Cultivation of Spirulina Air Lift Photo Reactor

Biochemical Engineering Journal 32 (2006) 13–18

Cultivation of Spirulina platensis in a combined airlift-tubular reactor system Attilio Converti ∗ , Alessandra Lodi, Adriana Del Borghi, Carlo Solisio Department of Chemical and Process Engineering, University of Genoa, Via Opera Pia 15, 16145 Genoa, Italy Received 22 February 2005; received in revised form 5 July 2006; accepted 24 August 2006

Abstract This preliminary study aims at evaluating the efficiency of a bench-scale tubular photobioreactor by means of batch cultivations of Spirulina platensis under light-limited conditions. The most interesting feature of this plant configuration is the use of an airlift system for biomass re-cycling instead of traditional pumps to avoid the well-known problems of trichome damage owing to mechanical stress. A maximum cell concentration of 10.6 g l−1 was attained after 15 days of cultivation using a photosynthetic active radiation of 120 ␮mol photons m−2 s−1 . Although the system operated in laminar flow under all the conditions investigated in this study, excess thricome stress was prevented only at relatively low air flow rates (<4.5 l min−1 ), corresponding to culture speeds lower than 0.21 m s−1 . © 2006 Elsevier B.V. All rights reserved. Keywords: Tubular bioreactor; Spirulina platensis; Light intensity; Biomass growth; Culture speed

1. Introduction Spirulina platensis is a marine microalga whose cultivation is particularly attractive for several commercial purposes; it can be used either as nutritional supplement for humans and animals [1] or as source of active principles in pharmaceutical and cosmetic industries [2]. Moreover, this microalga has been successfully employing in integrated systems for wastewater treatment [3], recovered and re-utilised [4] also as adsorbent material for heavy metals [5]. For the above reasons, its large-scale production is of great interest; the most widely used systems are the outdoor cultures that allow obtaining large amounts of biomass at low costs. Nowadays, the commercial production of this microalga is carried out almost exclusively in open systems [6–8], which do not require either particular care or control of the environmental conditions (light and temperature). However, such systems did not allow reaching very high biomass concentration because of the difficulty of maintaining the optimal temperature, easiness of contamination and limited exploitability of light due to low surface/volume ratio [9]. In addition, during winter, this alga cannot

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1369-703X/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.bej.2006.08.013

grow in open ponds, except in the tropics, so as its production must be resumed once winter is over [10]. The use of a tubular bioreactor [11] can reduce these disadvantages owing to its particular structure. In fact, being closed, it is able to provide a controlled environment preventing contamination. Besides, thanks to its large outer surface exposed to the light, it increases the surface/volume ratio with respect to other configurations and reduces the shadow effect, which is the main cause of growth inhibition in open ponds. Finally, such a plant configuration makes the control of the operational parameters easier, hence resulting in an increased biomass production. However, the peculiar fragility of the sheath of S. platensis and its filamentous morphology [12,13] impose some constraints in the design of a photobioreactor. The experience gathered over many years on the culture of this microalga in tubular reactor points out the diameter of the tubes, the length of the reactor tube, the mixing of the culture and the circulation device as the main factors influencing its performance [14]. The surface/volume ratio is mainly regulated by the diameter of the tubes, therefore this factor has a strong impact upon the irradiation intensity on the culture. On the other hand, the tube length influences the circulation of the cultivation medium inside the reactor, i.e. the residence time. During biomass circulation, the photosynthetic activity of the cells causes the oxygen concentration to increase [15] and rate depends on light intensity,

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A. Converti et al. / Biochemical Engineering Journal 32 (2006) 13–18

