Skip to main content
SpringerLink
Log in

Spectrophotometry can monitor changes in algal metabolism triggered by nutrient deficiency in Nannochloropsis oculata cultured under various light-emitting diode light regimes

  • Original Article
  • Aquaculture
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Efficient production of beneficial metabolites by microalgae using light-emitting diodes (LED) is attracting more interest. In batch cultures, metabolic changes that occur with nutrient deficiency over time must be monitored to estimate the metabolite content. Our previous study showed that nutrient deficiency in Nannochloropsis oculata can be briefly evaluated by measuring the absorption ratio at 490 and 680 nm (Abs490/Abs680). However, little is known about the relation with this ratio and metabolic change, particularly in LED light-conditioned cultures. In this study, we investigate if Abs490/Abs680 can be an indicator of the biochemical status of N. oculata cultured under various LED color regimes. Three LED treatments were used: Blue (B), Blue + Red (BR), and Red (R). In all LED treatments, the Abs490/Abs680 decreased for several days and then increased when phosphate was limited or non-existent. The trends in the C16:0 and C20:5ɷ3 proportions and chlorophyll a content commonly changed at the turning points of the Abs490/Abs680. Furthermore, significant correlations were found among the metabolic state and absorption ratio, except in treatment R. We suggest that spectrophotometry can be used for monitoring metabolic changes in N. oculata cultures under various LED irradiance, unless there is excessive 630 nm-red light exposure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andrews T, Lorimer GH (2003) Manipulating ribulose bisphosphate carboxylase/oxygenase in the chloroplasts of higher plants. Arch Biochem Biophys 414:159–169

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Berner T, Dubinsky Z, Wyman K, Falkowski PG (1989) Photoadaptation and the package effect in Dunaliella tertiolecta (Chlorophyceae). J Phycol 25:70–78

    Article  CAS  Google Scholar 

  • Blair MF, Kokabian B, Gude VG (2014) Light and growth medium effect on Chlorella vulgaris biomass production. J Environ Chem Eng 2:665–674

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  Google Scholar 

  • Brown MR, Dunstan GA, Norwood SJ, Miller KA (1996) Effects of harvest stage and light on the biochemical composition of the diatom Thalassiosira pseudonana. J Phycol 32:64–73

    Article  CAS  Google Scholar 

  • Carvalho AP, Silva SO, Baptista JM, Malcata FX (2011) Light requirements in microalgal photobioreactors: an overview of biophotonic aspects. Appl Microbiol Technol 89:1275–1288

    Article  CAS  Google Scholar 

  • Chen C-Y, Chen Y-C, Huang H-C, Ho S-H, Chang J-S (2015) Enhancing the production of eicosapentaenoic acid (EPA) from Nannochloropsis oceanica CY2 using innovative photobioreactors with optimal light source arrangements. Bioresour Technol 191:407–413

    Article  CAS  PubMed  Google Scholar 

  • Connor WE (2000) Importance of n-3 fatty acids in health and disease. Am J Clin Nutr 71:171–175

    Article  Google Scholar 

  • Das P, Lei W, Aziz SS, Obbard JP (2011) Enhanced algae growth in both phototrophic and mixotrophic culture under blue light. Bioresour Technol 102:3883–3887

    Article  CAS  Google Scholar 

  • Falkowski PG, Owens TG (1980) Light-shade adaptation. Two strategies in marine phytoplankton. Plant Physiol 66:592–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fidalgo JP, Cid A, Torres E, Sukenik A, Herrero C (1998) Effects of nitrogen source and growth phase on proximate biochemical composition, lipid classes and fatty acid profile of the marine microalga Isochrysis galbana. Aquaculture 166:105–116

    Article  CAS  Google Scholar 

  • Glemser M, Heining M, Schmidt J, Becker A, Garbe D, Buchholz R, Brück T (2016) Application of light-emitting diodes (LEDs) in cultivation of phototrophic microalgae: current state and perspectives. Appl Microbiol Biotechnol 100:1077–1088

