HE Meilin,CHI Qiaoyun,WANG Changhai.Research progress of the adaptive mechanisms of polar microalgae in response to extreme environment[J].Journal of Nanjing Agricultural University,2019,42(2):201-208.[doi:10.7685/jnau.201807013]





Research progress of the adaptive mechanisms of polar microalgae in response to extreme environment
何梅琳 迟巧云 王长海
南京农业大学资源与环境科学学院/江苏省海洋生物学重点实验室, 江苏 南京 210095
HE Meilin CHI Qiaoyun WANG Changhai
College of Resources and Environmental Sciences/Jiangsu Key Laboratory of Marine Biology, Nanjing Agricultural University, Nanjing 210095, China
polar regionmicroalgaethe adaptive mechanisms to extreme environmentlow temperatureultraviolet radiationomics
Since polar region is an important potential resource of microorganisms,the researches on its bioresource exploration and utilization has become one of the global hot issues. Microalgae is the primary biomass producer of polar region,and the studies on the strain breeding,cultivation and stress-resistant mechanisms of polar algae has attracted strong interests of scientists. The polar habitat is characterized by freezing temperature,seasonal variation of irradiation and temperature,strong ultraviolet(UV) radiation,and so on. Polar microalgae develop unique adaptive mechanisms to such extreme environment in the progress of long-term acclimation and evolution. The synthesis and accumulation of special physiological or pharmacological bioactive compounds,and induction of stress-resistant novel genes enable polar algae to survive the extreme polar region. This paper aims to review the recent research progress on the stress-resistant and adaptive mechanisms of microalgae from Antarctic and Arctic region in response to temperature,irradiation and UV radiation,and provides a summary of the application of various omics technology on microalgae stress biology. This review will help us better understand the underlying adaptive mechanisms of microalgae to extreme stresses,and reveal the unique phylogenetic role of microalgae in polar ecological system.


[1] 王长海,刘兆普. 海洋生化工程原理[M]. 北京:化学工业出版社,2011. Wang C H,Liu Z P. Principles of Marine Biochemical Engineering[M]. Beijing:Chemical Industry Press,2011(in Chinese).
[2] McClintock J B,Amsler C D,Baker B J,et al. Ecology of Antarctic marine sponges:an overview[J]. Integrative and Comparative Biology,2005,45(2):359-368.
[3] Margesin R. Psychrophiles:from Biodiversity to Biotechnology[M]. Cham:Springer International Publishing,2017.
[4] 林学政,边际,何培青. 极地微生物低温适应性的分子机制[J]. 极地研究,2003,15(1):75-82. Lin X Z,Bian J,He P Q. Molecular mechanism of cold-adaptation of polar microorganisms[J]. Chinese Journal of Polar Research,2003,15(1):75-82(in Chinese with English abstract).
[5] Thomas D N,Dieckmann G S. Antarctic sea ice:a habitat for extremophiles[J]. Science,2002,295(5555):641-644.
[6] Mock T,Valentin K. Photosynthesis and cold acclimation:molecular evidence from a polar diatom[J]. Journal of Phycology,2004,40(4):732-741.
[7] Forland E J,Benestad R,Hanssen-Bauer I,et al. Temperature and precipitation development at Svalbard 1900-2100[J]. Advances in Meteorology,2011,2011:1-14.
[8] Leya T. Snow algae:adaptation strategies to survive on snow and ice[M]//Seckbach J,Oren A,Stan-Lotter H. Polyextremophiles. Dordrecht:Springer,2013:401-423.
[9] 王以斌,张爱军,刘芳明,等. 南极冰藻对南极极端环境的适应性研究进展[J]. 生物技术通报,2016,32(10):128-134. Wang Y B,Zhang A J,Liu F M,et al. Advances in studies on the acclimation of Antarctic ice microalgae to extreme environments[J]. Biotechnology Bulletin,2016,32(10):128-134(in Chinese with English abstract).
[10] Sommer U. Maximal growth rates of Antarctic phytoplankton:only weak dependence on cell size[J]. Limnology and Oceanography,1989,34(6):1109-1112.
[11] Teoh M L,Chu W L,Marchant H,et al. Influence of culture temperature on the growth,biochemical composition and fatty acid profiles of six Antarctic microalgae[J]. Journal of Applied Phycology,2004,16(6):421-430.
