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Treatment with Algae Extracts Promotes Flocculation, and Enhances Growth and Neutral Lipid Content in Nannochloropsis oculata—a Candidate for Biofuel Production

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Abstract

Marine microalgae represent a potentially valuable feedstock for biofuel production; however, large-scale production is not yet economically viable. Optimisation of productivity and lipid yields is required and the cost of biomass harvesting and dewatering must be significantly reduced. Microalgae produce a wide variety of biologically active metabolites, many of which are involved in inter- and intra-specific interactions (the so-called infochemicals). The majority of infochemicals remain unidentified or uncharacterised. Here, we apply known and candidate (undefined extracts) infochemicals as a potential means to manipulate the growth and lipid content of Nannochloropsis oculata—a prospective species for biofuel production. Five known infochemicals (β-cyclocitral, trans,trans-2,4-decadienal, hydrogen peroxide, norharman and tryptamine) and crude extracts prepared from Skeletonema marinoi and Dunaliella salina cultures at different growth stages were assayed for impacts on N. oculata over 24 h. The neutral lipid content of N. oculata increased significantly with exposure to three infochemicals (β-cyclocitral, decadienal and norharman); however the effective concentrations affected a significant decrease in growth. Exposure to particular crude extracts significantly increased both growth and neutral lipid levels. In addition, water-soluble extracts of senescent S. marinoi cultures induced a degree of flocculation in the N. oculata. These preliminary results indicate that artificial manipulation of N. oculata cultures by application of algae infochemicals could provide a valuable tool towards achieving economically viable large-scale algae biofuel production.

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References

  • Barofsky A, Vidoudez C, Pohnert G (2009) Metabolic profiling reveals growth stage variability in diatom exudates. Limnol Oceanogr Methods 7:382–390

    Article  CAS  Google Scholar 

  • Barofsky A, Simonelli P, Vidoudez C, Troedsson C, Nejstgaard JC, Jakobsen HH, Pohnert G (2010) Growth phase of the diatom Skeletonema marinoi influences the metabolic profile of the cells and the selective feeding of the copepod Calanus spp. J Plankton Res 32:263–272

    Article  CAS  Google Scholar 

  • Bilanovic D, Shelef G, Sukenik A (1988) Flocculation of microalgae with cationic polymers — effects of medium salinity. Biomass 17:65–76

    Article  CAS  Google Scholar 

  • Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustainable Energy Rev 14:557–577

    Article  CAS  Google Scholar 

  • Brown MR, Miller KA (1992) The ascorbic acid content of eleven species of microalgae used in mariculture. J Appl Phycol 4:205–215

    Article  CAS  Google Scholar 

  • Caldwell GS (2009) The influence of bioactive oxylipins from marine diatoms on invertebrate reproduction and development. Mar Drugs 7:367–400

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Zhang C, Song L, Sommerfeld M, Hu Q (2009) A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae. J Microbiol Methods 77:41–47

    Article  PubMed  CAS  Google Scholar 

  • Chisti Y (2008) Biodiesel from microalgae beats bioethanol. Trends Biotechnol 26:126–131

    Article  PubMed  CAS  Google Scholar 

  • Chung CC, Hwang SPL, Chang J (2008) Nitric oxide as a signaling factor to upregulate the death-specific protein in a marine diatom, Skeletonema costatum, during blockage of electron flow in photosynthesis. Appl Environ Microbiol 74:6521–6527

    Article  PubMed  CAS  Google Scholar 

  • Churro C, Alverca E, Sam-Bento F, Paulino S, Figueira VC, Bento AJ, Prabhakar S, Lobo AM, Calado AJ, Pereira P (2009) Effects of bacillamide and newly synthesized derivatives on the growth of cyanobacteria and microalgae cultures. J Appl Phycol 21:429–442

    Article  CAS  Google Scholar 

  • Churro C, Fernandes AS, Alverca E, Sam-Bento F, Paulino S, Figueira VC, Bento AJ, Prabhakar S, Lobo AM, Martins LL, Mourato MP, Pereira P (2010) Effects of tryptamine on growth, ultrastructure, and oxidative stress of cyanobacteria and microalgae cultures. Hydrobiologia 649:195–206

    Article  CAS  Google Scholar 

  • Das P, Aziz SS, Obbard JP (2011) Two phase microalgae growth in the open system for enhanced lipid productivity. Renew Energy 36:2524–2528