    Article  CAS  PubMed  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Guillard RRL, Sieracki MS (2005) Counting cells in cultures with the light microscope. In: Anderson RA (ed) Algal culturing techniques. Elsevier, New York, pp 239–252

    Google Scholar 

  • Harrison PJ, Thompson PA, Calderwood GS (1990) Effects of nutrient and light limitation on the biochemical composition of phytoplankton. J Appl Phycol 2:45–56

    Article  Google Scholar 

  • Hodgson PA, Henderson RJ, Sargent JR, Leftley JW (1991) Patterns of variation in the lipid class and fatty acid composition of Nannochloropsis oculata (Eustigmatophyceae) during batch culture. J Appl Phycol 3:169–181

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hyka P, Lickova S, Přibyl P, Melzoch K, Kovar K (2013) Flow cytometry for the development of biotechnological processes with microalgae. Biotechnol Adv 31:2–16

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa T, Isowa K (2012) Cultivation of microalgae for live food under white light-emitting diodes (LEDs). J Fish Technol 4:51–55 (in Japanese with English abstract)

    Google Scholar 

  • Juaneda P, Rocquelin G (1985) Rapid and convenient separation of phospholipids and non phosphorus lipids from rat heart using silica cartridges. Lipids 20:40–41

    Article  CAS  PubMed  Google Scholar 

  • Kandilian R, Lee E, Pilon L (2013) Radiation and optical properties of Nannochloropsis oculata grown under different irradiances and spectra. Bioresour Technol 137:63–73

    Article  CAS  PubMed  Google Scholar 

  • Kawamura G (2006) Application of LED to fisheries field. In: Association of Agricultural Electrification (ed) Application of LED to agriculture, forestry and fisheries. Association of Agricultural Electrification, Tokyo, pp 51–62

    Google Scholar 

  • Kim S-K, Ravichandran YD, Khan SB, Kim YT (2008) Prospective of the cosmeceuticals derived from marine organisms. Biotechnol Bioprocess Eng 13:511–523

    Article  CAS  Google Scholar 

  • Kim T-H, Lee Y, Han S-H, Hwang S-J (2013) The effects of wavelength and wavelength mixing ratios on microalgae growth and nitrogen, phosphorus removal using Scenedesmus sp. for wastewater treatment. Bioresour Technol 130:75–80

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Korbee N, Figueroa FL, Aguilera J (2005) Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J Photochem Photobiol, B 80:71–78

    Article  CAS  Google Scholar 

  • Lacour T, Sciandra A, Talec A, Mayzaud P, Bernard O (2012) Diel variations of carbohydrates and neutral lipids in nitrogen-sufficient and nitrogen-starved cyclostat cultures of Isochrysis sp. J Phycol 48:966–975

    Article  PubMed  Google Scholar 

  • Lee TH, Chang JS, Wang HY (2013) Current developments in high-throughput analysis for microalgae cellular contents. Biotechnol J 8:1301–1314

    Article  CAS  PubMed  Google Scholar 

  • Ley AC, Mauzerall DC (1982) Absolute absorption cross-sections for photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris. Biochim Biophys Acta 680:95–106

    Article  CAS  Google Scholar 

  • Malapascua J, Jerez C, Sergejevová M, Figueroa F, Masojídek J (2014) Photosynthesis monitoring to optimize growth of microalgal mass cultures: application of chlorophyll fluorescence techniques. Aquat Biol 22:123–140

    Article  Google Scholar 

  • Maruyama I, Nakamura T, Matsubayashi T, Ando Y, Maeda T (1986) Identification of the alga known as ‘marine Chlorella’ as a member of the Eustigmatophyceae. Jpn J Phycol 34:319–325

    Google Scholar 

  • Matsui H, Okawa R, Anraku K, Kotani T (2017) Application of spectrophotometry to estimate the optimum culture conditions for Nannochloropsis oculata as a diet for zooplankton. Aquacult Sci 65:209–219

    Google Scholar 

  • Mayers JJ, Flynn KJ, Shields RJ (2014) Influence of the N: P supply ratio on biomass productivity and time-resolved changes in elemental and bulk biochemical composition of Nannochloropsis sp. Bioresour Technol 169:588–595

