Skip to main content
SpringerLink
Log in

Interspecific biodiversity enhances biomass and lipid productivity of microalgae as biofuel feedstock

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

Abstract

Large improvements in biomass and lipid production are required to make massive scale algal biodiesel production an economic reality. The application of the biodiversity strategy to enhance algal biomass as biofuel feedstock is little. The algal diversity was manipulated in this study to investigate the effects of a combination of biodiversity complementarity and a new medium consisting of seawater and agricultural fertilizer on lipid productivity. The algae diverse community includes two strains of Dunaliella salina (Dunaliella salina 19/30 and 19/18) and three species of Nannochloropsis (Nannochloropsis oculata, Nannochloropsis salina, and Nannochloropsis gaditana). The results showed that the most diverse community (5 species) produced an average of sixfold more biomass in the new medium than did the standard f/2 culture medium. The most diverse polyculture had the highest growth rate (1.01 day−1), biomass (1.2 g L−1), and lipid productivity (0.31 g L−1 day−1). The assessment of algal polycultures relative to monocultures is particularly interesting and novel for this biofuel field, and the observations that these polycultures resulted in significant lipid productivity improvements are very useful addition to the biofuel research. The possible mechanism (resource diversity) to explain the synergy in mixed cultures warrants further investigation.

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

Similar content being viewed by others

References

  • Andersen RA, Brett RW, Potter D, Sexton JP (1998) Phylogeny of the Eustigmatophyceae based upon 18S rDNA, with emphasis on Nannochloropsis. Protist 149:61–74

    Article  CAS  PubMed  Google Scholar 

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

  • Borowitzka LJ (1981) The microflora. Adaptations to life in extremely saline lakes. Hydrobiologia 81:33–46

    Article  Google Scholar 

  • Borowitzka MA, Borowitzka LJ (1988) Dunaliella. In: Borowitzka MA, Borowitzka LJ (eds) Micro-algal biotechnology. Cambridge University Press, Cambridge, pp 27–58

    Google Scholar 

  • Borowitzka MA, Moheimani NR (2013) Sustainable biofuels from algae. Mitig Adapt Strat Glob Chang 18:13–25

    Article  Google Scholar 

  • Boyer KE, Kertesz JS, Bruno JF (2009) Biodiversity effects on productivity and stability of marine macroalgal communities: the role of environmental context. Oikos 118:1062–1072

  • Bracken MES, Stachowicz JJ (2006) Seaweed diversity enhances nitrogen uptake via complementary use of nitrate and ammonium. Ecology 87:2397–2403

    Article  PubMed  Google Scholar 

  • Bruno JF, Lee SC, Kertesz JS, Carpenter RC, Long ZT, Emmett DJ (2006) Partitioning the effects of algal species identity and richness on benthic marine primary production. Oikos 115:170–178

  • Cardinale BJ (2011) Biodiversity improves water quality through niche partitioning. Nature 472:86–89

    Article  CAS  PubMed  Google Scholar 

  • Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS, Loreau M, Weis JJ (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci U S A 104:18123–18128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carvalho JM, Bezerra RP, Matsudo MC, Sato S (2013) Cultivation of Arthrospira (Spirulina) platensis by fed-batch process. In: Lee JW (ed) Advanced biofuels and bioproducts. Springer, New York, pp 781–805

    Chapter  Google Scholar 

  • Craggs R, Lundquist T, Benemann J (2013) Wastewater Treatment and Algal Biofuel Production. In: Borowitzka MA, Moheimani NR (eds) Algae for Biofuels and Energy. Springer Dordrecht, pp 153–163

  • de Fraiture C, Giordano M, Liao Y (2008) Biofuels and implications for agricultural water use: blue impacts of green energy. Water Policy 10:67–81

    Article  Google Scholar 

  • DOE (2010) National algal biofuels technology roadmap. US Department of Energy Office of Energy and Renewable Energy, Biomass Program

