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Journal of Applied Phycology

, Volume 30, Issue 6, pp 3121–3130 | Cite as

Gene expression profile of marine Chlorella strains from different latitudes: stress and recovery under elevated temperatures

  • Bahram Barati
  • Phaik-Eem LimEmail author
  • Sook-Yee Gan
  • Sze-Wan Poong
  • Siew-Moi Phang
8th Asian Pacific Phycological Forum

Abstract

Global warming, as a consequence of climate change, poses a critical threat to marine life, including algae. Studies on algal response at the molecular level to temperature stress have been significantly improved by advances in omics technologies. Algae are known to employ various strategies in response to heat stress. For example, algae regulate starch synthesis to provide energy for the cell or rebuild the damaged subunits of photosystems to regain photosynthetic activity. The aim of the present study is to examine the expression of selected photosynthesis-related genes of marine Chlorella originating from different latitudes, in response to heat stress and during the recovery period. In this study, marine Chlorella strains from the Antarctic, temperate region, and the tropics were grown at their ambient and stress-inducing temperatures. The maximum quantum efficiency (Fv/Fm) photosynthetic parameter was used to assess their stress levels. When subjected to heat stress, the Fv/Fm began to decline and when it reached ~ 0.2, the cultures were transferred to their respective ambient temperature for recovery. Total RNA was isolated from these cultures at Fv/Fm ~ 0.4, 0.2, and when it regained 0.4 during recovery. The expression of four genes including psbA, psaB, psbC, and rbcL was analyzed using RT-PCR. The housekeeping gene, histone subunit three (H3) was used for data normalization. Studying the genes involved in the adaptation mechanisms would enhance our knowledge on algal adaptation pathways and pave the way for genetic engineers to develop more tolerant strains.

Keywords

Abiotic stress Photosystem Photosynthesis Stress adaptation 

Notes

Funding information

The study was supported by research grants from the Ministry of Higher Education, Malaysia, HiCOE research grant (IOES-2014H), University of Malaya Postgraduate Research Fund (PG146-2015A), and the following University of Malaya Research Grants (RP002C-13SUS, RU009F-2015).

