Current Status, Future Developments and Recent ... - IngentaConnect

Send Orders for Reprints to [email protected] 80

Recent Patents on Engineering, 2015, 9, 80-90

Current Status, Future Developments and Recent Patents on Photobioreactor Technology Luis G. Ramírez-Mérida1,2, Leila Q. Zepka2 and Eduardo Jacob-Lopes2* 1

Applied Biotechnology Center, Department of Biology, University of Carabobo, Universidad Avenue, 2002, Valencia, Edo. Carabobo, Venezuela; 2Food Science and Technology Department, Federal University of Santa Maria, UFSM, Roraima Avenue 1000, 97105-900, Santa Maria, RS, Brazil Received: June 26, 2014; Revised: January 26, 2015; Accepted: February 6, 2015

Abstract: Carbon dioxide (CO2) has been regarded as one of the most important greenhouse gases. Microalgae are considered as a potential solution for the decrease of atmospheric CO 2 levels. The design of photobioreactors capable of capturing CO2 for bioconversion bioproducts is the main issue for techno-economic success in the field of phototrophic biotechnology. There are two kinds of large scale photobioreactors: open and closed system. The open systems are raceway ponds and closed systems are the flat plate, vertical tubular and horizontal tubular. These photobioreactors have their own advantages and disadvantages. Improvements in the design and configuration of photobioreactors are widely evaluated, with a focus on the utilization of physical parameter suitable for scaling. However, some considerations must be taken into account such as the height/diameter (H/D) ratio, an appropriate value, which maintains control from the structural and physicochemical point of view, helping to provide sufficient volume of microalgae culture, efficient transfer of mass, a reaction volume where light input to the system is adequate, good rate of culture mixture and better utilization of land space. This review seeks to show some photobioreactor designs, some patents and their scale-up to be implemented in the CO2 sequestration and biomass production.

Keywords: Biomass, bioproducts, carbon dioxide, microalgae, photobioreactor, scale-up. INTRODUCTION The greenhouse effect is the phenomenon whereby certain gases retain part of the energy that has been emitted by planetary surface which has been heated by solar radiation; one of the principal gases involved is carbon dioxide (CO2). Anthropogenic CO2 emissions from fossil fuel utilization especially from coal combustion are responsible for global climatic change. CO2 emissions have been studied and monitored because in recent decades they had influenced climate change. Accelerated increases in CO2 levels at the end of the last century have attracted the attention of international organizations [1]. The United Nations promoted the Kyoto Protocol in 1997, regulations were established to control air pollutant emission with the objective of reducing greenhouse gas on the basis of emissions in 1990, and more than 170 countries have ratified the protocol [2]. Various CO2 sequestration techniques have been developed worldwide. Of these, photosynthetic organisms as microalgae are promising in view of the advantage of utilizing solar energy. These systems aim to reduce CO2 emissions from various industrial manufacturing sectors, because microalgae use CO2 as a carbon source for synthesizing value *Address correspondence to this author at the Food Science and Technology Department, Federal University of Santa Maria, UFSM, Roraima Avenue 1000, 97105-900, Santa Maria, RS, Brazil; E-mail: [email protected] 2212-4047/15 $100.00+.00

added compounds of biomass rich in protein, biopolymers, volatile organic compounds, lipids, etc. [3,4]. Microalgae use CO2 efficiently, they have a high growth rate for biomass production and can be used in biotechnological systems, with the use of photobioreactors [5,6]. The available photobioreactor configurations are numerous however, the most commonly used are the tubular, flat plate and hybrid photobioreactor types [7]. The progress or development of technologies with the use of microalgae has been limited by its relatively low volumetric productivity in the existing industrial photobioreactors, which leads to a limited production of bioproducts as well as CO2 sequestration; due, in part, by the loss during the injection gas leak in the reactor [8]. Scale-up and configuration design of photobioreactors have not advanced sufficiently to develop optimal systems. For improvements in solving problems in configurations and mode of operation of the system, resolutions must be focused on: (i) providing efficient and adequate light source; (ii) injection of CO2 and reduction of exhaust; (iii) ensuring good mixing and mass transfer; (iv) using strains with fast growth and extreme temperature resistance, CO2 and other toxic compounds; (v) removal systems of photosynthetic oxygen (O2) and (vi) scalable photobioreactor technology [9,10]. This review article aims to describe the microalgae cultivation systems and considerations about physical parameters involved in microalgae cultivation with special attention to photobioreactors projected and used for CO2 mitigation. Furthermore, the scaling © 2015 Bentham Science Publishers

Current Status, Future Developments and Recent Patents on Photobioreactor Technology

up of photobioreactors for CO2 sequestration to be used in the future. GENERALITIES AND METABOLISM OF MICROALGAE Microalgae are microorganisms with photosynthetic metabolism that grow fast, generate valuable primary and secondary metabolites, and are easily harvested [11]. Eukaryotic microalgae besides the prokaryotes as cyanobacteria species have oxygenic photosynthesis for fixation of CO2 like macroalgae and plants [12]. They may have chlorophyll a and phycobiliproteins that are involved in light energy harvesting, thus allowing photosynthetic ability for biomass generation. In addition to photosynthesis, they show a versatile metabolism and high adaptability mechanisms such as respiration and nitrogen fixation, chromatic adaptation and the capacity for symbiosis with yeast, fungal, bacterial and plant cells [13]. The step of photosynthesis in which CO2 is converted into carbohydrates, catalyzed by the enzyme ribulose 1,5bisphosphate carboxylase/oxygenase (RuBisCO), is referred to as Calvin cycle [14]. The Calvin cycle is the metabolic mechanism for CO2 fixation in microalgae; this process comprises of three phases; carboxylation, reduction and regeneration. Photosystem II (PSII) complex is the starting point of photosynthesis, and then through the electron transport chain the electron is transferred to cytochrome b6f and PSI. A proton-motive force is created due to the pumping of electrons in the opposite directions, creating a separation of charge across the membrane. This is used for ATP synthesis and formation of ferredoxin and NADPH. The water is electron donor, forming O2 as a waste product [15,16]. To generate one molecule of carbohydrate (CH2O), O2 and H2, at least eight (8) photons are required. The mean energy content for photosynthetically active radiation (PAR) photons is near 220 kJ/mol and the total potential illumination energy used at photosynthesis is 1744 kJ/mol of CH2O. The theoretical maximum efficiency of conversion of light to ATP is around 27%. However, only 42.3% the PAR can be utilized [17]. Furthermore, intensity and quality light have a key role in kinetics of microbial growth [18]. PHOTOBIOREACTOR DESIGN FOR CO2 CONVERSION Two kinds of photobioreactors of large scale are open and closed systems. Open systems can be built more easily, are more economical and relatively simple in relation to closed systems. Amongst the different types of open systems designed, the most popular is the raceway pond. However, open systems have some disadvantages in the control of parameters such as availability of light, agitation, pH, temperature, water evaporation, loss of CO2, and large areas of land requirements [19]. Use of open systems for CO2 sequestration is not suitable, since the retention time of CO2 in these is low because of the fast evaporation. This makes the microalga not have the time needed to capture CO2, thus, productivity in terms of biomass and bioproducts are low. Moreover, the susceptibility to contamination of the system makes

