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Journal of Applied Phycology

, Volume 24, Issue 1, pp 45–54 | Cite as

The effect of species diversity on lipid production by micro-algal communities

  • Maria StockenreiterEmail author
  • Anne-Kathrin Graber
  • Florian Haupt
  • Herwig Stibor
Article

Abstract

Current research investigating the importance of diversity for biofuel lipid production remains limited. In contrast, the relationship between diversity and productivity within terrestrial and algal primary producers has been well documented in ecology. Hence, we set out to investigate, experimentally, whether diversity may also affect lipid production in micro-algae. We investigated the growth and lipid production of micro-algae using species from all major algal groups. Algae were grown in a large number of treatments differing in their diversity level. Additionally, we compared the growth and lipid production of laboratory communities to natural lake and pond phytoplankton communities of different diversity. Our results show that lipid production increased with increasing diversity in both natural and laboratory micro-algal communities. The underlying reason for the observed ‘diversity–productivity’ relationship seems to be resource use complementarity. We observed higher lipid production of highly diverse algal communities under the same growth and resource supply conditions compared to monocultures. Hence, the incorporation of the ecological advantages of diversity-related resource-use dynamics into algal biomass production may provide a powerful and cost effective way to improve biofuel production.

Keywords

Biofuel Complementarity Diversity Lipid Micro-algae Resource-use efficiency 

Notes

Acknowledgements

This study was supported by funding from Northern European Innovative Energy Research Program (N-INNER): Optimizing Lipid Production of Planktonic Algae (LIPIDO); 03SF0332; Forschungszentrum Jülich PT-JERG3. We thank Margit Feißel, Angelika Wild and Martin Steinböck for technical support during the experiment and two anonymous reviewers for helpful comments on the manuscript.

