Journal of Applied Phycology

, Volume 27, Issue 5, pp 1793–1804 | Cite as

Microalgal biofilms for biomass production

  • Florian Berner
  • Kirsten HeimannEmail author
  • Madoc Sheehan
5th Congress of the International Society for Applied Phycology


Microalgae are promising candidates for recycling of carbon dioxide (CO2) into renewable bioproducts. However, the low biomass concentration of current suspension culture systems leads to high water requirements, inefficient harvesting and high liquid transportation costs. Despite ongoing research, these still propose a challenge to the economic viability of microalgal cultivation. Microalgal biofilms provide an alternative approach to biomass production that could resolve these challenges by growing the cells attached to a surface, surrounded by a self-produced matrix of polymers. Microalgal biofilms have much higher biomass concentrations than suspension cultures, and the attached cells are easy to separate from the cultivation medium. However, cultivating microalgal biofilms requires the development of a purposefully designed cultivation system, especially due to interactions between cells and surface, persistent gradients in the biomass and the effects of flow, which play a critical role for biofilm productivity. A range of systems has been employed for the cultivation of microalgal biofilms, with biomass productivities of up to 60 grammes dry weight (g(DW)) m−2 day−1 (dry weight per ground area) outdoors and up to 80 g(DW) m−2 day−1 under laboratory conditions, respectively. However, there is considerable variation of reported results along with experimental conditions, which limits the capability for quantitative comparisons with other systems and hinders the identification of the drivers and variables that dictate microalgal biomass formation. Development of standard conditions and representative species would be required for closing this gap and for realising the full potential of microalgal biofilm cultivation as a viable process for industrial biomass production.


Microalgae Biofilm Attached cultivation Biomass production Bioproducts 


  1. Abe K, Matsumura I, Imamaki A, Hirano M (2003) Removal of inorganic nitrogen sources from water by the algal biofilm of the aerial microalga Trentepohlia aurea. World J Microbiol Biotech 19:325–328CrossRefGoogle Scholar
  2. Adey WH, Luckett C, Jensen K (1993) Phosphorus removal from natural waters using controlled algal production. Restor Ecol 1:29–39CrossRefGoogle Scholar
  3. Adey WH, Kangas PC, Mulbry W (2011) Algal turf scrubbing: cleaning surface waters with solar energy while producing a biofuel. Biosci 61:434–441CrossRefGoogle Scholar
  4. Avendano-Herrera RE, Riquelme CE (2007) Production of a diatom-bacteria biofilm in a photobioreactor for aquaculture applications. Aquac Eng 36:97–104CrossRefGoogle Scholar
  5. Barranguet C, Veuger B, Van Beusekom SAM, Marvan P, Sinke JJ, Admiraal W (2005) Divergent composition of algal-bacterial biofilms developing under various external factors. Eur J Phycol 40:1–8CrossRefGoogle Scholar
  6. Benemann J (2013) Microalgae for biofuels and animal feeds. Energies 6:5869–5886CrossRefGoogle Scholar
  7. Bernstein HC, Kesaano M, Moll K, Smith T, Gerlach R, Carlson RP, Miller CD, Peyton BM, Cooksey KE, Gardner R, Sims RC (2014) Direct measurement and characterization of active photosynthesis zones inside wastewater remediating and biofuel producing microalgal biofilms. Bioresour Technol 156:206–215CrossRefPubMedGoogle Scholar
  8. Blanken W, Janssen M, Cuaresma M, Libor Z, Bhaiji T, Wijffels RH (2014) Biofilm growth of Chlorella sorokiniana in a rotating biological contactor based photobioreactor. Biotechnol Bioeng 111:2436–2445CrossRefPubMedGoogle Scholar
  9. Blankenship JR, Mitchell AP (2006) How to build a biofilm: a fungal perspective. Cur Opin Microbiol 9:588–594.CrossRefGoogle Scholar
