Bioprocess considerations for microalgal-based wastewater treatment and biomass production.

Nowadays, microalgae received wide attention due to several advantages for biochemicals and renewable/sustainable biofuels production. Moreover, the utilization of microalgae as robust cellular species for biological nutrient removal from industrial and domestic wastewater streams has been of great research interest amongst the several biotechnological applications of microalgae. This is due to the capacity for effective photosynthetic uptake of high concentrations of minerals, ionogens, and organics by microalgae whilst simultaneously biosequestering carbon dioxide. This review discusses the utilization of microalgae for wastewater nutrients removal. It discusses the bioprocess potentials and challenges of using microalgal cells for full-scale microbial wastewater treatment under free and immobilized conditions. It also presents a mechanistic insight of the mass transfer processes essential for optimal uptake of nutrients during photobioreaction. A new bioprocess paradigm based on integrated upstream and downstream processes for multi-purpose microalgae bioprocessing and bioresource generation is discussed.

[1]  J. Iqbal,et al.  Removal and recovery of nickel(II) from aqueous solution by loofa sponge-immobilized biomass of Chlorella sorokiniana: characterization studies. , 2004, Journal of hazardous materials.

[2]  C. Soccol,et al.  Potential carbon dioxide fixation by industrially important microalgae. , 2010, Bioresource technology.

[3]  G. Dönmez,et al.  Simultaneous bioaccumulation of reactive dye and chromium(VI) by using thermophil Phormidium sp. , 2007 .

[4]  Michael Melkonian,et al.  Removal of nitrogen and phosphorus from wastewater using microalgae immobilized on twin layers: an experimental study , 2007, Journal of Applied Phycology.

[5]  F. Malcata,et al.  Cadmium Removal by Two Strains of Desmodesmus pleiomorphus Cells , 2010 .

[6]  Y. Chisti.  Biodiesel from microalgae. , 2007, Biotechnology advances.

[7]  Klaus S. Lackner,et al.  A Guide to CO2 Sequestration , 2003, Science.

[8]  Christer Jansson,et al.  Calcifying cyanobacteria--the potential of biomineralization for carbon capture and storage. , 2010, Current opinion in biotechnology.

[9]  P. N. Sarma,et al.  Potential of mixed microalgae to harness biodiesel from ecological water-bodies with simultaneous treatment. , 2011, Bioresource technology.

[10]  A. Shilton,et al.  Wastewater treatment high rate algal ponds for biofuel production. , 2011, Bioresource technology.

[11]  R. Borja,et al.  Heavy Metal Removal by Microalgae , 1999, Bulletin of environmental contamination and toxicology.

[12]  R. O. Cañizares-Villanueva,et al.  Acute toxicity to Daphnia magna of effluents containing Cd, Zn, and a mixture Cd‐Zn, after metal removal by Chlorella vulgaris , 2000 .

[13]  Yinghua Lu,et al.  Autotrophic cultivation of Spirulina platensis for CO2 fixation and phycocyanin production , 2012 .

[14]  B. Mattiasson,et al.  Sequential removal of heavy metals ions and organic pollutants using an algal-bacterial consortium. , 2006, Chemosphere.

[15]  M. Bakır,et al.  Treatment of dye-rich wastewater by an immobilized thermophilic cyanobacterial strain: Phormidium sp. , 2008 .

[16]  Ma Eugenia Martínez,et al.  Nitrogen and phosphorus removal from urban wastewater by the microalga Scenedesmus obliquus , 2000 .

[17]  I. Moreno-Garrido.  Microalgae immobilization: current techniques and uses. , 2008, Bioresource technology.

[18]  E. Fernández,et al.  Inorganic nitrogen assimilation in Chlamydomonas. , 2007, Journal of experimental botany.

[19]  B. Volesky.  Biosorption and me. , 2007, Water research.

[20]  Y. Bashan,et al.  Treatment of recalcitrant wastewater from ethanol and citric acid production using the microalga Chlorella vulgaris and the macrophyte Lemna minuscula. , 2002, Water research.

[21]  Teresa M. Mata,et al.  Microalgae for biodiesel production and other applications: A review , 2010 .

[22]  E. Benson,et al.  In vitro culture and conservation of microalgae: Applications for aquaculture, biotechnology and environmental research , 1999, In Vitro Cellular & Developmental Biology - Plant.

[23]  Nirbhay Kumar Singh,et al.  Microalgae as second generation biofuel. A review , 2011, Agronomy for Sustainable Development.

[24]  Y. Bashan,et al.  Recycling waste debris of immobilized microalgae and plant growth-promoting bacteria from wastewater treatment as a resource to improve fertility of eroded desert soil , 2012 .

[25]  N. Mallick.  Biotechnological potential of immobilized algae for wastewater N, P and metal removal: A review , 2002, Biometals.