Recent Patents on Engineering, 2015, Vol. 9, No. 2

81

it unsuitable for the elaboration of high value-added bioproducts [5]. Closed system provide greater control of CO2 and lighting, therefore there is better use for CO2 sequestration by microalgae, producing higher yields of biomass and bioproducts. Closed systems are currently tested for microalgae mass cultures in configurations such as flat-plate, vertical tubular, horizontal tubular and hybrid photobioreactors [20]. Although microalgae can mitigate CO2 and produce various compounds, large-scale cultivation with closed photobioreactors also have limitations motivated the development and installation costs. The scale-up and configuration development for photobioreactors are poorly developed at present. Various configurations and productivities of photobioreactor are shown in Table 1. It is clear to point out that we will observe different yields of biomass, which affect its productivity and CO2 fixation rate, all of them depend on the following factors: species of microalgae, types of photobioreactors, volume, intensity of illumination, aeration, etc. RACEWAY POND A raceway pond is constructed of a closed loop recirculation channel and fabricated of different materials. Mixing and circulation of the suspended microalgae are done by a paddle wheel which prevents sedimentation of microalgae at the bottom. The paddle wheel also mixes air into the water and creates turbulence when feeding the culture [7]. The raceway pond can work with continuous feeding of CO2 and culture medium and exhibit low productivity due to reduced light penetration in the water column. The time estimated to reach maximum values of biomass in these pond is 8 weeks. Raceway pond is cheap to build and fairly easy to clean but has several technical and operational disadvantages including: (i) variations under weather conditions making it nearly impossible to control illumination intensity and temperature which makes it difficult to keep the environment constant at optimal growth conditions, (ii) requiring a great deal of water (due to high evaporative losses), this high volume of water magnifies the cost of processing/harvesting/ separation, (iii) requiring large extensions of land which does not compensate for low productivity, (iv) accelerated diffusion of CO2 into the atmosphere that the gas bubbled in growth medium presents low residence time and gives little time for microalgae to sequester CO2 from flue gases therefore making it impossible to control the diffusion of CO2, (v) contamination risk, the microalgal culture in direct contact with the environment is susceptible to contamination by insects or other microorganisms as yeast, fungi or bacteria, amoebas and rotifers, (vi) failures in stirring and mixing that lead to poor mass transfer rate, (vii) inability to control photoinhibition at constant and high light intensities, (viii) only the top portion of the pond is illuminated efficiently creating a very poor illuminated surface area to volume ratio resulting in low volumetric productivity, (ix) consumption of tremendous amounts of energy in their attempts to effectively stir large culture volumes by pump and centrifuge, (x) highest operating cost in the harvesting due to the biomass concentration is usually low and the volume is up to several hundred tons for the system, (xi) cannot be operated at depths greater than 30 cm (generally maintained between 15 – 30 cm) thus reducing the possibility of reaching higher volumes,

82


Table 1.

Ramírez-Mérida et al.

Photobioreactor designs and productivities for microalgae culture.

Photobioreactor

Microalgae strain

Biomass concentration (g/L/d)

Capacity (L)

CO2 consumption rate (mg/L/d)

Horizontal Tubular

Spirulina

0.025

10000

---

Chlorella sp.

0.7

---

1.316

20% injection of CO2

[22]

Chlorella vulgaris

0.04

230

0.075

0.03% injection of CO2

[23]

Nannochloropsis

0.032 – 0.095

200

---

[24]

Chlorella

0.109 – 0.264

200

---

[24]

Chlorella sp.

0.610

---

1.147

Monoraphidium

0.023

4.5

---

Chlorella sp.

0.94

Aphanothece microscopica Nägeli

0.78

Synechococcus sp. (Anacystis nidulans)

Vertical Tubular Airlift

Vertical Tubular Column bubble

Flat-Plate

Raceway

Comment

Ref.

[21]

10% injection of CO2 , operation in Semi-batch

[25] [26]

1.767

10% injection of CO2

[27]

2

1.440

15% injection of CO2 , operation in batch

[4]

0.43

2.5

0.75

The light illuminating method was fluorescent-lamp

[28]


0.38

2.5

0.66

The light illuminating method was optical-fiber

[28]


0.53

2.5

0.92

The light illuminating method was fluorescent-lamp/opticalfiber

[28]

Haematococcus pluvialis

0.010

25000

---

[29]

Nannochloropsis

0.26

400

---

[30]

Dunaliella

1.5

3.4

---

[31]

Synechocystis aquatilis

0.3

---

0.5

Continued operation, 0.05 vvm and 10% of CO2 input

[32]

Chlorella, Arthrospira, and Dunaliella sp.

0.027-0.082

---

---

Land area 450m2

[33]

(xii) only suitable for a small number of microalgae that tolerate extreme environmental conditions and which can therefore compete with other species [5, 7, 34]. The raceway ponds are not considered productive for CO2 conversion and formation of bioproducts as these are not used industrially, rather only for producing high value-added products. FLAT PLATE PHOTOBIOREACTOR These photobioreactors are prepared with glass walls or transparent plastic to prevent retention in illumination intensity. Generally have vertical design and wide surface area, and are placed in a strategic position to allow better use of light intensity [35, 36]. Higher yields in biomass and CO 2 capture are achieved with greater turbulence mixing by air

input. This allows better CO2 mass transfer and removal of additional O2 in the liquid culture medium, without introducing damage by stress [37]. According to the results by Hu and Richmond [38], the maximum biomass production in flat plate photobioreactors, was 17.5 g L-1 of the cyanobacterium Spirulina platensis. Zhang et al. [37] employed outdoor flat panels using Synechocystis aquatilis for obtaining a biomass productivity of 1.0 g L-1per day with at an optimum aeration. Despite their simplicity, these systems are rarely used in the industrial cultivation of biomass due to high cost of transparent materials and laborious operation. The limitations, disadvantages and faults of the flat plate photobioreactors are presented for various reasons such as: (i) the limitation of the cultivation volumes is an attempt to increase the surface area


to volume (S/V) ratio allowing light to penetrate better, but the problem is that it may lead to biofouling and increase in the cost of pumping the microalgae through smaller volumes, (ii) the quality of glass, plastic and bonding techniques used for construction will directly affect the stability of the reactor; because depending on the dimension, the fluid around the structure will increase pressure in glass sheet which could cause rupture of the bioreactor, (iii) the removal and cleaning of adhered internal surface microalgae can create tremendous photo-efficiency issues as well as dramatically increase maintenance costs, (iv) should be equipped with coils for water cooling and perforated pipes for mixing and aeration of the cell culture in addition, device of input medium culture and oxygen, harvesting and spray cleaning of the interior that raises costs, (v) cell damage by excess aeration. By this, the scale-up has yet been unsuccessful due to complexity of the configuration and requirement installation. The temperature control is difficult furthermore, problem related light conditions at high culture densities, carbon dioxide diffusion rate and some degree of wall growth are reported [36]. Some properties are shown in Table 2. VERTICAL TUBULAR PHOTOBIOREACTOR Among vertical tubular photobioreactors are bubble column and airlift configurations which differ in the circulation liquid flow. They are simple to assemble and operate outdoors. Although they show high effectiveness and productivity in terms of biomass and CO2 capture their configuration in terms of length and height presents limitations for the control of some parameters; CO2 depletion and excess O2 removal [39] (Table 2). For scale-up of these photobioreactors, it is important to maintain parameters such as the ratio height/diameter column (H/D) below 2.0, thereby achieving conditions close to the ideal mixing [42]. Usually, these reactors are projected Table 2.