  • Dong Q, Zhao X (2004) In situ carbon dioxide fixation in the process of natural astaxanthin production by a mixed culture of Haematococcus pluvialis and Phaffia rhodozyma. Catalysis Today 98:537–544

  • Fon Sing S, Isdepsky A, Borowitzka MA, Lewis DM (2014) Pilot-scale continuous recycling of growth medium for the mass culture of a halotolerant Tetraselmis sp. in raceway ponds under increasing salinity: a novel protocol for commercial microalgal biomass production. Bioresour Technol 161:47–54

    Article  CAS  PubMed  Google Scholar 

  • Fox JW (2005) Interpreting the ‘selection effect’ of biodiversity on ecosystem function. Ecol Lett 8:846–856

    Article  Google Scholar 

  • Gamfeldt L, Hillebrand H (2008) Biodiversity effects on aquatic ecosystem functioning—maturation of a new paradigm. Int Rev Hydrobiol 93:550–564

    Article  Google Scholar 

  • Gamfeldt L, Hillebrand H (2011) Effects of total resources, resource ratios, and species richness on algal productivity and evenness at both metacommunity and local scales. PLoS One 6(7):e21972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Georgianna DR, Mayfield SP (2012) Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488:329–335

  • Griffiths MJ, Harrison STL (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507

    Article  CAS  Google Scholar 

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

  • Hector A (2011) Ecology: diversity favours productivity. Nature 472:45–46

    Article  CAS  PubMed  Google Scholar 

  • Hillebrand H, Lehmpfuhl V (2011) Resource stoichiometry and consumers control the biodiversity-productivity relationship in pelagic metacommunities. Am Nat 178:171–181

    Article  PubMed  Google Scholar 

  • Hillebrand H, Matthiessen B (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12:1405–1419

    Article  PubMed  Google Scholar 

  • Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Hudson ED, Helleur RJ, Parrish CC (2001) Thin-layer chromatography-pyrolysis-gas chromatography–mass spectrometry: a multidimensional approach to marine lipid class and molecular species analysis. J Chromatogr Sci 39:146–152

    Article  CAS  PubMed  Google Scholar 

  • Jiang L, Luo S, Fan X, Yang Z, Guo R (2011) Biomass and lipid production of marine microalgae using municipal wastewater and high concentration of CO2. ApplEnergy 88:3336–3341

  • Kleinegris DM, Janssen M, Brandenburg W, Wijffels R (2010) The selectivity of milking of Dunaliella salina. Mar Biotechnol 12:14–23

    Article  CAS  PubMed  Google Scholar 

  • Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76

    Article  CAS  PubMed  Google Scholar 

  • Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  CAS  PubMed  Google Scholar 

  • Maeder P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697

    Article  Google Scholar 

  • Matthiessen B, Ptacnik R, Hillebrand H (2010) Diversity and community biomass depend on dispersal and disturbance in microalgal communities. Hydrobiologia 653:65–78

  • Nascimento I, Marques S, Cabanelas I, Pereira S, Druzian J, Souza C, Vich D, Carvalho G, Nascimento M (2013) Screening microalgae strains for biodiesel production: lipid productivity and estimation of fuel quality based on fatty acids profiles as selective criteria. BioEnergy Res 6:1–13

    Article  CAS  Google Scholar 

  • Norberg J, Swaney DP, Dushoff J, Lin J, Casagrandi R, Levin SA (2001) Phenotypic diversity and ecosystem functioning in changing environments: A theoretical framework. Proc Nat Acad Sci 98:11376–11381

  • Olguín EJ (2012) Dual purpose microalgae–bacteria-based systems that treat wastewater and produce biodiesel and chemical products within a biorefinery. Biotechnol Adv 30:1031–1046

    Article  PubMed  Google Scholar 

  • 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 Nat Acad Sci 105:5134–5138

  • Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3:686. doi:10.1038/ncomms1688

    Article  PubMed  PubMed Central  Google Scholar 

  • Russell G, Fielding AH (1974) The competitive properties of marine algae in culture. J Ecol 62:689–698

