Microalgal biomass production as a sustainable

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c Plant Pathology Department, University of Kentucky, Lexington, ... Nowadays, fossil fuels; including coal, oil, and natural gas; are the world's ... to develop a new renewable energy sources that could replace fossil fuels. .... production was estimated by 127.7 billion liters during 2014 with ...... J Remsay Soc 1980;81:27–8.

Renewable and Sustainable Energy Reviews 64 (2016) 596–606

Contents lists available at ScienceDirect

Renewable and Sustainable Energy Reviews journal homepage: www.elsevier.com/locate/rser

Microalgal biomass production as a sustainable feedstock for biodiesel: Current status and perspectives Abd El-Fatah Abomohra a,b, Wenbiao Jin a,n, Renjie Tu a, Song-Fang Han a, Mohammed Eid b,c, Hamed Eladel d a

School of Civil and Environmental Engineering, Harbin Institute of Technology Shenzhen Graduate School, 518055 Shenzhen, China Botany Department, Faculty of Science, Tanta University, 31527 Tanta, Egypt c Plant Pathology Department, University of Kentucky, Lexington, 40546-0312 KY, USA d Botany Department, Faculty of Science, Benha University, 13518 Benha, Egypt b

art ic l e i nf o

a b s t r a c t

Article history: Received 4 April 2016 Received in revised form 20 May 2016 Accepted 26 June 2016

Nowadays, fossil fuels; including coal, oil, and natural gas; are the world's primary energy sources required for industry, lighting, transportation and heating. Their needs increased dramatically due to the vast expansion in human population and economy. In contrast, a greenhouse gas emission is a serious problem arose from such uses that might lead to potentially catastrophic changes in the earth's climate. In addition, fossil fuels are limited non-renewable resources that will run out in few decades. These factors motivated many researchers to develop a new renewable energy sources that could replace fossil fuels. Biodiesel is considered as the best candidate for this purpose. Recently, microalgae were discussed as a promising feedstock for biodiesel production. This review presents a critical overview of engineered challenges compilations related to microalgal biomass production. In addition, advantages and current limitations of biodiesel production, quantitative and qualitative feasibility of microalgal biodiesel, and its economic feasibility are discussed. & 2016 Elsevier Ltd. All rights reserved.

Keywords: Biodiesel Microalgae Raceway ponds Photobioreactors Lipids Fatty acids

Contents 1. 2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 596 Microalgae and their industrial significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598 2.1. Microalgae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598 2.2. Marketing of microalgae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598 2.3. Microalgae for biofuel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598 3. Large scale cultivation of microalgae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598 3.1. Open pond systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 599 3.2. Closed photobioreactors (PBRs). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 600 4. Quantitative and qualitative feasibility of microalgal biodiesel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 601 4.1. Quantitative and qualitative feasibility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 601 4.1.1. Lipids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 601 4.1.2. Fatty acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 602 4.2. Economic feasibility. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 604 5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 604 Acknowledgement. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 604 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 605

1. Introduction n

Corresponding author. E-mail address: [email protected] (W. Jin).

http://dx.doi.org/10.1016/j.rser.2016.06.056 1364-0321/& 2016 Elsevier Ltd. All rights reserved.

Continuous growth of human population resulted in increasing of energy demands all over the world. The current consumption of

A.E.-F. Abomohra et al. / Renewable and Sustainable Energy Reviews 64 (2016) 596–606

Nomenclature A h V Q v c/2 P dh



surface area of the open pond (m2) liquid depth (m) working volume (m3) volume flow rate (m3 s  1) flow velocity (m s  1) channel width (m) total power requirement hydraulic diameter density of the culture liquid (kg m  3) gravitational acceleration

