Journal of Applied Phycology

, Volume 30, Issue 5, pp 2815–2825 | Cite as

The ‘stress’ concept in microalgal biology—homeostasis, acclimation and adaptation

  • Michael A. Borowitzka
6th Congress of the International Society for Applied Phycology


The term ‘stress’ is widely used in the algal literature, usually in the context of the response of algae to changed abiotic and biotic factors. ‘Stress’ is seen as the cause of changes in algal metabolism and composition and often as a factor inducing the overproduction of particular desirable secondary metabolites. However, ‘stress’ is used differently by different authors and is often ill-defined, with no clear separation of cause and effect. This lack of a defined stress concept leads to poor experimental design, miscommunication of results and potentially erroneous conclusions. This paper reviews the stress concept as it applies to algae, especially microalgae. Here, stress is defined as the disruption of homeostasis due to a stressor and the stress response represents the changes in cell metabolism during acclimation and the restoration of homeostasis. Once homeostasis is restored the cell is no longer stressed. The stages of the stress response, i.e. alarm, regulation, acclimation and adaptation, are described. The well-studied responses of the green halophilic alga Dunaliella to changes in salinity are used as an example to illustrate the stress response and acclimation to the changed salinity.


Stress Regulation Acclimation Adaptation Stress signalling Reactive oxygen species Homeostasis 



The motivation for writing this paper has come from reading many papers which superficially attribute a multitude of metabolic changes in algal cultures to ‘stress’, but which appear to have no clear concept of what constitutes ‘stress’. This paper has greatly benefitted from discussions with John Raven, John Beardall, Avigad Vonshak, David Suggett and Navid Moheimani and their comments on drafts of this paper; however, the views contained herein are wholly my own. Many discussions with students also helped to clarify my understanding of what is meant by stress in algae. I would also like to thank the three reviewers for their incisive comments which have helped to improve this paper.


  1. Affenzeller MJ, Darehshouri A, Andosch A, Lütz C, Lütz-Meindl U (2009) Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J Exp Bot 60:939–954PubMedPubMedCentralGoogle Scholar
  2. Azachi M, Sadka A, Fisher M, Goldshlag P, Gokhman I, Zamir A (2002) Salt induction of fatty acid elongase and membrane lipid modifications in the extreme halotolerant alga Dunaliella salina. Plant Physiol 129:1320–1329PubMedPubMedCentralGoogle Scholar
  3. Belmans C, van Laere A (1987) Glycerol cycle enzymes and intermediates during adaptation of Dunaliella tertiolecta cells to hyperosmotic stress. Plant Cell Environ 10:185–190Google Scholar
  4. Berges JA, Falkowski PG (1998) Physiological stress and cell death in marine phytoplankton: induction of proteases in response to nitrogen or light limitation. Limnol Oceanogr 43:129–135Google Scholar
  5. Bickerton P, Sello S, Brownlee C, Pittman JK, Wheeler GL (2016) Spatial and temporal specificity of Ca2+ signalling in Chlamydomonas reinhardtii in response to osmotic stress. New Phytol 212:920–933PubMedPubMedCentralGoogle Scholar
  6. Borowitzka MA, Huisman JM (1993) The ecology of Dunaliella salina (Chlorophyceae, Volvocales)—effect of environmental conditions on aplanospore formation. Bot Mar 36:233–243Google Scholar
  7. Borowitzka MA, Siva CJ (2007) The taxonomy of the genus Dunaliella (Chlorophyta, Dunaliellales) with emphasis on the marine and halophilic species. J Appl Phycol 19:567–590Google Scholar
  8. Borowitzka MA, Huisman JM, Osborn A (1991) Culture of the astaxanthin-producing green alga Haematococcus pluvialis 1. Effects of nutrients on growth and cell type. J Appl Phycol 3:295–304Google Scholar
  9. Bravo I, Figueroa R (2014) Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2:11–32PubMedPubMedCentralGoogle Scholar
  10. Brown AD, Borowitzka LJ (1979) Halotolerance of Dunaliella. In: Levandowsky M, Hutner SH (eds) Biochemistry and physiology of protozoa, vol 1. Academic Press, New York, pp 139–190Google Scholar
  11. Brussaard CPD, Noordeloos AAM, Riegman R (1997) Autolysis kinetics of the marine diatom Ditylum brightwellii (Bacillariophyceae) under nitrogen and phosphorus limitation and starvation. J Phycol 33:980–987Google Scholar
  12. Cannon WB (1932) The wisdom of the body. W.W. Norton, NYGoogle Scholar
  13. Carl C, de Nys R, Lawton RJ, Paul NA (2014) Methods for the induction of reproduction in a tropical species of filamentous Ulva. PLoS One 9(5):e97396PubMedPubMedCentralGoogle Scholar
  14. Chen H, Jiang J-G, Wu G-H (2009) Effects of salinity changes on the growth of Dunaliella salina and its isozyme activities of glycerol-3-phosphate dehydrogenase. J Agric Food Chem 57:6178–6182PubMedGoogle Scholar
  15. Chen H, Chen S-L, Jiang J-G (2011) Effect of Ca2+ channel block on glycerol metabolism in Dunaliella salina under hypoosmotic and hyperosmotic stresses. PLoS One 6(12):e28613PubMedPubMedCentralGoogle Scholar
  16. Choudhury FK, Rivero RM, Blumwald E, Mittler R (2016) Reactive oxygen species, abiotic stress and stress combination. Plant J.
