Abstract
A key aspect of the industrial development of microalgal production processes is the excessive cost of biomass production. A solution is a combination of biodiesel production and wastewater treatment. The microalga Scenedesmus has a high lipid content and a potential extracellular phenoloxidase activity, which could improve the phycoremediation of phenolic pollutants. In this work, the most suitable growth conditions to obtain this twofold aim were analyzed. First, different strains of Scenedesmus vacuolatus microalga were tested at different pH, salinity and CO2 concentration in the gas phase. The two most promising strains were then cultivated in autotrophic and heterotrophic conditions, and were investigated in terms of efficient nitrogen removal, fatty acid profile and maximized extracellular phenoloxidase activity in the medium. The results showed two extreme conditions: (1) biomass productivity doubled when photobioreactors were sparged with 5% CO2 supplemented air with respect to cultures sparged with air (the steady state values of strain 53 were 0.138 g L−1 day−1 in the presence of air, and 0.243 in the presence of CO2 addition), and N-starvation under 5% CO2enhanced the transesterified fraction of lipids (strain 53 FAME fraction in the presence of N-starvation was 33%, in the presence of nitrogen FAME fraction was 22%); (2) phenoloxidase activity was completely suppressed by presence of 5% CO2 in the gas phase (strain 53 0.21 U mL−1), indicating clear catabolite repression for the induction of this enzyme in the algal metabolism.
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Ajayan KV, Selvaraju M, Unnikannan P, Sruthi P (2015) Phycoremediation of tannery wastewater using microalgae Scenedesmus species. Int J Phytoremediation 17:907–916
Benavente-Valdés JB, Aguilar C, Contreras Esquivel JC, Méndez-Zavala A, Montañez J (2016) Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnol Rep 10:117–125
Busca G, Berardinelli S, Resini C, Arrighi L (2008) Technologies for the removal of phenol from fluid streams: a short review of recent developments. J Hazard Mater 160:265–288
Carbone DA, Gargano I, Pinto G, De Natale A, Pollio A (2017a) Evaluating microalgal attachment to surfaces: a first approach towards a laboratory integrated assessment. Chem Eng Trans 57:73–78
Carbone DA, Olivieri G, Pollio A, Pinto G, Melkonian M (2017b) Growth and biomass productivity of Scenedesmus vacuolatus on a twin layer system and a comparison with other types of cultivations. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-017-8515-y
Dev Goswami RC, Kalita MC (2011) Scenedesmus dimorphus and Scenedesmus quadricauda : two potent indigenous microalgae strains for biomass production and CO2 mitigation—a study on their growth behaviour and lipid productivity under different concentration of urea as nitrogen source. J Algal Biomass Util 2:42–49
Escapa C, Coimbra RN, Paniagua S, García AI, Otero M (2016) Comparative assessment of diclofenac removal from water by different microalgae strains. Algal Res 18:127–134
Fleeger JW, Carman KR, Nisbet RB (2003) Indirect effect of contaminants in aquatic ecosystem. Sci Total Environ 170:207–233
Gad NS, Saad AS (2008) Effect of environmental pollution by phenol on some physiological parameters of Oreochromis niloticus. Glob Vet 2:312–319
Gargano I, Olivieri G, Spasiano D, Andreozzi R, Pollio A, Marotta R, D’Ambrosio N, Marzocchella A (2015) Kinetic characterization of the photosynthetic reaction centres in microalgae by means of fluorescence methodology. J Biotechnol 212:1–10
Gargano I, Olivieri G, Andreozzi R, Marotta R, Marzocchella A, Pollio A (2016) Biodiesel production in outdoor cultures of Scenedesmus vacuolatus. Chem Eng Trans 49:397–402
Guillard RRL (1973) Methods for microflagellates and nanoplankton. In: Stein J (ed) Handbook of phycological methods. Cambridge University Press, Cambridge, pp 80–81
He Y, Zhou L, Xu X, Wang S, Wang C, Dai B (2014) Uniform design for optimizing biomass and intracellular polysaccharide production from self-flocculating Scenedesmus sp. Ann Microbiol 64(4):1779–1787
Hena S, Fatimah S, Tabassum S (2015) Cultivation of algae consortium in a dairy farm wastewater for biodiesel production. Water Resour Industry 10:1–14
Jácome Pilco CR, Cristiani Urbina E, Flores-Cotera LB, Velasco-García R, Ponce-Noyola T, Cañizares Villanueva R (2009) Continuous Cr(VI) removal by Scenedesmus incrassatulus in an airlift photobioreactor. Bioresour Technol 100:2388–2391
Jais NM, Mohamed RMR, Apandi WAMN, Peralta HMM (2015) Removal of nutrients and selected heavy metals in wet market wastewater by using microalgae Scenedesmus sp. Appl Mechanics Materials 773:1210–1214
