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Heterotrophic flagellates increase microalgal biomass yield

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Abstract

In time of scarcity of fossil energies, microalgae are attracting interest as a potential source of renewable energy due to their high growth rates and potential high lipid contents. Additionally, cultivation may be an abatement measure to remove surplus nutrients from eutrophicated ecosystems. At present, microalgal cultivations for biomass production are run mainly in monocultures, which are easily contaminated with competing microalgae or grazers. Furthermore, heterotrophic bacteria are highly abundant and may strongly reduce the yield in the target microalgae through competition for nutrients. In three laboratory experiments, we tested whether heterotrophic flagellates (Oxyrrhis marina and Cafeteria roenbergensis) can make nutrients bound in bacteria available for marine diatoms (Coscinodiscus granii and Odontella sinensis) and can shift the competition for inorganic nutrients towards the microalgae. Cultures were run with and without flagellates, under different conditions: without an external carbon source, in presence of organic matter (barley grains) or biogas wastewater. The presence of flagellates had a positive effect on microalgal growth, but this was context and species specific. The presence of the flagellates affected the maximum algal growth rates (r) especially in Coscinodiscus granii. A maximal biomass increase (29.93 ± 2.98 %) (mean ± standard deviation, n = 3) was observed for Coscinodiscus granii in F/2 + Si medium. Furthermore, although the flagellates were attributed to the detrital fraction, their presence resulted in a significant reduction of detritus. In conclusion, heterotrophic flagellates have the potential to increase nutrient use efficiency especially in algae bioreactors with slow-growing large phytoplankton taxa. This effect may be particularly relevant in organic polluted water.

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References

  • Ammerman JW, Fuhrman JA, Hagström Å, Azam F (1984) Bacterioplankton growth in seawater: I. Growth kinetics and cellular characteristics in seawater cultures. Mar Ecol Prog Ser 18:31–39

    Article  Google Scholar 

  • Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  • Barsanti L, Gualtieri P (2006) Algae anatomy, biochemistry and biotechnology. CRC Press, Boca Raton

    Google Scholar 

  • Barton AD, Finkel ZV, Ward BA, Johns DG, Follows MJ (2013) On the roles of cell size and trophic strategy in North Atlantic diatom and dinoflagellate communities. Limnol Oceanogr 58:254–266

    Article  Google Scholar 

  • Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306

    Article  CAS  PubMed  Google Scholar 

  • Christenson L, Sims R (2011) Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 29:686–702

    Article  CAS  PubMed  Google Scholar 

  • Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Ann Rev Ecol Syst 13:291–314

    Article  Google Scholar 

  • Cole JJ, Likens GE, Strayer DL (1982) Photosynthetically produced dissolved organic carbon: an important carbon source for planktonic bacteria. Limnol Oceanogr 27:1080–1090

    Article  CAS  Google Scholar 

  • de-Bashan LE, Hernandez JP, Morey T, Bashan Y (2004) Microalgae growth-promoting bacteria as “helpers” for microalgae: a novel approach for removing ammonium and phosphorus from municipal wastewater. Water Res 38:466–474

    Article  CAS  PubMed  Google Scholar 

  • Eccleston-Parry JD, Leadbeater SC (1995) Regeneration of phosphorus and nitrogen by four species of heterotrophic nanoflagellates feeding on three nutritional states of a single bacterial strain. Appl Environ Microbiol 61:1033–1038

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fenchel T (1982) Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumer. Mar Ecol Prog Ser 9:35–42

    Article  Google Scholar 

  • Feuilladea M, Dufourb P, Feuilladea J (1988) Organic carbon release by phytoplankton and bacterial reassimilation. Swiss J Hydrol 50:115–135

    Article  Google Scholar 

  • Fishman D, Majumdar R, Morello J, Pate R, Yang J (2010) National Algal Biofuels Technology Roadmap A technology roadmap resulting from the National Algal Biofuels Workshop December 9–10, 2008 College Park, Maryland. U.S. Department of Energy, Office of Energy Efficiency and Renewable Energy, Biomass Program

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 26–60

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424

    Article  Google Scholar 

  • Hoffmann JP (1998) Wastewater treatment with suspended and nonsuspended algae. J Phycol 34:757–763

    Article  CAS  Google Scholar 

  • Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639

    Article  CAS  PubMed  Google Scholar 

  • Jeong HJ, Song JE, Kang NS, Kim S, Yoo YD, Park JY (2007) Feeding by heterotrophic dinoflagellates on the common marine heterotrophic nanoflagellate Cafeteria sp. Mar Ecol Prog Ser 333:151–160

    Article  Google Scholar 

  • Johannes RE (1965) Influence of marine protozoa on nutrient regeneration. Limnol Oceanogr 10:434–442