References

  1. Beckmann J, Lehr F, Finazzi G, Hankamer B, Posten C, Wobbe L, Kruse O (2009) Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii. J Biotechnol 142:70–77PubMedCrossRefGoogle Scholar
  2. Borowitzka MA (1999) Commercial production of microalgae: ponds, tanks, tubes and fermenters. J Biotechnol 70:313–321CrossRefGoogle Scholar
  3. Carpenter SR, Kitchell JF (1993) The trophic cascade in lakes. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  4. Cellamare M, Leitão M, Coste M, Dutartre A, Haury J (2010) Tropical phytoplankton taxa in Aquitaine lakes (France). Hydrobiologia 639:129–145CrossRefGoogle Scholar
  5. Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM et al (2000) Consequences of changing biodiversity. Nature 405:234–242PubMedCrossRefGoogle Scholar
  6. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306PubMedCrossRefGoogle Scholar
  7. Chrisostomou A, Moustaka-Gouni M, Sgardelis S, Lanaras T (2009) Air-dispersed phytoplankton in a mediterranean river-reservoir system (Aliakmon-Polyphytos, Greece). J Plankton Res 31:877–884CrossRefGoogle Scholar
  8. Connell J (1978) Diversity in tropical rain forests and coral reefs. Science 199:1304–1310CrossRefGoogle Scholar
  9. Cooksey KE, Guckert JB, Williams SA, Callis PR (1987) Fluorometric determination of the neutral lipid content of microalgal cells using Nile Red. J Microbiol Methods 6:333–345CrossRefGoogle Scholar
  10. Dean AP, Sigee DC, Estrada B, Pittman JK (2010) Using FTIR spectroscopy for rapid determination of lipid accumulation in response to nitrogen limitation in freshwater microalgae. Bioresource Technol 101:4499–4507CrossRefGoogle Scholar
  11. Dickman EM, Vanni MJ, Horgan MJ (2006) Interactive effects of light and nutrients on phytoplankton stoichiometry. Oecologia 149:676–689PubMedCrossRefGoogle Scholar
  12. Downing AL, Leibold MA (2002) Ecosystem consequences of species richness and composition in pond food webs. Nature 416:837–841PubMedCrossRefGoogle Scholar
  13. Elsey D, Jameson D, Raleigh B, Cooney MJ (2007) Fluorescence measurements of microalgal neutral lipids. J Microbiol Methods 68:639–642PubMedCrossRefGoogle Scholar
  14. Eltgroth ML, Watwood RL, Wolfe GV (2005) Production and cellular localization of neutral long-chain lipids in the haptophyte algae Isochrysis galbana and Emiliana huxleyi. J Phycol 41:1000–1009CrossRefGoogle Scholar
  15. Fornara DA, Tilman D (2008) Plant functional composition influences rates of soil carbon and nitrogen accumulation. J Ecol 96:314–322CrossRefGoogle Scholar
  16. Fox JW (2005) Interpreting the “selection effect” of biodiversity on ecosystem function. Ecol Lett 8:846–856CrossRefGoogle Scholar
  17. Gaedeke A, Sommer U (1986) The influence of periodic disturbances on the maintenance of phytoplankton diversity. Oecologia 71:98–102CrossRefGoogle Scholar
  18. Griffiths MJ, Harrison STL (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507CrossRefGoogle Scholar
  19. Guillard RRL, Lorenzen CJ (1972) Yellow-green algae with chlorophyllide C1, 2. J Phycol 8:10–14Google Scholar
  20. Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  21. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M et al (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639PubMedCrossRefGoogle Scholar
  22. Huisman J, Weissing FJ (1999) Biodiversity of plankton by species oscillations and chaos. Nature 402:407–410CrossRefGoogle Scholar
  23. Hutchinson GE (1961) The paradox of plankton. Am Nat 95:137–147CrossRefGoogle Scholar
  24. Lee SJ, Yoon B-D, Oh H-M (1998) Rapid method for the determination of lipid from the green alga Botryococcus braunii. Biotechnol Tech 12:553–556CrossRefGoogle Scholar
  25. Lehr F, Posten C (2009) Closed photo-bioreactors as tools for biofuel production. Curr Opin Biotech 20:280–285PubMedCrossRefGoogle Scholar
  26. Li Y, Horsman M, Wang B, Wu N, Lan CQ (2008) Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans. Appl Microbiol Biotechnol 81:629–636PubMedCrossRefGoogle Scholar
  27. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76PubMedCrossRefGoogle Scholar
  28. Lund JWG, Kipling C, le Cren ED (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimation by counting. Hydrobiologia 11:143–170CrossRefGoogle Scholar
  29. McGinnis KM, Dempster TA, Sommerfeld MR (1997) Characterization of the growth and lipid content of the diatom Chaetoceros muelleri. J Appl Phycol 9:19–24CrossRefGoogle Scholar
