Skip to main content
Log in

Growth factors in oceanic sediment significantly stimulate the biomass and lipid production of two oleaginous microalgae

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

This study demonstrates the effects of growth stimulators in oceanic sediment on biomass and lipid production of two oleaginous microalgae, Botryococcus braunii LB572 and Phaeodactylum tricornutum B2089. At the optimal mixing ratio of culture medium and oceanic sediment extract of 6:4 (v/v), specific growth rates of B. braunii LB572 and P. tricornutum B2089 increased 13.0- and 11.3-fold, respectively, compared to a sediment-free medium. The maximum biomass and lipid productions of B. braunii LB572 were 5.54 and 3.09 g L−1, and those of P. tricornutum B2089 were 6.41 and 3.61 g L−1, respectively, indicating that biomass and lipid production in both microalgae increased at least 6- and 8-fold, respectively. Thus, their cultivation time was reduced by at least 6 days. A positive effect of nitrate in the sediment on biomass and lipid production was not found. Fe3+ and Ca2+ promoted biomass and lipid production as their concentrations increased. However, metal ion concentration is not as critical to biomass and lipid production as humic acid, a chelating substance to enhance bioavailability of metal ions to the microalgae. The optimal humic acid concentration for maximal biomass and lipid production was 80 mg L−1, which is the concentration contained in the culture medium mixed with sediment extract at a ratio of 6:4 (v/v). Thus, low-cost oceanic sediment can supply sufficient growth stimulators, especially humic acid, for mass production of biomass and lipid in both microalgae.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abd El Baky HH, El-Baroty GS, Bouaid A, Martinez M, Aracil J (2012) Enhancement of lipid accumulation in Scenedesmus obliquus by optimizing CO2 and Fe3+ levels for biodiesel production. Bioresour Technol 119:429–432

    Article  CAS  PubMed  Google Scholar 

  • APHA (1995) Standard methods for the examination of water and wastewater, 19th ed. Washington, D.C.

  • Becker EW (1994) Microalgae: biotechnology and microbiology. Cambridge University Press, Cambridge

    Google Scholar 

  • Ben Amor-Ben Ayed H, Taidi B, Ayadi H, Pareau D, Stambouli M (2015) Effect of magnesium ion concentration in autotrophic culture of Chlorella vulgaris. Algal Res 9:291–269

    Article  Google Scholar 

  • Carlsson P, Granéli E, Segatto AZ (1999) Cycling of biologically available nitrogen in riverine humic substances between marine bacteria, a heterotrophic nanoflagellate and photosynthetic dinoflagellate. Aquat Microb Ecol 18:23–36

    Article  Google Scholar 

  • Cerón García MC, García Camacho F, Sanchez Miron A, Fernandez Sevilla JM, Chisti Y, Molina Grima E (2006) Mixotrophic production of marine microalga Phaeodactylum tricornutum on various carbon sources. J Microbiol Bitechnol 16:689–694

    Google Scholar 

  • Che R, Huang L, Yu X (2015) Enhanced biomass production, lipid yield and sedimentation efficiency by iron ion. Bioresour Technol 192:795–798

    Article  CAS  PubMed  Google Scholar 

  • Concas A, Steriti A, Pisu M, Cao G (2014) Comprehensive modeling and investigation of the effect of iron on the growth rate and lipid accumulation of Chlorella vulgaris cultured in batch photobioreactors. Bioresour Technol 153:340–350

    Article  CAS  PubMed  Google Scholar 

  • Dera J, Gohs L, Wozniak B (1978) Experimental study of the composite parts of the light-beam attenuation process in waters of the Gulf of Gdańsk. Oceanology 10:5–26

    Google Scholar 

  • Doering PH, Oviatt CA, McKenna JH, Reed LW (1994) Mixing behavior of dissolved organic carbon and its potential biological significance in the Pawcatuck River Estuary. Estuaries 17:521–536

    Article  CAS  Google Scholar 

  • Droop MR (1962) On cultivating Skeletonema costatum: some problems. In: Pirson A (eds.) Fisher, Stuttgart, pp 77–82

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Gerringa LJA, De Baar HJW, Timmermans KR (2000) A comparison of iron limitation of phytoplankton in natural oceanic waters and laboratory media conditioned with EDTA. Mar Chem 68:335–346

    Article  CAS  Google Scholar 

  • Gim GH, Kim JK, Kim HS, Kathiravan MN, Yang H, Jeong S-H, Kim SW (2014) Comparison of biomass production and total lipid content of freshwater green microalgae cultivated under various culture conditions. Bioprocess Biosyst Eng 37:99–106

    Article  CAS  PubMed  Google Scholar 

  • Gorain PC, Bagchi SK, Mallick N (2013) Effect of calcium, magnesium and sodium chloride in enhancing lipid accumulation in two green microalgae. Environ Technol 34:1887–1894

    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 

  • Hasegawa H, Tate Y, Ogino M, Maki T, Begum ZA, Ichijo T, Rahman IMM (2017) Laboratory culture experiments to study the effect of lignite humic acid fractions on iron solubility and iron uptake rates in phytoplankton. J Appl Phycol 29:903–915