with H/D ratio between 5-10, which severely limits the scale-up. Furthermore, it is not advisable to increase height of the column because the mixture would be affected causing poor mass transfer and could be damaged in places with strong winds [43]. Sanchez Mirón et al. [44], reported that variations in the diameter and configurations of vertical tubular photobioreactors, bubble column and airlift types up to a maximum of 0.19 m biomass yields comparable to those found in the horizontal tube photobioreactors. Scale-up of photobioreactors is complicated by the difficulty of successfully completing mass transfer and fluid dynamics in large volumes, so a physicochemical knowledge of these processes is essential for precise and accurate scaling. When designing a photobioreactor, the combination of large diameter and height is preferred because the gas flow rate is great and with these configurations there is a greater chance of obtaining higher levels of conversion. During fluid circulation, mixing occurs appropriately at the diameter of the column, but is not covered in the column length thus; a good liquid circulation rate will depend on an appropriate H/D ratio in the photobioreactor [45]. Therefore, vertical tubular photobioreactors have low surface areas of lighting, which are limited for outdoor use though they may be relatively easy to build furthermore, scaling is complex, so to maintain high production levels, several photobioreactor units are to be built [46]. Photosynthetic efficiency has a direct influence on production and yields of biomass and bioproducts, so the regime of light and darkness are important for the development or inhibition of microalgal growth. Jacob-Lopes et al. [4], reported the values of 5.100 g/L and 1.440 g/L/d for biomass concentration and CO2 biofixation rate, respectively, in vertical tubular photobioreactor type bubble column for Aphanothece microscopica Nägeli with continuous lighting cycles, demonstrating the importance of light regime in the photosynthetic productivity and yield. Moreover López et al. [47] in continuous cultures of Anabaena sp. reported 1,450 mg/L/d and a maximum CO2 fixation rate of

Properties of different closed photobioreactors used in growing microalgae.

Type photoreactor

Vertical Tubular Airlift Vertical Tubular Column bubble

Mixing efficiency

Efficient use of light

Mass transfer

Shear stress

Scale-up

H-M

M

H

L

R

M

M

M

L

R

Flat-Plate

H

H

H

L-M

D

Horizontal Tubular

H

H

L-H

L-H

R

Hybrid

H-M

H

H-M

L

R

H: high; M: medium; L: low; D: Difficult; R: Reasonable

83

Perspectives

Limitation

Displays low energy consumption, easy to sterilize, reduce photoinhibition and photooxidation

Needs sophisticated materials of construction, small surface area of illumination

High biomass productivity, economical, easy cleaning, low oxygen accumulation

Difficulty in temperature control, a degree of growth of the wall

Adequate for cultivation in open spaces, high productivity, economic

pH gradient formation, dissolution of oxygen and CO2 along tube

Ref.

[39]

[35]

[35]

[40] [41]

84


1.45 g/L/d which is still, far from being considered a largescale production. Therefore, the main error in utilizing the photobioreactors on an industrial scale is the inappropriate handling of the H/D ratio, which creates various difficulties in physical and biological terms that have an impact in obtaining high yields. HORIZONTAL TUBULAR PHOTOBIOREACTOR Another type of closed photobioreactors for mass cultures, consist of an array of straight transparent tubes aligned with the sun rays. They are placed horizontally and have different designs and configurations. Usually plastic or glass is used to construct tubes of the horizontal tubular photobioreactors, and install pumps for the re-circulation of culture medium. The dimensions of the tubes are generally 0.03 to 0.1 m internal diameter and 20 to 100 m in length. They have a wide area of illumination and can be placed so that natural sunlight fall properly to generate higher photosynthetic efficiency but between the major drawbacks is the poor mass transfer, high investment and operation cost which become a difficult episode to cope with when the tubular photobioreactors are scaled-up. Tubes of this type of photobioreactors are not very long, for the oxygen that is produced in photosynthesis to be released, since the accumulation in the long tubes produces photoinhibition which prevents the growth of microalgae [11, 35]. The diameter must be balanced for optimum areal and volumetric productivity. One way to increase the volume of the reactor to carry greater scale-up is to increase the diameter or length of the circulation pipe. Furthermore, there must be turbulence in the tube of liquid fluid to reduce light/dark cycles. However, the circulation flow rate should not be too high to avoid shear stresses in cells. Tredici and Zittelli [35] reported volumetric and areal yields of 1.3 g/L/d and 28 g/m2/d respectively in cultures of A. platensis. Travieso et al. [48], showed 400 mg/L/d of maximum productivity for Spirulina sp. in tubular photobioreactor with 0.9 m high and 0.25 m2 basal area, the tube length was 60 m with inner diameter of 0.016 m. The working volume was 21 L and lighted steadily with cool white fluorescent lamps. Molina-Grima et al. [49] presented a horizontal tubular photobioreactor type Plexiglass loop immersed in a pool that regulates the temperature by obtaining a productivity of 0.32 g/L/d for Isochrysis galbana. Richmond et al. [50] described a tubular photobioreactor constructed with polycarbonate transparent tubes horizontally disposed of 0.03 m internal diameter and 20 m length. The temperature was controlled with spreader water, the productivity reached 1.5 g/L/d for S. platensis. In both horizontal tubular photobioreactors presented the area of land used was very large, leading to high investment costs so that an economic feasibility study is conducted. The main fault and the greatest drawbacks of horizontal tubular photobioreactor is the lack of scalability. The volume of this type of photobioreactor is relatively small compared to the area required by the system for the installation. This type of configuration requires a lot of land area for installation. Due to the complexity of the structure in terms of size