[12] Teoh M L,Phang S M,Chu W L. Response of Antarctic,temperate,and tropical microalgae to temperature stress[J]. Journal of Applied Phycology,2013,25(1):285-297.
[13] Cao K,He M,Yang W,et al. The eurythermal adaptivity and temperature tolerance of a newly isolated psychrotolerant Arctic Chlorella sp.[J]. Journal of Applied Phycology,2016,28(2):877-888.
[14] La Rocca N,Sciuto K,Meneghesso A,et al. Photosynthesis in extreme environments:responses to different light regimes in the Antarctic alga Koliella antarctica[J]. Physiologia Plantarum,2015,153(4):654-667.
[15] Madronich S,McKenzie R L,Bj?rn L O,et al. Changes in biologically active ultraviolet radiation reaching the Earth’s surface[J]. Journal of Photochemistry and Photobiology B:Biology,1998,46(1/2/3):5-19.
[16] Karsten U,Wulff A,Roleda M Y,et al. Physiological responses of polar benthic algae to ultraviolet radiation[J]. Botanica Marina,2009,52(6):639-654.
[17] van Leeuwe M,Tedesco L,Arrigo K R,et al. Microalgal community structure and primary production in Arctic and Antarctic sea ice:a synthesis[J]. Elem Sci Anth,2018,6(1):4.
[18] Morgan-Kiss R M,Ivanov A G,Pocock T,et al. The Antarctic psychrophile,Chlamydomonas raudensis Ettl(UWO241) (Chlorophyceae,Chlorophyta),exhibits a limited capacity to photoacclimate to red light[J]. Journal of Phycology,2005,41(4):791-800.
[19] Szyszka B,Ivanov A G,Hüner N P A. Psychrophily is associated with differential energy partitioning,photosystem stoichiometry and polypeptide phosphorylation in Chlamydomonas raudensis[J]. Biochimica et Biophysica Acta,2007,1767(6):789-800.
[20] Dolhi J,Maxwell D,Morgan-Kiss R. Review:the Antarctic Chlamydomonas raudensis:an emerging model for cold adaptation of photosynthesis[J]. Extremophiles,2013,17(5):711-722.
[21] Raymond J A,Morgan-Kiss R. Separate origins of ice-binding proteins in antarctic Chlamydomonas species[J]. PLoS One,2013,8(3):e59186.
[22] 吕娜. 雪衣藻响应和适应环境胁迫分子调节的多组学研究[D]. 广州:华南理工大学,2014. Lü N. Molecular regulation of snow alga Chlamydomonas nivalis in response to stress conditions using multi-omics study[D]. Guangzhou:South China University of Technology,2014(in Chinese with English abstract).
[23] An M L,Mou S L,Zhang X W,et al. Temperature regulates fatty acid desaturases at a transcriptional level and modulates the fatty acid profile in the Antarctic microalga Chlamydomonas sp. ICE-L[J]. Bioresource Technology,2013,134:151-157.
[24] Liu C L,Wu G T,Huang X H,et al. Validation of housekeeping genes for gene expression studies in an ice alga Chlamydomonas during freezing acclimation[J]. Extremophiles,2012,16(3):419-425.
[25] Liu S H,Zhang P Y,Cong B L,et al. Molecular cloning and expression analysis of a cytosolic Hsp70 gene from Antarctic ice algae Chlamydomonas sp. ICE-L[J]. Extremophiles,2010,14(3):329-337.
[26] Liu C,Wang X,Sun C. Acclimation of Antarctic Chlamydomonas to the sea-ice environment:a transcriptomic analysis[J]. Extremophiles,2016,20(4):437-450.
[27] Poong S W,Lim P E,Phang S M,et al. Transcriptome sequencing of an Antarctic microalga,Chlorella sp.(Trebouxiophyceae,Chlorophyta) subjected to short-term ultraviolet radiation stress[J]. Journal of Applied Phycology,2018,30(1):87-99.
[28] Yang W N,Zou S M,He M L,et al. Growth and lipid accumulation in three Chlorella strains from different regions in response to diurnal temperature fluctuations[J]. Bioresource Technology,2016,202:15-24.