    Article  CAS  Google Scholar 

  • Fang X, Wei C, Zhao-Ling C, Fan O (2004) Effects of organic carbon sources on cell growth and eicosapentaenoic acid content of Nannochloropsis sp. J Appl Phycol 16:499–503

    Article  CAS  Google Scholar 

  • Fogg GE, Thake B (1987) Algal cultures and phytoplankton ecology. University of Wisconsin Press, Madison

    Google Scholar 

  • Francisco EC, Neves DB, Jacob-Lopes E, Franco TT (2010) Microalgae as feedstock for biodiesel production: Carbon dioxide sequestration, lipid production and biofuel quality. J Chem Technol Biotechnol 85:395–403

    Article  CAS  Google Scholar 

  • Greenwell HC, Laurens LML, Shields RJ, Lovitt RW, Flynn KJ (2010) Placing microalgae on the biofuels priority list: a review of the technological challenges. J R Soc Interface 7:703–726

    Article  PubMed  CAS  Google Scholar 

  • Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms: 1. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • Guschina IA, Harwood JL (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45:160–186

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Ianora A, Miralto A (2010) Toxigenic effects of diatoms on grazers, phytoplankton and other microbes: a review. Ecotoxicology 19:493–511

    Article  PubMed  CAS  Google Scholar 

  • Ianora A, Miralto A, Poulet SA, Carotenuto Y, Buttino I, Romano G, Casotti R, Pohnert G, Wichard T, Colucci-D’amato L, Terrazzano G, Smetacek V (2004) Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429:403–407

    Article  PubMed  CAS  Google Scholar 

  • Ianora A, Boersma M, Casotti R, Fontana A, Harder J, Hoffmann F, Pavia H, Potin P, Poulet SA, Toth G (2006) New trends in marine chemical ecology. Estuar Coasts 29:531–551

    CAS  Google Scholar 

  • Ianora A, Bentley MG, Caldwell GS, Casotti R, Cembella AD, Engström-Öst J, Halsband C, Sonnenschein E, Legrande C, Llewellyn CA, Paldavičienë A, Pilkaityte R, Pohnert G, Razinkovas A, Romano G, Tillmann U, Vaiciute D (2011) The relevance of marine chemical ecology to plankton and ecosystem function: an emerging field. Mar Drugs 9:1625–1648

    Article  PubMed  CAS  Google Scholar 

  • Imada N, Kobayashi K, Isomura K, Saito H, Kimura S, Tahara K, Oshima Y (1992) Studies on the autoinhibitor produced by Skeletonema costatum: 2. Isolation and identification of an autoinhibitor produced by Skeletonema costatum. Nippon Suisan Gakkaishi 58:1687–1692

    Article  Google Scholar 

  • Jüttner F, Watson SB, Von Elert E, Köster O (2010) β-Cyclocitral, a grazer defence signal unique to the cyanobacterium Microcystis. J Chem Ecol 36:1387–1397

    Article  PubMed  Google Scholar 

  • Lardon L, Helias A, Sialve B, Stayer JP, Bernard O (2009) Life-cycle assessment of biodiesel production from microalgae. Environ Sci Technol 43:6475–6481

    Article  PubMed  CAS  Google Scholar 

  • Lincoln RA, Strupinski K, Walker JM (1990) Biologically active compounds from diatoms. Diatom Res 5:337–350

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Naviner M, Berge JP, Durand P, Le Bris H (1999) Antibacterial activity of the marine diatom Skeletonema costatum against aquacultural pathogens. Aquaculture 174:15–24

    Article  CAS  Google Scholar 

  • Paul C, Barofsky A, Vidoudez C, Pohnert G (2009) Diatom exudates influence metabolism and cell growth of co-cultured diatom species. Mar Ecol Prog Ser 389:61–70

    Article  Google Scholar 

  • Perez-Garcia O, Escalante FME, De-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: Metabolism and potential products. Water Res 45:11–36

    Article  PubMed  CAS  Google Scholar 

  • Pohnert G (2010) Chemical noise in the silent ocean. J Plankton Res 32:141–144

    Article  CAS  Google Scholar 

  • Poulson KL, Sieg RD, Kubanek J (2009) Chemical ecology of the marine plankton. Nat Prod Rep 26:729–745

    Article  PubMed  CAS  Google Scholar 

  • Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: Strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112

    Article  PubMed  CAS  Google Scholar 

  • Roessler PG (1990) Environmental control of glycerolipid metabolism in microalgae: commercial implications and future research directions. J Phycol 26:393–399

    Article  CAS  Google Scholar 

  • Salim S, Bosma R, Vermuë MW (2011) Harvesting of microalgae by bio-flocculation. J Appl Phycol 23:849–855