and tubes, initial and operational costs severely limit mass scale implementation as it is expensive to operate. Other known faults and drawbacks of this system are the necessary mixing by large pumps, this leads to high energy consumption and operational expenses besides causing cell damage. The pumps used for recirculation of culture medium can generate shear stress, although this also depends on the type of microalgal strain used. Yield issues have also been discovered when there is oxygen accumulated during photosynthesis inside the tube. Furthermore, the challenge to gather many units for mass production of microalgae is huge. Considering the fact that horizontal tubular photobioreactors have limitations in the penetration and distribution of light, the pipe fluid dynamics therefore tend to have a significant “dark zone” where the exchanges of excessive of O2 with CO2 occur. Microalgae in dark zone develop the biochemical process of cellular respiration, halting photosynthesis. Horizontal tubular photobioreactors are still not sufficiently productive, having a high risk of biofouling whereby microalgae accumulate on the interior surfaces of the tubes and reduce their transparency. Therefore, these types of photobioreactors have significant limitations when being scaled. HYBRID PHOTOBIOREACTOR Hybrid photobioreactor is a combination of at least two types of different photobioreactor. These type of photobioreactors compensate the drawback caused by the limitation of S/V ratio and scale-up of tubular photobioreactor [12]. Lee et al. [41] reported biomass concentration of 10 g dry weight/L of Chlorella pyrenoidosa in a tubular photobioreactor containing 20 parallel polyvinyl chloride tubes (divided into two series) of 0.025 m internal diameter and 25 m length each, placed at 25 degrees relative to the horizontal tube and connected at one end to a receiver tank, and to a vertical airriser tube of 0.032 m internal diameter and 5 m height, with working volume of 300 L and with a land area of 12 m2. Morita [51] developed a hybrid photobioreactor with conical tank and PVC pipe 0.16 m internal diameter coiled in tank with one heat exchanger and degassing unit. The culture medium is driven by an air pump upward to the light collecting unit which is connected to degasser; then the culture medium returns to the heat exchanger unit downstream. The major disadvantage is that because the angle of disposition of the pipes and tank height are defined; so to increase the volume several identical units of the photobioreactor must be reproduced which requires a greater land area. Thereafter many other prototype reactors have emerged, such as that developed by Broneske et al. [52] this invention relates to a method for microalgae cultivation with the purpose of biomass production by photosynthetic metabolism through capturing CO2 from combustion gases. The photobioreactor hybrids have some advantages, such as better control of the physical-chemical variables in the culture medium, greater productivity, less cost in energy consumption, a good biological yield, etc. However, there are still issues that must be resolved to keep photobioreactors economically viable and efficient, as it is the use of large tracts of land, the optimization of lighting by areas of surface, the geometrical structure. Making a good job of the H/D ratio in photobioreactors could give optimum results.


INDUSTRIAL PHOTOBIOREACTORS The industrial production of microalgae and bioproducts are limited by the development of an ideal photobiorreactor. The development of photobioreactors is one of the main steps which should be understood to obtain an efficient formation of biomass and bioproducts microalgae. Some considerations on the system configuration should be taken into account during installation at the industrial level. The closed photobioreactors are essential to produce compounds with higher value. Some authors have suggested some methods to enhance productivity in large-scale installations. The possible solution is not just about adding individual items, it must be seen as a whole and focusing on the associated costs of scale-up [5, 21, 34, 53]. Although there have been changes in the culture systems, to overcome low yield have mostly been ineffective. The problems encountered so far, in addition to the low efficiency in design and configuration of photobioreactors have led to many failed scaling attempts, and among the most notable are Santa Ana, Murcia, Spain and La Rioja, Argentina [54]. At the global level, there are some industries with large commercial systems such as: the plant built by Ökologische Produkte Altmark GmbH in Germany, Micro Gaia Inc, Aquasearch Hawaii Inc (USA), Seambiotic Ltd in Israel, among others [55, 56]. Many efforts have been made to develop reactors for mass production of microalgae and bioproducts, however to date not a single photobioreactor has been found that meet the needs of the theoretical production. Depending on the Table 3.


85

type of photobioreactor, the scale-up is performed by increasing the diameter, length, height or the number of units. In search of the ideal photobioreactor, computer simulations and predictive models are used for simulations yields, biomass productivity and high value biomolecules aggregate [34]. Greater productivity and yield in industrial scale processes are recommended by the various considerations that are summarized in Table 3. Unfortunately, the implementation is not simple. Many efforts are made in search of the ideal photobioreactor. Thus there has existed a long-felt need for a system and method for high capacity production of biomass. Biotechnological processes are framed in the developing of hybrid photobioreactors that improves the light absorption, controls duration of irradiation and energy levels and other parameters described for improving growth rate and increasing productivity of microalgae cultures. RECENT PATENTS ON PHOTOBIOREACTORS The development of the new reactors seek to optimize conditions to generate higher productivity and microalgal growth. These optimizations provide improvements in the design, lighting system, incorporation of nutrients, mixing and circulation. Therefore, several international patents are trying to resolve these parameters. In recent years, many patents of photobioreactors, have emerged in attempt to advance to a system applicable to industrial operations, aimed at converting CO2 and obtain bio-products.

Variables to consider to improve productivity in large-scale processes. Variable

Comment

Ref.

Pathlength length

Refers to the route by which the light penetrates the culture medium. For tube refers to the diameter. Thinner tubes with 0.03 to 0.1 m internal diameter for horizontal tubular photobioreactor. For flat plate is the distance between the primary faces of the panels which have been reported among 0.013 - 0.1 m. Shallower systems such as raceway ponds with a depth ranging from 15 – 30 cm, have been suggested to enhance cell growth rates due to the fact that microalgae and cyanobacteria absorb light progressively decreasing the dark areas.

[35, 57]

Mixing

Increased turbulence brings better advantage of light, CO2 mass transfer and removal of excess oxygen in the culture medium; it should not be very strong to avoid cell injury due to which shear stress causes a decrease in cell viability.

[37, 58]

Nutrient content and supply

Optimize CO2 and nitrogen input to the reactor for maximum utilization and fixation. The photosynthetic metabolism needs CO2, which must be added at an appropriate rate to maintain the optimal pH. Nitrogen is important for the metabolic processes. Ammonium is among the most common chemical forms of nitrogen that can be readily absorbed by microalgae.

[19, 20]

Geometric relation (H/D ratio)

In order to provide an adequate volume of culture medium, and an acceptable mass transfer, the diameter of photobioreactor should be high. In biochemical applications the value of H/D ratio should be between 1.0 1.5 given that a large gas flow is involved in these equipment, a large diameter is required to ensure proper gases transfer, generating greater utilization by microalgae an adequate reaction volume and thereby getting a good liquid circulation rate to achieve conditions close to the ideal mixing. It also provides greater input of light for better utilization by microalgae.

[42, 45]

Cultivation procedure

Batch, continuous, semi-continuous. Dependent on the type of the product to be obtained between the advantages offered are: easiest to set up and control, most reliable, versatile, efficient.

[42]

Photosynthetic system

Reduce the antenna size, helps control the effect of photosaturation and reduce the photoinhibition. Smaller size antennas, allow higher but not linear efficiency.