[26]  A. Ahluwalia,et al.  Microalgae: a promising tool for carbon sequestration , 2012, Mitigation and Adaptation Strategies for Global Change.

[27]  G. Gadd,et al.  Accumulation of cobalt, zinc and manganese by the estuarine green microalga Chlorella salina immobilized in alginate microbeads , 1992 .

[28]  R. Tischner,et al.  Reduction of the nitrogen and carbon content in swine waste with algae and bacteria , 1999, Applied Microbiology and Biotechnology.

[29]  Paul Chen,et al.  A hetero-photoautotrophic two-stage cultivation process to improve wastewater nutrient removal and enhance algal lipid accumulation. , 2012, Bioresource technology.

[30]  Mogens Henze,et al.  Wastewater treatment. Biological and chemical processes (in Chinese) , 1999 .

[31]  Michael A. Borowitzka,et al.  Micro-algal biotechnology. , 1988 .

[32]  C. Ugwu,et al.  Photobioreactors for mass cultivation of algae. , 2008, Bioresource technology.

[33]  M. Spalding,et al.  Microalgal carbon-dioxide-concentrating mechanisms: Chlamydomonas inorganic carbon transporters. , 2007, Journal of experimental botany.

[34]  Qingyu Wu,et al.  Large‐scale biodiesel production from microalga Chlorella protothecoides through heterotrophic cultivation in bioreactors , 2007, Biotechnology and bioengineering.

[35]  Bo Hu,et al.  A novel method to harvest microalgae via co-culture of filamentous fungi to form cell pellets. , 2012, Bioresource technology.

[36]  E. Olguín.  Dual purpose microalgae-bacteria-based systems that treat wastewater and produce biodiesel and chemical products within a biorefinery. , 2012, Biotechnology advances.

[37]  Y. Bashan,et al.  Starvation enhances phosphorus removal from wastewater by the microalga Chlorella spp. co-immobilized with Azospirillum brasilense , 2006 .

[38]  S. Wilkinson,et al.  Mercury removal by immobilized algae in batch culture systems , 1990, Journal of Applied Phycology.

[39]  P. R. M. Lopes,et al.  Textile Dye Treated Photoelectrolytically and Monitored by Winogradsky Columns , 2012 .

[40]  P. Robinson,et al.  Immobilized algae: a review , 1986 .

[41]  Zhijian Pei,et al.  Microalgae Mass Production Methods , 2009 .

[42]  Y. Bashan,et al.  Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense. , 2002, Canadian journal of microbiology.

[43]  Y. Bashan,et al.  Immobilized microalgae for removing pollutants: review of practical aspects. , 2010, Bioresource technology.

[44]  J. Pittman,et al.  The potential of sustainable algal biofuel production using wastewater resources. , 2011, Bioresource technology.

[45]  F. G. Fernández,et al.  Comparative analysis of the outdoor culture of Haematococcus pluvialis in tubular and bubble column photobioreactors. , 2006, Journal of biotechnology.

[46]  F. Lawson,et al.  Cadmium uptake by unicellular green microalgae , 1996 .

[47]  Y. Bashan,et al.  Biological deterioration of alginate beads containing immobilized microalgae and bacteria during tertiary wastewater treatment , 2013, Applied Microbiology and Biotechnology.

[48]  C. Steinberg,et al.  Removal of bisphenol A by the freshwater green alga Monoraphidium braunii and the role of natural organic matter. , 2012, The Science of the total environment.

[49]  Y. Bashan,et al.  Heterotrophic cultures of microalgae: metabolism and potential products. , 2011, Water research.

[50]  J. Zhou,et al.  Sorption and desorption of Cu and Cd by macroalgae and microalgae. , 1998, Environmental pollution.

[51]  J. Kozinski,et al.  Biosorption of heavy metal ions using wheat based biosorbents--a review of the recent literature. , 2010, Bioresource technology.

[52]  Michele Dassisti,et al.  State of the art of biofuels from pure plant oil , 2012 .

[53]  A. Drobac,et al.  Co-cultivation of N2-fixing cyanobacteria and some agriculturally important plants in liquid and sand cultures , 1997 .

[54]  Yinghua Lu,et al.  NaCS-PDMDAAC immobilized autotrophic cultivation of Chlorella sp. for wastewater nitrogen and phosphate removal , 2012 .

[55]  Katarzyna Chojnacka,et al.  Kinetic and Stoichiometric Relationships of the Energy and Carbon Metabolism in the Culture of Microalgae , 2004 .

[56]  K. Semple,et al.  Biodegradation of phenols by the alga Ochromonas danica , 1996, Applied and environmental microbiology.

[57]  Mogens Henze,et al.  Wastewater Treatment: Biological and Chemical Processes , 1995 .