  17. Collins S, Bell G (2004) Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431:566–569PubMedGoogle Scholar
  18. Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211Google Scholar
  19. 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 Bioenerg 1847:468–485Google Scholar
  20. Dietz K-J, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171:1541–1550PubMedPubMedCentralGoogle Scholar
  21. Ehrenfeld J, Cousin J-L (1984) Ionic regulation of the unicellular green alga Dunaliella tertiolecta: response to hypertonic shock. J Membr Biol 77:45–55Google Scholar
  22. El-Baky HHA, El Baz FK, El-Baroty GS (2004) Production of antioxidant by the green alga Dunaliella salina. Int J Agric Biol 6:49–57Google Scholar
  23. Fang L, Qi S, Xu Z, Wang W, He J, Chen X, Liu J (2017) De novo transcriptomic profiling of Dunaliella salina reveals concordant flows of glycerol metabolic pathways upon reciprocal salinity changes. Algal Res 23:135–149Google Scholar
  24. Fisher M, Gokhman I, Pick U, Zamir A (1996) A salt-resistant plasma membrane carbonic anhydrase is induced by salt in Dunaliella salina. J Biol Chem 271:11718–17723Google Scholar
  25. Fisher M, Zamir A, Pick U (1998) Iron uptake by the halotolerant alga Dunaliella is mediated by a plasma membrane transferrin. J Biol Chem 273:17553–17558PubMedGoogle Scholar
  26. Fogg GE (2001) Algal adaptation to stress—some general remarks. In: Rai L, Gaur J (eds) Algal adaptation to environmental stresses. Springer, Berlin, pp 1–19Google Scholar
  27. Galluzzi L, Bravo-San Pedro JM, Kepp O, Kroemer G (2016) Regulated cell death and adaptive stress responses. Cell Mol Life Sci 73:2405–2410PubMedGoogle Scholar
  28. Gaspar T, Franck T, Bisbis B, Kevers C, Jouve L, Hausman JF, Dommes J (2002) Concepts in plant stress physiology. Application to plant tissue cultures. Plant Growth Regul 37:263–285Google Scholar
  29. Gee R, Goyal A, Byerrum RU, Tolbert NE (1993) Two isoforms of dihydroxyacetone phosphate reductase from the chloroplasts of Dunaliella tertiolecta. Plant Physiol 103:243–249PubMedPubMedCentralGoogle Scholar
  30. Giordano M (2013) Homeostasis: an underestimated focal point of ecology and evolution. Plant Sci 211:92–101PubMedGoogle Scholar
  31. Goldstein DS, Kopin IJ (2007) Evolution of concepts of stgress. Stress 10:109–120PubMedGoogle Scholar
  32. Goyal A (2007a) Osmoregulation in Dunaliella, Part I: effects of osmotic stress on photosynthesis, dark respiration and glycerol metabolism in Dunaliella tertiolecta and its salt-sensitive mutant (HL 25/8). Plant Physiol Biochem 45:696–704PubMedGoogle Scholar
  33. Goyal A (2007b) Osmoregulation in Dunaliella, Part II: photosynthesis and starch contribute carbon for glycerol synthesis during a salt stress in Dunaliella tertiolecta. Plant Physiol Biochem 45:705–710PubMedGoogle Scholar
  34. Grime JP (1989) The stress debate: symptom of impending synthesis? Biol J Linn Soc 37:3–17Google Scholar
  35. Hamilton ES, Schlegel AM, Haswell ES (2015) United in diversity: mechanosensitive ion channels in plants. Annu Rev Plant Biol 66:113–127PubMedGoogle Scholar
  36. Hill AE, Shachar-Hill Y (2015) Are aquaporins the missing transmembrane osmosensors? J Membr Biol 248:753–765PubMedGoogle Scholar
  37. Hinkle LE (1974) The concept of “stress” in the biological and social sciences. Int J Psychiatry Med 5:335–357PubMedGoogle Scholar
  38. Hohmann S (2009) Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae. FEBS Lett 583:4025–4029PubMedGoogle Scholar
  39. Imai I, Itakura S (1999) Importance of cysts in the population dynamics of the red tide flagellate Heterosigma akashiwo (Raphidophyceae). Mar Biol 133:755–762Google Scholar