[59]

86


A recent patent with application number patent P201200903, (19 September of 2013) entitled “Photobioreactor for mass cultivation of microalgae" [60], presented a photobioreactor that combines the mechanism of a bubble column with an air-lift to increase productivity in biomass compared to systems operating separately. In this sense, it has developed a vertical photobioreactor of cylindrical shape with flat or conical bottom constructed of transparent material for light transmission. To prevent ingress of contaminants and evaporation of the liquid medium in the photobioreactor, which can be closed with a loosely fitting transparent cover to allow the exhaust. It also contains heat exchanging device to maintain the optimum temperature of microalgal growth and conduit circulation to ensure adequate mixing. This invention solves the problem of illumination by placing an illumination sheet of mesh in wall allowing full and simultaneous illumination of all microalgae running along the said sheet. Also, easy oxygen removal is possible as the outer face of the geotextile is exposed to the atmosphere while the internal surface receives the CO2 distribution in proper proportion. The disadvantage is that not considering the H/D ratio, the installation on an industrial scale would require many units of photobioreactor for obtaining high reaction volumes. In addition the design is limited for structural reasons, since the height of the photobioreactor provides shading between different subunits. Another recent patent with International Publication Number U.S. Patent 20140017769 A1 (16 January, 2014) [61], presented a method for the cultivation of phototrophic microorganisms; where a tubular bioreactor wherein the liquid culture medium containing bicarbonate buffer system is moved by circulation through a plastic tube to the tank. The invention results in surprising and synergistic advantages as the transfer of O2 and CO2 from the liquid phase to gas-phase and vice versa is improved and at the same time the pH buffering capacity of the system is improved. Furthermore an increase in the surface to volume ratio of the culture medium is achieved which means a smaller average light path, thereby allowing higher volumetric productivities. The industrial cultivation of photosynthetic microorganisms is dependent on physicochemical parameters presented in the culture medium. The design of this photobioreactor refers mainly to a good availability of light for the microorganisms. Additionally, variations in the pH during the cell growth in culture affects microalgae kinetics. Production or consumption of CO2 by microorganisms has strong effects on the pH of the cultivation medium. Therefore, the good transfer of O2/CO2 referred to in this invention is advantageous to control pH. This patent, with the S/V ratio being high, complicates the industrial usage of this photobioreactor. This is because it cannot scale structure, so that it would have to place more reactors units. When considering the L/D ratio, it can store a greater volume in less land area lowering costs of production area. A recent patent with the number U.S. Patent 20130029404 A1, (31 January of 2013) entitled "Photobioreactor in a closed environment for cultivating photosynthetic micro-organisms" [62], discloses a photobioreactor for cultivating a photosynthetic microorganism, comprising a holding tank where the culture medium is continuously irradiated


by photovoltaic cells that emit light toward the surface of the tank. The photovoltaic cells are arranged around the photobioreactor by lighting panels that are placed in a sealed tube made of transparent material which is immersed in the culture medium. The photovoltaic cells are used in reverse emission mode, i.e. as a light source. They are powered with an electric current called an “injection current” that produces light. Similarly, to provide greater illumination, the patent with International Publication Number U.S. Patent 20090203116 A1, (13 August, 2009) [63], showed a system to improve algae production in a photobioreactor that provides a method of internal illumination in photobioreactor by optical fiber for biodiesel production through microalgae growth. The patent further provided an enhancer method of supplying nutrients and CO2 to culture medium. The invention shows a photobioreactor with high performance biomass production and small expenditure of energy. Addition can be extrapolated to any configuration of photobioreactor for supplying an external lighting for cell growth. In these two patents mentioned, the high cost of installation and operation of artificial light sources is a major problem. The biggest obstacle to their practical application is the high power consumption and operating cost due to the need for artificial light. Therefore, a photobioreactor that improves the supply of sun light or combination with artificial light in short time and a good volume circulation rate of liquid with a certain H/D ratio allow less energy consumption costs. The energy efficiency of the lighting method inside the photobioreactor could produce better results since the light sources are closer to and coupled better with the culture medium. Nevertheless, the use of light sources introduced into the photobioreactor, needs to account for further major problems. First instance in the spread of the light beam, the culture medium has direct relation to with the cell density. When cell density increases, the path of the light beam from one point to another in liquid phase is hindered. Solutions consisting of illuminating the inner wall of the photobioreactor thus, cannot be extrapolated at an industrial scale by single homothety. The heat management is the second major problem to be solved. This depends on the kind of lamp, but regardless of the type of light sources used; there is an additional problem of the cost of the photobioreactor if the artificial light sources are multiplied significantly. The patent with International Publication Number W.O. Patent 2007011343 A1, (24 January of 2007) [64], showed a photobioreactor apparatus comprising of a liquid growth medium with a type of photosynthetic microorganisms. The method employs the photobioreactor as a processing device for generating combustion gases and biofuel, decreasing the emission of greenhouse gases. The invention comprises of a conduit having a surface that is moderately light transparent, allowing the incoming illumination intensity for photosynthesis. The conduit has a smallest internal cross-sectional dimension that is at least one (1) meter. Furthermore, the method comprises of receiving a gas from a fermentation process to remove the CO2 generation. The W.O. Patent 2008008262 A2, (17 January, 2008) [65], entitled “Photobioreactor systems and methods for


treating CO2-enriched gas and producing biomass” described the photobioreactor units whereby liquid culture medium and gas stream to feed microalgae species. The system can be used to remove gaseous pollutants to produce biofuels and generate a gas treatment process by photosynthesis. A part of the liquid phase is deflected from a photobioreactor unit for reincorporated upstream. The photobioreactor system and methods provided can be used as part of an integrated combustion method. All these aforementioned patents seek to solve basic problems as, illumination, mass balance, temperature, etc. But, the scale-up is still complicated in terms of productivity and economy which remains unresolved and needs production of biomass for commercial purposes. CURRENT & FUTURE DEVELOPMENTS The development of photobioreactors for CO2 sequestration using fast-growing microalgae is a potential and promising technology for biomass production and commercially valuable products. The main problem to be solved in the design and configuration of efficient photobioreactors for CO2 sequestration is that to obtain as much light as possible it is essential to maintain S/V ratio. Also other parameters such as easy operation control, scalability, mixing and mass transfer also contribute to a better performance of the photobioreactor. The configurations of photobioreactors designed are extrapolations which adapt chemical reactors in the industries. These systems, as well as their variations have been developed and adapted for meeting the peculiarities of bioprocesses involving microalgae. In laboratory and pilot scale, these settings have attended the basic needs of these processes. In the meantime with the increase in scale, they present operational problems in the demand for lighting and space; for this reason photobioreactors with appropriate H/D ratio would represent an advancement in the field. Despite the development of some existing photobioreactors with good productivity and biomass yields, the technological future of the photobioreactors designed aims at the development of hybrid reactors. Considering the H/D ratio of the correct tubular column and the appropriate specifications of parallel tubes in relation to diameter and length. This could avoid photoinhibition and photooxidation of the biomass and offers a good performance. Also, this process has a high capacity for oxygen removal and does not experiment photoinhibition for oxygen. We must bear in mind that there are biological problems that are involved directly with the low productivity in terms of yields for biomass, CO2 sequestration and formation of bioproducts. These biological problems involve important things, which include the microbiological species to use, the speed of growth, compounds generated by metabolism, photosynthetic capacity and cell morphology. Although, molecular studies have been developed to improve the photosynthetic metabolism, there are still numerous investigations using microalgae, in its natural state, assessing intensities and incidences of lighting that can provide an optimum photosynthetic activity and production, and thus avoid molecular transformation procedures that would cause substantial costs at the industry level. For this reason, a photobioreactor with