  10. Boelee NC, Temmink H, Janssen M, Buisman CJN, Wijffels RH (2011) Nitrogen and phosphorus removal from municipal wastewater effluent using microalgal biofilms. Water Res 45:5925–5933CrossRefPubMedGoogle Scholar
  11. Boelee NC, Janssen M, Temmink H, Shrestha R, Buisman CJ, Wijffels RH (2013a) Nutrient removal and biomass production in an outdoor pilot-scale phototrophic biofilm reactor for effluent polishing. Appl Biochem Biotechnol 172:405–422CrossRefPubMedGoogle Scholar
  12. Boelee NC, Janssen M, Temmink H, Taparavičiūtė L, Khiewwijit R, Jánoska A, Buisman CJN, Wijffels RH (2013b) The effect of harvesting on biomass production and nutrient removal in phototrophic biofilm reactors for effluent polishing. J Appl Phycol 26:1439–1452CrossRefGoogle Scholar
  13. Boelee NC, Temmink H, Janssen M, Buisman CJN, Wijffels RH (2014) Balancing the organic load and light supply in symbiotic microalgal–bacterial biofilm reactors treating synthetic municipal wastewater. Ecol Eng 64:213–221CrossRefGoogle Scholar
  14. Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756CrossRefGoogle Scholar
  15. Bruno L, Di Pippo F, Antonaroli S, Gismondi A, Valentini C, Albertano P (2012) Characterization of biofilm-forming cyanobacteria for biomass and lipid production. J Appl Microbiol 113:1052–1064CrossRefPubMedGoogle Scholar
  16. Buhmann M, Kroth PG, Schleheck D (2012) Photoautotrophic-heterotrophic biofilm communities: a laboratory incubator designed for growing axenic diatoms and bacteria in defined mixed-species biofilms. Environ Microbiol Rep 4:133–140CrossRefPubMedGoogle Scholar
  17. Cao J, Yuan WQ, Pei ZJ, Davis T, Cui Y, Beltran M (2009) A preliminary study of the effect of surface texture on algae cell attachment for a mechanical-biological energy manufacturing system J Manuf Sci Eng-Trans ASME 131Google Scholar
  18. Cheng PF, Ji B, Gao LL, Zhang W, Wang JF, Liu TZ (2013) The growth, lipid and hydrocarbon production of Botryococcus braunii with attached cultivation. Bioresour Technol 138:95–100CrossRefPubMedGoogle Scholar
  19. Christenson LB, Sims RC (2011) Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 29:686–702CrossRefPubMedGoogle Scholar
  20. Christenson LB, Sims RC (2012) Rotating algal biofilm reactor and spool harvester for wastewater treatment with biofuels by-products. Biotechnol Bioeng 109:1674–1684CrossRefPubMedGoogle Scholar
  21. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Ann Rev Microbiol 49:711–745CrossRefGoogle Scholar
  22. Craggs RJ, Adey WH, Jessup BK, Oswald WJ (1996a) A controlled stream mesocosm for tertiary treatment of sewage. Ecol Eng 6:149–169CrossRefGoogle Scholar
  23. Craggs RJ, Adey WH, Jenson KR, St John MS, Green FB, Oswald WJ (1996b) Phosphorus removal from wastewater using an algal turf scrubber. Water Sci Technol 33:191–198CrossRefGoogle Scholar
  24. Cui Y, Yuan W (2013) Thermodynamic modeling of algal cell–solid substrate interactions. Appl Energy 112:485–492CrossRefGoogle Scholar
  25. De Beer D, Glud A, Epping E, Kühl M (1997) A fast-responding CO2 micro-electrode for profiling sediments, microbial mats, and biofilms. Limnol Oceanogr 42:1590–1600CrossRefGoogle Scholar
  26. Decho AW (2000) Microbial biofilms in intertidal systems: an overview. Continent Shelf Res 20:1257–1273CrossRefGoogle Scholar
  27. Demirbas MF (2011) Biofuels from algae for sustainable development. Appl Energy 88:3473–3480CrossRefGoogle Scholar
  28. Doucha J, Livansky K (2009) Outdoor open thin-layer microalgal photobioreactor: potential productivity. J Appl Phycol 21:111–117CrossRefGoogle Scholar
  29. Flemming HC, Wingender J (2010) The biofilm matrix. Nature Rev Microbiol 8:623–633Google Scholar
  30. Grobbelaar JU (2010) Microalgal biomass production: challenges and realities. Photosynth Res 106:135–144CrossRefPubMedGoogle Scholar
