Evaluating potential of green alga Chlorella vulgaris to accumulate phosphorus and to fertilize nutrient-poor soil substrates for crop plants

  • Christina Schreiber
  • Henning Schiedung
  • Lucy Harrison
  • Christoph Briese
  • Bärbel Ackermann
  • Josefine Kant
  • Silvia D. Schrey
  • Diana Hofmann
  • Dipali Singh
  • Oliver Ebenhöh
  • Wulf Amelung
  • Ulrich Schurr
  • Tabea Mettler-Altmann
  • Gregor Huber
  • Nicolai David Jablonowski
  • Ladislav Nedbal
6th Congress of the International Society for Applied Phycology

Abstract

Algae are capable of accumulating nutrients from aqueous waste, which makes them a potential fertilizer. The ability of the fast growing Chlorella vulgaris strain IPPAS C1 to accumulate phosphorus (P) was probed in V-shaped plastic foil photobioreactors. The P uptake was 0.13–0.53 g(P)·m−2·day−1 when the algal culture densities were kept between 0.1 and 1.0 g(DW)·L−1 in a typical summer irradiance of Central Europe. The algal biomass can be effectively utilized for soil fertilization only if the algal cells release nutrients into the soil in a form that would be available to roots and at a rate sufficient to support plant growth. To examine this, we compared the growth of wheat, Triticum aestivum L., in two nutrient-deficient substrates: “Null Erde” and sand, with and without fertilization by wet and spray-dried algae. Plants grown in the two nutrient-deficient substrates supplemented by mineral fertilizer served as a control representing optimal nutrient supply. Plants grown in a high-nutrient substrate (SoMi 513) were used as an additional reference representing the maximum growth potential of wheat. Wheat growth was monitored for 8 weeks and measured, including the increase of the leaf area as well as shoot and root dry weight in 10 randomized replicates for each substrate and fertilization variant. After harvest, the biomass and N, P, and C contents of the plant shoots and roots were recorded. Algae fertilization of “Null Erde” led to wheat growth, including root hair production, which was similar to mineral-fertilized “Null Erde” and only slightly less vigorous than in the nutrient-rich SoMi 513 substrate. The plants grown in sand were smaller than the plants in “Null Erde” but fertilization by algae nevertheless led to growth that was comparable to mineral fertilizer. These results unambiguously demonstrate that algal biomass is a viable option for delivering nutrients to support agriculture on marginal soils.

Keywords

Chlorophyceae; phosphorus uptake Marginal soil Mineralization Wheat 

Notes

Acknowledgements

The authors appreciate critical reading of the manuscript by Alexei Solovchenko and language correction by Carol Richards.

Supplementary material

10811_2018_1390_MOESM1_ESM.docx (3 mb)
ESM 1 (DOCX 3077 kb)