petroleum is about 105 times faster than nature can create [1]. According to the Energy Information Administration report (2014), the world energy consumption will grow by 56% between 2010 and 2040, from 524 quadrillion British thermal units (Btu) to 820 quadrillion Btu. If this development continues, the world will be threatened with an energy crisis, as the worldwide fossil oil reserves will be exhausted in shorter than 30 years. In addition to the fact of limited oil resources, extensive use of fossil fuel contributes to increase the atmospheric CO2 that results in global warming [2,3]. This phenomenon may lead to catastrophic changes in earth's climate, as some of the available evidence suggests that scientists have been conservative in their predictions of the impacts on climate change [4,5]. Fig. 1 shows that global CO2 emission increased by 51% during the last 20 years as a result of fossil fuel combustion. Therefore, the continued use of fossil fuels as a main energy source is now widely documented to be unsustainable. This forced governments and research sectors to find substitutes for the fossil fuels by other renewable clean resources. By 2014, about 23% of total energy consumption (13.5  103 Mtoe) was derived from renewable sources (Fig. 2). Renewable fuels derived from biologically based feedstocks are known as biofuels. Recently, they have attracted a great attention and become increasingly necessary for the global fuel market. Global biofuel production was estimated by 127.7 billion liters during 2014 with

Fig. 1. Total global CO2 emission as a result of fuel combustion [7].

Fig. 2. Global energy production, consumption and percent of renewable energy in consumption [7].


e efficiency of the paddlewheel motor fM manning channel roughness factor (s m  0.33) M quantity of algal biomass (tons) Epetroleum energy contained in a barrel of crude petroleum q biogas volume produced by anaerobic digestion w oil content of the biomass (% of dry weight) Ebiogas energy content of the generated biogas y yield of biodiesel produced from algal oil Ebiodiesel average energy content of the biodiesel Ppetroleum price of a barrel of crude petroleum (US$) ACalgae microalgal oils production costs

23% as biodiesel. The top countries for total production of biofuels were the United States (60 billion liters), Brazil (29.9 billion liters), Germany (4.3 billion liters), China (3.9 billion liters) and Argentina accounted for 3.6 billion liters [6]. Biodiesel is considered as the main alternative for fossil fuel and, recently, it is receiving much attention all over the world. It is defined as the fatty acid methyl esters derived from the transesterification of renewable oil feedstocks using alcohol and acid or base as a catalyst. Biodiesel can be produced from vegetable oils, animal fats, waste cooking oils, or lipids of microalgae [8,9]. Evaluation of biodiesel feedstock relies mainly on its net benefit to society, which depends on many factors such as its impact on the net energy supply, greenhouse gases (GHG) emissions, water and air quality and global food impact [10]. In addition to the fact that it is a renewable fuel that could be sustainably supplied, adopting biodiesel has a number of advantages; (1) substituting biodiesel for petroleum diesel results in substantial reductions of soot, sulphur and unburned hydrocarbon emissions. In addition, because biofuel is derived from biomass, it does not contribute to atmospheric CO2 emissions [11]; (2) biodiesel can be used in existing diesel engines, blended with petroleum diesel or can be used unblended in slightly modified engines with better engine performance [12]; (3) biodiesel has lubrication properties that can actually improve engine life because it has twice the viscosity of petroleum diesel [13]; (4) it is highly biodegradable and, therefore, has minimal toxicity [14,15]; and (5) biodiesel investment will has significant improvement of rural economic potential. The primary biodiesel feedstocks for different producing countries are provided in Table 1. Global biodiesel production increased 13% to 29.4 billion liters in 2014. The top biodiesel-producing countries in 2014 were United States (16% of global biodiesel production), Brazil, Germany (both with 11%), Indonesia (10%) and Europe accounted for 39% of global biodiesel production [6]. Using of biodiesel produced from cultivated plants, as a substitution for the currently used fuel in the transport sector, Table 1 Current biodiesel feedstocks worldwide. Country/region


USA Europe Western Canada Africa India Malaysia and Indonesia Philippines China Spain Greece Brazil

Soybeans Rapeseed, sunflower Canola oil Jatropha Jatropha Palm Coconut Waste cooking oil Linseed oil Cottonseed Sugarcane

Modified from Ahmad et al. [10]


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dramatically affect huge land areas that are presently harnessed to produce human food. Palm oil is one of the largest oil-producing crops, with annual oil productivity average of 4.5 t per hectare [16]. Even with the use of palm oil, production of sufficient amount of biodiesel, that meets the diesel demand of road transport sector in the United Kingdom (22.7 million tons [17]), requires more than 200 times of the total UK area. In addition, using of food crops to produce fuel have heightened arguments worldwide [18,19]. This trend implies the need for large supply of vegetable oils, which may lead to food security and ethical issues [20]. One possibility to overcome the mentioned problems is to cultivate microalgae as a biological fuel source. The main aim of the present review is to provide the reader with an overview on microalgal biomass production technologies with particular emphasis as a source for biodiesel.

