Bioresource Technology 187 (2015) 255–262

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Harvesting green algae from eutrophic reservoir by electroflocculation and post-use for biodiesel production Enrique Valero a, Xana Álvarez a,⇑, Ángeles Cancela b,1, Ángel Sánchez b,1 a AF4 Research Group, Department of Natural Resources and Environment Engineering, Forestry Engineering College, University of Vigo, Campus A Xunqueira s/n, 36005 Pontevedra, Spain b Chemical Engineering Department, Industrial Engineering College, University of Vigo, Campus Lagoas-Marcosende s/n, 36310 Vigo, Pontevedra, Spain

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 Harvesting by electroflocculation is

effective with green algae mixture in freshwater.  Cyanobacterial blooms can be solvent without fluvial ecosystem damage.  A real pilot plant can be design from these results.

a r t i c l e

i n f o

Article history: Received 2 February 2015 Received in revised form 27 March 2015 Accepted 29 March 2015 Available online 1 April 2015 Keywords: Microcystis sp. Scenedesmus spp. Kirchneriella sp. Cyanobacterial blooms Biodiesel

a b s t r a c t Each year there are more frequent blooms of green algae and cyanobacteria, representing a serious environmental problem of eutrophication. Electroflocculation (EF) was studied to harvest the algae which are present in reservoirs, as well as different factors which may influence on the effectiveness of the process: the voltage applied to the culture medium, run times, electrodes separation and natural sedimentation. Finally, the viability of its use to obtain biodiesel was studied by direct transesterification. The EF process carried out at 10 V for 1 min, with an electrode separation of 5.5 cm and a height of 4 cm in culture vessel, obtained a recovery efficiency greater than 95%, and octadecenoic and palmitic acids were obtained as the fatty acid methyl esters (FAMEs). EF is an effective method to harvest green algae during the blooms, obtaining the greatest amount of biomass for subsequent use as a source of biodiesel. Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction The eutrophication process is a specific consequence of water pollution caused by the increase of nutrients, particularly phosphorus and nitrogen (Paerl et al., 2011; Khan et al., 2014). The increase of these nutrients allows the algae population to improve their ⇑ Corresponding author. Tel.: +34 986 801959. E-mail addresses: [email protected] (E. Valero), [email protected] (X. Álvarez), [email protected] (Á. Cancela), [email protected] (Á. Sánchez). 1 Tel.: +34 986 81383. http://dx.doi.org/10.1016/j.biortech.2015.03.138 0960-8524/Ó 2015 Elsevier Ltd. All rights reserved.

growth and development, especially when weather conditions are favorable such as temperature (Xue et al., 2005) and solar radiation (Liu et al., 2011). All this leads to algal blooms, affecting the coloration of the water, especially when green algae are present, and implying a negative impact on the ecosystem of rivers, lakes, reservoirs, etc. (Smith, 2003), as well as some alterations in the physical–chemical conditions (Alvarez Cobelas and Arauzo, 1994; Lee et al., 2012). Nowadays, eutrophication is one of the effects triggered by the population growth and economic development (Khan et al., 2014) affecting 53% of lakes and reservoirs in Europe (ILEC, 1994). For this

