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Evaluation of Neochloris Oleoabundans As Sustainable Source of Oil‑Rich Biomass

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Evaluation of Neochloris Oleoabundans As Sustainable Source of Oil‑Rich Biomass Brazilian Journal of Chemical Engineering (2020) 37:41–48 https://doi.org/10.1007/s43153-020-00011-3 ORIGINAL PAPER Evaluation of Neochloris oleoabundans as sustainable source of oil‑rich biomass Ivan A. Avila‑León1 · Marcelo C. Matsudo2 · Lívia S. Ferreira‑Camargo3 · Juliana N. Rodrigues‑Ract1 · João C. M. Carvalho1 Received: 15 July 2019 / Revised: 24 September 2019 / Accepted: 11 November 2019 / Published online: 3 February 2020 © Associação Brasileira de Engenharia Química 2020 Abstract In microalgae biotechnology, several strategies have been used aiming to increase biomass productivity and oil content, for example, by exploring novel bioreactor design and cultivation techniques. In the present study, the infuence of stressing agents (sodium thiosulphate, sodium chloride, and glycerol), under nitrogen starvation, were evaluated for lipid accumulation in Neochloris oleoabundans. Additionally, diferent light regimes and the use of LED were also evaluated. The results showed that sodium thiosulfate, glycerol, and sodium chloride addition resulted in a reduction in biomass concentration, but, at the same time, an increase in lipid content. 2.5 mM of sodium thiosulfate provided the highest percentage of lipid content up to 44.7%. In a tubular photobioreactor, despite the twofold increase in biomass concentration, there was a decrease in lipid content, compared with cultures in Erlenmeyer fasks. Also, the use of white LED in combination with traditional fuorescent lamp (12 h:12 h) could efciently replace 24 h light with fuorescent lamp for producing oil-rich N. oleoabundans biomass. Keywords Microalgae · Lipid · Bio-oil · Biomass · Biofuel Introduction high amounts of lipid, that could be converted to biodiesel (Pandey 2017). Taking into account the unprecedented global energy crisis, Inside the cell, fatty acids and other lipids are essential mainly related to fossil fuel exhaustion, several research- constituents that have important functions, such as structural ers around the world are looking for alternative sources of components of biological membranes, nutrients storage, and renewable energy, mainly in those countries without con- energy production (Gurr et al. 2002; Guschina and Harwood ventional fuel resources. In this scenario, microalgal bio- 2013a, b). This cell lipid content can be increased by using technology seems to have high potential for biodiesel pro- biotechnological approaches that will result in values much duction (Huang et al. 2010; Chen et al. 2018). Microalgae higher than that observed in plants used for the production may be considered as an important alternative source of of biodiesel, like soybean and oil palm (Chisti 2008). Other biofuel, since some of their species are able to accumulate advantages of microalgae are: the fast growth that results in high biomass productivities in comparison with plants; possibility of cultivation in various environment conditions, * João C. M. Carvalho including non-arable land; and non-potable water may be [email protected] employed, even municipal or industrial wastewater (Gouveia and Oliveira 2009; Benedetti et al. 2018; Chen et al. 2018). 1 Department of Biochemical and Pharmaceutical Technology, Faculty of Pharmaceutical Sciences, University of São Despite the thousands of known microalgae species, only Paulo, Av. Prof. Lineu Prestes 580, Bl. 16, São Paulo, a few of them have been employed for commercial produc- SP 05508-900, Brazil tion, such as Arthrospira (Spirulina) platensis, Chlorella 2 Institute of Natural Resources, Federal University vulgaris, Dunaliella salina, and Haematococcus pluvialis of Itajubá, Av. Benedito Pereira dos Santos, 1303, Itajubá, (Mobin and Alam 2017). Oil producing algae may be found MG 37500-903, Brazil in diverse taxonomic groups, with varied total lipid content 3 Center of Natural and Human Sciences, Federal University in diferent species or strains. Most of the species studied of ABC, Av. dos Estados, 5001 Bl. B, Santo André, up to date belong to the green algae group, mainly because SP 09210-580, Brazil 1 3 Vol.:(0123456789) 42 Brazilian Journal of Chemical Engineering (2020) 37:41–48 they are ubiquitous in varied habitats, can be easily isolated, Bench scale tubular photobioreactor and generally show better growth under artifcial conditions (Hu et al. 2008). Considering the runs in Erlenmeyer fasks, a scaling up In the present study, Neochloris oleoabundans was cul- to a tubular photobioreactor was performed to reproduce tivated in a bench scale tubular photobioreactor, with the the best results. aim of increasing cellular lipid content by evaluating the The tubular photobioreactor was built at the Laboratory addition of diferent components in the cultivation medium. of microalgal biotechnology at the University of Sao Paulo. Additionally, light emitting diode (LED) was evaluated as It is made of transparent glass tubes (internal diameter of energy source for oilirich microalgal biomass. 