  31. Gross M, Henry W, Michael C, Wen Z (2013) Development of a rotating algal biofilm growth system for attached microalgae growth with in situ biomass harvest. Bioresour Technol 150:195–201CrossRefPubMedGoogle Scholar
  32. Guzzon A, Bohn A, Diociaiuti M, Albertano P (2008) Cultured phototrophic biofilms for phosphorus removal in wastewater treatment. Water Res 42:4357–4367CrossRefPubMedGoogle Scholar
  33. Haubner N, Schumann R, Karsten U (2006) Aeroterrestrial microalgae growing in biofilms on facades—response to temperature and water stress. Microb Ecol 51:285–293CrossRefPubMedGoogle Scholar
  34. Higgins BT, Kendall A (2012) Life cycle environmental and cost impacts of using an algal turf scrubber to treat dairy wastewater. J Ind Ecol 16:436–447CrossRefGoogle Scholar
  35. Hu Q, Kurano N, Kawachi M, Iwasaki I, Miyachi S (1998) Ultrahigh-cell-density culture of a marine green alga Chlorococcum littorale in a flat-plate photobioreactor. Appl Microbiol Biotechnol 49:655–662CrossRefGoogle Scholar
  36. Ji B, Zhang W, Zhang N, Wang J, Lutzu GA, Liu T (2013a) Biofilm cultivation of the oleaginous microalgae Pseudochlorococcum sp. Bioprocess Biosyst Eng 7:1369–1375Google Scholar
  37. Ji C, Wang J, Zhang W, Liu J, Wang H, Gao L, Liu T (2013b) An applicable nitrogen supply strategy for attached cultivation of Aucutodesmus obliquus. J Appl Phycol 26:173–180CrossRefGoogle Scholar
  38. Johnson MB, Wen Z (2010) Development of an attached microalgal growth system for biofuel production. Appl Microbiol Biotechnol 85:525–534CrossRefPubMedGoogle Scholar
  39. Kebede-Westhead E, Pizarro C, Mulbry WW (2004) Treatment of dairy manure effluent using freshwater algae: elemental composition of algal biomass at different manure loading rates. J Agri Food Chem 52:7293–7296CrossRefGoogle Scholar
  40. Kebede-Westhead E, Pizarro C, Mulbry WW (2006) Treatment of swine manure effluent using freshwater algae: production, nutrient recovery, and elemental composition of algal biomass at four effluent loading rates. J Appl Phycol 18:41–46CrossRefGoogle Scholar
  41. Kesaano M, Sims RC (2014) Algal biofilm based technology for wastewater treatment. Algal Res 5:231–240CrossRefGoogle Scholar
  42. Khatoon H, Yusoff F, Banerjee S, Shariff M, Bujang JS (2007) Formation of periphyton biofilm and subsequent biofouling on different substrates in nutrient enriched brackishwater shrimp ponds. Aquaculture 273:470–477CrossRefGoogle Scholar
  43. Kliphuis AMJ, de Winter L, Vejrazka C, Martens DE, Janssen M, Wijffels RH (2010) Photosynthetic efficiency of Chlorella sorokiniana in a turbulently mixed short light-path photobioreactor. Biotechnol Prog 26:687–696CrossRefPubMedGoogle Scholar
  44. Largeau C, Casadevall E, Berkaloff C, Dhamelincourt P (1980) Sites of accumulation and composition of hydrocarbons in Botryococcus braunii. Phytochemistry 19:1043–1051CrossRefGoogle Scholar
  45. Lee Y-K (2001) Microalgal mass culture systems and methods: their limitation and potential. J Appl Phycol 13:307–315CrossRefGoogle Scholar
  46. Liu T, Wang J, Hu Q, Cheng P, Bei J, Liu J, Chen Y, Zhang W, Chen X, Chen L, Gao L, Ji C, Wang H (2013) Attached cultivation technology of microalgae for efficient biomass feedstock production. Bioresour Technol 127:216–222CrossRefPubMedGoogle Scholar
  47. Mieszkin S, Callow ME, Callow JA (2013) Interactions between microbial biofilms and marine fouling algae: a mini review. Biofouling 29:1097–1113CrossRefPubMedGoogle Scholar
  48. Milledge JJ (2011) Commercial application of microalgae other than as biofuels: a brief review. Rev Environ Sci Bio-Technol 10:31–41CrossRefGoogle Scholar
  49. Molina Grima E, Belarbi E-H, Acién Fernández F, Robles Medina A, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20:491–515CrossRefPubMedGoogle Scholar