    Article  CAS  PubMed  Google Scholar 

  • Meng Y, Jiang J, Wang H, Cao X, Xue S, Yang Q, Wang W (2015) The characteristics of TAG and EPA accumulation in Nannochloropsis oceanica IMET1 under different nitrogen supply regimes. Bioresour Technol 179:483–489

    Article  CAS  PubMed  Google Scholar 

  • Merzlyak MN, Chivkunova OB, Gorelova OA, Reshetnikova IV, Solovchenko AE, Khozin-Goldberg I, Cohen Z (2007) Effect of nitrogen starvation on optical properties, pigments, and arachidonic acid content of the unicellular green alga Parietochloris incisa (Trebouxiophyceae, Chlorophyta). J Phycol 43:833–843

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Muller-Feuga A, Moal J, Kaas R (2003) The micro algae of aquacutlrue. In: Støttrup JG, Mc Ecoy LA (eds) Live feeds in marine aquaculture. Blackwell, Oxford, pp 206–252

    Chapter  Google Scholar 

  • Okauchi M (2012) Changes in nutritive value of Pavlova sp. collected from different population growth phases in batch style culture assessed from cell ultra-structure. Algal Resour 8:11–22

    Google Scholar 

  • Okauchi M (2013) III-1. Energy conservation culture of microalgae as live feed using an energy-saving illuminator. Nippon Suisan Gakkaishi 79:886 (in Japanese)

    Article  Google Scholar 

  • Okauchi M, Wen-Jian Z, Wan-Hong Z, Kunihiko F, Kanazawa A (1990) Difference in nutritive value of a microalga Nannochloropsis oculata at various growth phases. Nippon Suisan Gakkaishi 56:1293–1298

    Article  Google Scholar 

  • Okumura H (2008) Study of the efficiental cultivation of marine microalgae on mass algae cultivation system for mariculture breeding. Sci Rep Hokkaido Fish Exp Stn 73:9–29 (in Japanese with English abstract)

    CAS  Google Scholar 

  • Okumura H, Nakajima K, Masuda A, Takahashi M, Kosaka S, Horaguchi K, Matsuyama K, Murakami K (2001) Experimental mass culturing of Pavlova lutheri using step-style light control. J Illum Engng Inst Jpn 85:571–575 (in Japanese with English abstract)

    Article  Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) Nutrients. In: Parsons TR, Maita Y, Lalli CM (eds) A manual of chemical and biological methods for seawater analysis. Pergamon, Oxford, pp 3–36

    Chapter  Google Scholar 

  • Petkov G, Garcia G (2007) Which are fatty acids of the green alga Chlorella? Biochem Syst Ecol 35:281–285

    Article  CAS  Google Scholar 

  • Priyadarshani I, Rath B (2012) Commercial and industrial applications of micro algae: a review. J Algal Biomass Util 3:89–100

    Google Scholar 

  • Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221

    CAS  Google Scholar 

  • Reichardt TA, Collins AM, Garcia OF, Ruffing AM, Jones HDT, Timlin JA (2012) Spectroradiometric monitoring of Nannochloropsis salina growth. Algal Res 1:22–31

    Article  CAS  Google Scholar 

  • Reitan KI, Rainuzzo JR, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30:972–979

    Article  CAS  Google Scholar 

  • Richardson K, Beardall J, Raven JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191

    Article  Google Scholar 

  • Roscher E, Zetsche K (1986) The effects of light quality and intensity on the synthesis of ribulose-1,5-bisphosphate carboxylase and its mRNAs in the green alga Chlorogonium elongatum. Planta 167:582–586

    Article  CAS  PubMed  Google Scholar 

  • Santos-Ballardo DU, Rossi S, Hernández V, Vázquez-Gómez R, Rendón-Unceta MC, Caro-Corrales J, Valdez-Ortiz A (2015) A simple spectrophotometric method for biomass measurement of important microalgae species in aquaculture. Aquaculture 448:87–92