1.0 cm), with an inclination of 2%, connected by silicone tubes, and with a total volume of 3.5 L. In the lower part of the reactor, there is a Y shaped connector allowing the addition of pressurized air, which propels cells upwards Materials and methods to a fask that also act as degasser (Carlozzi and Pinzani 2005; Ferreira et al. 2012). A 0.2 µm flter membrane was Microorganism employed for sterilizing pressurized air. Fluorescent lamps (20 W) were used for providing a continuous light intensity The strain N. oleoabundans UTEX 1185 was acquired from of 60 µmol photons m−2 s−1. Room temperature was set at the UTEX Culture Collection of Algae. It was maintained in 25 ± 2 °C. pH values were maintained at 7.5 ± 0.3 with the BOLD 3N medium with 2% agar (UTEX n.d.). use of a solenoid valve coupled to a METTLER TOLEDO For inoculum preparation, N. oleoabundans was culti- M300 device, which monitored the culture pH with an elec- vated in 500 mL Erlenmeyer fasks containing 200–300 mL trode. When the medium pH increased, the solenoid valve of BOLD Standard medium (UTEX n.d.), previously auto- allowed CO2 to enter the photobioreactor. claved at 121 °C for 30 min. The culture was maintained Considering previous results, nitrogen was added dur- in an orbital shaker at 12 RPM, light intensity of 33 µmol ing the cultivation by a fed-batch process in accordance photons m−2 s−1 (with the use of 40 W fuorescent lamps), with daily productivity (Ávila-Leon 2014). and 25 °C (Tornabene et al. 1983). Additional cultivations were carried out with the aim of reducing energy consumption, by evaluating 12:12 h light/dark cycles or replacing 12 h dark regime by 12 h Cultivations for increasing oil content in N. illumination with red and white LED. Light inten- oleoabundans sity was 20 ± 2 µmol photons m−2 s−1 for red LED and 15 ± 2 µmol photons m−2 s−1 for white LED. Diferent compounds were evaluated for promoting an envi- ronmental stress condition for N. oleoabundans: sodium thi- osulfate (Na2S2O3), for increasing reducing power; sodium Analytical techniques chloride for increasing osmolarity (Table 1). Additionally, glycerol was used for providing a complementary organic Biomass concentration was measured by turbidimetry in a carbon source. spectrophotometer (FEMTO 700 Plus) at 495 nm, by using These cultivations were performed in 500 mL Erlen- a calibration curve correlating absorbance and biomass con- meyer fasks containing 350 mL of sterilized BOLD medium centration (dry weight; mg L−1) (Leduy and Therien 1977). (3N:3P) (UTEX) (Ávila-Leon 2014). Cultures were main- At the end of the cultivation, N. oleoabundans biomass tained at 25 ± 2 °C, 60 ± 5 µmol photons m−2 s−1, with the was harvested by centrifugation, washed with distilled addition of sterilized air. water, and dried at 55 °C for 12 h (Pelizer et al. 1999). Dried biomass was macerated and kept at 4 °C before the Table 1 Addition of diferent compounds for increasing lipid content biochemical composition analysis. Total lipid content was determined by extrac- Compound Final concentration Additional run (mM) tion with organic solvents. In a Soxhlet extractor chloroform:methanol (2:1 v/v) was refuxed until the liquid Sodium thiosulfate 1.2 2.5 3.8 Middle of exponential became clear (Piorreck et al. 1984; Olguín et al. 2001). growth Total protein content was determined by the Kjeldahl End of exponential method, considering 6.25 as the conversion factor from growth total nitrogen content (Association of Ofcial Analytical Sodium chloride 1.0 2.2 4.5 – Chemists 1984). Glycerol P.A 340 680 1020 1360 – 1 3 Brazilian Journal of Chemical Engineering (2020) 37:41–48 43 Fatty acids content was determined by frst extracting the lipid by the Soxhlet method. The lipid was recovered with petroleum ether, and the fatty acids were converted to the corresponding methyl esters (Hartman and Lago 1973). The analysis of fatty acid methyl ester was performed in a gas chromatograph (Agilent Model 7890 CX) in accordance with Rodrigues-Ract and Gioielli (2008) and Pérez-Mora et al. (2016), in which the components identifcation was performed by comparing their retention time with the stand- ard 37 FAME mix (Supelco). Fig. 1 Infuence of diferent concentrations of sodium thiosulfate Results and discussion (Na2S2O3) on maximum biomass concentration (Xm), lipid content, and protein content in Neochloris oleoabundans cultivated in Erlen- meyer fasks Cultivations in Erlenmeyer fasks: addition of sodium thiosulfate 2.5 mM (3.8 mM), sodium thiosulfate seems to inhibit cell In a frst cultivation, 2.5 mM (Mandal and Mallick 2009) of growth (546 ± 127.5 mg L−1) with a decrease of 10.5% sodium thiosulfate was added on the 7th (middle of expo- in lipid content, in comparison with the cultivation with nential growth) or the 10th day of cultivation (fnal of expo- 2.5 mM. nential growth), and the results are presented in Table 2. Single addition of 2.5 mM sodium thiosulfate, in the mid- Cultivations in Erlenmeyer fasks: addition dle of exponential growth (7th day) helped to improve lipid of glycerol accumulation, but it slightly reduced biomass concentration, in comparison with the control run (without sodium thiosul- In Fig.
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