    Article  Google Scholar 

  • Jürgens K, Güde H (1990) Incorporation and release of phosphorus by planktonic bacteria and phagotrophic flagellates. Mar Ecol Prog Ser 59:271–284

    Article  Google Scholar 

  • Larsson U, Hagström Å (1979) Phytoplankton exudate release as an energy source for the growth of pelagic bacteria. Mar Biol 52:199–206

    Article  Google Scholar 

  • Litchman E, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10:1170–1181

    Article  PubMed  Google Scholar 

  • Lowe CD, Martin LE, Roberts EC, Watts PC, Wootton EC, Montagnes DJS (2010) Collection, isolation and culturing strategies for the maintenance of Oxyrrhis marina. J Plankton Res 1–10

  • Neilson AH, Larsson T (1980) The utilization of organic nitrogen for growth of algae: physiological aspects. Physiol Plant 48:542–553

    Article  CAS  Google Scholar 

  • Oswald WJ, Gotaas HB, Golueke CG, Kellen WR (1957) Algae in waste treatment. Sew Ind Wastes 29:437–455

    Google Scholar 

  • Park JBK, Craggs RJ, Shilton AN (2011) Wastewater treatment high rate algal ponds for biofuel production. Bioresour Technol 102:35–42

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Andrew P, Dean AP, Osundeko O (2011) The potential of sustainable algal biofuel production using wastewater resources. Bioresour Technol 102:17–25

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Rawat I, Ranjith Kumar R, Mutanda T, Bux F (2011) Dual role of microalgae: phycoremediation of domestic wastewater and biomass production for sustainable biofuels production. Appl Energy 88:3411–3424

    Article  CAS  Google Scholar 

  • Roberts EC, Wooton EC, Davidson K, Jeong HJ, Lowe CD, Montagnes DJS (2011) Feeding in the dinoflagellate Oxyrrhis marina: linking behaviour with mechanisms. J Plankton Res 33:603–614

    Article  Google Scholar 

  • Rothhaupt KO (1997) Nutrient turnover by freshwater bacterivorous flagellates: differences between a heterotrophic and a mixotrophic chrysophyte. Aquat Microb Ecol 12:65–70

    Article  Google Scholar 

  • Shirvani T, Yan X, Inderwildi OR, Edwards PP, King DA (2011) Life cycle energy and greenhouse gas analysis for algae-derived biodiesel. Energy Environ Sci 4:3773–3778

    Article  CAS  Google Scholar 

  • Shurin JB, Abbott RL, Deal MS, Kwan GT, Litchman E, McBride RC, Mandal S, Smith VH (2013) Industrial-strength ecology: trade-offs and opportunities in algal biofuel production. Ecol Lett 16:1393–1404

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sommer U (1994) Planktologie. Springer, Berlin

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Thompson PA, Levasseur ME, Harrison PJ (1989) Light-limited growth on ammonium vs. nitrate: what is the advantage for marine phytoplankton? Limnol Oceanogr 34:1014–1024

    Article  CAS  Google Scholar 

  • Uduman N, Qi Y, Danquah MK, Forde GM, Hoadley A (2010) Dewatering of microalgae cultures: a major bottleneck to algae based fuels. J Renew Sust Energ 2:1–15

    Article  Google Scholar 

  • Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Theor Angew Limnol 9:1–38 (In German)

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  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 

Download references

Acknowledgments

This study was embedded in the Enercoast Project, Project coordination: COAST Centre for Environment and Sustainable Development Research, University of Oldenburg, Germany. We thank the LUFA Nord-West: Institut für Boden und Umwelt, Oldenburg, Germany, for providing the biogas wastewater from a biogas plant in Wiefelstede, Germany; H.J. Rick for the identification of Coscinodiscus granii; and Hartmut Arndt for providing the Cafeteria roenbergensis culture. We thank Cedric Meunier for providing us with a culture of Oxyrrhis marina.

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Correspondence to Wiebke Anne Plötner.

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Fig. 4

Growth rates of Coscinodiscus granii (CG) and Odontella sinensis (OD) at different light intensities (120, 56, 29, 23, 14 μmol photons m−2 s−1) in the light experiments. All light levels were replicated twice and observed for ten days. The broken line indicates the light intensity (~60 μmol photons m−2 s−1) used in the main experiments. Due to nutrient limitation the growth rate at D6-D7 decreases rapidly. After splitting the cultures in two and the dilution of one half with F/2 + Si medium on day seven, growth rates increased again (Note that growth rates are presented in different scales) (JPEG 88 kb)

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Plötner, W.A., Hillebrand, H., Ptacnikova, R. et al. Heterotrophic flagellates increase microalgal biomass yield. J Appl Phycol 27, 87–96 (2015). https://doi.org/10.1007/s10811-014-0286-6

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  • DOI: https://doi.org/10.1007/s10811-014-0286-6

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