2. Microalgae and their industrial significance 2.1. Microalgae Microalgae are prokaryotic or eukaryotic photosynthetic organisms that are characterized by being adapted to live in an extremely broad spectrum of environments due to their unicellular or simple multicellular structure. They use carbon dioxide (CO2) to grow photoautotrophically producing approximately half of the atmospheric oxygen [21]. In terms of abundance, Sheehan et al. [22] and Chen et al. [23] concluded that the four most important divisions of microalgae are Cyanophyta (blue-green algae), Chlorophyta (green algae), Bacillariophyta (diatoms) and Chrysophyta (golden algae). 2.2. Marketing of microalgae Among different algal species, those that provide possible commercial applications have been found to be used in aquaculture, human food, value added products for pharmaceutical purposes and as energy feedstocks. The annual world production of microalgal biomass was estimated of about 5000–7500 t, generating average annual income of US$ 1.25 billion [24]. Spolaore et al. [25] reported that the annual world sale of Chlorella sp. was higher than US$ 38 billion for human food, animal feed and as food additives, and about US$ 10 billion for nutritional supplements produced by microalgae Schizochytrium sp. and Crypthecodinium sp. Additionally, estimated world market of astaxanthin produced by Haematococcus pluvialis was US$ 200 million [24]. More detailed comparison of market and cost of various types of high molecules derived from microalgae are available by Spolaore et al. [25] and Koller et al. [26]. 2.3. Microalgae for biofuel The idea of using microalgae as a source of fuel is not new [27,28] but now microalgae receive an increasing interest as a source for renewable energy. Microalgae can be used for the production of various energy carriers, including biodiesel, by transesterification of lipids [29], syngas by gasification of biomass [30], ethanol by carbohydrates saccharification [31], direct synthesis of hydrogen gas [32] and gasoline production by cracking of hydrocarbons and isoprenoids [33]. Many research reports and articles described the advantages of microalgae for biodiesel production in comparison with other feedstocks [9,34–36]. From the practical point of view, they are easy to cultivate using water inappropriate for human use like seawater or municipal/industrial wastewater. Microalgae are also characterized by higher lipid productivity and growth rate comparing to the yielding of

traditional crops, consequently they require significant smaller growing areas than other feedstocks of agricultural origin [9,37]. Moreover, as microalgae need only sunlight and some simple nutrients, they can grow almost everywhere; and their specific growth rates can be enhanced by the addition of definite nutrients with CO2 enriched air [38,39]. Furthermore, microalgae can be cultivated using marine or wastewater, thus they do not compete for the freshwater. Various species of microalgae can acclimatize to grow in various environmental conditions. Therefore, it is possible to find the most specific algal species to grow under local conditions, which is not possible in the case of other biodiesel feedstocks. Interestingly, utilizing of microalgae for biofuels production can also provide other functions including; (1) removal of CO2 from industrial flue gases through CO2 bio-fixation [40], reducing the GHG emissions of a company or process while producing biodiesel. (2) Wastewater treatment by removal of ammonia, nitrate and phosphate making algae to grow using these water contaminants as nutrients for dual propose to produce biomass and to treat wastewater [41]. (3) Due to its high N:P ratio, the residual algal biomass after oil extraction can be processed into biogas, used as biofertilizers or for animal feeding [9,42]. (4) Depending on the microalgal species, other compounds with valuable applications in different industrial sectors; such as polyunsaturated fatty acids, natural dyes, pigments, antioxidants and high-value bioactive compounds; may also be extracted [43–45].