[29] Kan G F,Miao J L,Shi C J,et al. Proteomic alterations of Antarctic ice microalga Chlamydomonas sp. under low-temperature stress[J]. Journal of Integrative Plant Biology,2006,48(8):965-970.
[30] Morgan-Kiss R M,Priscu J C,Pocock T,et al. Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments[J]. Microbiology and Molecular Biology Reviews,2006,70(1):222-252.
[31] Feller G,Gerday C. Psychrophilic enzymes:hot topics in cold adaptation[J]. Nature Reviews Microbiology,2003,1(3):200-208.
[32] di Rigano V M,Vona V,Lobosco O,et al. Temperature dependence of nitrate reductase in the psychrophilic unicellular alga Koliella antarctica and the mesophilic alga Chlorella sorokiniana[J]. Plant Cell Environment,2006,29(7):1400-1409.
[33] Devos N,Ingouff M,Loppes R,et al. Rubisco adaptation to low temperatures:a comparative study in psychrophilic and mesophilic unicellular algae[J]. Journal of Phycology,1998,34(4):655-660.
[34] Ensminger I,Busch F,Huner N P A. Photostasis and cold acclimation:sensing low temperature through photosynthesis[J]. Physiologia Plantarum,2006,126(1):28-44.
[35] Morgan-Kiss R,Ivanov A,Huner N. The Antarctic psychrophile,Chlamydomonas subcaudata,is deficient in stateⅠ-state Ⅱ transitions[J]. Planta,2002,214(3):435-445.
[36] Morgan R M,Ivanov A G,Priscu J C,et al. Structure and composition of the photochemical apparatus of the Antarctic green alga,Chlamydomonas subcaudata[J]. Photosynthesis Research,1998,56(3):303-314.
[37] Maxwell D P,Falk S,Trick C G,et al. Growth at low temperature mimics high-light acclimation in Chlorella vulgaris[J]. Plant Physiology,1994,105(2):535-543.
[38] Sanina N M,Goncharova S N,Kostetsky E Y. Seasonal changes of fatty acid composition and thermotropic behavior of polar lipids from marine macrophytes[J]. Phytochemistry,2008,69(7):1517-1527.
[39] Ahn J W,Hwangbo K,Lee S Y,et al. A new Arctic Chlorella species for biodiesel production[J]. Bioresource Technology,2012,125:340-343.
[40] Orsini M,Costelli C,Malavasi V,et al. Complete sequence and characterization of mitochondrial and chloroplast genome of Chlorella variabilis NC64A[J]. Mitochondrial DNA:Part A,2016,27(5):3128-3130.
[41] Mock T,Kroon B M A. Photosynthetic energy conversion under extreme conditions. Ⅰ:Important role of lipids as structural modulators and energy sink under N-limited growth in Antarctic sea ice diatoms[J]. Phytochemistry,2002,61(1):41-51.
[42] Mock T,Kroon B M A. Photosynthetic energy conversion under extreme conditions. Ⅱ:The significance of lipids under light limited growth in Antarctic sea ice diatoms[J]. Phytochemistry,2002,61(1):53-60.
[43] Gwak I G,Jung W S,Kim H J,et al. Antifreeze protein in antarctic marine diatom,Chaetoceros neogracile[J]. Marine Biotechnology,2010,12(6):630-639.
[44] van de Poll W H,Eggert A,Buma A G,et al. Temperature dependence of UV radiation effects in Arctic and temperate isolates of three red macrophytes[J]. European Journal of Phycology,2002,37(1):59-68.
[45] Cruces E,Huovinen P,Gómez I. Interactive effects of UV radiation and enhanced temperature on photosynthesis,phlorotannin induction and antioxidant activities of two sub-Antarctic brown algae[J]. Marine Biology,2013,160(1):1-13.
[46] Ralph P J,McMinn A,Ryan K G,et al. Short-term effect of temperature on the photokinetics of microalgae from the surface layers of Antarctic pack ice[J]. Journal of Phycology,2005,41(4):763-769.
[47] Robinson D H,Kolber Z,Sullivan C W. Photophysiology and photoacclimation in surface sea ice algae from McMurdo sound,Antarctica[J]. Marine Ecology Progress Series,1997,147:243-256.
[48] Hihara Y,Kamei A,Kanehisa M,et al. DNA microarray analysis of cyanobacterial gene expression during acclimation to high light[J]. The Plant Cell,2001,13(4):793-806.