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reason and the implications that it involve, water managers and the proper authorities on issues of nature conservation are concerned about how to solve this phenomenon, specifically if we take into account that in many algal blooms and eutrophication processes there are toxic cyanobacteria, whose environmental effects are worse, even to human health (Kim et al., 2010; Xuguang et al., 2011), as is the case of Microcystis sp., which has not solution when bloom occurs. One possible solution is to harvest algae from the medium (lakes, reservoir, estuaries, coasts, etc.). There are several methods of harvesting algae such as sedimentation, this method of particle separation is popular in wastewater treatment, and is relatively inexpensive to install and operate and it does not require specialized operations (Timmons et al., 2002). According to Pienkos and Darzins (2009) centrifugation is very expensive in an integrated system producing lower-value products, such as algal oils for biofuel production. There are several recent studies in others techniques such as the coagulation, flocculation, electrocoagulation and electroflocculation process, such as the research of Matos et al. (2013), who studied Electrocoagulation as a process to harvest the marine Nannochloropsis sp. microalga; Wang et al. (2012) investigated the combination of algaecide and flocculants to control cyanobacterial blooms. Some researchers have separated microalgae by electroflocculation, such as Xu et al. (2010) who developed an electroflocculation technology for harvesting microalgae (Botryococcus braunii). Lee et al. (2013) concluded in their study that electroflocculation is potentially a low cost Tetraselmis sp. microalgal harvesting technique; and Alfafara et al. (2002) who combined the electroflocculation with electrocoagulation. Highlight the researched carried out by Liang et al. (2008) who tried to eliminated the microcystin-LR during the cyanobacterial inactivation by electooxidation, obtaining more than 98% removal for total. On the other hand, the microalgae are been recognized as a source for obtaining biodiesel (Phukan et al., 2011) and the transesterification represents a key process for biodiesel production (Griffiths et al., 2010). Particularly, vegetable oils, after transesterification with methanol produce fatty acid methyl ester (FAME) as the precursor to biodiesel and glycerol as a by-product (Demirbas and Demirbas, 2010). Recent studies carried out by the Regional Government of Galicia concluded that there are eutrophication and algae blooms in A Baxe reservoir (Augas de Galicia, 2011). The aim of this research is to harvest the green algae without damage to the ecosystem. This means that chemical flocculants, which remain in the aquatic ecosystem affecting the organisms that inhabit, cannot be used. The electroflocculation technique (EF) was selected to apply it separately and without affect natural water composition. Therefore, in this investigation the microalgae present in water samples from ‘‘A Baxe’’ reservoir (with no isolated strains) have been cultivated. Different factors which may influence the effectiveness of the process were evaluated, specifically, the voltage applied, runs, distance between electrodes and the height of the culture column, as well as EF/gravity sedimentation effectiveness at different temperatures. Finally, the algae harvested in this process have been used as a direct source for the biodiesel production, for alae valorisation.

2. Methods 2.1. Microalgae Water samples collected in March of 2014 from the ‘‘A Baxe’’ reservoir (Umia River, Northwest of Spain) were used in the study.

The microalgae were grown in a medium with two different solutions: one of macronutrients (NaNO3, KH2PO4, MgSO47H2O and Na2CO3) and the second solution was micronutrients (MgCl26H2O, CaCl22H2O, H3BO3, MnCl24H2O, ZnCl2, FeCl36H2O, CoSO47H2O, Na2MoO42H2O, CuSO45H2O and Na2EDTA2H2O) provided by the ECIMAT (Estación de Ciencias Mariñas de Toralla, University of Vigo, Spain). The experimental work was carried out in six 250 ml Erlenmeyer flasks. The microalgae from the reservoir were grown for 20 days at 28 °C, with constant stirring (Magnetic Mini-Stirrer 220/230 V) and a light cycle of 24:0 Light/ Dark. There were three different algae growing together: Scenedesmus spp. (24%), Kirchneriella sp (1%). and Microcystis sp. (75%). Cultures raised to a density of 106 cell ml1. 2.2. Harvesting by electroflocculation The EF experiments were performed with a power source (DC Power Supply, FREAK EP-603) in three different vessels (1000; 250 and 150 ml) with a wall thickness of 2 mm. Different factors that could influence the process of collecting the algae by EF were evaluated: (1) separation of iron electrodes (Lee et al., 2013). The distance between the two electrodes was varied in order to evaluate which is the most effective for harvesting green algae. To this purpose, the height of the culture column was kept constant (4 cm). (2) The column height of culture (h), (3) natural sedimentation, (4) application of different current applied (Ilhan et al., 2008; Vandamme et al., 2011), and (5) run times of the electric current (Matos et al., 2013). Measurement runs have been made three times each. For specific details of each process see Figs. 1–3. As was carried out each EF processes, the decisions were made based on the best results obtained in the previous process. The most efficient separation between electrodes (Test No. 1) was chosen and fixed for the next tests where the effect of the height of the culture column were evaluated (Test No. 2). For this reason, subsequent experiments were carried out with the best results obtained in previous test. The iron electrode plate had an area of 2  9 cm and a thickness of 2 mm. Two iron electrode plates were placed along two opposite walls in the vessels and were submerged 7 cm. When these kinds of electrodes are used, the following reactions occur (Ilhan et al., 2008): At the cathode