3. Large scale cultivation of microalgae Microalgae exist in different habitats and need inorganic nutrients to nurture, which allow them to grow on industrial and municipal wastewater. Moreover, some species of microalgae, called halophilic, tolerate high concentrations of salts allowing them to grow on sea water, hence they do not compete for the freshwater. In addition to water, photosynthetic growth requires some inorganic salts, carbon dioxide and light. Growth medium must provide the essential inorganic salts which mainly constitute the algal cell including nitrogen, phosphorus and iron. The minimal nutritional requirements were estimated by Chisti [37] using the approximate molecular formula of the microalgal biomass as CO0.48H1.83N0.11P0.01. Phosphorus as a nutrient must be supplied in a significant excess amounts, because it forms complexes with other metal ions, that limit its availability. Thereby, algae can be used for dual propose; as biomass production and wastewater treatment by removing of nitrogen and phosphorus from the contaminated water [41,46,47]. In addition, natural sea water, supplemented with some commercial fertilizers containing nitrate and phosphate, is commonly used for cultivation of marine microalgae [48]. Carbon content in photosynthetic microalgal biomass represents approximately 50% by dry weight [49]. All of this carbon is typically derived from the continually supplied carbon dioxide during daylight hours. Producing 100 t of algal biomass fixes roughly 183 t of carbon dioxide [50]. Therefore, biodiesel production from microalgae can potentially use some of CO2 released from burning fossil fuels in power plants, which is often available at little or no cost. Different algal production systems have already achieved economic feasibility for production of high-value compounds from microalgae such as astaxanthin produced from H. pluvialis and ßcarotene from Dunaliella salina, in addition to other nutraceutical compounds. Algae can be cultivated in the traditional cultivation systems known as “raceway ponds”, which are normally open shallow ponds or channel type systems, or in closed systems known as “photobioreactors (PBRs)”.

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desired algal species, undesired organisms will certainly be introduced overtime and can severely reduce the biomass yield of the inoculated species. Once a significant competitor has taken residence in the pond, it is enormously difficult to eliminate. Out of 3000 microalgal species collected through aquatic species program, none of them was able to constantly dominate in an open pond with desirable biofuel properties [22]. Though sustained cultivation of a single species in raceway open ponds can only be done by cultivation of extremophiles; that can tolerate certain extreme environmental conditions, like high or low pH, and/or salinity, so that they can easily outcompete other organisms. For example, Spirulina sp. survives and grows well at extremely high pH (9 to 11.5); therefore it is commonly dominant species in highly alkaline ponds. The unicellular green alga D. salina rapidly grows in highly saline waters due to its high intracellular glycerol content, that provide a protection against osmotic pressure [58], and hence it is commonly dominant in highly saline ponds. In raceway cultivation system, an area is divided into a rectangular grid; each rectangle is oval shape containing a paddlewheel which is used to drive water flow continuously around the circuit. Assuming a negligible thickness for the central baffle in relation to the pond area, the surface area of the open pond shown in Fig. 3A can be calculated as follows;

A=( πc2/4)+bc Fig. 3. Surface view of a raceway cultivation system.

3.1. Open pond systems Nowadays, extensive experience exists on construction and operation of raceways for microalgal biomass production, as they have been used since the 1950s. Raceway channels are built in concrete or compacted earth, and usually lined with white material [37]. They have a variety of shapes and sizes, but the most commonly used design is the raceway pond (Fig. 3). It is a closedloop channel, in which circulation and mixing are achieved by a paddlewheel. The culture medium is added continuously in front of the paddlewheel where the flow begins, while harvest takes place commonly behind the paddlewheel, on completion of the circulation loop [37]. Production of microalgal biomass in raceway ponds as a feedstock for biodiesel has been extensively studied during the US Department of Energy's Aquatic Species Program [22]. Although raceways are low-cost algal cultivation systems, they have a low biomass productivity compared with photobioreactors. Table 2 represents the biomass productivities of different open raceway ponds located at different countries. The main disadvantages of open algal biomass production system are water loss by evaporation, due to their opening feature, and susceptibility of contamination by unwanted species. Although the open raceway pond is typically inoculated with the Table 2 Biomass productivities of different open raceway ponds. Microalgae

Anabaena sp. Botryococcus bruanii Haematococcus pluvialis Phaeodactylum tricornutum Spirulina platensis Spirulina platensis Spirulina sp

Total volume (L)

Productivity (g CDW L  1 d  1)

Location References

300 2000 100,000

0.031–0.078 0.114 0.122

Spain India China

[51] [52] [53]