biomass concentration and temperature. Since a high concentration of dissolved oxygen affects both growth and protein synthesis [16], the cultivation conditions should be selected so as to prevent oxygen accumulation. Mixing is necessary to assure a good exposure of biomass to light and an adequate distribution of nutrients. Finally, the selection of the re-cycling device is crucial for the successful design of a bioreactor, since it can exert a negative effect of mechanical stress on the cells [17]. The airlift system is increasingly used for this purpose in the presence of very dense cultures of filamentous cyanobacteria such as S. platensis, because it allows avoiding damages to the sheath [18]. S. platensis cultivations were carried out in this work in two bench-scale open ponds and one bench-scale tubular reactor, in order to evaluate and compare the performance of these different reactor configurations. The efficiency of the tubular reactor, which was composed of a set of glass tubes disposed to form a “loop” and an airlift system for biomass re-cycling, was then checked by varying the main parameters typically influencing the algal growth, i.e. the light intensity and the re-cycling flow rate. 2. Materials and methods 2.1. Microorganism S. platensis (UTEX 1926) was obtained from the Culture Collection of the University of Texas. Cells were maintained in the medium of Schlösser [19], whose composition was as follows (per liter): 13.6 g NaHCO3 , 4.03 g Na2 CO3 , 0.50 g K2 HPO4 , 2.50 g NaNO3 , 1.00 g K2 SO4 , 1.00 g NaCl, 0.20 g MgSO4 ·7H2 O, 0.04 g CaCl2 ·2H2 O, pH 9.6. All the nutrients were dissolved in distilled water containing (per liter): 6.0 ml of metal solution (97.0 mg FeCl3 ·6H2 O, 41.0 mg MnCl2 ·4H2 O, 5.0 mg ZnCl2 , 2.0 mg CoCl2 ·6H2 O, 4.0 mg Na2 MoO4 ·2H2 O), 1.0 ml of micronutrient solution (50.0 mg Na2 EDTA, 618 mg H3 BO3 , 19.6 mg CuSO4 ·5H2 O, 44.0 mg ZnSO4 ·7H2 O, 20.0 mg CoCl2 ·6H2 O, 12.6 mg MnCl2 ·4H2 O, 12.6 mg Na2 MoO4 ·2H2 O) and 1.0 ml of a 1.5 ␮g l−1 B12 vitamin solution. A suspension collected at the latest exponential growth phase was harvested, filtered, washed with 0.9% NaCl solution and used to inoculate either the ponds or the tubular photobioreactor.

Fig. 1. Experimental set-up of open ponds.

2.3. Cultivations in tubular reactor The tubular reactor (Fig. 2) was composed of a set of 21 glass tubes, each having a length of 1 m, inner and outer diameters of 12 and 14 mm, respectively. The tubes were arranged horizontally with a slight inclination and placed on two parallel planes so that they were not superimposed each other and could feel the same light intensity. The culture was continuously mixed by injecting compressed air at the bottom of the tubes by means of a pump blowing air into a vertical pipe used as a riser. A 3.0-l Erlenmeyer flask closed with cotton cap was used at the top of photobioreactor as a reservoir and degasser. The air bubbles provided efficient de-oxygenation by scouring the inner surface of the tubes. The total volume of the culture (tubes plus reservoir) was 5.5 l, the illuminated surface area and the surface/volume ratio were 0.40 m2 and 135 m−1 , respectively. Culture temperature was monitored at 30 ± 1 ◦ C by incubation of the equipment within a thermostatted chamber. The pH was daily adjusted at 9.5 whenever it exceeded 10.0 by bubbling gaseous CO2 . Cultivations were carried out in the tubular reactor with the aim of comparing the efficiency of this system with that of the ponds. For this purpose, preliminary experiments were performed at Xo = 0.15 g l−1 under the same conditions of light intensity and temperature as those employed in the ponds. Successively, according to the literature [20,21], light intensity was

2.2. Cultivations in open ponds Three batch cultivations were performed in quadruplicate in two open ponds at different starting biomass concentrations, namely 0.15, 0.30 and 0.50 g l−1 . Each pond (Fig. 1), having a surface area of 0.13 m2 and a water depth of 5 cm, was continuously illuminated by eight fluorescent lamps (40 W), located at about 40 cm over its surface, furnishing a light intensity of 55 ␮mol photons m−2 s−1 . Culture mixing was assured by paddled wheels at 25 rpm. Temperature was kept at the optimum value suggested by the literature for S. platensis growth (30 ± 1 ◦ C) [8,20] by means of electrical heaters. The pH, which was daily monitored by a pH meter, never exceeded 9.5, hence assuring bicarbonate availability for microalga growth.

Fig. 2. Experimental set-up of the combined airlift-tubular reactor system.