2H2 O þ 2e ! H2 þ 2OH and at the anode

FeðsÞ ! Fe2þ þ 2e The distance between cathode and anode was studied during the process of EF number 1 (Fig. 1) and it varied depending on the vessels used. In the second test, different water column heights were evaluated through the variation of culture volumes according to Fig. 2. The influence of different electric current intensities, as well as the natural sedimentation of algae without electricity were evaluated at 8 and 22 °C. On the other hand, different run times of this electric current were assessed in the third test (Fig. 3). 2.3. Microalgae biomass characterisation Cell growth was measured by means of absorbance of the suspension at 690 nm in accordance to Becker (1994) with a digital spectrophotometer Spectro 22 (Labomed, USA). Correlations between absorbance and cell concentration were previously established by a polynomial equation as:

y ¼ 0:0011x2 þ 0:0113x  0:012 ðR2 ¼ 0:9991; P < 0:05Þ

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Fig. 1. Process carried out in tests by EF algae harvesting, evaluating different distances between the iron electrodes, with a culture column height of 4 cm, 10 V for 1 min.

Fig. 2. Process carried out in tests by EF algae harvesting, evaluating different culture column height, with 5.5 cm of separation between electrodes, 10 V for 1 min.

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Fig. 3. Process carried out in tests by EF algae harvesting, evaluating different values of voltage applied to the cultures, and with different run times, comparing it with the natural sedimentation of the algae (without EF).

where y (g ml1) is the cell concentration measured in 106 cells per ml and x is the absorbance. On the other hand, the absorbance was determined in the medium surface at the beginning of the experiment (before applying the EF), as well as in the vessels of the three experiments, for each variable studied, after applying the EF. In this last case, vessels were left standing to allow the concentration of the microalgae in different times after each experience. The samples were taken below the medium surface to measure the concentration in clean water. The algae were identified microscopically (BX 51, Olympus, Japan). 2.4. Electroflocculation effectiveness The effectiveness of EF was determined by the recovery efficiency (RE) which is defined as the ratio of the recovered biomass to the total biomass (Vandamme et al., 2011; Lee et al., 2013) and is determined by: RE = (Abs0  Absst)/Abs0; where Abs0 is the absorbance of t suspension before the EF treatment and Absst is the absorbance at the chosen sedimentation time (st) after EF treatment. 2.5. Direct transesterification In this experiment a direct transesterification of algae (Wahlen et al., 2011) was carried out. The algae were dried at 90 °C until the weight of samples remained constant, them were mixed with

methanol (12:1 vol methanol/wt dried algae) according to Cancela et al. (2012), and sodium hydroxide (1% g NaOH/g algae) at 62 °C during 3 h in a reactor. This sample was mixed with the internal standard C17-ME for subsequent analysis by gas chromatography. The composition and quantity of methyl ester in biodiesel was determined according to biodiesel test method UNE-EN ISO 14103:2003. 2.6. Statistical analysis Mean and standard deviation values for the recovery efficiency were calculated for each test three times. Kruskal–Wallis test for the resulting differences were calculated (electrode separation, height of the culture column, volts and runs) and the Mann– Whitney test for the natural sedimentation differences. Statistical analysis was performed using SPSS Statistics v19 (SPSS, Inc., and IBM Company1989, 2010). 3. Results and discussion 3.1. Effect of electrodes On increasing electrode distance (max. 11 cm) the EF process is more effective (Fig. 4), this result was found also by Crespilho and Rezende (2004). This was checked by measuring the absorbance of the surface water, these data show that the lowest concentration of algae was during the first two hours (after EF), with more than 32%