[58]  E. Molina Grima,et al.  Conversion of CO2 into biomass by microalgae: how realistic a contribution may it be to significant CO2 removal? , 2012, Applied Microbiology and Biotechnology.

[59]  A. Olabi,et al.  Mechanical pretreatment effects on macroalgae-derived biogas production in co-digestion with sludge in Ireland , 2013 .

[60]  James P. Hoffmann,et al.  WASTEWATER TREATMENT WITH SUSPENDED AND NONSUSPENDED ALGAE , 1998 .

[61]  Yun Cheng,et al.  Biodiesel production from Jerusalem artichoke (Helianthus Tuberosus L.) tuber by heterotrophic microalgae Chlorella protothecoides , 2009 .

[62]  Hong-Ying Hu,et al.  Effects of different nitrogen and phosphorus concentrations on the growth, nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. , 2010, Bioresource technology.

[63]  Norio Sugiura,et al.  Development of a high performance electrochemical wastewater treatment system. , 2003, Journal of hazardous materials.

[64]  A. Ferrer,et al.  Characterisation of phosphorous forms in wastewater treatment plants. , 2003 .

[65]  Y. Wong,et al.  Wastewater Nutrients (N and P) Removal by Carrageenan and Alginate Immobilized Chlorella Vulgaris , 1997 .

[66]  Toshiharu Suzuki,et al.  An immobilized cell system in polyurethane foam for the lipophilic micro-alga Prototheca zopfii , 1999 .

[67]  G. Gadd,et al.  Salt-stimulation of caesium accumulation in the euryhaline green microalga Chlorella salina: potential relevance to the development of a biological Cs-removal process , 1993 .

[68]  Y. Bashan,et al.  Alginate beads provide a beneficial physical barrier against native microorganisms in wastewater treated with immobilized bacteria and microalgae , 2011, Applied Microbiology and Biotechnology.

[69]  Andrew Hoadley,et al.  Dewatering of microalgal cultures : a major bottleneck to algae-based fuels , 2010 .

[70]  S. Barrington,et al.  Microalgae for phosphorus removal and biomass production: a six species screen for dual‐purpose organisms , 2012 .

[71]  Oliver R. Inderwildi,et al.  Life cycle energy and greenhouse gas analysis for algae-derived biodiesel , 2011 .

[72]  S. Baena,et al.  Efficiency of ammonia and phosphorus removal from a colombian agroindustrial wastewater by the microalgae Chlorella vulgaris and Scenedesmus dimorphus , 1997 .

[73]  M. Alvim-Ferraz,et al.  Carbon dioxide capture from flue gases using microalgae: Engineering aspects and biorefinery concept , 2012 .

[74]  C. Lan,et al.  Biomass production and nitrogen and phosphorus removal by the green alga Neochloris oleoabundans in simulated wastewater and secondary municipal wastewater effluent. , 2011, Bioresource technology.

[75]  Yinghua Lu,et al.  Comparative physicochemical analysis of suspended and immobilized cultivation of Chlorella sp , 2013 .

[76]  Yujie Feng,et al.  Lipid production of Chlorella vulgaris cultured in artificial wastewater medium. , 2011, Bioresource technology.

[77]  K. Iyer,et al.  Nitrate removal from liquid effluents using microalgae immobilized on chitosan nanofiber mats , 2012 .

[78]  Y. Bashan,et al.  Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum brasilense. , 2002, Water research.

[79]  J. Dewulf,et al.  Enhanced CO(2) fixation and biofuel production via microalgae: recent developments and future directions. , 2010, Trends in biotechnology.

[80]  J. Karthikeyan,et al.  Biological decolourisation of simulated azo dye in aqueous phase by algae Spirogyra species , 2004 .

[81]  E. Olguín,et al.  Annual productivity of Spirulina (Arthrospira) and nutrient removal in a pig wastewater recycling process under tropical conditions , 2003, Journal of Applied Phycology.

[82]  L. Kautsky,et al.  Integrated marine cultivation of Gracilaria chilensis (Gracilariales, Rhodophyta) and salmon cages for reduced environmental impact and increased economic output , 1997 .

[83]  Ayhan Demirbas,et al.  Biodiesel from oilgae, biofixation of carbon dioxide by microalgae: A solution to pollution problems , 2011 .

[84]  Guangce Wang,et al.  Immobilization of Chlorella sorokiniana GXNN 01 in alginate for removal of N and P from synthetic wastewater. , 2012, Bioresource technology.

[85]  E. Kwon,et al.  Microalgae Production Using Wastewater: Effect of Light-Emitting Diode Wavelength on Microalgal Growth , 2012 .

[86]  Michael K. Danquah,et al.  Microalgae bioengineering: From CO2 fixation to biofuel production , 2011 .