282 750 135,000

0.183 0.06–0.18 0.006–0.07

Italy Israel Spain

[55] [56] [57]


Chisti [59] reported that b:c ratio is usually not less than 10, since the too low b:c ratio results in disturbances in the flow caused by the bends at the ends of the raceway which affects the flow in the straight sections of the channel. The working liquid depth in different algal pond usually ranges from 0.25 to 0.30 m. Chisti [59] reported that low depths are preferred to improve light penetration, but it cannot be much less than 0.25 m in order to avoid nutrients concentration by water evaporation. On the other hand, depths higher than 0.30 m lag light penetration which results in lower photosynthetic activity. In an open pond with a given liquid depth, the working volume can be calculated as follow;


V =Ah

The volume flow rate of the pond depends on the flow velocity, the channel width, and the liquid depth as shown in Eq. (3);

Q =vh

c 2


Open-pond design needs to consider the requirements of culture mixing, feeding, harvesting, carbon dioxide supply, drainage, possible overflow and cleaning. For culturing algae, the flow in the raceway channel should be turbulent to keep a satisfactory mixing, prevent stratification and improve desorption of the oxygen produced by photosynthesis. The homogeneity of the open pond is controlled by the paddlewheel which operates all the time to prevent sedimentation. Chisti [59] calculated the total power requirement in an open pond with water flowing at a given velocity in a straight channel of hydraulic diameter as follow;


1. 59Aρgv 3fM 2 edh0.33

(4) 2

The gravitational acceleration is 9.81 m s , and the efficiency of the motor drive of the paddlewheel is about 0.17 for the paddlewheel located in a channel with a flat bottom as calculated by Borowitzka [60]. Values for the manning factors for channels made of various materials that might be used in raceway pond construction are summarized in Table 3. In view of Eq. (4), the power demand for open pond operation depends on the flow velocity. Therefore, it must be kept to the minimum value that consistent with a satisfactory operation.


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Table 3 Manning roughness factor ( fM ) for some surfaces materials. Surface

fM (s m  0.33)

Smooth steel Smooth plastic Compacted gravel Compacted gravel lined with polymer Cement mortar lined Unfinished concrete Finished concrete Asphalt Brick

0.012 0.011 0.025 0.012 0.011 0.015 0.012 0.016 0.015

Becker [61] reported that a velocity of 0.05 m s  1 is sufficient to prevent thermal stratification, but a higher velocity of 0.1 m s  1 is needed to prevent sedimentation of algal cells. Even though, in practice, the flow is not uniform everywhere in a raceway, so that a velocity of at least 0.2 m s  1 is used to keep the flow above the minimum acceptable speed [59]. 3.2. Closed photobioreactors (PBRs) Recently, closed PBRs have been successfully used for high microalgal biomass production. Unlike open ponds, PBRs allow unialgal dominant culture growth for prolonged durations. In addition, they have minimum contamination while having the advantage of using the solar light and a higher amount of CO2 [62– 64]. Table 4 shows a comparison between PBRs and open raceway ponds for several growth and operation parameters. Noteworthy, the comparison may not be easy, as the evaluation depends on several factors; such as algal species, cultivation conditions and the method used to calculate the productivity. There is still a gap between designing a cheap photobioreactor on one hand, and building a suitable one that meets all demands of the algal cells, for enhancing the economic viability of the process, on the other hand. However, the most important advantage of closed PBRs, which might make them the system of choice for biomass production, is that they support over ten-fold higher volumetric productivity than open raceway ponds; consequently they have a smaller “footprint” on a biomass productivity basis. It means that a higher bioreactor costs can be compensated Table 4 Comparison of some parameters of open raceway ponds and photobioreactors. Parameters Operation regime

Raceway ponds

Batch or semicontinuous Volumetric productivity 0.117 3 1 (kg m d ) 56.8 Oil production (m3 ha  1)a 7828 Area needed (m  2)b Biomass production 0.14 3 (kg m ) 183,333 Annual CO2 consumption (kg)c Light utilization Poor efficiency Scale-up Difficult Process control Difficult Species control Difficult Mixing Very poor Operation costs Low Water losses High a b c



Batch or semicontinuous 1.54




5681 4

[37] [37]



Highly efficient


Easy Easy Possible Uniform High Low

[67] [65] [65] [65] [65] [65]


For microalgae with 40% dry weight oil. For meeting 50% of all transport fuel needs of the United States. Corresponding to annual biomass production of 100 t.