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and 43% of reduction of algal concentration respectively (Table 1), therefore, the algae were sediment at the bottom of the vessels. Although, absorbance values did not show statistically significant differences between distinct values of electrodes separation (X2 = 0.218; p = 0.897). As time goes, and the algae sediment, the most effectiveness results (95%) occurred with a smaller electrode separation (5.5 cm) after 24 h. This was 2.61% more effective than with an electrode separation of 7 cm, and 3.15% than 11 cm separation (Table 1). The greater the electrode distance, the greater should the difference in applied potential be (Cerqueira et al., 2009). Finally, 5.5 cm was the best separation between electrodes because it allowed the sedimentation of the whole alae mass. Ilhan et al. (2008) concluded that Al electrodes showed a higher treatment efficiency than Fe ones, with a rate of removals of 56% and 35% respectively. In addition, Cerqueira et al., (2009) concluded that the distance between the aluminum electrodes did not cause a significant increase in the removal efficiency of contaminants, while the distance between iron electrodes influenced the EF process. Although the most advantageous results of the aluminum, in this investigation iron electrodes were used instead of the first ones because aluminum has been associated with alterations in biological systems, especially fish, and its implications in the development of neurodegenerative diseases (RondonBarragán et al., 2007). 3.2. Effect of the height of the culture column Experimental results show that better electrodes distance is 5.5 cm. For this reason, experiments described below were made with this value. When the height of the culture column changes, the higher effectiveness of the separation method corresponds to the height of 2.7 cm. The absorbance measures can conclude that the concentration of algae was lower when the culture column was reduced. The culture height is approximately a 2% more efficient, when is compared with the other levels (5.2 and 6.4 cm) at the end of the EF process, as can be seen in Table 1. These values indicate that the differences were not statistically significant (X2 = 0.353; p = 0.838). Furthermore, it can be concluded that with a culture height of 4 cm the EF effectiveness was higher than in the tests with 2.7 cm. Therefore, the subsequent tests were performed with a culture column height of 4 cm and an electrode separation of 5.5 cm.

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3.3. Effect of voltage The algae recovery efficiency reached over 90% at all electrical powers tested, but the best results in the sedimentation of algae were obtained with 10 V (95.61%) as shown in Fig. 5. The lower effectiveness of EF was obtained with 20 V (94.37%). Very similar values were also obtained in the case of 15 V with 94.58%. The results of the Kruskal–Wallis test were not statistically significant (X2 = 0.067; p = 0.967). Since the electric current is applied, the process is more effective with voltages of 15 and 20 V. Xu et al. (2010) tested various voltages and concluded that the EF time was shortened significantly when the voltage was increased, which is in line with our experiments. In the case of 10 V, after 60 min the efficiency was reversed to better results, which is according with the results showed in this research, Xu et al. (2010), who obtained greater efficiency in the first minutes of the sedimentation process. The applied current is also an important variable in the EF process (Vandamme et al., 2011), as a result, higher electrical power produced more flocculants to enhance algal flocculation (Alfafara et al., 2002). All these results, as well as those obtained during the sedimentation time are summarized in Table 1.

3.4. Effect of the run times As discussed earlier, best results in the performed test were obtained with 10 V. This is why, to assess the effect of run times of electric current in the separation of algae from the water, experiments were carried out with 10 V. The concentration of algae after the test was always lower when we applied 3 min of 10 V, although there were not statistic differences (X2 = 0.067; p = 0.967). This happened from the first time of the separation process to 24 h later, when the last values were measured. Emphasize that after an entire day, the results between 1 and 3 min only differed on 0.07%.

3.5. Effect of temperature in natural sedimentation At ambient conditions (22 °C in the laboratory at the moment of the study), natural sedimentation is more effective than at 8 °C without statistical differences (U = 32.000; p = 0.489). This effectiveness exceeds 0.58% in the case of cold setting (8 °C). But in

Fig. 4. Mean absorbance values of different separation electrode (3 replicates in each test).