  30. McGrady-Steed J, Harris PM, Morin PJ (1997) Biodiversity regulates ecosystem predictability. Nature 390:162–165CrossRefGoogle Scholar
  31. McNaughton SJ (1977) Diversity and stability of ecological communities: a comment on the role of empiricism in ecology. Am Nat 111:515–525CrossRefGoogle Scholar
  32. Messikommer E (1943) Untersuchungen über die passive Verbreitung der Algen. Aquat Sci 9:310–316Google Scholar
  33. Miao X, Wu Q (2004) High yield bio-oil production from fast pyrolysis by metabolic controlling of Chlorella protothecoides. J Biotechnol 110:85–93PubMedCrossRefGoogle Scholar
  34. Power LD, Cardinale BJ (2009) Species richness enhances both algal biomass and rates of oxygen production in aquatic microcosms. Oikos 118:1703–1711CrossRefGoogle Scholar
  35. Ptacnik R, Solimini AG, Andersen T, Tamminen T, Brettum P, Lepistö L, Willén E, Rekolainen S (2008) Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proc Natl Acad Sci USA 105:5134–5138PubMedCrossRefGoogle Scholar
  36. Pulz O (2001) Photobioreactors: production systems for phototrophic microorganisms. Appl Microbiol Biotechnol 57:287–293PubMedCrossRefGoogle Scholar
  37. Reynolds CS (2006) Ecology of phytoplankton. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  38. Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N et al (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112PubMedCrossRefGoogle Scholar
  39. Schenk PM, Thomas-Hall SR, Stephens E, Marx UC, Mussgnug JH, Posten C, Kruse O, Hankamer B (2008) Second generation biofuels: high-efficiency microalgae for biodiesel production. Bioenerg Res 1:20–43CrossRefGoogle Scholar
  40. Sheehan J, Dunahay T, Benemann J, Roessler P (1998) A look back at the U.S. Department of Energy’s Aquatic Species Program: Biodiesel from Algae. Close-Out report. National Renewable Energy Lab, Department of Energy, Golden, Colorado, U.S.A. Report number NREL/TP-580-24190, dated July 1998Google Scholar
  41. Smith VH, Foster BL, Grover JP, Holt RD, Leibold MA, Holt RD, Leibold MA, DeNoyelles F (2005) Phytoplankton species richness scales consistently from laboratory microcosms to the world's oceans. Proc Natl Acad Sci USA 102:4393–4396PubMedCrossRefGoogle Scholar
  42. Smith VH, Sturm BSM, deNoyelles FJ, Billings SA (2010) The ecology of algal biodiesel production. Trends Ecol Evol 25:301–309PubMedCrossRefGoogle Scholar
  43. Sommer U, Padisák J, Reynolds CS, Juhász-Nagy P (1993) Hutchinson’s heritage: the diversity–disturbance relationship in phytoplankton. Hydrobiologia 249:1–7CrossRefGoogle Scholar
  44. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96PubMedCrossRefGoogle Scholar
  45. Striebel M, Behl S, Stibor H (2009a) The coupling of biodiversity and productivity in phytoplankton communities: consequences for biomass stoichiometry. Ecology 90:2025–2031PubMedCrossRefGoogle Scholar
  46. Striebel M, Behl S, Diehl S, Stibor H (2009b) Spectral niche complementarity and carbon dynamics in pelagic ecosystems. Am Nat 174:141–147PubMedCrossRefGoogle Scholar
  47. Tilman D (1996) Biodiversity: population versus ecosystem stability. Ecology 77:350–363CrossRefGoogle Scholar
  48. Tilman D, Reich PB, Knops J, Wedin D, Mielke T et al (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845PubMedCrossRefGoogle Scholar
  49. Tran H-L, Hong S-J, Lee C-G (2009) Evaluation of extraction methods for recovery of fatty acids from Botryococcus braunii LB 572 and Synechocystis sp. PCC 6803. Biotechnol Bioprocess Eng 14:187–192CrossRefGoogle Scholar
  50. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Verein Theor Angew Limnol 9:1–38Google Scholar
  51. Vanelslander B, deWever A, van Oostende N, Kaewnuratchadasorn P, Vanormelingen P, Hendrickx F, Sabbe K, Vyverman W (2009) Complementarity effects drive positive diversity effects on biomass production in experimental benthic diatom biofilms. J Ecol 97:1075–1082CrossRefGoogle Scholar
  52. Zhou X, Xiao B, Ochieng RM, Yang J (2009) Utilization of carbon-negative biofuels from low-input high-diversity grassland biomass for energy in China. Renew Sustain Energy Rev 13:479–485CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Maria Stockenreiter
    • 1
    Email author
  • Anne-Kathrin Graber
    • 1
  • Florian Haupt
    • 1
  • Herwig Stibor
    • 2
  1. 1.Department Biologie IILudwig-Maximilians-Universität MünchenPlanegg-MartinsriedGermany
  2. 2.European Institute for Marine Studies, Technopole Brest-IroisePlouzaneFrance

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