Advertisement

Influence of spectral intensity and quality of LED lighting on photoacclimation, carbon allocation and high-value pigments in microalgae

  • Dónal McGeeEmail author
  • Lorraine Archer
  • Gerard T. A. Fleming
  • Eoin Gillespie
  • Nicolas Touzet
Original article

Abstract

Tailoring spectral quality during microalgal cultivation can provide a means to increase productivity and enhance biomass composition for downstream biorefinery. Five microalgae strains from three distinct lineages were cultivated under varying spectral intensities and qualities to establish their effects on pigments and carbon allocation. Light intensity significantly impacted pigment yields and carbon allocation in all strains, while the effects of spectral quality were mostly species-specific. High light conditions induced chlorophyll photoacclimation and resulted in an increase in xanthophyll cycle pigments in three of the five strains. High-intensity blue LEDs increased zeaxanthin tenfold in Rhodella sp. APOT_15 relative to medium or low light conditions. White light however was optimal for phycobiliprotein content (11.2 mg mL−1) for all tested light intensities in this strain. The highest xanthophyll pigment yields for the Chlorophyceae were associated with medium-intensity blue and green lights for Brachiomonas submarina APSW_11 (5.6 mg g−1 lutein and 2.0 mg g−1 zeaxanthin) and Kirchneriella aperta DMGFW_21 (1.5 mg g−1 lutein and 1 mg g−1 zeaxanthin), respectively. The highest fucoxanthin content in both Heterokontophyceae strains (2.0 mg g−1) was associated with medium and high white light for Stauroneis sp. LACW_24 and Phaeothamnion sp. LACW_34, respectively. This research provides insights into the application of LEDs to influence microalgal physiology, highlighting the roles of low light on lipid metabolism in Rhodella sp. APOT_15, of blue and green lights for carotenogenesis in Chlorophyceae and red light-induced photoacclimation in diatoms.

Keywords

Carbon allocation Carotenoids LEDs Microalgal physiology Phycobiliproteins 

Abbreviations

Chl a

Chlorophyll-a

Chl b

Chlorophyll-b

Chl c

Chlorophyll-c

Lu

Lutein

Ze

Zeaxanthin

Dd

Diadinoxanthin

Dt

Diatoxanthin

PBP

Phycobiliproteins

LL

Low light

ML

Medium light

HL

High light

Notes

Acknowledgements

We would like to thank Ken Henry, JohnJoe Mc Gloin and Aine Fox of the School of Science for their technical support. The authors would like to thank the anonymous reviews whose suggestions helped improve and clarify this manuscript.

Funding

This work was supported by Science Foundation Ireland (SFI) as part of the METALGAE research programme (12/IP/1497).

Compliance with ethical standards

Conflict of interest

No conflicts of interest declared.

Supplementary material

11120_2019_686_MOESM1_ESM.docx (1.4 mb)
Supplementary material 1 (DOCX 1455 kb)