  40. Issa AA (1996) The role of calcium in the stress response of the halotolerant green alga Dunaliella bardawil Ben-Amotz et Avron. Phyton (Horn) 36:295–302Google Scholar
  41. Jiménez C, Berl T, Rivard CJ, Edelstein CL, Capasso JM (2004) Phosphorylation of MAP kinase-like proteins mediate the response of the halotolerant alga Dunaliella viridis to hypertonic shock. Biochim Biophys Acta Mol Cell Res 1644:61–69Google Scholar
  42. Katz A, Pick U, Avron M (1992) Modulation of Na+/H+ antiporter activity by extreme pH and salt in the halotolerant alga Dunaliella salina. Plant Physiol 100:1224–1229PubMedPubMedCentralGoogle Scholar
  43. Katz A, Waridel P, Shevchenko A, Pick U (2007) Salt-induced changes in the plasma membrane proteome of the halotolerant alga Dunaliella salina as revealed by blue native gel electrophoresis and nano-LC-MS/MS analysis. Mol Cell Proteomics 6:1459–1472PubMedGoogle Scholar
  44. Kessly DS, Brown AD (1981) Salt relations of Dunaliella. Transitional changes in glycerol content and oxygen exchange reactions on water stress. Arch Microbiol 129:154–159Google Scholar
  45. Khona DK, Shirolikar SM, Gawde KK, Hom E, Deodhar MA, D'Souza JS (2016) Characterization of salt stress-induced palmelloids in the green alga, Chlamydomonas reinhardtii. Algal Res 16:434–448Google Scholar
  46. Kirk DL, Kirk MM (1986) Heat shock elicits production of sexual inducer in Volvox. Science 231:51–54PubMedGoogle Scholar
  47. Klaas RT, Marcel JWV, Corina PDB (2007) Cell death in three marine diatom species in response to different irradiance levels, silicate, or iron concentrations. Aquat Microb Ecol 46:253–261Google Scholar
  48. Kranner I, Minibayeva FV, Beckett RP, Seal CE (2010) What is stress? Concepts, definitions and applications in seed science. New Phytol 188:655–673PubMedGoogle Scholar
  49. Lachapelle J, Bell G, Colegrave N (2015) Experimental adaptation to marine conditions by a freshwater alga. Evolution 69:2662–2675PubMedGoogle Scholar
  50. Lakeman MB, von Dassow P, Cattolico RA (2009) The strain concept in phytoplankton ecology. Harmful Algae 8:746–758Google Scholar
  51. Larcher W (1987) Streß bei Pflanzen. Naturwissenschaften 74:158–167Google Scholar
  52. Lavaud J (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. Funct Plant Sci Biotechnol 1:267–287Google Scholar
  53. Lei G, Qiao D, Bai L, Xu H, Cao Y (2008) Isolation and characterization of a mitogen-activated protein kinase gene in the halotolerant alga Dunaliella salina. J Appl Phycol 20:13–17Google Scholar
  54. Lichtenthaler HK (1988) In vivo chlorophyll fluorscence as a tool for stress detection in plants. In: Lichtenthaler HK (ed) Applications of chlorophyll fluorescence. Kluwer, Dordrecht, pp 129–142Google Scholar
  55. Lichtenthaler HK (1996) Vegetation stress: an introduction to the stress concept in plants. J Plant Physiol 148:4–14Google Scholar
  56. Lichtenthaler HK (1998) The stress concept in plants: an introduction. Ann N Y Acad Sci 851:187–189PubMedGoogle Scholar
  57. Lilley RM, Goyal A, Marengo T, Brown AD (1987) The response of Dunaliella to salt stress: a comparison of effects on photosynthesis, and on the intracellular levels of the osmoregulatory solute glycerol, the adenine nucleotides and the pyridine nucleotides. In: Biggens J (ed) Progress in photosynthesis research, vol IV. Martinus Nijhoff Publishers, Dordrecht, pp 193–196Google Scholar
  58. Lohbeck KT, Riebesell U, Collins S, Reusch TBH (2013) Functional genetic divergence in high CO2 adapted Emiliania huxleyi populations. Evolution 67:1892–1900PubMedGoogle Scholar
  59. Lohbeck KT, Riebesell U, Reusch TBH (2014) Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification. Proc R Soc B 281(1786):20140003PubMedGoogle Scholar