    Article  Google Scholar 

  • Savage N (2011) Algae: the scum solution. Nature:S15–S16

  • Shehata SA, Lasheen MR, Ali GH, Kobbia IA (1999) Toxic effect of certain metals mixture on some physiological and morphological characteristics of freshwater algae. Water Air Soil Pollut 110:119–135

    Article  CAS  Google Scholar 

  • Shimamatsu H (2004) Mass production of Spirulina, an edible microalga. In: Ang P Jr (ed) Asian Pacific phycology in the 21st century: prospects and challenges. Springer, Netherlands, pp 39–44

    Chapter  Google Scholar 

  • Shu C-H, Tsai C-C, Liao W-H, Chen K-Y, Huang H-C (2012) Effects of light quality on the accumulation of oil in a mixed culture of Chlorella sp. and Saccharomyces cerevisiae. J Cheml Technol Biotechnol 87(5):601–607

  • Shurin JB, Mandal S, Abbott RL (2014) Trait diversity enhances yield in algal biofuel assemblages. J Appl Ecol 51:603–611

  • Stachowicz JJ, Best RJ, Bracken MES, Graham MH (2008a) Complementarity in marine biodiversity manipulations: Reconciling divergent evidence from field and mesocosm experiments. Proc Natl Acad Sci 105:18842–18847.

  • Stachowicz JJ, Graham M, Bracken MES, Szoboszlai AI (2008b) Diversity enhances cover and stability of seaweed assemblages: the role of heterogeneity and time. Ecology 89:3008–3019

  • Stockenreiter M, Graber AK, Haupt F, Stibor H (2012) The effect of species diversity on lipid production by microalgal communities. J Appl Phycol 24:45–54

    Article  CAS  Google Scholar 

  • Striebel M, Behl S, Diehl S, Stibor H (2009) Spectral niche complementarity and carbon dynamics in pelagic ecosystems. Am Nat 174:141–147

  • Vanelslander B, De Wever 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 97:1075–1082

  • Weis JJ, Cardinale BJ, Forshay KJ, Ives AR (2007) Effects of species diversity on community biomass production change over the course of succession. Ecology 88:929–939

  • Weis JJ, Madrigal DS, Cardinale BJ (2008) Effects of algal diversity on the production of biomass in homogeneous and heterogeneous nutrient environments: a microcosm experiment. PLoS One 3(7):e2825

    Article  PubMed  PubMed Central  Google Scholar 

  • Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799

    Article  CAS  PubMed  Google Scholar 

  • Williams PJB, Laurens LML (2010) Microalgae as biodiesel & biomass feedstocks: review & analysis of the biochemistry, energetics & economics. Energy Environ Sci 3:554–590

    Article  CAS  Google Scholar 

  • Zhu Y, Chen H, Fan J, Wang Y, Li Y, Chen J, Fan J, Yang S, Hu L, Leung H, Mew TW, Teng PS, Wang Z, Mundt CC (2000) Genetic diversity and disease control in rice. Nature 406:718–722

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The author would like to thank the China Scholarship Council (CSC) and Carbon Trust (UK) for supporting this research financially and thank Professor Steve Wilkinson for writing assistance, Dr. Jim Gilmour and Dr. Krys Bangert for laboratory assistance and very helpful suggestions.

Author information

Author notes

  1. Junying Liu

    Present address: The Engineering Research Center for Biomass Conversion, Ministry of Education, Nanchang University, Nanchang, 330047, China

Authors and Affiliations

  1. Department of Chemical and Biological Engineering, University of Sheffield, Mappin St., Sheffield, UK

    Junying Liu

Authors
  1. Junying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Junying Liu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 159 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, J. Interspecific biodiversity enhances biomass and lipid productivity of microalgae as biofuel feedstock. J Appl Phycol 28, 25–33 (2016). https://doi.org/10.1007/s10811-015-0535-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-015-0535-3

Keywords

Search

Navigation