References

  1. Abiusi F, Sampietro G, Marturano G et al (2014) Growth, photosynthetic efficiency, and biochemical composition of Tetraselmis suecica F&M-M33 grown with LEDs of different colors. Biotechnol Bioeng 111:956–964.  https://doi.org/10.1002/bit.25014 CrossRefPubMedGoogle Scholar
  2. Atta M, Idris A, Bukhari A, Wahidin S (2013) Intensity of blue LED light: a potential stimulus for biomass and lipid content in fresh water microalgae Chlorella vulgaris. Bioresour Technol 148:373–378.  https://doi.org/10.1016/j.biortech.2013.08.162 CrossRefPubMedGoogle Scholar
  3. Baer S, Heining M, Schwerna P et al (2016) Optimization of spectral light quality for growth and product formation in different microalgae using a continuous photobioreactor. Algal Res 14:109–115.  https://doi.org/10.1016/J.ALGAL.2016.01.011 CrossRefGoogle Scholar
  4. BCC Research (2015) The Global Market for Carotenoids—FOD025C. http://www.bccresearch.com/market-research/food-and-beverage/carotenoids-market-fod025c.html. Accessed 27 Jan 2016
  5. Beel B, Prager K, Spexard M et al (2012) A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell 24:2992–3008.  https://doi.org/10.1105/tpc.112.098947 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Beer S, Eshel A (1985) Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Mar Freshw Res 36:785.  https://doi.org/10.1071/MF9850785 CrossRefGoogle Scholar
  7. Bohne F, Linden H (2002) Regulation of carotenoid biosynthesis genes in response to light in Chlamydomonas reinhardtii. Biochim Biophys Acta 1579:26–34.  https://doi.org/10.1016/S0167-4781(02)00500-6 CrossRefPubMedGoogle Scholar
  8. Bolatkhan K, Kossalbayev BD, Zayadan BK et al (2019) Hydrogen production from phototrophic microorganisms: reality and perspectives. Int J Hydrog Energy 44:5799–5811.  https://doi.org/10.1016/J.IJHYDENE.2019.01.092 CrossRefGoogle Scholar
  9. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brunet C, Chandrasekaran R, Barra L et al (2014) Spectral radiation dependent photoprotective mechanism in the diatom Pseudo-nitzschia multistriata. PLoS ONE 9:e87015.  https://doi.org/10.1371/journal.pone.0087015 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Carter JD, Leblond JD (2018) Red (hot) algae: modulation of mono- and digalactosyldiacylglycerol-associated fatty acids of Polysiphonia sp. and Porphyridium sp. in response to growth temperature. Eur J Phycol 53:460–470.  https://doi.org/10.1080/09670262.2018.1469049 CrossRefGoogle Scholar
  12. Cassie V (1976) New records of two species of planktonic algae in New Zealand. New Zeal J Bot 14:349–354CrossRefGoogle Scholar
  13. Chandrasekaran R, Barra L, Carillo S et al (2014) Light modulation of biomass and macromolecular composition of the diatom Skeletonema marinoi. J Biotechnol 192:114–122.  https://doi.org/10.1016/J.JBIOTEC.2014.10.016 CrossRefPubMedGoogle Scholar
  14. Chen T, Liu J, Guo B et al (2015) Light attenuates lipid accumulation while enhancing cell proliferation and starch synthesis in the glucose-fed oleaginous microalga Chlorella zofingiensis. Sci Rep 5:14936.  https://doi.org/10.1038/srep14936 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Coble PG (2007) Marine optical biogeochemistry: the chemistry of ocean color. Chem Rev 107:402–418.  https://doi.org/10.1021/CR15+ CrossRefPubMedGoogle Scholar
  16. Coward T, Fuentes-Grünewald C, Silkina A et al (2016) Utilising light-emitting diodes of specific narrow wavelengths for the optimization and co-production of multiple high-value compounds in Porphyridium purpureum. Bioresour Technol 221:607–615.  https://doi.org/10.1016/j.biortech.2016.09.093 CrossRefPubMedGoogle Scholar