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increased up to 120 ␮mol photons m−2 s−1 and re-cycling flow rate was progressively raised from 0.34 to 4.5 l min−1 to evaluate the influence of these parameters on the reactor performance. 2.4. Analytical procedures Cell concentration was determined by dry weight after filtration through Millipore filters (0.45-␮m pore diameter) and washing with 3.0N acetic acid solution to eliminate precipitates. The light intensity was measured by an irradiometer (Delta OHM, mod. HD 9021, Padua, Italy) as photon flux density (PPFD). This parameter is usually converted in photosynthetically active radiation (PAR) (␮mol photons m−2 s−1 ), expressing the effective radiation quantity that the alga is able to utilise. The measurements were performed at different points of the plant surface to ensure an average illumination intensity. The input of PAR (IPAR), expressing the quantity of radiation impacting on the reactor, was calculated as suggested by Watanabe and Hall [22] as the product of PAR (kJ m−2 d−1 ) and the illuminated surface (m2 ). For the conversion of PAR expressed as ␮mol photons m−2 s−1 to kJ m−2 d−1 , the conversion factor 18.78 kJ s d−1 ␮mol−1 for cool white fluorescent lamps has been used [23]. According to Watanabe and Saiki [24], the photosynthetic efficiency (%) (PE) was calculated as: PE =

rG HG × 100 IPAR

(1)

where rG is the maximum daily growth (gDB d−1 ) and HG the enthalpy of dry biomass (21.01 kJ gDB −1 ) [25]. 3. Results and discussions Fig. 3 shows the behavior of S. platensis growth in ponds at two different inoculum concentrations, namely Xo = 0.15 and 0.50 mg l−1 . At given light intensity and temperature, a higher inoculum level (Xo = 0.50 g l−1 ) allowed the system to reach the maximum growth (1.5 g l−1 ) in shorter time (about 10–15 d) than at Xo = 0.15 g l−1 (about 20 d). The dramatic increase in biomass concentration observed in the tubular reactor at Xo = 0.15 g l−1 in the same figure demonstrates the better performance of such a configuration with respect to the ponds. The successive tests

Fig. 3. Comparison of S. platensis growth performed in tubular reactor (() Xo = 0.15 g l−1 ); ponds ((䊉) Xo = 0.15 g l−1 ; () Xo = 0.50 g l−1 ).

Fig. 4. Biomass growth in tubular reactor at different light intensities. PAR (␮mol photons m−2 s−1 ): (䊉) 55; () 80; () 120.

were then performed in tubular reactor, and the influence of light intensity and air flow rate on S. platensis growth were explored. Fig. 4 illustrates the growth behavior versus time at different PAR values (55, 80 and 120 ␮mol photons m−2 s−1 ). The light intensity did not seem to influence biomass growth up to a cell concentration of about 1 g l−1 , while a positive effect is evident beyond this threshold. Besides, PAR = 55 ␮mol photons m−2 s−1 allowed producing a maximum cell concentration (Xm ) of only 6.5 g l−1 , hence evidencing a clear photolimitation effect; increasing the light intensity up to 80 and 120 ␮mol photons m−2 s−1 , biomass level increased, reaching Xm = 10.6 g l−1 within 19 and 15 days, respectively. The different kinetics of these cultivations suggests that no photoinhibition took place under the conditions investigated in this study. These results can be considered to be a significant advance if compared with those obtained in raceway ponds (Xm = 0.8 g l−1 ) [26], tubular airlift reactor (Xm = 4.2 g l−1 ) [17] and elevated panels (Xm = 5.0 g l−1 ) [27]. Since Xm did not increase further when raising the light intensity from 80 to 120 ␮mol photons m−2 s−1 , it is likely that a shading effect limited the biomass growth [29] when its level exceeded a critical threshold. In fact, the amount of light that impinges on the cells does depend not only on the surface exposed to radiation but also on the depth of the culture, if ponds are used, or the degree of turbulence and the population density, if the tubular reactor is employed [4,28], as the superficial film of biomass hinders the light through the inner biomass, thus preventing the optimal enlightenment. Table 1 summarizes the main results of these tests, highlighting the performance of the tubular reactor in comparison with that of the ponds (Table 2) in terms either of biomass productivity or photosynthetic efficiency. A PAR increase from 55 to 120 ␮mol photons m−2 s−1 resulted in a corresponding increase in productivity from 0.29 to 0.62 gDB l−1 d−1 , whereas PE resulted to be practically independent of the light intensity (PE = 8.0–8.1%), which is consistent with the above suggested light-limited conditions in the tubular reactor. These results also confirm that, at the same light intensity (55 ␮mol photons m−2 s−1 ), the tubular reactor allowed for better exposition and higher photosynthetic efficiency with respect to the ponds, where the cells likely experienced full light radiation at the surface and darkness at the bottom.