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the first 60 min, the difference between both conditions was 3.14% of RE. Comparing the results obtained in the process of natural sedimentation (8 and 22 °C), i.e. without movements of the samples and without EF, less effectiveness was obtained after 24 h in the first case, approximately 10% less than other processes (Table 1). But results after 60 min show an efficiency of more than 74%. To achieve this efficiency in the other tests it took 3 h.

and higher recovery values with several freshwater chlorophyte species by coagulation. Mixson et al. (2014) achieved more that 95% of biomass recovery when they harvested (Dunaliella viridis) via pH-induced flocculation and via indirect electrocoagulation, and more than 99% when hollow fiber filtration was used. On the other hand, Nannochloropsis sp. was recovered by electrocoagulation and the best recovery (>97%) was obtained using a current density of 8.3 mA/cm2 over 10 min (Matos et al., 2013). Although the algae studied were different, it can be considered that the results were similar to those obtained in this investigation. Research conducted by Alfafara et al. (2002) who studied the Microcystis sp., concluded that electro-flotation alone is not efficient but the combination of electro-flocculation and electro-flotation causes >90% removal of it.

3.6. Comparison between EF and other algae harvesting method Others where processes, such as electrocoagulation, coagulation, etc.; were tested too. This research reaches higher RE values than those obtained by Granados et al. (2012), who found 90%

Table 1 Mean electroflocculation effectiveness in % [determined by: RE = (Abs0  Absst)/Abs0] and standard deviation of different tests carried out varying: (a) the electrode separation and the height of the culture column. (b) The variation of voltage and the run times at different times of EF treatment, as well as natural sedimentation at different temperatures. (n = 3 for each electrode separation and for each time.) Time (min)

Electrode separation (cm) 5.5

(a) 20 40 60 120 180 300 360 1260 1440 Time (min)

(b) 20 40 60 120 180 300 360 1260 1440

Height of the culture column (cm)

7

11

2.7

5.2

6.4

Mean RE

SD

Mean RE

SD

Mean RE

SD

Mean RE

SD

Mean RE

SD

Mean RE

SD

28.120 35.160 40.470 60.910 70.520 78.330 85.320 93.000 95.610

0.018 0.015 0.009 0.015 0.030 0.032 0.012 0.009 0.023

25.790 34.670 39.370 58.980 65.160 75.980 84.230 92.040 93.000

0.017 0.041 0.047 0.032 0.015 0.015 0.020 0.011 0.022

32.780 37.770 43.350 70.040 75.360 81.110 88.520 92.040 92.460

0.009 0.041 0.033 0.044 0.043 0.029 0.026 0.011 0.013

27.680 35.440 39.850 57.380 70.670 78.670 84.960 91.250 94.550

0.019 0.014 0.003 0.015 0.041 0.042 0.036 0.033 0.041

26.330 35.150 38.220 56.130 59.510 73.330 82.330 90.260 92.120

0.022 0.027 0.017 0.042 0.004 0.021 0.009 0.017 0.028

30.860 34.080 36.990 52.330 54.910 69.450 81.120 89.650 92.000

0.025 0.007 0.035 0.005 0.018 0.034 0.037 0.024 0.033

Volts (V)

Run times at 10 V (min)