  17. Craig Bailey J, Bidigare RR, Christensen SJ, Andersen RA (1998) Phaeothamniophyceae classis nova: a new lineage of chromophytes based upon photosynthetic pigments, rbcL sequence analysis and ultrastructure. Protist 149:245–263.  https://doi.org/10.1016/S1434-4610(98)70032-X CrossRefPubMedGoogle Scholar
  18. Cunningham FX, Dennenberg RJ, Mustardy L et al (1989) Stoichiometry of photosystem I, photosystem II, and phycobilisomes in the Red Alga porphyridium cruentum as a function of growth irradiance. Plant Physiol 91(3):1179–1187.  https://doi.org/10.1104/pp.91.3.1179 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Depauw FA, Rogato A, Ribera d’Alcala M, Falciatore A (2012) Exploring the molecular basis of responses to light in marine diatoms. J Exp Bot 63:1575–1591.  https://doi.org/10.1093/jxb/ers005 CrossRefPubMedGoogle Scholar
  20. Egeland ES, Garrido JL, Clementson L, Andersen K, Thomas CS, Zapata M, Airs R, Llewellyn CA, Newman GL, Rodriguez F, Roy S (2011) Part VII Data sheets aiding identification of phytoplankton carotenoids and chlorophylls. In: Roy S, Llewellyn CA, Egeland ES, Johnson G (eds) Phytoplankton pigments: characterization, chemotaxonomy and applications in oceanography. Cambridge University Press, Cambridge, pp 665–822Google Scholar
  21. Falciatore A, Bowler C (2005) The evolution and function of blue and red light photoreceptors. Curr Top Dev Biol 68:317–350.  https://doi.org/10.1016/S0070-2153(05)68011-8 CrossRefPubMedGoogle Scholar
  22. Ferroni L, Baldisserotto C, Pantaleoni L et al (2007) High salinity alters chloroplast morpho-physiology in a freshwater Kirchneriella species (Slelnastraceae) from Ethiopian Lake Awasa 1. Am J Bot 94:1972–1983.  https://doi.org/10.3732/ajb.94.12.1972 CrossRefPubMedGoogle Scholar
  23. Finazzi G, Minagawa J (2014) High light acclimation in green microalgae. In: Demmig-Adams B, Garab G, Adams W III, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria: Advances in photosynthesis and respiration (Including bioenergy and related processes), vol 40. Springer, DordrechtCrossRefGoogle Scholar
  24. Frampton DMF, Gurney RH, Dunstan GA et al (2013) Evaluation of growth, nutrient utilization and production of bioproducts by a wastewater-isolated microalga. Bioresour Technol 130:261–268.  https://doi.org/10.1016/j.biortech.2012.12.001 CrossRefPubMedGoogle Scholar
  25. Fu W, Gudmundsson O, Feist AM et al (2012) Maximizing biomass productivity and cell density of Chlorella vulgaris by using light-emitting diode-based photobioreactor. J Biotechnol 161:242–249.  https://doi.org/10.1016/J.JBIOTEC.2012.07.004 CrossRefPubMedGoogle Scholar
  26. Fu W, Guðmundsson O, Paglia G et al (2013) Enhancement of carotenoid biosynthesis in the green microalga Dunaliella salina with light-emitting diodes and adaptive laboratory evolution. Appl Microbiol Biotechnol 97:2395–2403.  https://doi.org/10.1007/s00253-012-4502-5 CrossRefPubMedGoogle Scholar
  27. Geider RJ (1987) Light and temperature dependance of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol 106:1–34.  https://doi.org/10.1111/j.1469-8137.1987.tb04788.x CrossRefGoogle Scholar
  28. Gillan FT, Mcfadden GI, Wetherbee R, Johns RB (1981) Sterols and fatty acids of an antarctic sea ice diatom, Stauroneis amphioxys. Phytochemistry 20:1935–1937.  https://doi.org/10.1016/0031-9422(81)84038-1 CrossRefGoogle Scholar
  29. Guihéneuf F, Stengel DB (2015) Towards the biorefinery concept: interaction of light, temperature and nitrogen for optimizing the co-production of high-value compounds in Porphyridium purpureum. Algal Res 10:152–163.  https://doi.org/10.1016/j.algal.2015.04.025 CrossRefGoogle Scholar
  30. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Springer, BostonGoogle Scholar