    Article  PubMed  Google Scholar 

  • Sarno D, Kooistra W, Medlin LK, Percopo I, Zingone A (2005) Diversity in the genus Skeletonema (Bacillariophyceae): II. An assessment of the taxonomy of S. costatum-like species with the description of four new species. J Phycol 41:151–176

    Article  Google Scholar 

  • Shifrin NS, Chisholm SW (1981) Phytoplankton lipids: interspecific differences and effects of nitrate, silicate and light-dark cycles. J Phycol 17:374–384

    Article  CAS  Google Scholar 

  • Sieg RD, Poulson-Ellestad KL, Kubanek J (2010) Chemical ecology of the marine plankton. Nat Prod Rep 28:388–399

    Article  PubMed  Google Scholar 

  • Solovchenko A, Khozin-Goldberg I, Recht L, Boussiba S (2011) Stress-induced changes in optical properties, pigment and fatty acid content of Nannachloropsis sp.: implications of non-destructive assay of total fatty acids. Mar Biotechnol 13:527–535

    Article  PubMed  CAS  Google Scholar 

  • Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96

    Article  PubMed  CAS  Google Scholar 

  • Steinke M, Malin G, Liss PS (2002) Trophic interactions in the sea: an ecological role for climate relevant volatiles? J Phycol 38:630–638

    Article  CAS  Google Scholar 

  • Sukenik A, Bilanovic D, Shelef G (1988) Flocculation of microalgae in brackish and sea waters. Biomass 15:187–199

    Article  Google Scholar 

  • Sukenik A, Carmeli Y, Berner T (1989) Regulation of fatty acid composition by irradiance level in the Eustigmatophyte Nannochloropsis sp. J Phycol 25:686–692

    Article  CAS  Google Scholar 

  • Uduman N, Qi Y, Danquah MK, Forde GM, Hoadley A (2010) Dewatering of microalgal cultures: a major bottleneck to algae-based fuels. J Renew Sustainable Energy 2:012701

    Article  Google Scholar 

  • Vandamme D, Foubert I, Meesschaert B, Muylaert K (2010) Flocculation of microalgae using cationic starch. J Appl Phycol 22:525–530

    Article  Google Scholar 

  • Vardi A, Formiggini F, Casotti R, De Martino A, Ribalet F, Miralto A, Bowler C (2006) A stress surveillance system based on calcium and nitric oxide in marine diatoms. PLoS Biol 4:411–419

    Article  CAS  Google Scholar 

  • Vardi A, Bidie KD, Kwityn C, Hirsh DJ, Thompson SM, Callow JA, Falkowski P, Bowler C (2008) A diatom gene regulating nitric-oxide signaling and susceptibility to diatom-derived aldehydes. Curr Biol 18:895–899

    Article  PubMed  CAS  Google Scholar 

  • Vidoudez C, Nejstgaard JC, Jakobsen HH, Pohnert G (2011) Dynamics of dissolved and particulate polyunsaturated aldehydes in mesocosms inoculated with different densities of the diatom Skeletonema marinoi. Mar Drugs 9:345–358

    Article  PubMed  CAS  Google Scholar 

  • Volk RB, Furkert FH (2006) Antialgal, antibacterial and antifungal activity of two metabolites produced and excreted by cyanobacteria during growth. Microbiol Res 161:180–186

    Article  PubMed  CAS  Google Scholar 

  • Watson SB, Jüttner F, Koester O (2007) Daphnia behavioural responses to taste and odour compounds: ecological significance and application as an inline treatment plant monitoring tool. Water Sci Technol 55:23–31

    PubMed  CAS  Google Scholar 

  • Weinberger F (2007) Pathogen-induced defense and innate immunity in macroalgae. Biol Bull 213:290–302

    Article  PubMed  CAS  Google Scholar 

  • Wolfe GV (2000) The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts. Biol Bull 198:225–244

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was generously supported by a grant from the Carbon Trust as part of the Algae Biofuels Challenge directed research programme. The assistance of A. Cangardel with particle settlement assays is appreciated.

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Correspondence to Gary S. Caldwell.

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Taylor, R.L., Rand, J.D. & Caldwell, G.S. Treatment with Algae Extracts Promotes Flocculation, and Enhances Growth and Neutral Lipid Content in Nannochloropsis oculata—a Candidate for Biofuel Production. Mar Biotechnol 14, 774–781 (2012). https://doi.org/10.1007/s10126-012-9441-8

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