Skip to main content

Advertisement

Log in

Immobilized microalgae for nutrient recovery from source-separated human urine

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

Abstract

Shortages in nutrients and freshwater for a growing population are critical global issues. Source separation of waste streams combined with decentralized resource recovery is a promising approach to address this problem. Urine contains within 1% of household wastewater up to 80% of nitrogen (N) and 50% of phosphorus (P). Since microalgae are efficient at nutrient uptake, growing them in urine is a promising technology to clean urine and produce biomass as fertilizer. The aim of this study was to develop a process for nutrient recovery from minimally diluted human urine using immobilized cultivation of microalgae on porous substrate photobioreactors (PSBRs). Treatment of urine, unamended except for a 1:1 dilution with tap water, was performed with the green alga Desmodesmus abundans, chosen among 96 algal strains derived from urine-specific enrichments and culture collections. A growth rate of 7.2 g dry weight m−2 day−1 and removal efficiencies for N and P of 13.1 and 94.1% were determined. Pre-treatment of urine with activated carbon was found to eliminate potentially detrimental effects of pharmaceuticals. In combination with other technologies, PSBRs could be applied in decentralized resource recovery systems, helping to close the link between sanitation and food production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Acién FG, Fernández JM, Magán JJ, Molina E (2012) Production cost of a real microalgae production plant and strategies to reduce it. Biotechnol Adv 30:1344–1353

    Article  PubMed  Google Scholar 

  • Adamsson M (2000) Potential use of human urine by greenhouse culturing of microalgae (Scenedesmus acuminatus), zooplankton (Daphnia magna) and tomatoes (Lycopersicon). Ecol Eng 16:243–254

    Article  Google Scholar 

  • Adnan A, Mavinic DS, Koch FA (2003) Pilot-scale study of phosphorus recovery through struvite crystallization—examining the process feasibility. J Environ Eng Sci 2:315–324

    Article  CAS  Google Scholar 

  • Ahn Y-H (2006) Sustainable nitrogen elimination biotechnologies: a review. Process Biochem 41:1709–1721

    Article  CAS  Google Scholar 

  • Ashley K, Cordell D, Mavinic D (2011) A brief history of phosphorus: from the philosopher’s stone to nutrient recovery and reuse. Chemosphere 84:737–746

    Article  CAS  PubMed  Google Scholar 

  • Aulakh MS, Pasricha NS, Bahl GS (2003) Phosphorus fertilizer response in an irrigated soybean–wheat production system on a subtropical, semiarid soil. Field Crop Res 80:99–109

    Article  Google Scholar 

  • Azov Y, Goldman JC (1982) Free ammonia inhibition of algal photosynthesis in intensive cultures. Appl Environ Microbiol 43:735–739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bácsi I, B-Béres V, Kókai Z et al (2016) Effects of non-steroidal anti-inflammatory drugs on cyanobacteria and algae in laboratory strains and in natural algal assemblages. Environ Pollut 212:508–518

    Article  PubMed  Google Scholar 

  • Ban ZS, Dave G (2004) Laboratory studies on recovery of N and P from human urine through struvite crystallisation and zeolite adsorption. Environ Technol 25:111–121

    Article  CAS  PubMed  Google Scholar 

  • Beler-Baykal B, Bayram S, Akkaymak E, Cinar S (2004) Removal of ammonium from human urine through ion exchange with clinoptilolite and its recovery for further reuse. Water Sci Technol 50:149–156

    CAS  PubMed  Google Scholar 

  • Benstein RM, Çebi Z, Podola B, Melkonian M (2014) Immobilized growth of the peridinin-producing marine dinoflagellate Symbiodinium in a simple biofilm photobioreactor. Mar Biotech 16:621-628 

  • Bester K, Scholes L, Wahlberg C, McArdell CS (2008) Sources and mass flows of xenobiotics in urban water cycles—an overview on current knowledge and data gaps. Water Air Soil Pollut Focus 8:407–423

    Article  CAS  Google Scholar 

  • Boelee NC, Temmink H, Janssen M, Buisman CJ, Wijffels RH (2011) Nitrogen and phosphorus removal from municipal wastewater effluent using microalgal biofilms. Water Res 45:5925–5933

    Article  CAS  PubMed  Google Scholar 

  • Cabrera ML, Beare MH (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57:1007

    Article  CAS  Google Scholar 

  • Cai T, Park SY, Li Y (2013) Nutrient recovery from wastewater streams by microalgae: status and prospects. Renew Sust Energ Rev 19:360–369

    Article  CAS  Google Scholar 

  • Chang Y, Wu Z, Bian L, Feng D, Leung DYC (2013) Cultivation of Spirulina platensis for biomass production and nutrient removal from synthetic human urine. Appl Energy 102:427–431

    Article  CAS  Google Scholar 

  • Cleuvers M (2004) Mixture toxicity of the anti-inflammatory drugs diclofenac, ibuprofen, naproxen, and acetylsalicylic acid. Ecotoxicol Environ Saf 59:309–315