  31. Higgins HW, Wright SW, Schlüter L (2011) Quantitative interpretation of chemotaxonomic pigment data. In: Roy S, Llewellyn C, Egeland ES, Johnsen G (eds) Phytoplankton pigments. Cambridge University Press, Cambridge, pp 257–313CrossRefGoogle Scholar
  32. Ho S-H, Chan M-C, Liu C-C et al (2014) Enhancing lutein productivity of an indigenous microalga Scenedesmus obliquus FSP-3 using light-related strategies. Bioresour Technol 152:275–282.  https://doi.org/10.1016/j.biortech.2013.11.031 CrossRefPubMedGoogle Scholar
  33. Hultberg M, Jönsson HL, Bergstrand K-J, Carlsson AS (2014) Impact of light quality on biomass production and fatty acid content in the microalga Chlorella vulgaris. Bioresour Technol 159:465–467.  https://doi.org/10.1016/J.BIORTECH.2014.03.092 CrossRefPubMedGoogle Scholar
  34. Huner NPA, Öquist G, Hurry VM et al (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39.  https://doi.org/10.1007/BF02185436 CrossRefPubMedGoogle Scholar
  35. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193.  https://doi.org/10.1016/j.bbabio.2011.04.012 CrossRefPubMedGoogle Scholar
  36. Jeffrey SW, Mantoura RFC, Wright SW, et al (1997) Phytoplankton pigments in oceanography: guidelines to modern methods. In: Jeffrey SW, Mantoura RFC, Wright SW (eds). UNESCO Pub, Paris, p 661Google Scholar
  37. Jeffrey SW, Wright SW, Zapata M (2011) Microalgal classes and their signature pigments. In: Roy S, Llewellyn C, Egeland ES, Johnsen G (eds) Phytoplankton Pigments. Cambridge University Press, Cambridge, pp 3–77CrossRefGoogle Scholar
  38. Jungandreas A, Schellenberger Costa B, Jakob T et al (2014) The acclimation of Phaeodactylum tricornutum to blue and red light does not influence the photosynthetic light reaction but strongly disturbs the carbon allocation pattern. PLoS ONE 9:e99727.  https://doi.org/10.1371/journal.pone.0099727 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kim DG, Lee C, Park S-M, Choi Y-E (2014) Manipulation of light wavelength at appropriate growth stage to enhance biomass productivity and fatty acid methyl ester yield using Chlorella vulgaris. Bioresour Technol 159:240–248.  https://doi.org/10.1016/J.BIORTECH.2014.02.078 CrossRefPubMedGoogle Scholar
  40. Kowallik W, Schätzle S (1980) Enhancement of carbohydrate degradation by blue light. In: Senger H (ed) The blue light syndrome: proceedings in life sciences. Springer, BerlinGoogle Scholar
  41. Lee C, Ahn J-W, Kim J-B et al (2018) Comparative transcriptome analysis of Haematococcus pluvialis on astaxanthin biosynthesis in response to irradiation with red or blue LED wavelength. World J Microbiol Biotechnol 34:96.  https://doi.org/10.1007/s11274-018-2459-y CrossRefPubMedGoogle Scholar
  42. Lepetit B, Goss R, Jakob T, Wilhelm C (2012) Molecular dynamics of the diatom thylakoid membrane under different light conditions. Photosynth Res 111:245–257.  https://doi.org/10.1007/s11120-011-9633-5 CrossRefPubMedGoogle Scholar
  43. MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38.  https://doi.org/10.1046/j.1529-8817.2002.00094.x CrossRefGoogle Scholar
  44. Mayers JJ, Flynn KJ, Shields RJ (2013) Rapid determination of bulk microalgal biochemical composition by Fourier-Transform Infrared spectroscopy. Bioresour Technol 148:215–220.  https://doi.org/10.1016/j.biortech.2013.08.133 CrossRefPubMedGoogle Scholar
  45. Mc Gee D, Archer L, Paskuliakova A et al (2018) Rapid chemotaxonomic profiling for the identification of high-value carotenoids in microalgae. J Appl Phycol.  https://doi.org/10.1007/s10811-017-1247-7 CrossRefGoogle Scholar
  46. Mihova SG, Georgiev DI, Minkova KM, Tchernov AA (1996) Phycobiliproteins in Rhodella reticulata and photoregulatory effects on their content. J Biotechnol 48:251–257.  https://doi.org/10.1016/0168-1656(96)01515-5 CrossRefGoogle Scholar