    Article  CAS  Google Scholar 

  • Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553

    Article  CAS  Google Scholar 

  • Skjånes K, Rebours C, Lindblad P (2013) Potential for green microalgae to produce hydrogen, pharmaceuticals and other high value products in a combined process. Crit Rev Biotechnol 33:172–215

    Article  CAS  PubMed  Google Scholar 

  • Smith VH, Sturm BSM, DeNoyelles FJ, Billings SA (2010) The ecology of algal biodiesel production. Trends Ecol Evol 25:301–309

    Article  PubMed  Google Scholar 

  • Solovchenko A, Khozin-Goldberg I, Recht L, Boussiba S (2011) Stress-induced changes in optical properties, pigment and fatty acid content of Nannochloropsis sp.: implications for non-destructive assay of total fatty acids. Mar Biotechnol 13:527–535

    Article  CAS  PubMed  Google Scholar 

  • Stansell GR, Gray VM, Sym SD (2012) Microalgal fatty acid composition: implications for biodiesel quality. J Appl Phycol 24:791–801

    Article  CAS  Google Scholar 

  • Sukenik A (1991) Ecophysiological considerations in the optimization of eicosapentaenoic acid production by Nannochloropsis sp. (Eustigmatophyceae). Bioresour Technol 35:263–269

    Article  CAS  Google Scholar 

  • Teo CL, Atta M, Bukhari A, Taisir M, Yusuf AM, Idris A (2014a) Enhancing growth and lipid production of marine microalgae for biodiesel production via the use of different LED wavelengths. Bioresour Technol 162:38–44

    Article  CAS  PubMed  Google Scholar 

  • Teo CL, Idris A, Zain NAM, Taisir M (2014b) Synergistic effect of optimizing light-emitting diode illumination quality and intensity to manipulate composition of fatty acid methyl esters from Nannochloropsis sp. Bioresour Technol 173:284–290

    Article  CAS  PubMed  Google Scholar 

  • Ueno J (2003) Cultivation of microalgae using light-emitting diodes (LED). Aquanet 6:48–52 (in Japanese)

    Google Scholar 

  • Vadiveloo A, Moheimani NR, Cosgrove JJ, Bahri PA, Parlevliet D (2015) Effect of different light spectra on the growth and productivity of acclimated Nannochloropsis sp. (Eustigmatophyceae). Algal Res 8:121–127

    Article  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  • White S, Anandraj A, Bux F (2011) PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. Bioresour Technol 102:1675–1682

    Article  CAS  PubMed  Google Scholar 

  • Yeh N, Chung J-P (2009) High-brightness LEDs—Energy efficient lighting sources and their potential in indoor plant cultivation. Renew Sustain Energy Rev 13:2175–2180

    Article  CAS  Google Scholar 

  • You T, Barnett SM (2004) Effect of light quality on production of extracellular polysaccharides and growth rate of Porphyridium cruentum. Biochem Eng J 19:251–258

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Professor Shunsuke Koshio and Manabu Ishikawa and assistant professor Saichiro Yokoyama for lending us the gas chromatography. We would like to thank associate professor Hikaru Endo for the review and discussion. We are grateful to Iris Ann Borlongan and Viliame Pita Waqalevu for some advice on how to brush up the paper. We would like to thank Enago (www.enago.jp) for the English language review.

Author information

Authors and Affiliations

  1. The United Graduate School of Agricultural Sciences, Kagoshima University, Korimoto 1-21-24, Kagoshima, 890-0065, Japan

    Hideaki Matsui

  2. Faculty of Fisheries, Kagoshima University, Shimoarata 4-50-20, Kagoshima, 890-0056, Japan

    Kazuhiko Anraku & Tomonari Kotani

Authors
  1. Hideaki Matsui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuhiko Anraku
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomonari Kotani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomonari Kotani.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matsui, H., Anraku, K. & Kotani, T. Spectrophotometry can monitor changes in algal metabolism triggered by nutrient deficiency in Nannochloropsis oculata cultured under various light-emitting diode light regimes. Fish Sci 85, 167–176 (2019). https://doi.org/10.1007/s12562-018-1261-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-018-1261-y

Keywords

Search

Navigation