density, photoperiod and O2 and CO2 concentrations on growth rates of the symbiotic dinoflagellate, Amphidinium sp. J Appl Phycol 20:737–742CrossRefGoogle Scholar
  30. Kobiyama A, Tanaka S, Kaneko Y, Lim PT, Ogata T (2010) Temperature tolerance and expression of heat shock protein 70 in the toxic dinoflagellate Alexandrium tamarense (Dinophyceae). Harmful Algae 9:180–185CrossRefGoogle Scholar
  31. Li Y, Qin JG (2005) Comparison of growth and lipid content in three Botryococcus braunii strains. J Appl Phycol 17:551–556CrossRefGoogle Scholar
  32. Li X, Hu HY, Zhang YP (2011) Growth and lipid accumulation properties of a freshwater microalga Scenedesmus sp. under different cultivation temperature. Bioresour Technol 102:3098–3102PubMedCrossRefGoogle Scholar
  33. Lim SL, Chu WL, Phang SM (2010) Use of Chlorella vulgaris for bioremediation of textile wastewater. Bioresour Technol 101:7314–7322PubMedCrossRefGoogle Scholar
  34. Lovejoy C, Vincent WF, Bonilla S, Roy S, Martineau MJ, Terrado R, Potvin M, Massana R, Pedros-Alio C (2007) Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in Arctic seas. J Phycol 43:78–89CrossRefGoogle Scholar
  35. Maazouzi C, Masson G, Izquierdo MS, Pihan JC (2008) Midsummer heat wave effects on lacustrine plankton: variation of assemblage structure and fatty acid composition. J Therm Biol 33:287–296CrossRefGoogle Scholar
  36. Mangelsdorf K, Finsel E, Liebner S, Wagner D (2009) Temperature adaptation of microbial communities in different horizons of Siberian permafrost-affected soils from the Lena Delta. Chem Erde-Geochem 69:169–182CrossRefGoogle Scholar
  37. Maxwell DP, Falk S, Trick CG, Huner NPA (1994) Growth at low temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol 105:535–543PubMedGoogle Scholar
  38. Mock T, Hoch N (2005) Long-term temperature acclimation of photosynthesis in steady-state cultures of the polar diatom Fragilariopsis cylindrus. Photosynth Res 85:307–317PubMedCrossRefGoogle Scholar
  39. Mock T, Valentin K (2004) Photosynthesis and cold acclimation: molecular evidence from a polar diatom. J Phycol 40:732–741CrossRefGoogle Scholar
  40. Montes-Hugo M, Doney SC, Ducklow HW, Fraser W, Martinson D, Stammerjohn SE, Schofield O (2009) Recent changes in phytoplankton communities associated with rapid regional climate change along the western Antarctic Peninsula. Science 323:1470–1473PubMedCrossRefGoogle Scholar
  41. Morgan-Kiss R, Ivanov AG, Williams J, Mobashsher K, Huner NP (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 1561:251–265PubMedCrossRefGoogle Scholar
  42. Morgan-Kiss RM, Priscu JP, Pocock T, Gudynaite-Savitch L, Huner NPA (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70:222–252PubMedCrossRefGoogle Scholar
  43. 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 12:701–711PubMedCrossRefGoogle Scholar
  44. Muhling M, Belay A, Whitton BA (2005) Variation in fatty acid composition of Arthrospira (Spirulina) strains. J Appl Phycol 17:137–146CrossRefGoogle Scholar
  45. Nagashima H, Matsumoto GI, Ohtani S, Momose H (1995) Temperature acclimation and fatty acid composition of an Antarctic Chlorella. Proc NIPR Symp Polar Biol 8:194–199Google Scholar
  46. 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 48:130–135CrossRefGoogle Scholar
  47. Patil V, Kallqvist T, Olsen E, Vogt G, Gislerod HR (2007) Fatty acid composition of 12 microalgae for possible use in aquaculture feed. Aquacult Int 15:1–9CrossRefGoogle Scholar
  48. Phang SM, Chu WL (1999) University of Malaya Algae Culture Collection (UMACC). Catalogue of strains. Institute of Postgraduate Studies and Research, Kuala Lumpur, p 77Google Scholar
  49. Phang SM, Chu WL (2004) The University of Malaya Algae Culture Collection (UMACC) and potential applications of a unique Chlorella from the collection. Jap J Phycol 52:221–224Google Scholar
  50. Phang SM, Marimuthu S, Chu WL, Gan SY (2009) Phylogeny of Chlorella strains isolated from different latitudes from the North to South Pole. Phycologia 48:106Google Scholar
  51. Poerschmann J, Spijkerman E, Langer U (2004) Fatty acid patterns in Chlamydomonas sp. as a marker for nutritional regimes and temperature under extremely acidic conditions. Microb Ecol 48:78–89PubMedCrossRefGoogle Scholar
  52. Pratoomyot J, Srivilas P, Noiraksar T (2005) Fatty acids composition of 10 microalgal species. Songklanakarin J Sci Technol 27:1179–1187Google Scholar