    Article  CAS  Google Scholar 

  • Huang L, Xu J, Li T, Wang L, Deng T, Yu X (2014) Effect of additional Mg2+ on the growth, lipid production, and fatty acid composition of Monoraphidium sp. FXY-10 under different culture conditions. Ann Microbiol 64:1247–1256

    Article  CAS  Google Scholar 

  • International Humic Substances Society (IHSS) (2008) http://humic-substances.org/

  • Jin X, Chu Z, Yan F, Zeng Q (2009) Effects of lanthanum (III) and EDTA on the growth and competition of Microcystis aeruginosa and Scenedesmus quadricauda. Limnologica 39:86–93

    Article  CAS  Google Scholar 

  • Koukal B, Guéguen C, Pardos M, Dominik J (2003) Influence of humic substances on the toxic effects of cadmium and zinc to the green alga Pseudokirchneriella subcapitata. Chemosphere 53:953–961

    Article  CAS  PubMed  Google Scholar 

  • Liu Z-Y, Wang G-C, Zhou B-C (2008) Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 99:4717–4722

    Article  CAS  PubMed  Google Scholar 

  • Livne A, Sukenik A (1992) Lipid synthesis and abundance of acetyl CoA carboxylase in Isochrysis galbana (Prymnesiophyceae) following nitrogen starvation. Plant Cell Physiol 33:1175–1181

  • Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14:217–232

    Article  CAS  Google Scholar 

  • Ohkubo N, Yagi O, Okada M (1998) Effect of humic acid and fulvic acids on the growth of Microcystis aeruginosa. Environ Technol 19:611–617

    Article  CAS  Google Scholar 

  • Pempkowiak J, Kosakoeska A (1998) Accumulation of cadmium by green algae Chlorella vulgaris in the presence of marine humic substances. Environ Int 24:583–588

    Article  CAS  Google Scholar 

  • Petersen RC Jr (1991) The contradictory biological behavior of humic substances in the aquatic environment. In: Allard B, Borén H, Grimvall A (eds) Humic substances in the aquatic and terrestrial environments. Springer, Berlin, pp 367–390

    Chapter  Google Scholar 

  • Ren H-Y, Liu B-F, Kong F, Zhao L, Xie G-J, Ren N-Q (2014) Enhanced lipid accumulation of green microalga Scenedesmus sp. by metal ions and EDTA addition. Bioresour Technol 169:763–767

    Article  CAS  PubMed  Google Scholar 

  • Ruangsomboon S, Ganmanee M, Choochote S (2013) Effects of different nitrogen, phosphorus, and iron concentrations and salinity on lipid production in newly isolated strain of the tropical green microalga, Scenedesmus dimorphus KMITL. J Appl Phycol 25:867–874

    Article  CAS  Google Scholar 

  • Steelink C (1977) Humates and other natural organic substances in the aquatic environment. J Chem Educ 54:599–603

    Article  CAS  Google Scholar 

  • Stumm W, Morgan JJ (1996) Aquatic chemistry: chemical equilibria and rates in natural waters, 3rd edn. Wiley, New York

    Google Scholar 

  • Sunda WG, Huntsman SA (1995) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chem 50:189–206

    Article  CAS  Google Scholar 

  • Sunda WG, Huntsman SA, Harvey GR (1983) Photoreduction of manganese oxides in seawater and its geochemical and biological implications. Nature 301:234–236

    Article  CAS  Google Scholar 

  • Sweeney BM (1954) Gymnodinium splendens, a marine dinoflagellate requiring vitamin B12. Am J Bot 41:821–824

    Article  CAS  Google Scholar 

  • Thompson AS, Rhodes JC, Pettman I (1988) Natural environmental research council culture collection of algae and protozoa: catalogue of strains. Freshwater Biological Association, Ambleside

    Google Scholar 

  • Wan M, Jin X, Xia J, Rosenberg JN, Yu G, Nie Z, Oyler GA, Betenbaugh MJ (2014) The effect of iron on growth, lipid accumulation, and gene expression profile of the freshwater microalga Chlorella sorokiniana. Appl Microbiol Biotechnol 98:9473–9481

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Xu M, Zhang X, Hu Q, Sommerfeld M, Chen Y (2011) Life-cycle analysis on biodiesel production from microalgae: water footprint and nutrients balance. Bioresour Technol 102:159–165

    Article  CAS  PubMed  Google Scholar 

  • Yeesang C, Cheirsilp B (2014) Low-cost production of green microalga Botryococcus braunii biomass with high lipid content through mixotrophic and photoautotrophic cultivation. Appl Biochem Biotechnol 174:116–129

    Article  CAS  PubMed  Google Scholar 

  • Yokoi H, Maki R, Hirose S, Hayashi S (2002) Microbial production of hydrogen from starch-manufacturing wastes. Biomass Bioenergy 22:389–395

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by research grant of the Ministry of Science and ICT (NRF-2015R1D1A3A01020290) and partially by the Research Fund of Chosun University (2014), Republic of South Korea.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Si Wouk Kim.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gim, G.H., Kim, S.W. Growth factors in oceanic sediment significantly stimulate the biomass and lipid production of two oleaginous microalgae. J Appl Phycol 31, 49–59 (2019). https://doi.org/10.1007/s10811-018-1509-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1509-z

Keywords

Navigation