Fig. 4. Schema of the tubular photobioreactor system (A), and partial view of the tubular loop of the PBR (B) located in Klötze, Germany (http://www.suprabio.eu/ suprabio-consortium/igv-gmbh-igv-biotech/).

by higher biomass productivity, which is a very important goal to collect as much solar energy as possible from a given land area. The most common closed PBRs geometries are flat-plate reactors, tubular reactors and bubble column reactors [66,68–70]. The tubular system is the most efficient PBR geometry, which facilitates the diffusion of CO2, maximizes the use of solar light, by avoiding large areas of shade, as well as controlling the given temperature [37,70]. A tubular PBR (Fig. 4) consists of an array of straight transparent tubes (solar collector tubes) that are usually made of transparent plastic or glass. The construction of the world’s largest tubular photobioreactor was started in 1999 in Klötze (Saxon-Anhalt, Germany) by BisanTech, following the instructions of IGV-Biotech GmbH [68] after a test phase in a pilot scale plant which was started in 1996. The tubular PBR system, with annual algal biomass production up to 100 t, consisted of 20 independent modules with a total volume of about 700 m3. They were distributed in 500 km of tubes in a greenhouse of 1.2 ha [71]. In order to ensure a high biomass productivity of the tubular photobioreactor, the solar collector tubes diameter is generally 10 cm or less, to allow deep light penetration in the dense culture broth. The solar collector should be oriented in a position where maximize sunlight capture [48,72]. The ground beneath the solar collector is often covered with white plastic sheets or painted white to increase reflectance. A high light reflection increases the total light received by the tubes. In addition, tubular PBRs might vertically arranged in the form of helical coil using flexible plastic tubes coiled around a supporting frame. Biomass sedimentation in the tubes is prevented by high turbulence, using either an airlift pump or mechanical pump. However, airlift pumps have been used successfully than the mechanical pump [66,73,74]. The acceptable reactor cost was estimated by Schenk et al. [71] as not

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Fig. 5. Cultivation of algae in vertical hanged plastic sleeves (A) and flat-panel photobioreactors mounted on a solar tracker (B) located in Hamburg, Germany.

exceed US$ 15 per m2. Abomohra et al. [9] cultivated the green microalga Scenedesmus obliquus in a cost-effective outdoor bubble column reactor made of plastic sleeves (Fig. 5A). They confirmed that the damaged bags can be cheaply replaced; besides the technology employing plastic sleeves is simple and scalable enough to support the commercial production of a new algae-based biofuels. Although high light intensities load the photosynthetic photosystems with energy, they can lead to low yield efficiency, photoinhibition or even photo-bleaching [75,76]. Consequently, microalgae have photoprotective mechanisms which rapidly squander the excess energy as fluorescence and heat. This energy wastage can be decreased or even avoided by exposing the algal cells into low light/high light cycles. Janssen et al. [77] concluded that the frequency of these cycles should be 10 Hz or faster with dark/ light period up to 10. As a result, the algal cells behave similarly as if they are exposed to constant moderate light [78]. The flashing light effect in photobioreactors can be fully controlled by mixing through the optimized cell transfer from bright zones to dark zones and vice versa in a regular mode [79]. In order to provide moderate light intensities for the algal cells, the PBR should be designed to distribute light over a large surface area “light dilution”. This approach is usually achieved by arranging the reactors units in a fence-like structure. The fences should be adjusted in a south-north direction to avoid direct bright light and increase the period of exposure [80]. Moreover, there is a complex interchange between culture mixing and light attenuation inside the reactor, as each single algal cell passes through dark and light zones in different statistical manners [81]. Schenk et al. [71] concluded that the light dilution effect in tubular PBRs can be optimized by adjusting the surface reactor area up to ten times larger than the equivalent footprint area. Similar statements can be made for bubble columns or plate PBRs by mounting them at a defined angle to the sun. Nevertheless, one basic design principle is to increase the “surface to volume ratio” which results in shorter light path lengths and higher biomass yield. Values of 400 m2 m  3 are state of the art for such designs, so that a small culture volume and less energy for mixing are required for a given biomass yield. Mixing is necessary in all PBRs, as it prevents sedimentation of the cells and provides homogenous distribution of CO2 and O2 [48]. A partial CO2 pressure of at least 0.15 kPa has to be maintained to prevent kinetic CO2 uptake limitation. In addition, a stoichiometric concentration of 1.8 kg CO2 per kg of biomass has to be provided, which makes using of flue gas useful [50]. A first demonstration microalgal pilot plant used for bio-fixation of CO2 produced by a local power plant has been built in Hamburg, Germany in 2008. The plant is located in Hamburg-Reitbrook in Northern Germany (53°28′12″N; 10°10′40″E). The outdoor flat-PBRs (European patent