References

  1. Aitchison PA, Butt VS (1973) The relation between the synthesis of inorganic polyphosphate and phosphate uptake by Chlorella vulgaris. J Exp Bot 24:497–510Google Scholar
  2. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538CrossRefGoogle Scholar
  3. Cordell D, White S (2014) Life’s bottleneck: implications of global phosphorus scarcity and pathways for a sustainable food system. Annu Rev Environ Resour 39:161–188CrossRefGoogle Scholar
  4. Doucha J, Lívanský K (2006) Productivity, CO2/O2 exchange and hydraulics in outdoor open high density microalgal (Chlorella sp.) photobioreactors operated in a middle and southern European climate. J Appl Phycol 18:811–826CrossRefGoogle Scholar
  5. Fletcher JE, Martin WP (1948) Some effects of algae and molds in the rain-crust of desert soils. Ecology 29:95–100CrossRefGoogle Scholar
  6. Fuller WH, Rogers RN (1952) Utilization of the phosphorus of algal cells as measured by the Neubauer technique. Soil Sci 74:417–430CrossRefGoogle Scholar
  7. Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (32 P) uptake from soil. Plant Soil 198:147–152CrossRefGoogle Scholar
  8. Grobbelaar JU (2009) Upper limits of photosynthetic productivity and problems of scaling. J Appl Phycol 21:519–522CrossRefGoogle Scholar
  9. Gupta DK, Chatterjee S, Datta S, Veer V, Walther C (2014) Role of phosphate fertilizers in heavy metal uptake and detoxification of toxic metals. Chemosphere 108:134–144CrossRefPubMedGoogle Scholar
  10. Gutser R, Ebertseder T, Weber A, Schraml M, Schmidhalter U (2005) Short-term and residual availability of nitrogen after long-term application of organic fertilizers on arable land. J Plant Nutr Soil Sci 168:439–446CrossRefGoogle Scholar
  11. Harrison AF (1987) Soil organic phosphorus: a review of world literature. Commonwealth Agricultural Bureaux International, WallingfordGoogle Scholar
  12. Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–976CrossRefGoogle Scholar
  13. Herencia JF, Ruiz-Porras JC, Melero S, Garcia-Galavis PA, Morillo E, Maqueda C (2007) Comparison between organic and mineral fertilization for soil fertility levels, crop macronutrient concentrations, and yield. Agron J 99:973–983CrossRefGoogle Scholar
  14. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular 347, California Agricultural Experiment Station, University of California–Berkeley, BerkeleyGoogle Scholar
  15. Hsu PH (1964) Adsorption of phosphate by aluminum and iron in soils. Soil Sci Soc Am J 28:474–478CrossRefGoogle Scholar
  16. Huang Y, Huang Y, Liao Q, Fu Q, Xia A, Zhu X (2017) Improving phosphorus removal efficiency and Chlorella vulgaris growth in high-phosphate MFC wastewater by frequent addition of small amounts of nitrate. Int J Hydrog Energy 42:27749–27758CrossRefGoogle Scholar
  17. Mew MC (2016) Phosphate rock costs, prices and resources interaction. Sci Total Environ 542(Pt B):1008–1012CrossRefPubMedGoogle Scholar
  18. Miyachi S, Tamiya H (1961) Distribution and turnover of phosphate compounds in growing Chlorella cells. Plant Cell Physiol 2:405–414Google Scholar
  19. Nakhforoosh A, Bodewein T, Fiorani F, Bodner G (2016) Identification of water use strategies at early growth stages in durum wheat from shoot phenotyping and physiological measurements. Front Plant Sci 7:1155CrossRefPubMedPubMedCentralGoogle Scholar
  20. Nestler J, Keyes SD, Wissuwa M (2016) Root hair formation in rice (Oryza sativa L.) differs between root types and is altered in artificial growth conditions. J Exp Bot 67:3699–3708Google Scholar
  21. Porterfield WM (1922) References to the algae in the Chinese classics. Bull Torrey Bot Club 49:297–300CrossRefGoogle Scholar
  22. Ramulu US, Pratt PF, Page AL (1967) Phosphorus fixation by soils in relation to extractable iron oxides and mineralogical composition. Soil Sci Soc Am J 31:193–196CrossRefGoogle Scholar
  23. Rossi F, De Philippis R (2015) Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats. Life 5:1218–1238CrossRefPubMedPubMedCentralGoogle Scholar
  24. Rossi F, Li H, Liu Y, De Philippis R (2017) Cyanobacterial inoculation (cyanobacterisation): perspectives for the development of a standardized multifunctional technology for soil fertilization and desertification reversal. Earth Sci Rev 171:28–43CrossRefGoogle Scholar
  25. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453CrossRefPubMedPubMedCentralGoogle Scholar
  26. Schreiber C, Behrendt D, Huber G, Pfaff C, Widzgowski J, Ackermann B, Müller A, Zachleder V, Moudříková Š, Mojzeš P, Schurr U, Grobbelaar J, Nedbal L (2017) Growth of algal biomass in laboratory and in large-scale algal photobioreactors in the temperate climate of western Germany. Bioresour Technol 234:140–149CrossRefPubMedGoogle Scholar
  27. Solovchenko A, Verschoor AM, Jablonowski ND, Nedbal L (2016) Phosphorus from wastewater to crops: an alternative path involving microalgae. Biotechnol Adv 34:550–564CrossRefPubMedGoogle Scholar
  28. Sukačová K, Červený J (2017) Can algal biotechnology bring effective solution for closing the phosphorus cycle? Use of algae for nutrient removal—review of past trends and future perspectives in the context of nutrient recovery. Eur J Environ Sci 7:1Google Scholar
  29. Tiessen H, Moir J (2007) Characterization of available P by sequential extraction. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis, 2nd edn. CRC Press, Boca Raton, pp 293–306Google Scholar
  30. Tiessen H, Stewart JWB, Cole CV (1984) Pathways of phosphorus transformations in soils of differing pedogenesis. Soil Sci Soc Am J 48:853–858CrossRefGoogle Scholar
  31. Treves H, Raanan H, Finkel OM, Berkowicz SM, Keren N, Shotland Y, Kaplan A (2013) A newly isolated Chlorella sp. from desert sand crusts exhibits a unique resistance to excess light intensity. FEMS Microbiol Ecol 86:373–380CrossRefPubMedGoogle Scholar
  32. Von Wandruszka R (2006) Phosphorus retention in calcareous soils and the effect of organic matter on its mobility. Geochem Trans 7(1):6CrossRefGoogle Scholar
  33. West NE (1990) Structure and function of microphytic soil crusts in wildland ecosystems of arid to semi-arid regions. Adv Ecol Res 20:179–223CrossRefGoogle Scholar
  34. Witzenberger A, Hack H, Van Den Boom T (1989) Erläuterungen zum BBCH-Dezimal-Code für die Entwicklungsstadien des Getreides - mit Abbildungen. Gesunde Pflanzen 41:384–388Google Scholar

Copyright information

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

Authors and Affiliations

  • Christina Schreiber
    • 1
  • Henning Schiedung
    • 2
    • 3
  • Lucy Harrison
    • 1
  • Christoph Briese
    • 1
  • Bärbel Ackermann
    • 1
  • Josefine Kant
    • 1
  • Silvia D. Schrey
    • 1
  • Diana Hofmann
    • 2
  • Dipali Singh
    • 4
  • Oliver Ebenhöh
    • 4
  • Wulf Amelung
    • 2
    • 3
  • Ulrich Schurr
    • 1
  • Tabea Mettler-Altmann
    • 5
  • Gregor Huber
    • 1
  • Nicolai David Jablonowski
    • 1
  • Ladislav Nedbal
    • 1
  1. 1.Institute of Bio- and Geosciences / Plant Sciences (IBG-2)Forschungszentrum Jülich GmbHJülichGermany
  2. 2.Institute of Bio- and Geosciences / Agrosphere (IBG-3)Forschungszentrum JülichJülichGermany
  3. 3.Institute of Crop Science and Respource Conservation - Soil Science and Soil EcologyUniversity of BonnBonnGermany
  4. 4.Institute of Quantitative and Theoretical BiologyHeinrich Heine UniversitätDüsseldorfGermany
  5. 5.CEPLAS Plant Metabolism and Metabolomics Laboratory, Institute of Plant BiochemistryHeinrich Heine UniversitätDüsseldorfGermany

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