  60. Maeda M, Thompson JA (1986) On the mechanisms of rapid plasma membrane and chloroplast envelope expansion in Dunaliella salina exposed to hypo-osmotic shock. J Cell Biol 102:289–297PubMedGoogle Scholar
  61. Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosché M, Van Breusegem F, Kangasjärvi J (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot 67:3831–3844PubMedGoogle Scholar
  62. Minagawa J (2011) State transitions—the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta Bioenerg 1807:897–905Google Scholar
  63. Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19PubMedGoogle Scholar
  64. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309PubMedGoogle Scholar
  65. Moheimani NR, Borowitzka MA (2007) Limits to growth of Pleurochrysis carterae (Haptophyta) grown in outdoor raceway ponds. Biotechnol Bioeng 96:27–36PubMedGoogle Scholar
  66. Nedelcu AM (2005) Sex as a response to oxidative stress: stress genes co-opted for sex. Proc R Soc B 272:1935–1940PubMedGoogle Scholar
  67. Nedelcu AM, Marcu O, Michod RE (2004) Sex as a response to oxidative stress: a twofold increase in cellular reactive oxygen species activates sex genes. Proc R Soc Lond B 271:1591–1596Google Scholar
  68. Noctor G, Foyer CH (2016) Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol 171:1581–1592PubMedPubMedCentralGoogle Scholar
  69. Nowicka B, Pluciński B, Kuczyńska P, Kruk J (2016) Physiological characterization of Chlamydomonas reinhardtii acclimated to chronic stress induced by Ag, Cd, Cr, Cu and Hg ions. Ecotoxicol Environ Saf 130:133–145PubMedGoogle Scholar
  70. Parkhill J-P, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529Google Scholar
  71. Perrineau M-M, Zelzion E, Gross J, Price DC, Boyd J, Bhattacharya D (2014) Evolution of salt tolerance in a laboratory reared population of Chlamydomonas reinhardtii. Environ Microbiol 16:1755–1766PubMedGoogle Scholar
  72. Pick U (1992) ATPases and ion transport in Dunaliella. In: Avron M, Ben-Amotz A (eds) Dunaliella: physiology, biochemistry, and biotechnology. CRC Press, Boca Raton, pp 63–97Google Scholar
  73. Popova LG, Shumkova GA, Andreev IM, Balnokin YV (2005) Functional identification of electrogenic Na+-translocating ATPase in the plasma membrane of the halotolerant microalga Dunaliella maritima. FEBS Lett 579:5002–5006PubMedGoogle Scholar
  74. Raja V, Majeed U, Kang H, Andrabi KI, John R (2017) Abiotic stress: interplay between ROS, hormones and MAPKs. Environ Exp Bot 137(Suppl C):142–157Google Scholar
  75. Raven JA, Geider RJ (2003) Adaptation, acclimation and regulation in algal photosynthesis. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer Academic Publishers, Dordrecht, pp 385–412Google Scholar
  76. Remmers IM, Hidalgo-Ulloa A, Brandt BP, Evers WAC, Wijffels RH, Lamers PP (2017) Continuous versus batch production of lipids in the microalgae Acutodesmus obliquus. Bioresour Technol 244:1384–1392PubMedGoogle Scholar
  77. Rosenwasser S, Graff van Creveld S, Schatz D, Malitsky S, Tzfadia O, Aharoni A, Levin Y, Gabashvili A, Feldmesser E, Vardi A (2014) Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment. Proc Nat Acad Sci 111:2740–2745PubMedGoogle Scholar
  78. Sadka A, Lers A, Zamir A, Avron M (1989) A critical examination of the role of de novo protein synthesis in the osmotic adaptation of the halotolerant alga Dunaliella. FEBS Lett 244:93–98Google Scholar
  79. Sadka A, Himmelhoch S, Zamir A (1991) A 150 Kilodalton cell surface protein is induced by salt in the halotolerant green alga Dunaliella salina. Plant Physiol 95:822–831PubMedPubMedCentralGoogle Scholar
  80. Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192:289–316PubMedPubMedCentralGoogle Scholar
  81. Schaum C-E, Buckling A, Smirnoff N, Studholme D, Yvon-Durocher G (2017) Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. bioRxiv.