  47. Mimouni V, Couzinet-Mossion A, Ulmann L et al (2018) Lipids from microalgae. In: Ira A, Levine JF (eds) Microalgae in health and disease prevention, 1st edn. Elsevier, Amsterdam, pp 109–131CrossRefGoogle Scholar
  48. Mishra SK, Suh WI, Farooq W et al (2014) Rapid quantification of microalgal lipids in aqueous medium by a simple colorimetric method. Bioresour Technol 155:330–333.  https://doi.org/10.1016/j.biortech.2013.12.077 CrossRefPubMedGoogle Scholar
  49. Mohsenpour SF, Richards B, Willoughby N (2012) Spectral conversion of light for enhanced microalgae growth rates and photosynthetic pigment production. Bioresour Technol 125:75–81.  https://doi.org/10.1016/J.BIORTECH.2012.08.072 CrossRefPubMedGoogle Scholar
  50. Olenina I (2006) Biovolumes and size-classes of phytoplankton in the Baltic Sea. HELCOM Balt Sea Environ 106:144Google Scholar
  51. Ooms MD, Graham PJ, Nguyen B et al (2017) Light dilution via wavelength management for efficient high-density photobioreactors. Biotechnol Bioeng 114:1160–1169.  https://doi.org/10.1002/bit.26261 CrossRefPubMedGoogle Scholar
  52. Orefice I, Chandrasekaran R, Smerilli A et al (2016) Light-induced changes in the photosynthetic physiology and biochemistry in the diatom Skeletonema marinoi. Algal Res 17:1–13.  https://doi.org/10.1016/J.ALGAL.2016.04.013 CrossRefGoogle Scholar
  53. Ra C-H, Kang C-H, Jung J-H et al (2016) Effects of light-emitting diodes (LEDs) on the accumulation of lipid content using a two-phase culture process with three microalgae. Bioresour Technol 212:254–261.  https://doi.org/10.1016/J.BIORTECH.2016.04.059 CrossRefPubMedGoogle Scholar
  54. Sadvakasova AK, Akmukhanova NR, Bolatkhan K et al (2019) Search for new strains of microalgae-producers of lipids from natural sources for biodiesel production. Int J Hydrog Energy 44:5844–5853.  https://doi.org/10.1016/J.IJHYDENE.2019.01.093 CrossRefGoogle Scholar
  55. Schulze PSC, Barreira LA, Pereira HGC et al (2014) Light emitting diodes (LEDs) applied to microalgal production. Trends Biotechnol 32:422–430.  https://doi.org/10.1016/j.tibtech.2014.06.001 CrossRefPubMedGoogle Scholar
  56. Sheath RG, Sherwood AR (2002) Phylum Rhodophyta (Red Algae). In: John DM, Whitton BA, Brook AJ (eds) The freshwater algal flora of the British Isles. An identification guide to freshwater and terrestrial algae. Cambridge University Press, Cambridge, pp 123–143Google Scholar
  57. Shikata T, Iseki M, Matsunaga S et al (2011) Blue and Red Light-Induced Germination of Resting Spores in the Red-Tide Diatom Leptocylindrus danicus†. Photochem Photobiol 87:590–597.  https://doi.org/10.1111/j.1751-1097.2011.00914.x CrossRefPubMedGoogle Scholar
  58. Steinbrenner J, Linden H (2003) Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis: regulation by photosynthetic redox control. Plant Mol Biol 52:343–356.  https://doi.org/10.1023/A:1023948929665 CrossRefPubMedGoogle Scholar
  59. Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689–692.  https://doi.org/10.1038/nature02954 CrossRefPubMedGoogle Scholar
  60. Teo CL, Atta M, Bukhari A et al (2014) Enhancing growth and lipid production of marine microalgae for biodiesel production via the use of different LED wavelengths. Bioresour Technol 162:38–44.  https://doi.org/10.1016/j.biortech.2014.03.113 CrossRefPubMedGoogle Scholar
  61. Terry KL, Hirata J, Laws EA (1983) Light-limited growth of two strains of the marine diatom Phaeodactylum tricornutum Bohlin: chemical composition, carbon partitioning and the diel periodicity of physiological processes. J Exp Mar Bio Ecol 68:209–227.  https://doi.org/10.1016/0022-0981(83)90054-0 CrossRefGoogle Scholar