10

15

20

1

Natural sedimentation

2

3

8 °C

22 °C

Mean RE

SD

Mean RE

SD

Mean RE

SD

Mean RE

SD

Mean RE

SD

Mean RE

SD

Mean RE

SD

Mean RE

SD

28.12 36.77 40.47 60.91 70.52 78.33 85.32 93.00 95.61

0.008 0.006 0.019 0.029 0.034 0.025 0.017 0.033 0.027

26.74 39.17 45.68 58.52 68.56 76.15 86.15 91.25 94.58

0.031 0.042 0.031 0.005 0.015 0.028 0.019 0.046 0.019

31.03 37.45 42.36 58.28 68.00 75.95 81.76 90.99 94.37

0.009 0.017 0.036 0.022 0.013 0.030 0.014 0.026 0.031

28.12 34.67 40.47 60.91 70.52 78.33 85.32 93.00 95.61

0.040 0.033 0.019 0.012 0.015 0.006 0.017 0.033 0.041

44.80 38.85 56.38 68.78 72.49 78.77 86.34 90.12 93.19

0.041 0.032 0.019 0.022 0.031 0.019 0.018 0.033 0.041

45.29 38.44 55.45 68.28 75.03 79.26 88.60 91.29 95.54

0.013 0.018 0.003 0.040 0.034 0.017 0.016 0.033 0.029

17.35 46.08 70.98 71.49 73.40 76.54 80.44 82.14 84.71

0.013 0.009 0.009 0.029 0.033 0.049 0.019 0.037 0.029

13.92 52.94 74.12 74.85 77.11 79.38 82.97 83.56 85.29

0.038 0.016 0.041 0.022 0.050 0.009 0.012 0.037 0.027

Fig. 5. Mean absorbance values of different voltage (3 replicates in each test).

E. Valero et al. / Bioresource Technology 187 (2015) 255–262 Table 2 Fatty acid methyl esters in the biodiesel. Fatty acid methyl ester

Retention times (min)

Relative content (%)

Palmitic acid (C16) Octadecenoic acid (C18:1)

22.61 25.56

42.8 57.2

Many researchers have developed techniques for growing and harvesting algae for further use as biodiesel, many of them are summarized in the review conducted by Chen et al. (2011) where an analysis of the latest research is made up to 2011. Moreover, Ofir et al. (2007) compared EF and chemical flocculation for preprocess in wastewater treatment. Many other lines of research tested this method for the treatment of industrial wastewater (Zongo et al., 2009). While in the present study, the aim of harvesting the algae is a solution to an environmental problem which affects fluvial ecosystems. The goal has been to demonstrate that EF techniques can reduce the eutrophication of reservoirs as well as algae blooms that take place in them. If this technique were combined with preventive measures such as river restoration (Valero et al., 2014), it will be possible to reduce algal blooms, and even control them. 3.7. Direct transesterification FAME composition of algae after the transesterification reaction is shown in Table 2. Octadecenoic acid methyl ester and Palmitic acid methyl ester were the components of green algae growing in the reservoir under study and are also the most abundant in other microalgae species (Tang et al., 2011). The fatty acid profile for the FAMEs obtained from Microcystis sp., Scenedesmus spp. and Kirchneriella sp. were abundant in unsaturated fatty acids (Dijkstra, 2006). Therefore, the green algae that have been harvested in the reservoir could be used as a source of biodiesel, and translate this process to a real-scale one, as has been recently studied in European coasts (Blaas and Kroeze, 2014). 4. Conclusions Considering that the eutrophication and the blooms of algae and cyanobacteria take place in fluvial ecosystems, the EF does not damage the environment, it is a suitable method. Consequently, it is possibility to develop a system based on this technique on a real scale. Therefore, as the blooms appears, the water could be recirculated to from the reservoir to an annexed area, treated by EF and returned to its natural place. This would not affect other organisms which have the same habitat. Finally, the harvested algae can be reused as biodiesel. Acknowledgement We thank Professor Martyn Rich (Language Centre, University of Vigo) for revising the English version. References Alfafara, C.G., Nakano, K., Nomura, N., Igarashi, T., Matsumura, M., 2002. Operating and scale-up factors for the electrolytic removal of algae from eutrophied lakewater. J. Chem. Technol. Biotechnol. 77 (8), 871–876. Alvarez Cobelas, M., Arauzo, M., 1994. Phytoplankton responses of varying time scales in a eutrophic reservoir. Ergebnisse der Limnologie 40, 69-69. Augas de Galicia. 2011. Plan Integral de Actuación sobre a Microcystis sp. no Encoro de Caldas de Reis no Río Umia. (PLAN UMIA). Becker, E.W., 1994. Measurement of algal growth. In: Microalgae Biotechnology and Microbiology. pp. 56–62. Blaas, H., Kroeze, C., 2014. Possible future effects of large-scale algae cultivation for biofuels on coastal eutrophication in Europe. Sci. Total Environ. 496, 45–53.

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