87

an H/D ratio 1-1.5, would enable an optimal biological development, from the biochemical point of view, because these reactors will have a better incidence of lighting which would allow optimum growth and development by generating a high volumetric productivity. In addition, preventing irreversible cell damage due to pressure and currents of the fluid within the reactor, does not cause cell break age by force of friction, due to the presence of space for cell movement. The same way, a proper H/D ratio would generate configurations of reactors with heavy workloads in not very long cylinders, which could lead to a rapid elimination of free oxygen in the photosynthetic process thus avoiding a photoinhibition oxygen and therefore loss of production of bioproducts and low performance in CO 2 sequestration. For illustration, consider the comparison of a vertical tubular photobioreactor with an H/D ratio = 10 (ratio used for a tubular photobioreactor type bubble column) and other with an H/D ratio = 1.5 (ratio recommended). If we propose the construction of a photobioreactor with a length of 1.5 m (this distance ensures good mixing, mass transfer and exchange of CO2, preventing formation of dark zone, maintaining a good relationship S/V, reduce energy costs associated with mixing mechanism, etc.). Building on the indicated ratio H/D we would have the following characteristics: a.

H/D ratio = 10: diameter 0.15 m, total volume theorist 26.5 L.

b.

H/D ratio = 1.5: diameter 1 m, total volume theorist 1,178 L.

The total theoretical volume is calculated by taking into consideration the equation of the cylinder volume. Based on this 44 tubular column with H/D ratio = 10 would be needed to achieve the same volume in a tubular column H/D ratio= 1.5. This would lead to some advantages such as less use of land area with more culture volume, lower operating costs, greater stability of the reactor against mild winds or quakes. This type of scale-up would generate higher growth of microalgae, greater areal productivity, decrease in investment and production costs and greater possibility of increasing the percentage of CO2 fixation. So, keeping the aforementioned H/D ratio would be a fundamental aspect for future development in the scale-up photobioreactors. Figure 1 shows a building reactor for an area of 25 m2. Four (4) tubular column photobioreactors with H/D ratio =1.5 would be required, while for a tubular column photobioreactor H/D ratio =10 sixty-four (64) units would be required for the same area of land with the volume being 1,696 L, which would represent 35.99% of the total volume of the four reactors H/D ratio = 1.5 generating clear disadvantages. In that same vein, if we consider a photobioreactor with H/D ratio = 10 and one with H/D ratio = 1.5, both with the specifications outlined above, to estimate the CO2 consumption rate in a cement company would have the following. Considering that a metric ton of cement produces about 700 kg of CO2, and that the literature indicates that to produce one kg of dry biomass requires at least 1.88 kg CO 2 [66], theoretically, 700 kg CO2 could generate 372 kg dry biomass.

88



5m

5m b.

a.

5m

5m

Fig. (1). Comparison of two types of tubular column photobioreactors with different H/D ratio in an area of equal land. In a. tubular photobioreactors having H/D ratio = 10 is shown. In b. tubular photobioreactors with H/D ratio = 1.5.

Whereas if the chimney of a cement company discharges about 20% of CO2 and that same percentage is injected into the photobioreactor, a total culture volume of 3,500 L to consume those 700 kg would be needed. For this least three (3) units of photobioreactor with H/D ratio 1.5 (with characteristics shown in b) would be required; while it would take at least hundred thirty two (132) units of photobioreactor with H/D ratio 10 (with features shown in a). Following this, in the first case the process could be set in a land area of 25 m2, while for the second case 50 m2 land would be required. Under this same criterion one (1) unit of photobioreactor with H/D ratio 1.5; 1,178 L and with injection of 20% CO2, would have the approximate equivalent of 236 kg CO2 which could generate about 125 kg of dry biomass. For the same amount of biomass in the photobioreactor with ration H/D ratio 10; forty-five (45) units of photobioreactors would be necessary. Again we see that the H/D ratio 1.5 has advantages related to land space, which leads to lower costs and installation area, higher volumetric productivity, and prevents shading that might arise between units (as it can be set a little more distant from each one another), and to provide this H/D ratio 1.5 the input light facilitates and ensures good mixing in the culture medium necessary for the growth of microalgae.

[2]

[3]

[4]

[5]

[6]

[7]

[8]

[9]

[10]

CONFLICT OF INTEREST The authors confirm that this article content has no conflict of interest. ACKNOWLEDGEMENTS The authors would like to convey his heartfelt gratitude to the Federal University of Santa Maria, the University of Carabobo and The Gran Mariscal de Ayacucho Foundation (Fundayacucho) by financially supported.. REFERENCES [1]

C. Song, “Global challenges and strategies for control, conversion and utilization of CO2 for sustainable development involving energy, catalysis, adsorption and chemical processing”, Catal. Today, Vol. 115 (1–4), pp. 2-32, June 2006.

[11]

[12]

[13]

[14] [15] [16]