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Table 1 Cell productivities obtained for Spirulina platensis cultivations carried out in tubular photobioreactor under different condition PARa (␮mol m−2 s−1 )

IPARb (kJ d−1 )

Qx c (gDB l−1 d−1 )

vd (m s−1 )

μe (d−1 )

PEf (%)

55 80 120 55

413 601 901 413

0.29 0.42 0.62 0.18

0.05 0.05 0.05 0.21

0.17 1.7 0.19 0.13

8.1 8.1 8.0 4.9

Starting biomass concentration = 0.50 gDB l−1 . a PAR, photosynthetic active radiation. b IPAR, input of photosynthetic active radiation. c Q , average cell productivity. x d v, culture speed. e μ, average specific growth rate. f PE, photosynthetic efficiency.

Alternation of light and dark periods were considered to be as a crucial factor for a stable, high density culture of S. platensis [1]. During the dark period, some of biomass is in fact consumed by respiration [30], the consumed fraction consisting of reserve materials such as carbohydrates and lipids. Since the heterotrophic metabolism in the absence of light is notoriously quicker than the autotrophic one and energetically more profitable, it is possible that its occurrence would be fundamental to guarantee a long-term survival of photosynthetic organisms. In this sense, turbulence in outdoor systems may represent the most practical way to create an intermittent pattern to illuminate cells [31]. Such a necessary light–dark alternation was ensured in our system by lateral illumination in addition to the secondary motion caused by the centrifugal effect in correspondence of tube curvature [32]. During the growth in the tubular reactor, the microalga showed a tendency to settle in the tubes, probably due to the high biomass level; in order to reduce this disadvantage, a further test was performed under the same conditions (Xo = 0.5 g l−1 and PAR = 55 ␮mol photons m−2 s−1 ) but increasing the culture specific upward velocity from 0.05 up to 0.21 m s−1 so as to assure better mixing in the tubes. Biomass concentration reached a maximum (Xm = 2.75 g l−1 ) after 13 days (data not shown) and decreased slowly. The unsatisfactory productivity and photosynthetic efficiency (Qx = 0.18 g l−1 d−1 and PE = 4.9%, respectively) obtained under these conditions (Table 1) suggest a state of mechanical stress ascribable to excess flow rate, which was confirmed by the microscopial observation of necridia (sacrificial cells) in the trichome that lost its cellular content becoming colorless [12].

Mixing of the culture and then its rheological properties are very important for the operation of the bioreactor, because they influence nutrient supply, exposition to the light and mass transfer conditions [11]. So, culture circulation inside the airlifttubular reactor system becomes one of the main factors to be taken into account to improve its performance, especially in terms of productivity. In order to evaluate the effect of culture speed on the behavior of S. platensis culture, this parameter was gradually increased from 0.05 to 0.21 m s−1 by increasing the air flow rate from 0.33 to 4.5 l min−1 . According to Torzillo [11], these values were tested at two extreme biomass concentrations, namely at very low (about 0.05 g l−1 ) and high (10 g l−1 ) biomass levels. These authors did in fact demonstrate that S. platensis cultures behave as Newtonian fluids at biomass concentrations of about 2 g l−1 or lower, while over 4 g l−1 they showed a pseudoplastic behavior. Moreover, the experiments performed in the bioreactor revealed that an increase in biomass concentration up to 10 g l−1 led to an extensive entanglement of the culture; therefore, a progressive rise in the air flow was needed to favor its disentanglement. For high biomass concentration (X = 10 g l−1 ), the relation valid for the non-Newtonian fluids was then assumed according to Metzner and Reed [33]: NRe

Dn v(2−n ) ρ = K 8(n −1)

(2)

is the Reynolds number for non-Newtonian fluids, where NRe D the inner diameter of pipes, v the culture speed, ρ the culture density, n the flow behavior index and K is the consistency

Table 2 Cell productivities obtained for Spirulina platensis cultivations carried out in open ponds under different conditions Xo a (gDB l−1 )

PARb (␮mol m−2 s−1 )

IPARc (kJ d−1 )

Qx d (gDB l−1 d−1 )

μe (d−1 )

PEf (%)

0.15 0.30 0.50

55 55 55

134 134 134

0.050 0.054 0.060

0.12 0.098 0.081

5.9 6.4 7.1

a b c d e f

Xo , starting biomass concentration. PAR, photosynthetic active radiation. IPAR, input of photosynthetic active radiation. Qx , average cell productivity. μ, average specific growth rate. PE, photosynthetic efficiency.