References

  1. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550CrossRefGoogle Scholar
  2. Barati B, Lim PE, Gan SY, Poong SW, Phang SM, Beardall J (2018) Effect of elevated temperature on the physiological responses of marine Chlorella strains from different latitudes. J Appl Phycol 30:1–13CrossRefGoogle Scholar
  3. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113CrossRefGoogle Scholar
  4. Balczun C, Bunse A, Nowrousian M, Korbel A, Glanz S, Kück U (2005) DNA microarray and real-time PCR analysis of two nuclear photosystem I mutants from Chlamydomonas reinhardtii reveal downregulation of Lhcb genes but different regulation of Lhca genes. Biochim Biopgys Acta Gene Struct Expr 1732:62–68CrossRefGoogle Scholar
  5. Beardall J, Raven JA (2004) The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43:26–40CrossRefGoogle Scholar
  6. Behrenfeld MJ, Randerson JT, McClain CR, Feldman GC, Los SO, Tucker CJ, Esaias WE (2001) Biospheric primary production during an ENSO transition. Science 291:2594–2597CrossRefGoogle Scholar
  7. Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher-plants. Annu Rev Plant Physiol 31:491–543CrossRefGoogle Scholar
  8. Bi A, Fan J, Hu Z, Wang G, Amombo E, Fu J, Hu T (2016) Differential acclimation of enzymatic antioxidant metabolism and photosystem II photochemistry in tall fescue under drought and heat and the combined stresses. Front Plant Sci 7:453CrossRefGoogle Scholar
  9. Bilgin DD, Zavala JA, Zhu JIN, Clough SJ, Ort DR, Delucia E (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33:1597–1613CrossRefGoogle Scholar
  10. Biswal B, Joshi P, Raval M, Biswal U (2011) Photosynthesis, a global sensor of environmental stress in green plants: stress signalling and adaptation. Curr Sci 101:47–56Google Scholar
  11. Campbell SJ, McKenzie LJ, Kerville SP (2006) Photosynthetic responses of seven tropical seagrasses to elevated seawater temperature. J Exp Mar Biol Ecol 330:455–468CrossRefGoogle Scholar
  12. Cao K, He M, Yang W, Chen B, Luo W, Zou S, Wang C (2016) The eurythermal adaptivity and temperature tolerance of a newly isolated psychrotolerant Arctic Chlorella sp. J Appl Phycol 28:877–888CrossRefGoogle Scholar
  13. Chapman RL (2013) Algae: the world’s most important “plants”—an introduction. Mitig Adapt Strateg Glob Chang 18:5–12CrossRefGoogle Scholar
  14. Chong GL, Chu WL, Othman RY, Phang SM (2011) Differential gene expression of an Antarctic Chlorella in response to temperature stress. Polar Biol 34:637–645CrossRefGoogle Scholar
  15. Dall'Osto L, Bressan M, Bassi R (2015) Biogenesis of light harvesting proteins. Biochim Biophys Acta Bioenerg 1847:861–871CrossRefGoogle Scholar
  16. Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27:2–8CrossRefGoogle Scholar
  17. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci 105:6668–6672CrossRefGoogle Scholar
  18. Endres CH, Roth A, Brück TB (2016) Thermal reactor model for large-scale algae cultivation in vertical flat panel photobioreactors. Environ Sci Technol 50:3920–3927CrossRefGoogle Scholar
  19. Falkowski PG, Raven JA (2013) Aquatic photosynthesis. Blackwell Scientific Publishers, Oxford, p 375Google Scholar
  20. Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717CrossRefGoogle Scholar
  21. Fujimoto N, Inamori Y, Sugiura N, Sudo R (1994) Effects of temperature-change on algal growth. Environ Technol 15:497–500CrossRefGoogle Scholar
  22. Gierz SL, Forêt S, Leggat W (2017) Transcriptomic analysis of thermally stressed Symbiodinium reveals differential expression of stress and metabolism genes. Front Plant Sci 8:271CrossRefGoogle Scholar
  23. Gururani MA, Mohanta TK, Bae H (2015) Current understanding of the interplay between phytohormones and photosynthesis under environmental stress. Int J Mol Sci 16:19055–19085CrossRefGoogle Scholar
  24. Harbinson J, Genty B, Baker NR (1989) Relationship between the quantum efficiencies of photosystems I and II in pea leaves. Plant Physiol 90:1029–1034CrossRefGoogle Scholar
  25. Havaux M, Tardy F (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198:324–333CrossRefGoogle Scholar
  26. Hihara Y, Sonoike K (2001) Regulation, inhibition and protection of photosystem I. In: Aro E-M, Andersson B (eds) Regulation of photosynthesis. Springer, Berlin, pp 507–531Google Scholar