United Nations, “Kyoto Protocol to the United Nations Framework Convention on Climate Change”, 1998. [Online] Available From: http://unfccc. int/resource/docs/convkp/kpeng. pdf. [Accessed: March. 28, 2014]. P. Spolaore, C. Joannis-Cassan, E. Duran and A. Isambert, “Review: commercial applications of microalgae”, J. Biosci. Bioeng., Vol. 101, pp. 100–112, 2006. E. Jacob-Lopes, C. H. Gimenes Scoparo, L. C. M. Ferreira Lacerda and T. Teixeira Franco, “Effect of light cycles (night/day) on CO2 fixation and biomass production by microalgae in photobioreactors”, Chem. Eng. Proc., Vol. 48, pp. 306–310, 2009. A. P. Carvalho, L. A. Meireles and F. X. Malcata, “Microalgal reactors: a review of enclosed system designs and performances”, Biotechnol. Prog., Vol. 22, pp. 1490–1506, 2006. C. Y. Chen, K. L. Yeh, R. Aisyah, D. J. Lee and J. S. Chang, “Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: A critical review”, Bioresour. Technol., Vol. 102, pp. 71–81, 2011. C. Gonzalez-Fernandez, B. Molinuevo-Salces and M. C. GarcíaGonzález, “Open and enclosed photobioreactors comparison in terms of organic matter utilization, biomass chemical profile and photosynthetic efficiency”, Ecol. Eng., Vol. 36, pp. 1497–1501, 2010. E. Jacob-Lopes, L. Q. Zepka and M. I. Queiroz, “Cyanobacteria and carbon sequestration”. In: Cyanobac. An Econ.Perspec. 1Ed: Wiley Blackwell, pp. 65, 2014. E. Jacob-Lopes, S. Revah, S. Hernández, K. Shirai, and T. Teixeira Franco, “Development of operational strategies to remove carbon dioxide in photobioreactors”, Chem. Eng. J., Vol. 153, pp. 120– 126, 2009. E. Molina Grima, F. G. Acién Fernández, F. García Camacho and Y. Chisti, “Photobioreactors: light regime, mass transfer, and scaleup”, J. Biotechnol. Vol. 70, pp. 231–247, 1999. L. Ramírez-Mérida, Q. L. Zepka and E. Jacob-Lopes, “Microalgas y cianobacterias aplicación en medicina”, Rev. Elect. Portales Medicos. com., Vol. IX, nº 4, pp. 149, Feb 2014. K. Kumar, C. N. Dasgupta, B. Nayak, P. Lindblad and D. Das, “Development of suitable photobioreactors for CO2 sequestration addressing global warming using green algae and cyanobacteria”, Bioresour. Technol., Vol. 102, pp. 4945–4953, 2011. L. Bergman and D. G. A. Ran, “Cyanobacterial–plant symbioses: signalling and development”, In: The Cyanobac., Mol. Biol., Genomics and Evol., A. Herrero, E. Flores, Eds, Caister: Academic Press, Norfolk, UK, pp. 447–473, 2008. D. L. Nelson and M. M. Cox, “Lehninger principles of biochemistry”, Fourth Ed. W. H. Freeman & Co., New Jersey, 2005. M. Calvin, “40 years of photosynthesis and related activities”, Photosynth. Res., Vol. 21, pp. 3-16, 1989. T. M. Iverson, “Evolution and unique bioenergetic mechanisms in oxygenic photosynthesis”, Curr. Opin. Chem. Biol,. Vol. 10, pp. 91-100, 2006.

Current Status, Future Developments and Recent Patents on Photobioreactor Technology [17]

[18]

[19]

[20]

[21]

[22]

[23]

[24]

[25]

[26]

[27]

[28]

[29]

[30]

[31]

[32]

[33]

[34]

[35]

[36]

L. Brennan and P. Owende, “Biofuels from microalgae – a review of technologies for production, processing, and extractions of biofuels and co-products”, Renew. Sustain. Energ. Rev., Vol. 14, pp. 557–577, 2010. P. H. Ravelonandro, D. H. Ratianarivo, C. Joannis-Cassan, A. Isambert and M Raherimandimby, “Influence of light quality and intensity in the cultivation of Spirulina platensis from Toliara (Madagascar) in a closed system”, J. Chem. Technol. Biotechnol., Vol. 83, pp. 842–848, 2008. L. Ramírez-Mérida, Q. L. Zepka, E. Jacob-Lopes, “Photobioreactor: tool for mass cultivation of cyanobacteria”, Ciencia y Tecnología., Vol. 6 (2), ppt. 9-19, 2013. R. M. Singh and S. Sharma, “Development of suitable photobioreactor for algae production – A review”, Renew. Sustain. Energ. Rev., Vol. 16 (4), pp. 2347–2353, 2012. G. Torzillo, B. Pushparaj, F. Bocci, W. Balloni, R. Materassi and G. Florenzano, “Production of Spirulina biomass in closed photobioreactors”, Biomass., Vol. 11, pp 61-74, 1986. N. Sakai, Y. Sakamoto, N. Kishimoto, M. Chihara and I. Karube, “Chlorella strains from hot springs tolerant to high temperature and high CO2”, Energ. Convers. Manage., Vol. 36, pp. 693-696, JunSep 1995. A. Scragg, A. Illman, A. Carden and S. Shales, “Growth of microalgae with increased calorific values in a tubular bioreactor” Biomass Bioenerg., Vol. 23, pp. 67-73, Jul 2002. C. James and A. M. Al-Khars, “An intensive continuous culture system using tubular photobioreactors for producing microalgae”, Aquacult., Vol. 87, pp. 381-393, Jun 1990. S. Chiu, M. Tsai, C. Kao, S. Ong and C. Lin, “The air-lift photobioreactors with flow patterning for high-density cultures of microalga and carbon dioxide removal”, Eng. Life Sci., Vol. 9, pp. 254260, 2009. K. Miyamoto, O. Wable and JR. Benemann, “Vertical tubular reactor for microalgae cultivation”, Biotechnol. Lett., Vol. 10, pp. 703-708, Oct 1988. K. Sung, J. Lee, C. Shin and S. Park, “Isolation of a new highly CO2 tolerant fresh water microalga Chlorella sp. KR-1”, Renew Energ., Vol. 16, pp. 1019-1022, 1999. I. S. Suh, C. B. Park, J. K. Han and S. B. Lee, “Cultivation of cyanobacterium in various types of photobioreactors for biological CO2 fixation”, Stud. Surf. Sci. Catal., Vol. 114, pp. 471-474, 1998. M. Huntley and D. Redalje, “CO2 Mitigation and Renewable Oil from Photosynthetic Microbes: A New Appraisal”, Mitigation and Adaptation Strategies for Global Change, Vol. 12, pp. 573-608, May 2007. A. Richmond and Z. Cheng-Wu, “Optimization of a flat plate glass reactor for mass production of Nannochloropsis sp. outdoors” J. Biotechnol., Vol. 85, pp. 259-269, Feb 2001. M. Barbosa, J. Zijffers, A. Nisworo, W. Vaes, J. van Schoonhoven and R. Wijffels “Optimization of biomass, vitamins, and carotenoid yield on light energy in a flat-panel reactor using the A-stat technique” Biotechnol. Bioeng., Vol. 89, pp. 223-242, Jan 2005. K. Zhang, S. Miyachi and N. Kurano, “Evaluation of a vertical flatplate photobioreactor for outdoor biomass production and carbon dioxide biofixation: effects of reactor dimensions, irradiation and cell concentration on the biomass productivity and irradiation utilization efficiency”, Appl. Microbiol. Biotechnol., Vol. 55, pp. 428433, 2001. C. Jimenez, B. R. Cossio, D. Labella and F. X. Niell, “The Feasibility of industrial production of Spirulina (Arthrospira) in Southern Spain”, Aquacult., Vol. 217, pp. 179-190, 2003. I. S. Suh and C. G. Lee, “Photobioreactor engineering: design and performance”, Biotechnol. Bioprocess Eng., Vol. 8, pp. 313-321, 2003. M. R. Tredici and G. C. Zittelli, “Efficiency of sun light utilization: tubular versus flat photobioreactors”, Biotechnol. Bioeng., Vol. 57, pp. 187–97, 1998. P. M. Slegers, R. H. Wijffels, G. van Straten and A. J. B. van Boxtel, “Design scenarios for flat panel photobioreactors”, Appl. Energ., Vol. 88, pp. 3342–3353, 2011.