  50. Molino PJ, Wetherbee R (2008) The biology of biofouling diatoms and their role in the development of microbial slimes. Biofouling 24:365–379CrossRefPubMedGoogle Scholar
  51. Mulbry W, Wilkie AC (2001) Growth of benthic freshwater algae on dairy manures. J Appl Phycol 13:301–306CrossRefGoogle Scholar
  52. Mulbry W, Westhead EK, Pizarro C, Sikora L (2005) Recycling of manure nutrients: use of algal biomass from dairy manure treatment as a slow release fertilizer. Bioresour Technol 96:451–458CrossRefPubMedGoogle Scholar
  53. Mulbry W, Kondrad S, Pizarro C, Kebede-Westhead E (2008) Treatment of dairy manure effluent using freshwater algae: algal productivity and recovery of manure nutrients using pilot-scale algal turf scrubbers. Bioresour Technol 99:8137–8142CrossRefPubMedGoogle Scholar
  54. Murphy TE, Berberoglu H (2014) Flux balancing of light and nutrients in a biofilm photobioreactor for maximizing photosynthetic productivity. Biotechnol Prog 30:348–359CrossRefPubMedGoogle Scholar
  55. Murphy TE, Fleming E, Bebout L, Bebout B, Berberoglu H (2013) A novel micronial cell cultivation platform for space applications. Amer Astronaut Soc Sci Technol Ser 114:335–338Google Scholar
  56. Murphy TE, Fleming E, Berberoglu H (2014) Vascular structure design of an artificial tree for microbial cell cultivation and biofuel production. Transp Porous Med 104:25–41.CrossRefGoogle Scholar
  57. Naumann T, Çebi Z, Podola B, Melkonian M (2013) Growing microalgae as aquaculture feeds on twin-layers: a novel solid-state photobioreactor. J Appl Phycol 25:1413–1420CrossRefGoogle Scholar
  58. Nichols HW, Bold HC (1965) Trichosarcina polymorpha Gen. et Sp. Nov J Phycol 1:34–38CrossRefGoogle Scholar
  59. Nowack EC, Podola B, Melkonian M (2005) The 96-well twin-layer system: a novel approach in the cultivation of microalgae. Protist 156:239–251CrossRefPubMedGoogle Scholar
  60. O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Ann Rev Microbiol 54:49–79CrossRefGoogle Scholar
  61. Orandi S, Lewis DM, Moheimani NR (2012) Biofilm establishment and heavy metal removal capacity of an indigenous mining algal-microbial consortium in a photo-rotating biological contactor. J Ind Microbiol Biotechnol 39:1321–1331CrossRefPubMedGoogle Scholar
  62. Ozkan A, Berberoglu H (2013) Adhesion of algal cells to surfaces. Biofouling 29:469–482CrossRefPubMedGoogle Scholar
  63. Ozkan A, Kinney K, Katz L, Berberoglu H (2012) Reduction of water and energy requirement of algae cultivation using an algae biofilm photobioreactor. Bioresour Technol 114:542–548CrossRefPubMedGoogle Scholar
  64. Pizarro C, Kebede-Westhead E, Mulbry W (2002) Nitrogen and phosphorus removal rates using small algal turfs grown with dairy manure. J Appl Phycol 14:469–473CrossRefGoogle Scholar
  65. Pizarro C, Mulbry W, Blersch D, Kangas P (2006) An economic assessment of algal turf scrubber technology for treatment of dairy manure effluent. Ecol Eng 26:321–327CrossRefGoogle Scholar
  66. Posadas E, Garcia-Encina PA, Soltau A, Dominguez A, Diaz I, Munoz R (2013) Carbon and nutrient removal from centrates and domestic wastewater using algal-bacterial biofilm bioreactors. Bioresour Technol 139:50–58CrossRefPubMedGoogle Scholar
  67. Qian PY, Lau SCK, Dahms HU, Dobretsov S, Harder T (2007) Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Mar Biotechnol 9:399–410CrossRefPubMedGoogle Scholar
  68. Riding R (2000) Microbial carbonates: the geological record of calcified bacterial–algal mats and biofilms. Sedimentology 47:179–214CrossRefGoogle Scholar
  69. Sakiadis B (1961) Boundary-layer behavior on continuous solid surfaces: II. The boundary layer on a continuous flat surface. AIChE J 7:221–225CrossRefGoogle Scholar