index. In this equation, n and K can be considered as the degree of non-Newtonian fluid behavior of the culture and the culture consistency, respectively. For Newtonian fluids, n = 1 and K reduces to viscosity of the fluid, therefore for low biomass concentration (X = 0.05 g l−1 ) the relation valid for the Newtonian fluids may be applied: NRe =

Dvρ μv

where μv is the culture viscosity (kg m−1 s−1 ). The parameter K is defined as: 3n − 1 n K = K 4n

(3)

(4)

where K (dynes sn cm−2 ) is the power law constant of the exponential equation of Ostwald-de Waele: τw = K(γw )n

(5)

being τw (dynes cm−2 ) is the shear stress and γw (s−1 ) is the shear rate. It should be noticed that the n parameter appearing in Eqs. (4) and (5), denominated power law index, corresponds to the non-Newtonian behavior index (n ) of Eq. (2). Assuming for n and K the values calculated by Torzillo for a biomass concentration of 10.2 g l−1 , namely 0.540 and 0.577 dynes sn cm−2 [11], it was possible to evaluate the fluid dynamic behavior of the system under the above two limit conditions (Fig. 5). The values of the Reynolds number were low in both cases, even when the maximum air flow rate was applied at the lower biomass concentration, hence indicating that the system always worked in laminar flow. It was suggested that the Reynolds number should be higher than 2100 to assure turbulence flow [17]; therefore, these conditions could be only get at very high concentration of biomass, but a high air flow led to cells damage probably produced in the bubbled section, and during bubble disengagement. Because significant increases in the culture speed (from 0.05 to 0.21 m s−1 ) did not imply any proportional increase in the culture re-cycling flow, it can be deduced that low culture speeds (0.16 m s−1 or lower) should

Fig. 5. Dependence of the Reynolds number on the culture re-cycling flow rate at different biomass concentrations: () 10 g l−1 ; (䊉) 0.05 g l−1 .

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Table 3 Different fluid dynamic conditions tested for Spirulina platensis cultivations performed in the airlift-tubular photobioreactor Air flow rate (l min−1 )

Culture re-cycling flow rate (l min−1 )

Culture speed (m s−1 )

0.33 1.0 2.0 3.5 4.5

0.34 0.78 1.07 1.34 1.40

0.05 0.11 0.16 0.20 0.21

be sufficient to assure good mixing of the culture, avoiding cell damage. The plant configuration proposed in this study did not allow even at the highest tested flow rate reaching turbulent regime conditions, which were considered by some authors to be crucial to ensure significant productivity increases [34,35]. Nevertheless, it was demonstrated that the optimal conditions of turbulence regime were very narrow (2680 < NRe < 4000) in the specific photobioreactor they utilised and that a turbulence excess was deleterious for the culture [35]. As described in Table 3, an increased air flow rate (from 3.5 to 4.5 l min−1 ) did not result in any significant increase either in the culture re-cycling flow rate or in the culture speed. This suggests that the best operating conditions for the tubular photobioreactor would be those of a laminar regime preventing culture damage. The next effort will deal with improvement of the bubbled section so as to minimize cell damage at high culture speed. 4. Conclusions The main novelty of this work was the simultaneous use of a tubular photobioreactor with slightly inclined tubes, so that the fluid circulation was guaranteed by the simple gravity force, and an airlift system to prevent shear stress to a culture of S. platensis. The experimental biomass concentrations obtained under different conditions were higher than those reported in the literature for analogous systems and much higher than those obtained in open ponds. The results presented in this study confirm that, under lightlimited and laminar flow conditions, the air flow rate in the airlift system for S. platensis re-cycling appreciably influences biomass productivity and photosynthetic efficiency of a tubular photobioreactor. In fact, if from the one hand, turbulent conditions should favor the cultivation because of enhanced mass transfer, from the other hand, they can induce cell damage when filamentous microorganisms like S. platensis are used, hence requiring an optimum compromise between these opposite requirements. The proposed plant configuration proved to be very promising under the suboptimal conditions investigated in this preliminary study; therefore, in order to get a clearer picture of its potential, a set of additional fed-batch tests will be performed in next work, varying the light intensity, the regime conditions and comparing the results with those of tests to be performed alternating dark and light periods.

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Cultivation of Spirulina Air Lift Photo Reactor

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