[37]

[38]

[39]

[40]

[41]

[42] [43]

[44]

[45] [46]

[47]

[48]

[49]

[50]

[51]

[52]

[53]

[54]

[55]

[56]

[57]


89

K. Zhang, S. Miyachi and N. Kurano, “Photosynthetic performance of a cyanobacterium in a vertical flat-plate photobioreactor for outdoor microalgal production and fixation of CO2”, Biotechnol. Lett., Vol. 23, pp. 21–26, 2001. Q. Hu and A. Richmond, “Productivity and photosynthetic efficiency of Spirulina platensis as affected by light intensity, algal density and rate of mixing in a flat plate photobioreactor”, J. Appl. Phycol., Vol. 8, pp. 139–145, 1996. L. Xu, P. J. Weathers, X. R. Xiong and C. Z. Liu, “Microalgal bioreactors: challenges and opportunities”, Eng. Life Sci., Vol. 9 pp. 178–89, 2009. A. A. Henrard, M. G. de Morais and J. A. V. Costa, “Vertical tubular photobioreactor for semicontinuous culture of Cyanobium sp. ”, Bioresour. Technol., Vol. 102, pp 4897–4900, 2011. Y. K. Lee, S. Y. Ding, C. S. Low, Y. C. Chang, W. L. Forday and P. C. Chew, “Design and performance of an α-type tubular photobioreactor for mass cultivation of microalgae”, J. Appl. Phycol., Vol. 7, pp. 47–51, 1995. N. Blakeborough, “Fundamentals of fermenter design”, Pure Appli. Chem., Vol. 36 pp. 305-315, 1973. K. K. Vasumathi, M. Premalatha and P. Subramanian. “Parameters influencing the design of photobioreactor for the growth of microalgae”, Renew. Sustain. Energ. Rev., Vol. 16, Issue 7, pp 54435450, Sep 2012. A. Sánchez Mirón, M. C. Cerón, F. García Camacho, E. Molina Grima and Y. Chisti, “Growth and biochemical characterization of microalgal biomassproduced in bubble column and airlift photobioreactors:studies in fed-batch culture”, Enzyme Microb. Technol., Vol. 31, pp. 1015–1023, 2002. N. Kantarci, F. Borak and K. Ulgen, “Bubble column reactors”, Process Biochem., Vol. 40, pp. 2263–2283, 2005. C. U. Ugwu, H. Aoyagi and H. Uchiyama, “Photobioreactors for mass cultivation of algae”, Bioresour. Technol. Vol. 99, pp. 4021– 4028, 2008. C. V. G. López, F. G. A. Fernández, J. M. F. Sevilla, J. F. S. Fernández, M. C. C. García, and E. Molina Grima, “Utilization of the cyanobacteria Anabaena sp ATCC 33047 in CO2 removal processes”, Bioresour. Technol., Vol. 100, pp. 5904–5910, 2009. L. Travieso, D. O. Hall, K. K. Rao, F. Benítez, E. Sánchez and R. Borja, “A helical tubular photobioreactor producing Spirulina in a semicontinuous mode”, Int. Biodeterior. Biodegrad., Vol. 47, pp 151–155, 2001. E. Molina-Grima, J. Pérez, F. Camacho, J. Sánchez, F. Fernández, and D. Alonso, “Outdoor cultivation of Isochrysisgalbana ALII-4 in a closed tubular photobioreactor”, J. Biotechnol., Vol. 37, pp. 159-166, 1994. A. Richmond, S. Boussiba, A. Vonshak and R. Kopel, “A new tubular reactor for mass production of microalgae outdoors”, J. Appl. Phycol., Vol. 5, pp. 327-332, 1993. M. Morita, Y. Watanable, H. Saiki, “Investigation of photobioreactor design for enhancing the photosynthetic productivity of microalgae”, Biotechnol. Bioeng., Vol. 69, pp. 693-698, 2000. J. Broneske, O. Pulz, H. Franke, K. Doebel, H. U. Oehlmann and R. Uphoff, “Method for producing biomass by photosynthesis”, W. O. Patent 19988045409 A1, Oct. 15, 1998. J. U. Grobbelaar, “Physiological and technological considerations for optimising mass algal cultures”, J. Appl. Phycol., Vol. 12, pp. 201-206, 2000. A. Richmond, “Microalgal biotechnology at the turn of the millennium: A personal view”, J. Appl. Phyco., Vol. 12, pp. 441-451, 2000. M. Olaizola, “Commercial production of astaxanthin from Haematococcuspluvialis using 25,000-liter outdoor photobioreactors”, J. Appl. Phycol., Vol. 12, pp. 499–506, 2000. O. Pulz, K. Scheibenbogen and W. Grob, “Biotechnology with cyanobacteria and microalgae”, In: Rehm HJ, Reed G, Puhler A, Stadler P, editors. Biotechnology. Weinheim: Wiley-VCH, Vol. 10, 2001, pp. 107–136. P. Zemke, “Mass Cultivation of Phototrophic Microalgae”, In: Recent Adv. Microalgal. Biotechnol., 1Ed: OMICS Group eBooks, Foster City, USA, 2014, pp. 003.

90 [58]

[59]

[60] [61]

Recent Patents on Engineering, 2015, Vol. 9, No. 2 J. Ramirez-Duque, D. Marín-Quintero and C. García-Pulido, “Evaluation of Microalgal Mortality in a Centrifugal Pump of a Tubular Photobioreactor”, Ing. Univ. Bogotá (Colombia), Vol. 16, pp. 333 – 347, Jul-Dec, 2012. H. Kirst and A. Melis, “The chloroplast signal recognition particle (CpSRP) pathway as a tool to minimize chlorophyll antenna size and maximize photosynthetic productivity”, Biotechnol. Adv., Vol. 32, pp. 66 – 72, Issue 1, Jan–Feb, 2014. J. Fernández González, “Photobioreactor for mass cultivation of microalgae”, Patent P201200903, September 19, 2012. S. Schuessler, E. J. A. Roebroeck, S. H. E. Hazewinkel and O. J. H Hazewinkel, “Method and bioreactor for the cultivation of microorganisms”, U. S. Patent 20140017769 A1, January 16, 2014.

Ramírez-Mérida et al. [62]

[63] [64]

[65]

[66]

J. Bourgoin, M. Conin, A. Friederich, S. Guocai, “Photobioreactor in a closed environment for cultivating photosynthetic microorganisms”, U. S. Patent 20130029404 A1, January 31, 2013. K. Bazaire, “System to improve algae production in a photobioreactor”, U. S. Patent 20090203116 A1, Aug. 13, 2009 I. Berzin, X. Wu, “Photobioreactor and process for biomass production and mitigation of pollutants in flue gases” W. O. Patent 2007011343 A1, January 25, 2007. J. Lewnard and X. Wu, “Photobioreactor systems and methods for treating CO2-enriched gas and producing biomass” W. O. Patent 2008008262 A2, January 17, 2008. Y. Chisti, “Biodiésel from microalgae beats bioethanol”, Trends Biotechnol., Vol. 26 (3), pp. 126-131, 2008.