Johannes C, Majchercsyk A (2000) Laccase activity tests and laccase inhibitors. J Biotechnol 78:193–199
Kirroliaa A, Bishnoia NR, Singhb N (2011) Salinity as a factor affecting the physiological and biochemical traits of Scenedesmus quadricauda. J Algal Biomass Util 2:28–34
Kong QX, Li L, Martinez B, Chen P, Ruan R (2010) Culture of microalgae Chlamydomonas reinhardtii in wastewater for biomass feedstock production. Appl Biochem Biotechnol 160:9–18
Li L, Xu F, Eriksson KEL (1999) Comparison of fungal laccases and redox mediators in oxidation of nonphenolic lignin model compound. J Appl Environ Microbiol 65:2654–2660
Mata TM, Martins A, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sustain Energy Rev 14:217–232
Michałowicz J, Duda W (2007) Phenols—sources and toxicity. Polish J Environ Stud 16:347–362
Olivieri G, Gargano I, Andreozzi R, Marotta R, Marzocchella A, Pinto G, Pollio A (2013) Effects of photobioreactors design and operating conditions on Stichococcus bacillaris biomass and biodiesel production. Biochem Eng J 74:8–14
Otto B, Schlosse D, Werner R (2010) First description of a laccase-like enzyme in soil algae. Arch Microbiol 192:759–768
Pacheco MM, Hoeltz M, Moraes MSA, Schneider RCS (2015) Microalgae: cultivation techniques and wastewater phycoremediation. J Environ Health Sci Eng 50:585–601
Paskuliakova A, Tonry S, Touzet N (2016) Phycoremediation of landfill leachate with chlorophytes: phosphate a limiting factor on ammonia nitrogen removal. Water Res 99:180–187
Pinto G, Pollio A, Previtera L, Temussi L (2002) Biodegradation of phenols by microalgae. Biotechnol Lett 24:2047–2051
Pinto G, Pollio A, Previtera L, Stanzione M, Temussi F (2003) Removal of low molecular weight phenols from olive oil mill wastewater using microalgae. BiotechLett 25:1657–1659
Piscitelli A, Giardina P, Mazzoni C, Sannia G (2005) Recombinant expression of Pleurotus ostreatus laccases in Kluyveromyces lactis and Saccharomyces cerevisiae. Appl Microbiol Biotechnol 69:428–439
Pollio A, Pinto G, Ligrone L, Aliotta G (1993) Effects of the potential allelochemical α-asarone on growth, physiology and ultrastructure of two unicellular green algae. J Appl Phycol 5:395–403
Rawat I, Ranjith Kumar R, Mutanda E, Bux F (2011) Dual role of microalgae: phycoremediation of domestic wastewater and biomass production for sustainable biofuels production. Appl Energy 88:3411–3424
Ren H, Liu B, Chao M, Lei Z, Ren N (2013) A new lipid-rich microalga Scenedesmus sp. strain R-16 isolated using Nile red staining: effects of carbon and nitrogen sources and initial pH on the biomass and lipid production. Biotech Biofuels 6:143–148
Riva S (2006) Laccases: blue enzymes for green chemistry. Trends Biotechnol 24:219–226
Sánchez JF, Fernández-Sevilla, JM, AciénFG, CerónMC, Pérez-Parra J, Molina-Grima E (2008) Biomass and lutein productivity ofScenedesmus almeriensis:influence of irradiance, dilution rate and temperature. Appl Microbiol Biotechnol 79:719–729
Sforza E, Grisa B, Carlos I, Farias S, Morosinotto T, Bertucco A (2014) Effects of light on cultivation of Scenedesmus obliquus in batch and continuous flat plate photobioreactor. Chem Eng Trans 38:211–216
Shih H, Chun Yen C, Jo Shu C (2012) Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresour Technol 113:244–252
Si L, Ruixue K, Lin S, Sifan L, Shuangchun Y (2013) Study on treatment methods of phenol in industrial wastewater. Int J Sci Res Sci Eng Technol 4:230–232
Silva HJ, Pirt SJ (1984) Carbon dioxide inhibition of photosynthetic growth of Chlorella. Microbiology 130:2833–2838
Strong PJ, Claus H (2011) Laccase: a review of its past and its future in bioremediation. Crit Rev Environ Sci Technol 41:373–434
Yen HW, Hu IC, Chen CY, Ho SH, Lee DJ, Chang JS (2013) Microalgae-based biorefinery: from biofuels to natural products. Bioresour Technol 135:166–174
Wasi S, Tabrez S, Ahmad M (2013) Toxicological effect of major environmental pollutants: an overview. Environ Monitor Assess 185:2585–2593
Zhang X, Luo S, Yang Q, Zhang H, Li J (1997) Accumulation of uranium at low concentration by the green alga Scenedesmus Obliquus 34. J Appl Phycol 1:65–71
Zhou GJ, Peng FQ, Zhang LJ, Ying GG (2012) Biosorption of zinc and copper from aqueous solutions by two freshwater green microalgae Chlorella pyrenoidosa and Scenedesmus obliquus. Environ Sci Pollut Res Int 19:918–929
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Carbone, D.A., Gargano, I., Chiaiese, P. et al. Scenedesmus vacuolatus cultures for possible combined laccase-like phenoloxidase activity and biodiesel production. Ann Microbiol 68, 9–15 (2018). https://doi.org/10.1007/s13213-017-1309-8
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DOI: https://doi.org/10.1007/s13213-017-1309-8