No. 2228432, developed by SSC Ltd.) use natural sunlight and flue gas from the power plant as energy and carbon sources, respectively. Up to seven PBR panels were mounted on one solar tracker, each covering 2 m2 and containing 30–45 L of microalgal suspensions (Fig. 5B). The irradiance on the surface of each PBR was controlled by the solar tracker by adjusting it to the sun at two different orientations. In order to obtain maximum irradiance, the PBRs were always exposed perpendicularly to the sun (standard orientation). However, Hindersin et al. [66] reported that at biomass concentrations below 1.1 g L  1 and irradiances of Z 1000 mmol photons m  2 s  1 photosynthetic active radiation (PAR), photoinhibition of about 35% takes place with fast increase in temperature within 3 h from 12 to 35 °C. They adjusted new modes; “offset mode” to overcome photoinhibition by light control, and “temperature mode” to overcome overheating by temperature control. In offset and temperature modes, the solar trackers turned away automatically from the sun when the light intensity or temperature of the culture medium, respectively, increased above a certain set values. These new orientations enhanced the cellular growth by reduction of the photoinhibition and temperature increase with average areal productivity of 9 g m  2 d  1 [82]. As a general statement, choice of the suitable cultivation system is situation-dependent, dictated by both the final intended purpose of biomass and the used algal strain. However, attention has shifted mostly on closed PBRs, because of the need of accurate control which impaired the use of open raceway ponds. Despite several research efforts for the design and operation of different PBRs; developing of a suitable reactor with optimum cultivation procedures, to increase the efficiency of using solar energy and carbon dioxide with lower operation costs, is a major challenge for the industrial microalgal biomass production.

4. Quantitative and qualitative feasibility of microalgal biodiesel 4.1. Quantitative and qualitative feasibility 4.1.1. Lipids Over the past few decades, several thousands of algae have been screened for high lipid content. Several hundreds of them were identified as oleaginous species which are belong to diverse taxonomic algal groups. The lipid content of microalgae varies obviously among different species and strains within and between taxonomic groups. The division Chlorophyta represents the largest taxonomic group from which oleaginous algae have been identified. This may be not because of the higher lipid content of the green algae compared with other algal taxa, but rather because the


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Table 5 Average laboratory lipid content and lipid productivity for some microalgae reported in the literature. Algal Species

Taxaa Lipid content Lipid productivity (% CDW) (mg L  1 d  1)


Ankistrodesmus falcatus Botryococcus braunii Chaetoceros calcitrans Chaetoceros muelleri Chlamydomonas reinhardtii Chlorella emersonii Chlorella minutissima Chlorella pyrenoidosa Chlorella sorokiniana Chlorella vulgaris Chlorella zofingiesis Chlorococcum oleofaciens Chlorococcum sp. Ellipsoidion parvum Haematococcus pluvialis Isochrysis galbana Koliella antarctica Monodus subterraneus Nannochloropsis oceanica Nitzschia palea Pavlova lutheri Pavlova salina Phaeodactylum tricornutum Porphyridium purpureum Porphyridium cruentum Scenedesmus obliquus Scenedesmus quadricauda Skeletonema costatum Synechococcus sp. Tetraselmis suecica Thalassiosira pseudonana