  27. Huner NP, Oquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39CrossRefGoogle Scholar
  28. Hwang Y-s, Jung G, Jin E (2008) Transcriptome analysis of acclimatory responses to thermal stress in Antarctic algae. Biochem Biophys Res Commun 367:635–641CrossRefGoogle Scholar
  29. Jueterbock A, Kollias S, Smolina I, Fernandes JMO, Coyer JA, Olsen JL, Hoarau G (2014) Thermal stress resistance of the brown alga Fucus serratus along the North-Atlantic coast: acclimatization potential to climate change. Mar Genomics 13:27–36CrossRefGoogle Scholar
  30. Kebeish R, El-Ayouty Y, Husain A (2014a) Effect of copper on growth, bioactive metabolites, antioxidant enzymes and photosynthesis-related gene transcription in Chlorella vulgaris. World J Biol Biol Sci 2:34–43Google Scholar
  31. Kebeish R, El-Ayouty Y, Hussein A (2014b) Effect of salinity on biochemical traits and photosynthesis-related gene transcription in Chlorella vulgaris. Egypt J Bot 54:281–294CrossRefGoogle Scholar
  32. Krienitz L, Hegewald EH, Hepperle D, Huss VAR, Rohrs T, Wolf M (2004) Phylogenetic relationship of Chlorella and Parachlorella gen. nov. (Chlorophyta, Trebouxiophyceae). Phycologia 43:529–542CrossRefGoogle Scholar
  33. Krienitz L, Huss VA, Bock C (2015) Chlorella: 125 years of the green survivalist. Trends Plant Sci 20:67–69CrossRefGoogle Scholar
  34. Liu L, Zhu B, Wang GX (2015) Azoxystrobin-induced excessive reactive oxygen species (ROS) production and inhibition of photosynthesis in the unicellular green algae Chlorella vulgaris. Environ Sci Pollut Res 22:7766–7775CrossRefGoogle Scholar
  35. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408CrossRefGoogle Scholar
  36. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefGoogle Scholar
  37. Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta Bioenerg 1058:87–106CrossRefGoogle Scholar
  38. 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 323:1470–1473CrossRefGoogle Scholar
  39. Moreno-Risueno MA, Busch W, Benfey PN (2010) Omics meet networks—using systems approaches to infer regulatory networks in plants. Curr Opin Plant Biol 13:126–131CrossRefGoogle Scholar
  40. Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NP (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70:222–252CrossRefGoogle Scholar
  41. Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim Biophys Acta Bioenerg 1817:247–257CrossRefGoogle Scholar
  42. Nouri MZ, Moumeni A, Komatsu S (2015) Abiotic stresses: insight into gene regulation and protein expression in photosynthetic pathways of plants. Int J Mol Sci 16:20392–20416CrossRefGoogle Scholar
  43. Pabinger S, Rödiger S, Kriegner A, Vierlinger K, Weinhäusel A (2014) A survey of tools for the analysis of quantitative PCR (qPCR) data. Biomol Detect Quantif 1:23–33CrossRefGoogle Scholar
  44. Peng H, Wei D, Chen G, Chen F (2016) Transcriptome analysis reveals global regulation in response to CO2 supplementation in oleaginous microalga Coccomyxa subellipsoidea C-169. Biotechnol Biofuels 9:151CrossRefGoogle Scholar
  45. Phang SM, Chu WL (1999) University of Malaya Algae Culture Collection (UMACC). Catalogue of strains. Institute of Postgraduate Studies and Research, University of Malaya, Kuala Lumpur 77 pp.Google Scholar
  46. 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
  47. Piette F, D'Amico S, Mazzucchelli G, Danchin A, Leprince P, Feller G (2011) Life in the cold: a proteomic study of cold-repressed proteins in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Appl Environ Microbiol 77:3881–3883CrossRefGoogle Scholar
  48. Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine-phytoplankton. J Mar Res 38:687–701Google Scholar
  49. Poong SW, Lim PE, Lai JWS, Phang SM (2017) Optimization of high quality total RNA isolation from the microalga, Chlorella sp. (Trebouxiophyceae, Chlorophyta) for next-generation sequencing. Phycol Res 65:146–150CrossRefGoogle Scholar
  50. Poong SW, Lee KK, Lim PE, Pai TW, Wong CY, Phang SM, Chen CM, Yang CH Liu CC (2018) RNA-Seq-mediated transcriptomic analysis of heat stress response in a polar Chlorella sp. (Trebouxiophyceae, Chlorophyta). J Appl Phycol.  https://doi.org/10.1007/s10811-018-1455-9
  51. Qian H, Xu X, Chen W, Jiang H, Jin Y, Liu W, Fu Z (2009a) Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere 75:368–375CrossRefGoogle Scholar