  53. Reaser JK, Pomerance R, Thomas PO (2000) Coral bleaching and global climate change: scientific findings and policy recommendations. Conserv Biol 14:1500–1511CrossRefGoogle Scholar
  54. Renaud SM, Parry DL, Thinh LV (1994) Microalgae for use in tropical aquaculture. I: gross chemical and fatty acid composition of twelve species of microalgae from the Northern Territory, Australia. J Appl Phycol 6:337–345CrossRefGoogle Scholar
  55. 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 7:595–602CrossRefGoogle Scholar
  56. Renaud SM, Thinh LV, 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 211:195–214CrossRefGoogle Scholar
  57. Reuss N, Poulsen LK (2002) Evaluation of fatty acids as biomarkers for a natural plankton community. A field study of a spring bloom and a post-bloom period off West Greenland. Mar Biol 141:423–434CrossRefGoogle Scholar
  58. Rezanka T, Nedbalova L, Sigler K (2008) Unusual medium-chain polyunsaturated fatty acids from the snow alga Chloromonas brevispina. Microbiol Res 163:373–379PubMedCrossRefGoogle Scholar
  59. Rose KC, Williamson CE, Saros JE, Sommaruga R, Fischer JM (2009) Differences in UV transparency and thermal structure between alpine and subalpine lakes: implications for organisms. Photochem Photobiol Sci 8:1244–1256PubMedCrossRefGoogle Scholar
  60. Sakai N, Sakamoto Y, Kishimoto N, Chihara M, Karube I (1995) Chlorella strains from hot springs tolerant to high temperature and high CO2. Energy Convers Manag 36:693–696CrossRefGoogle Scholar
  61. Sandnes JM, Kallqvist T, Wenner D, Gislerod HR (2005) Combined influence of light and temperature on growth rates of Nannochloropsis oceanica: linking cellular responses to large-scale biomass production. J Appl Phycol 17:515–525CrossRefGoogle Scholar
  62. Seaburg KG, Parker BC, Wharton RA, Simmons GM (1981) Temperature-growth responses of algal isolates from Antarctic oases. J Phycol 17:353–360CrossRefGoogle Scholar
  63. Singh V, Singh B, Goyle MR (1994) Influence of temperature on cell biomass and biochemical composition of the thermophilic cyanobacterium, Mastigocladus laminosus. Phykos 33:59–65Google Scholar
  64. Smith REH, Stapleford LC, Ridings RS (1994) The acclimated response of growth, photosynthesis, composition, and carbon balance to temperature in the psychrophilic ice diatom Nitzschia seriata. J Phycol 30:8–16CrossRefGoogle Scholar
  65. Strickland JDH, Parsons TR (1968) A practical handbook of seawater analysis. Bull Fish Res Bd Can 167:311Google Scholar
  66. Sushchik NN, Kalacheva GS, Zhila NO, Gladyshev MI, Volova TG (2003) A temperature dependence of the intra- and extracellular fatty-acid composition of green algae and cyanobacterium. Russ J Plant Physiol (English Translation) 50:374–380CrossRefGoogle Scholar
  67. Tangang FT, Juneng L, Ahmad S (2007) Trend and interannual variability of temperature in Malaysia: 1961–2002. Theor Appl Climatol 89:127–141CrossRefGoogle Scholar
  68. 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 16:421–430CrossRefGoogle Scholar
  69. Thompson PA, Guo M, Harrison PJ, Whyte JNC (1992) Effects of variation in temperature. II. On the fatty acid composition of eight species of marine phytoplankton. J Phycol 28:488–497CrossRefGoogle Scholar
  70. Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG (2005) The role and evolution of superoxide dismutases in algae. J Phycol 41:453–465CrossRefGoogle Scholar
  71. Wong CY, Chu WL, Marchant H, Phang SM (2004) Growth response, biochemical composition and fatty acid profiles of four Antarctic microalgae subjected to UV radiation stress. Mal J Sci 23:103–118Google Scholar
  72. Wong CY, Chu WL, Marchant H, Phang SM (2007) Comparing the response of Antarctic, tropical and temperate microalgae to ultraviolet radiation (UVR) stress. J Appl Phycol 19:689–699CrossRefGoogle Scholar
  73. Yun MS, Lee SH, Chung TK (2010) Photosynthetic activity of benthic diatoms in response to different temperatures. J Appl Phycol 22:559–562CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Institute of Ocean & Earth SciencesUniversity of MalayaKuala LumpurMalaysia
  2. 2.Institute of Biological Sciences, Faculty of ScienceUniversity of MalayaKuala LumpurMalaysia
  3. 3.International Medical UniversityKuala LumpurMalaysia

Personalised recommendations