  70. Schnurr PJ, Espie GS, Allen DG (2013) Algae biofilm growth and the potential to stimulate lipid accumulation through nutrient starvation. Bioresour Technol 136:337–344CrossRefPubMedGoogle Scholar
  71. Schultz MP, Bendick JA, Holm ER, Hertel WM (2011) Economic impact of biofouling on a naval surface ship. Biofouling 27:87–98CrossRefPubMedGoogle Scholar
  72. Shen Y, Xu X, Zhao Y, Lin X (2014a) Influence of algae species, substrata and culture conditions on attached microalgal culture. Bioprocess Biosyst Eng 37:441–450CrossRefPubMedGoogle Scholar
  73. Shen Y, Chen C, Chen W, Xu X (2014b) Attached culture of Nannochloropsis oculata for lipid production. Bioprocess Biosys Eng 37:1743–1748CrossRefGoogle Scholar
  74. Shi J, Podola B, Melkonian M (2007) Removal of nitrogen and phosphorus from wastewater using microalgae immobilized on twin layers: an experimental study. J Appl Phycol 19:417–423CrossRefGoogle Scholar
  75. Shi J, Podola B, Melkonian M (2014) Application of a prototype-scale twin-layer photobioreactor for effective N and P removal from different process stages of municipal wastewater by immobilized microalgae. Bioresour Technol 154:260–266CrossRefPubMedGoogle Scholar
  76. Slegers PM, Wijffels RH, van Straten G, van Boxtel AJB (2011) Design scenarios for flat panel photobioreactors. Applied Energy 88:3342–3353CrossRefGoogle Scholar
  77. Stanier R, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bact Rev 35:171–205PubMedPubMedCentralGoogle Scholar
  78. Stephens E, Ross IL, Hankamer B (2013) Expanding the microalgal industry—continuing controversy or compelling case. Cur Opin Chem Biol 17:444–452CrossRefGoogle Scholar
  79. Thompson RC, Moschella PS, Jenkins SR, Norton TA, Hawkins SJ (2005) Differences in photosynthetic marine biofilms between sheltered and moderately exposed rocky shores. Mar Ecol Progr Ser 296:53–63CrossRefGoogle Scholar
  80. Vert M, Doi Y, Hellwich KH, Hess M, Hodge P, Kubisa P, Rinaudo M, Schue F (2012) Terminology for biorelated polymers and applications (IUPAC Recommendations 2012). Pure Appl Chem 84:377–410CrossRefGoogle Scholar
  81. Walne PR (1970) Studies on the food value of nineteen genera of algae to juvenile bivalves of the genera Ostrea, Crassostrea, Mercenaria and Mytilus. Fishery Investigations Series II, Volume 26, Number 5.London: Ministry of Agriculture, Fisheries and Food. 62pGoogle Scholar
  82. Wijffels RH, Kruse O, Hellingwerf KJ (2013) Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Curr Opin Biotechnol 24:405–413CrossRefPubMedGoogle Scholar
  83. Wiley P (2013) Microalgae cultivation using offshore membrane enclosures for growing algae (OMEGA). J Sustain Bioen Syst 03:18–32Google Scholar
  84. Wilkie AC, Mulbry WW (2002) Recovery of dairy manure nutrients by benthic freshwater algae. Bioresour Technol 84:81–91CrossRefPubMedGoogle Scholar
  85. Wolf G, Picioreanu C, van Loosdrecht MC (2007) Kinetic modeling of phototrophic biofilms: the PHOBIA model. Biotechnol Bioeng 97:1064–1079CrossRefPubMedGoogle Scholar
  86. Zamalloa C, Boon N, Verstraete W (2013) Decentralized two-stage sewage treatment by chemical-biological flocculation combined with microalgae biofilm for nutrient immobilization in a roof installed parallel plate reactor. Bioresour Technol 130:152–160CrossRefPubMedGoogle Scholar
  87. Zippel B, Rijstenbil J, Neu TR (2007) A flow-lane incubator for studying freshwater and marine phototrophic biofilms. J Microbiol Meth 70:336–345CrossRefGoogle Scholar
  88. Zittelli GC, Biondi N, Rodolfi L, Tredici MR (2013) Photobioreactors for mass production of microalgae. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Wiley, London, pp 225–266CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Florian Berner
    • 1
  • Kirsten Heimann
    • 1
    Email author
  • Madoc Sheehan
    • 1
  1. 1.James Cook UniversityTownsvilleAustralia

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