[87]  Y. Bashan,et al.  Amendment of degraded desert soil with wastewater debris containing immobilized Chlorella sorokiniana and Azospirillum brasilense significantly modifies soil bacterial community structure, diversity, and richness , 2013, Biology and Fertility of Soils.

[88]  Zhiyou Wen,et al.  Development of an attached microalgal growth system for biofuel production , 2009, Applied Microbiology and Biotechnology.

[89]  Y. Bashan,et al.  Microalgae growth-promoting bacteria as "helpers" for microalgae: a novel approach for removing ammonium and phosphorus from municipal wastewater. , 2004, Water research.

[90]  Y. Ghasemi,et al.  Effect of alginate structure and microalgae immobilization method on orthophosphate removal from wastewater , 2012, Journal of Applied Phycology.

[91]  Y. Comeau,et al.  Phosphorus budget as a water quality management tool for closed aquatic mesocosms. , 2002, Water research.

[92]  J. Benemann,et al.  Bioremoval of heavy metals by the use of microalgae. , 1993, Biotechnology advances.

[93]  Wang TzuYen,et al.  Use of anthropic acclimated Spirulina platensis (Arthrospira platensis) bio-adsorption in the treatment of swine farm wastewater. , 2013 .

[94]  R. Muñoz,et al.  Efficient nutrient removal from swine manure in a tubular biofilm photo-bioreactor using algae-bacteria consortia. , 2008, Water science and technology : a journal of the International Association on Water Pollution Research.

[95]  T. Franco,et al.  Microalgae as feedstock for biodiesel production: Carbon dioxide sequestration, lipid production and biofuel quality , 2010 .

[96]  C. Howe,et al.  Life-Cycle Assessment of Potential Algal Biodiesel Production in the United Kingdom: A Comparison of Raceways and Air-Lift Tubular Bioreactors , 2010 .

[97]  X. Miao,et al.  High quality biodiesel production from a microalga Chlorella protothecoides by heterotrophic growth in fermenters. , 2006, Journal of biotechnology.

[98]  Paul Chen,et al.  Local bioprospecting for high-lipid producing microalgal strains to be grown on concentrated municipal wastewater for biofuel production. , 2011, Bioresource technology.

[99]  Yinghua Lu,et al.  Characterization of sodium cellulose sulphate/poly-dimethyl-diallyl-ammonium chloride biological capsules for immobilized cultivation of microalgae , 2013 .

[100]  W. Oswald,et al.  Biological transformation of solar energy. , 1960, Advances in applied microbiology.

[101]  R. Wijffels,et al.  An Outlook on Microalgal Biofuels , 2010, Science.

[102]  P. Qian,et al.  Integrated cultivation of the red alga Kappaphycus alvarezii and the pearl oyster Pinctada martensi , 1996 .

[103]  I. Kapdan,et al.  Batch kinetics of nitrogen and phosphorus removal from synthetic wastewater by algae , 2006 .

[104]  D. Turpin.  EFFECTS OF INORGANIC N AVAILABILITY ON ALGAL PHOTOSYNTHESIS AND CARBON METABOLISM , 1991 .

[105]  B. Volesky.  Advances in biosorption of metals: selection of biomass types. , 1994, FEMS microbiology reviews.

[106]  Paul Lessard,et al.  Biotreatment of fish farm effluents using the cyanobacterium Phormidium bohneri , 1998 .

[107]  J. Vermaat,et al.  The relative importance of Lemna gibba L., bacteria and algae for the nitrogen and phosphorus removal in duckweed-covered domestic wastewater , 1998 .

[108]  C. Pérez-Martínez,et al.  Growth and nutrient removal in free and immobilized planktonic green algae isolated from pig manure , 2004 .

[109]  Keat-Teong Lee,et al.  Microalgae biofuels: A critical review of issues, problems and the way forward. , 2012, Biotechnology advances.

[110]  M. Ishida,et al.  Immobilization of Prototheca zopfü in calcium-alginate beads for the degradation of hydrocarbons , 1998 .

[111]  Jo‐Shu Chang,et al.  Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: a critical review. , 2011, Bioresource technology.

[112]  M. Pilar Sánchez-Saavedra,et al.  Growth and removal of nitrogen and phosphorus by free-living and chitosan-immobilized cells of the marine cyanobacterium Synechococcus elongatus , 2009, Journal of Applied Phycology.

[113]  A. Olabi,et al.  Optimization of mechanical pre-treatment of Laminariaceae spp. biomass-derived biogas , 2014 .

[114]  F. G. Acién,et al.  Tubular photobioreactor design for algal cultures. , 2001, Journal of biotechnology.

[115]  T. Lebeau,et al.  Biotechnology of immobilized micro algae: a culture technique for the future? , 2006 .