  52. Qian H, Chen W, Li J, Wang J, Zhou Z, Liu W, Fu Z (2009b) The effect of exogenous nitric oxide on alleviating herbicide damage in Chlorella vulgaris. Aquat Toxicol 92:250–257CrossRefGoogle Scholar
  53. Qian H, Pan X, Shi S, Yu S, Jiang H, Lin Z, Fu Z (2011) Effect of nonylphenol on response of physiology and photosynthesis-related gene transcription of Chlorella vulgaris. Environ Monit Assess 182:61–69CrossRefGoogle Scholar
  54. Qian H, Pan X, Chen J, Zhou D, Chen Z, Zhang L, Fu Z (2012) Analyses of gene expression and physiological changes in Microcystis aeruginosa reveal the phytotoxicities of three environmental pollutants. Ecotoxicol 21:847–859CrossRefGoogle Scholar
  55. Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237CrossRefGoogle Scholar
  56. Ras M, Steyer J-P, Bernard O (2013) Temperature effect on microalgae: a crucial factor for outdoor production. Rev Environ Sci Biol 12:153–164CrossRefGoogle Scholar
  57. Raven JA, Geider RJ (1988) Temperature and algal growth. New Phytol 110:441–461CrossRefGoogle Scholar
  58. Robinson PJ (2001) On the definition of a heat wave. J Appl Meteorol 40:762–775CrossRefGoogle Scholar
  59. Safi C, Zebib B, Merah O, Pontalier P-Y, Vaca-Garcia C (2014) Morphology, composition, production, processing and applications of Chlorella vulgaris: a review. Renew Sust Energ Rev 35:265–278CrossRefGoogle Scholar
  60. Saibo NJM, Lourenco T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103:609–623CrossRefGoogle Scholar
  61. Stamenkovic M, Hanelt D (2013) Adaptation of growth and photosynthesis to certain temperature regimes is an indicator for the geographical distribution of Cosmarium strains (Zygnematophyceae, Streptophyta). Eur J Phycol 48:116–127CrossRefGoogle Scholar
  62. Stocker TF, Qin D, Plattner GK, Tignor MM, Allen SK, Boschung J et al. (2014) Climate Change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of IPCC the intergovernmental panel on climate change: Cambridge University PressGoogle Scholar
  63. Singh S, Singh P (2015) Effect of temperature and light on the growth of algae species: a review. Adv Mater Res 50:431–444Google Scholar
  64. Smith CR, De Leo FC, Bernardino AF, Sweetman AK, Arbizu PM (2008) Abyssal food limitation, ecosystem structure and climate change. Trends Ecol Evol 23:518–528CrossRefGoogle Scholar
  65. Teoh ML, Phang SM, Chu WL (2013) Response of Antarctic, temperate, and tropical microalgae to temperature stress. J Appl Phycol 25:285–297CrossRefGoogle Scholar
  66. Tripathi A, Tripathi DK, Chauhan D, Kumar N, Singh G (2016) Paradigms of climate change impacts on some major food sources of the world: a review on current knowledge and future prospects. Agric Ecosyst Environ 216:356–373CrossRefGoogle Scholar
  67. Wang L, Wang C, Zheng M, Lou Y, Song M, Wang Z, Zheng L (2014) Influence of tris(2,3-dibromopropyl) isocyanurate on the expression of photosynthesis genes of Nannochloropsis sp. Gene 540:68–70CrossRefGoogle Scholar
  68. Wang S, Xu Z (2016) Effects of dihydroartemisinin and artemether on the growth, chlorophyll fluorescence, and extracellular alkaline phosphatase activity of the cyanobacterium Microcystis aeruginosa. PLoS One 11:e0164842CrossRefGoogle Scholar
  69. Wong CY, Teoh ML, Phang SM, Lim PE, Beardall J (2015) Interactive effects of temperature and UV radiation on photosynthesis of Chlorella strains from polar, temperate and tropical environments: differential impacts on damage and repair. PLoS One 10:e0139469CrossRefGoogle Scholar
  70. Xu J, Zhang X, Ye N, Zheng Z, Mou S, Dong M, Miao J (2013) Activities of principal photosynthetic enzymes in green macroalga Ulva linza: functional implication of C4 pathway in CO2 assimilation. Sci China Life Sci 56:571–580CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Bahram Barati
    • 1
    • 2
  • Phaik-Eem Lim
    • 1
    Email author
  • Sook-Yee Gan
    • 3
  • Sze-Wan Poong
    • 1
  • Siew-Moi Phang
    • 1
    • 4
  1. 1.Institute of Ocean and Earth SciencesUniversity of MalayaKuala LumpurMalaysia
  2. 2.Institute of Graduate StudiesUniversity of MalayaKuala LumpurMalaysia
  3. 3.School of PharmacyInternational Medical UniversityKuala LumpurMalaysia
  4. 4.Institute of Biological SciencesUniversity of MalayaKuala LumpurMalaysia

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