[49] Kulkarni R D,Golden S S. Adaptation to high light intensity in Synechococcus sp. strain PCC 7942:regulation of three psbA genes and two forms of the D1 protein[J]. Journal of Bacteriology,1994,176(4):959-965.
[50] Vidhyavathi R,Venkatachalam L,Sarada R,et al. Regulation of carotenoid biosynthetic genes expression and carotenoid accumulation in the green alga Haematococcus pluvialis under nutrient stress conditions[J]. Journal of Experimental Botany,2008,59(6):1409-1418.
[51] Remias D. Cell structure and physiology of alpine snow and ice algae[M]//Remias D. Plants in Alpine Regions. Vienna:Springer,2011:175-185.
[52] Mou S,Zhang X,Ye N,et al. Cloning and expression analysis of two different LhcSR genes involved in stress adaptation in an Antarctic microalga,Chlamydomonas sp. ICE-L[J]. Extremophiles,2012,16(2):193-203.
[53] Hwang Y S,Jung G,Jin E. Transcriptome analysis of acclimatory responses to thermal stress in Antarctic algae[J]. Biochemical and Biophysical Research Communications,2008,367(3):635-641.
[54] Lyon B R,Mock T. Polar microalgae:new approaches towards understanding adaptations to an extreme and changing environment[J]. Biology,2014,3(1):56-80.
[55] Blanc G,Agarkova I,Grimwood J,et al. The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation[J]. Genome Biology,2012,13(5):R39.
[56] Wong C Y,Teoh M L,Phang S M,et al. Interactive effects of temperature and UV radiation on photosynthesis of Chlorella strains from polar,temperate and tropical environments:differential impacts on damage and repair[J]. PLoS One,2015,10(10):e0139469.
[57] Hader D P,Williamson C E,Wangberg S A,et al. Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors[J]. Photochemical & Photobiological Sciences,2015,14(1):108-126.
[58] Li Y,Gao K,Villafa?e V,et al. Ocean acidification mediates photosynthetic response to UV radiation and temperature increase in the diatom Phaeodactylum tricornutum[J]. Biogeosciences,2012,9(10):3931-3942.
[59] Thyssen M,Ferreyra G,Moreau S,et al. The combined effect of ultraviolet B radiation and temperature increase on phytoplankton dynamics and cell cycle using pulse shape recording flow cytometry[J]. Journal of Experimental Marine Biology and Ecology,2011,406(1):95-107.
[60] Gao K,Campbell D A. Photophysiological responses of marine diatoms to elevated CO2 and decreased pH:a review[J]. Functional Plant Biology,2014,41(5):449-459.
[61] Mock T,Otillar R P,Strauss J,et al. Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus[J]. Nature,2017,541(7638):536-540.
[62] 林敏卓. 南极冰藻Chlamydomonas sp. ICE-L低温胁迫相关基因的克隆和功能验证[D]. 济南:山东轻工业学院,2012. Lin M Z. Molecular cloning and funcional analysis of anti-freeze genes from Chlamydomonas sp. ICE-L[D]. Jinan:Shandong Polytechnic University,2012(in Chinese with English abstract).
[63] Lyon B R,Lee P A,Bennett J M,et al. Proteomic analysis of a sea-ice diatom:salinity acclimation provides new insight into the dimethylsulfoniopropionate production pathway[J]. Plant Physiology,2011,157(4):1926-1941.
[64] Choi K M,Lee M Y. Differential protein expression associated with heat stress in Antarctic microalga[J]. BioChip Journal,2012,6(3):271-279.
[65] Huseby S,Degerlund M,Zingone A,et al. Metabolic fingerprinting reveals differences between northern and southern strains of the cryptic diatom Chaetoceros socialis[J]. European Journal of Phycology,2012,47(4):480-489.
[66] Gao H,Wright D A,Li T,et al. TALE activation of endogenous genes in Chlamydomonas reinhardtii[J]. Algal Research,2014,5:52-60.
[67] Wang Q,Lu Y,Xin Y,et al. Genome editing of model oleaginous microalgae Nannochloropsis spp. by CRISPR/Cas9[J]. The Plant Journal,2016,88(6):1071-1081.


更新日期/Last Update: 1900-01-01