  82. Schulte BM (2014) What is environmental stress? Insights from fish living in a variable environment. J Exp Biol 217:23–34Google Scholar
  83. Selye H (1973) The evolution of the stress concept: the originator of the concept traces its development from the discovery in 1936 of the alarm reaction to modern therapeutic applications of syntoxic and catatoxic hormones. Am Sci 61(6):692–699PubMedGoogle Scholar
  84. Slaveykova V, Sonntag B, Gutiérrez JC (2016) Stress and protists: no life without stress. Eur J Protistol 55(A):39–49PubMedPubMedCentralGoogle Scholar
  85. Starr R (1970) Control of differentiation in Volvox. Dev Biol 4:59–100Google Scholar
  86. Strain LWS, Borowitzka MA, Daume S (2006) Growth and survival of juvenile greenlip abalone (Haliotis laevigata) feeding on germlings of the macroalgae Ulva sp. J Shellfish Res 25:239–247Google Scholar
  87. Strasser RJ (1988) A concept for stress and its application in remote sensing. In: Lichtenthaler HK (ed) Applications of chlorophyll fluorescence in photosynthesis research, stress physiology, hydrobiology and remote sensing. Kluwer, Dordrecht, pp 333–337Google Scholar
  88. Tammam AA, Fakry EM, El-Sheekh M (2011) Effect of salt stress on antioxidant system and the metabolism of the reactive oxygen species in Dunaliella salina and Dunaliella tertiolecta. Afr J Biotechnol 10:3795–3803Google Scholar
  89. Timmermans KR, Veldhuis MJW, Brussaard CPD (2007) Cell death in three marine diatom species in response to different irradiance levels, silicate, or iron concentrations. Aquat Microb Ecol 46:253–261Google Scholar
  90. Torzillo G, Vonshak A (2013) Environmental stress physiology with reference to mass cultures. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology. Wiley, Chichester, pp 90–111Google Scholar
  91. Tsukahara K, Sawayama S, Yagishita T, Ogi T (1999) Effect of Ca2+ channel blockers on glycerol levels in Dunaliella tertiolecta under hypoosmotic stress. J Biotechnol 70:223–225Google Scholar
  92. Weiss M, Pick U (1990) Transient Na+ flux following hyperosmotic shock in the halotolerant alga Dunaliella salina—a response to intracellular pH changes. J Plant Physiol 136:429–438Google Scholar
  93. Yuasa T, Muto S (1992) Ca2+-dependent protein kinase from the halotolerant green alga Dunaliella tertiolecta—partial purification and Ca2+-dependent association of the enzyme to the microsomes. Arch Biochem Biophys 296:175–182PubMedGoogle Scholar
  94. Yuasa T, Muto S (1996) Activation of 40-kDa protein kinases in response to hypo- and hyperosmotic shock in the halotolerant green alga Dunaliella tertiolecta. Plant Cell Physiol 37:35–42Google Scholar
  95. Yuasa T, Takahashi K, Muto S (1995) Purification and characterization of a Ca2+-dependent protein kinase from the halotolerant green alga Dunaliella tertiolecta. Plant Cell Physiol 36:699–708Google Scholar
  96. Zhang X, Tang X, Wang M, Zhang W, Zhou B, Wang Y (2017) ROS and calcium signaling mediated pathways involved in stress responses of the marine microalgae Dunaliella salina to enhanced UV-B radiation. J Photochem Photobiol B 173(Suppl C):360–367PubMedGoogle Scholar
  97. Zhao R, Ng DHP, Fang L, Chow YYS, Lee YK (2016) MAPK in Dunaliella tertiolecta regulates glycerol production in response to osmotic shock. Eur J Phycol 51:119–128Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Algae R&D CentreMurdoch UniversityMurdochAustralia

Personalised recommendations