    Article  CAS  PubMed  Google Scholar 

  • Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305

    Article  Google Scholar 

  • Damodar Reddy D, Subba Rao A, Sammi Reddy K, Takkar P (1999) Yield sustainability and phosphorus utilization in soybean–wheat system on vertisols in response to integrated use of manure and fertilizer phosphorus. Field Crop Res 62:181–190

    Article  Google Scholar 

  • Dockhorn T (2016) The resource economic dimension of wastewater treatment vs. green technologies. In: Ngo HH, Guo W, Surampalli RY, Zhang TC (eds) Green Technologies for Sustainable Water Management. American Society of Civil Engineers, Reston, p 755-756

  • Ellis K (1987) Slow sand filtration as a technique for the tertiary treatment of municipal sewages. Water Res 21:403–410

    Article  CAS  Google Scholar 

  • Etter B, Tilley E, Khadka R, Udert KM (2011) Low-cost struvite production using source-separated urine in Nepal. Water Res 45:852–862

    Article  CAS  PubMed  Google Scholar 

  • Feng D, Wu Z (2006) Culture of Spirulina platensis in human urine for biomass production and O2 evolution. J Zhejiang Univ Sci B 7:34–37

    Article  CAS  PubMed  Google Scholar 

  • Glibert PM, Harrison J, Heil C, Seitzinger S (2006) Escalating worldwide use of urea—a global change contributing to coastal eutrophication. Biogeochemistry 77:441–463

    Article  CAS  Google Scholar 

  • Green MB, Upton J (1994) Constructed reed beds: a cost-effective way to polish wastewater effluents for small communities. Water Environ Res 66:188–192

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hu Y, Barker AV (1999) A single plant tissue digestion for macronutrient analysis. Commun Soil Sci Plant Anal 30:677–687

    Article  CAS  Google Scholar 

  • Isherwood K (2000) Mineral fertilizer use and the environment. United Nations Environment Programme, Paris, p 40

  • Jaatinen S, Lakaniemi A-M, Rintala J (2016) Use of diluted urine for cultivation of Chlorella vulgaris. Environ Technol 37:1159–1170

    Article  CAS  PubMed  Google Scholar 

  • Jjemba PK (2006) Excretion and ecotoxicity of pharmaceutical and personal care products in the environment. Ecotoxicol Environ Saf 63:113–130

    Article  CAS  PubMed  Google Scholar 

  • Jönsson H (2004) EcoSanRes Programme: guidelines on the use of urine and faeces in crop production. Stockholm Environment Institute, Stockholm, p 17–20

  • 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 Agric Food Chem 52:7293–7296

    Article  CAS  PubMed  Google Scholar 

  • Kesaano M, Sims RC (2014) Algal biofilm based technology for wastewater treatment. Algal Res 5:231–240

    Article  Google Scholar 

  • Kiperstok AC, Sebestyén P, Podola B, Melkonian M (2016) Biofilm cultivation of Haematococcus pluvialis enables a highly productive one-phase process for astaxanthin production using high light intensities. Algal Res 21:213–222

    Article  Google Scholar 

  • Kuntke P, Śmiech KM, Bruning H, Zeeman G, Saakes M, Sleutels THJA, Hamelers HVM, Buisman CJN (2012) Ammonium recovery and energy production from urine by a microbial fuel cell. Water Res 46:2627–2636

    Article  CAS  PubMed  Google Scholar 

  • Langergraber G, Muellegger E (2005) Ecological sanitation—a way to solve global sanitation problems? Environ Int 31:433–444

    Article  CAS  PubMed  Google Scholar 

  • Larsen TA, Lienert J (2007) Novaquatis final report. NoMix - A new approach to urban water management. Swiss Federal Institute for Environmental Science (EAWAG), Duebendorf, p 4–5

  • Li T, Piltz B, Podola B, Dron A, de Beer D, Melkonian M (2016) Microscale profiling of photosynthesis-related variables in a highly productive biofilm photobioreactor. Biotechnol Bioeng 113:1046–1055

    Article  CAS  PubMed  Google Scholar 

  • Lind B-B, Ban Z, Bydén S (2000) Nutrient recovery from human urine by struvite crystallization with ammonia adsorption on zeolite and wollastonite. Bioresour Technol 73:169–174

    Article  CAS  Google Scholar 

  • Mallick N (2002) Biotechnological potential of immobilized algae for wastewater N, P and metal removal: a review. Biometals 15:377–390

    Article  CAS  PubMed  Google Scholar 

  • Maurer M, Pronk W, Larsen TA (2006) Treatment processes for source-separated urine. Water Res 40:3151–3166

    Article  CAS  PubMed  Google Scholar 

  • McFadden GI, Melkonian M (1986) Use of Hepes buffer for microalgal culture media and fixation for electron microscopy. Phycologia 25:551–557

    Article  CAS  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71

    Article  CAS  PubMed  Google Scholar 

  • Mnkeni PNS, Kutu FRF, Muchaonyerwa P, Austin LM (2008) Evaluation of human urine as a source of nutrients for selected vegetables and maize under tunnel house conditions in the Eastern Cape, South Africa. Waste Manag Res 26:132–139