  62. Tlalka M, Runquist M, Fricker M (1999) Light perception and the role of the xanthophyll cycle in blue-light-dependent chloroplast movements in Lemna trisulca L. Plant J 20:447–459.  https://doi.org/10.1046/j.1365-313x.1999.00614.x CrossRefPubMedGoogle Scholar
  63. Trevelyan WE, Forrest RS, Harrison JS (1952) Determination of yeast carbohydrates with the anthrone reagent. Nature 170:626–627.  https://doi.org/10.1038/170626a0 CrossRefPubMedGoogle Scholar
  64. Vernès L, Li Y, Chemat F, Abert-Vian M (2019) Biorefinery concept as a key for sustainable future to green chemistry—the case of microalgae. In: Li Y, Chemat F (eds) Plant Based “Green Chemistry 2.0″. Green chemistry and sustainable technology. Springer, SingaporeGoogle Scholar
  65. Villay A, Laroche C, Roriz D et al (2013) Optimisation of culture parameters for exopolysaccharides production by the microalga Rhodella violacea. Biores Technol 146:732–735.  https://doi.org/10.1016/j.biortech.2013.07.030 CrossRefGoogle Scholar
  66. Wagner H, Jakob T, Fanesi A, Wilhelm C (2017) Towards an understanding of the molecular regulation of carbon allocation in diatoms: the interaction of energy and carbon allocation. Philos Trans R Soc Lond B 372:20160410.  https://doi.org/10.1098/rstb.2016.0410 CrossRefGoogle Scholar
  67. Wang W-J, Wang F-J, Sun X-T et al (2013) Comparison of transcriptome under red and blue light culture of Saccharina japonica (Phaeophyceae). Planta 237:1123–1133.  https://doi.org/10.1007/s00425-012-1831-7 CrossRefPubMedGoogle Scholar
  68. Wang W, Yu L-J, Xu C et al (2019) Structural basis for blue-green light harvesting and energy dissipation in diatoms. Science.  https://doi.org/10.1126/science.aav0365 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Watanabe S, Tsuchimoto K, Floyd GL (1989) Light and electron microscopy of Brachiomonas submarina Bohlin (Chlamydomonadales, Chlorophyceae). Phycologia 28:188–196.  https://doi.org/10.2216/i0031-8884-28-2-188.1 CrossRefGoogle Scholar
  70. Wright SW, Jeffery SW, Mantoura RFCEN (1991) Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 77:183–196.  https://doi.org/10.3354/meps077183 CrossRefGoogle Scholar
  71. Xi T, Kim DG, Roh SW et al (2016) Enhancement of astaxanthin production using Haematococcus pluvialis with novel LED wavelength shift strategy. Appl Microbiol Biotechnol.  https://doi.org/10.1007/s00253-016-7301-6 CrossRefPubMedGoogle Scholar
  72. Xiuxia Y, Xiaoqi Z, Yupeng J, Qun L (2003) Effects of sodium nitrate and sodium acetate concentrations on the growth and fatty acid composition of Brachiomonas submarina. J Ocean Univ Qingdao 2:75–78.  https://doi.org/10.1007/s11802-003-0031-2 CrossRefGoogle Scholar
  73. Yallop ML, Anesio AM (2010) Benthic diatom flora in supraglacial habitats: a generic-level comparison. Ann Glaciol 51:15–22.  https://doi.org/10.3189/172756411795932029 CrossRefGoogle Scholar
  74. Yaron A, Dvir I, Maislos M et al (1995) The red microalga Rhodella reticulata as a source of a dietary ω-3 highly unsaturated fatty acid— Eicosapentaenoic acid. Dev Food Sci 37:665–674.  https://doi.org/10.1016/S0167-4501(06)80188-3 CrossRefGoogle Scholar
  75. Zhao P, Gu W, Wu S et al (2014) Silicon enhances the growth of Phaeodactylum tricornutum Bohlin under green light and low temperature. Sci Rep 4:23–35.  https://doi.org/10.1038/srep03958 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Dónal McGee
    • 1
    Email author
  • Lorraine Archer
    • 1
  • Gerard T. A. Fleming
    • 2
  • Eoin Gillespie
    • 1
  • Nicolas Touzet
    • 1
  1. 1.Department of Environmental Science, School of Science, CERIS, Centre for Environmental Research, Innovation and SustainabilityInstitute of Technology SligoSligoIreland
  2. 2.Microbiology Department, School of Natural SciencesNational University of IrelandGalwayIreland

Personalised recommendations