    Article  CAS  PubMed  Google Scholar 

  • 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 96:451–458

    Article  CAS  PubMed  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • 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 25:1413–1420

    Article  CAS  Google Scholar 

  • Nowack ECM, Podola B, Melkonian M (2005) The 96-well Twin-Layer system: a novel approach in the cultivation of microalgae. Protist 156:239–251

    Article  PubMed  Google Scholar 

  • Podola B, Li T, Melkonian M (2016) Porous substrate bioreactors: a paradigm shift in microalgal biotechnology? Trends Biotechnol. https://doi.org/10.1016/j.tibtech.2016.06.004

  • Posadas E, García-Encina P-A, Soltau A et al (2013) Carbon and nutrient removal from centrates and domestic wastewater using algal–bacterial biofilm bioreactors. Bioresour Technol 139:50–58

    Article  CAS  PubMed  Google Scholar 

  • Pringsheim E (1946) Pure cultures of algae. Hafner Publ Co, London, p 23–25

  • Putnam DF (1971) Composition and concentrative properties of human urine. Washington D.C, National Aeronautics and Space Administration (NASA), p 38

  • Rodhe L, Richert Stintzing A, Steineck S (2004) Ammonia emissions after application of human urine to a clay soil for barley growth. Nutr Cycl Agroecosyst 68:191–198

    Article  CAS  Google Scholar 

  • Ronteltap M, Maurer M, Gujer W (2007) Struvite precipitation thermodynamics in source-separated urine. Water Res 41:977–984

    Article  CAS  PubMed  Google Scholar 

  • Schultze LKP, Simon MV, Li T, Langenbach D, Podola B, Melkonian M (2015) High light and carbon dioxide optimize surface productivity in a twin-layer biofilm photobioreactor. Algal Res 8:37–44

    Article  Google Scholar 

  • 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 19:417–423

    Article  CAS  Google Scholar 

  • 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 154:260–266

    Article  CAS  PubMed  Google Scholar 

  • Smil V (2000) Phosphorus in the environment: natural flows and human interferences. Annu Rev Energy Environ 25:53–88

    Article  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Surek B, Melkonian M (2004) CCAC—Culture Collection of Algae at the University of Cologne: a new collection of axenic algae with emphasis on flagellates. Nova Hedwigia 79:77–92

    Article  Google Scholar 

  • Tortora GJ, Derrickson B (2006) The urinary system. In: Principles of anatomy and physiology, 11th edn. John Wiley & Sons, Hoboken, pp 992–1035

  • Tuantet K, Janssen M, Temmink H, Zeeman G, Wijffels RH, Buisma CJN (2014a) Microalgae growth on concentrated human urine. J Appl Phycol 26:287–297

    Article  CAS  Google Scholar 

  • Tuantet K, Temmink H, Zeeman G, Janssen M, Wijffels RH, Buisman CJN (2014b) Nutrient removal and microalgal biomass production on urine in a short light-path photobioreactor. Water Res 55:162–174

    Article  CAS  PubMed  Google Scholar 

  • Udert KM, Buckley CA, Wächter M, McArdell CS, Kohn T, Strande L, Zöllig H, Fumasoli A, Oberson A, Etter B (2015) Technologies for the treatment of source-separated urine in the eThekwini Municipality. Water SA 41:212–221

  • Verstraete W, Van de Caveye P, Diamantis V (2009) Maximum use of resources present in domestic “used water”. Bioresour Technol 100:5537–5545

    Article  CAS  PubMed  Google Scholar 

  • Warner R (1942) The kinetics of the hydrolysis of urea and of arginine. J Biol Chem 142:705–723

    CAS  Google Scholar 

  • Wilsenach JA, van Loosdrecht MC (2006) Integration of processes to treat wastewater and source-separated urine. J Environ Eng 132:331–341

    Article  CAS  Google Scholar 

  • Winker M, Vinnerås B, Muskolus A, Arnold U, Clemens J (2009) Fertiliser products from new sanitation systems: their potential values and risks. Bioresour Technol 100:4090–4096

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Liu H, Li M, Yu C, Yu G (2008) Treating urine by Spirulina platensis. Acta Astronaut 63:1049–1054

    Article  CAS  Google Scholar 

  • Yin CY, Aroua MK, Daud WMAW (2007) Review of modifications of activated carbon for enhancing contaminant uptakes from aqueous solutions. Sep Purif Technol 52:403–415

    Article  CAS  Google Scholar 

  • Zeeman G, Kujawa-Roeleveld K (2011) Resource recovery from source separated domestic waste(water) streams; full scale results. Water Sci Technol 64:1987–1992

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the University of Cologne (KST 158901001). The authors would like to thank Dr. Tong Li and Dr. Björn Podola (both from the University of Cologne) for helpful discussions and practical support in the course of this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bastian Piltz.

Electronic supplementary material

ESM 1

(DOCX 30 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Piltz, B., Melkonian, M. Immobilized microalgae for nutrient recovery from source-separated human urine. J Appl Phycol 30, 421–429 (2018). https://doi.org/10.1007/s10811-017-1266-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1266-4

Keywords

Navigation