Ch Oc Oc Ch

43 40 43.4 24

13 18 51.1 15

[84] [88] [88] [89]

Ch Ch Ch Ch Ch Ch Ch

29 31 34 10 53 55 17

8 10 48 97 144 22 35

[90] [90] [28] [90] [91] [92] [84]

Ch Es Ch

19 17 4

54 16 2

[35] [84] [84]

Ha St Es Es

20 22 16.1 54.3

30 17 30.4 444.7

[93] [84] [88] [94]

Ba Ha Ha Ba

47 35.5 30.9 18.7

48 50.2 49.4 44.8

[90] [88] [88] [88]









Ch Ch

19 18

41 35

[84] [88]

Oc Cy Ch Oc

21.1 29.0 12.9 20.6

17.4 35.9 36.4 17.4

[88] [95] [88] [88]

a Key to taxa: Ch Chlorophyta, Oc Ochrophyta, Es Eustigmatophyta, Ha Haptophyta, St Streptophyta, Ba Bacillariophyta, Rh Rhodophyta, Cy Cyanobacteria.

ubiquitous diverse of green algae in natural habitats and their higher growth rate [83,84]. Data of lipid content of different microalgae are available and consistently reported in the literatures. Table 5 summarizes the lipid content and lipid productivity reported in the literature for some of microalgae grown under laboratory conditions. However, the lipid content increases significantly under unfavorable culture conditions. Bhowmick et al. [85] and Singh et al. [86] reviewed the existing and emerging strategies towards achieving overproduction of lipids in microalgae. An additional algal characteristic for biodiesel production is the chemical suitability of the produced lipids, e.g. proportion of triglycerides, degree of fatty acids saturation and chain length. The majority of microalgae have a similar lipid profile commonly equivalent to vegetable oil; which is suitable, or sometimes superior, for biodiesel production [96]. Lipid content, proportion of various lipid classes (particularly triglycerides) and fatty acid profile vary widely according to the culture conditions [9,97] and other microorganisms grown symbiotically with microalgae. For instance, while screening of microorganisms in domestic municipal wastewater at Shenzhen university town in China for bacterial and microalgal biodiversity, we came across some microalgae with variable lipid contents and fatty acid profiles. The isolated

microalgae reacted differently as the composition of wastewater varied. In addition, a correlation was recorded between the lipid content of certain microalgae and specific bacterial strains numbers. The later aspect makes it difficult to compare the lipid content and fatty acid profile of different algal species. 4.1.2. Fatty acids In addition to increasing oil content and productivity of microalgae, it is also desirable to improve the quality of the produced biodiesel. Although fatty acid profile does not appear to have much impact on the production process of biodiesel by the transesterification, it affects the properties of the produced fuel. For example, the high proportion of saturated fatty acids enhances the oxidative stability and cetane number of the biodiesel, but rather with poor low-temperature properties and it more likely behaves as coagulate at ambient temperatures. Conversely, biodiesel produced from feedstocks with high proportion of polyunsaturated fatty acids (PUFAs) shows good cold-flow properties but with lower cetane number and poor oxidative stability during prolonged storage. Understanding the metabolic engineering of fatty acid biosynthesis promises to create a microalgal strain capable of economically producing a high quality biodiesel. Algae de novo synthesize fatty acids as building blocks for the formation of mono-, di- and triacylglycerides. According to Ohlrogge and Browse [98], acetyl-CoA enters the pathway as a substrate for acetyl-CoA carboxylase (ACC) as well as for the first condensation reaction catalyzed by 3-ketoacyl ACP synthase (KAS). Malonyl CoA: ACP transferase (MCAT) transfers malonyl from malonyl-CoA forming malonyl-ACP. The later is the carbon donor for subsequent elongation condensation reactions. After subsequent condensations, the 3-ketobutyryl-ACP is reduced, dehydrated and reduced again by 3-ketoacyl ACP reductase (KAR), 3-hydroxyacyl-ACP dehydrase (HAD) and enoyl-ACP reductase (EAR), respectively, forming butyryl-ACP (Fig. 6). The later is further elongated through condensation reaction catalyzed by KAS in a repeated cycle. Mühlroth et al. [99] reported that the first acylation occurs in endoplasmic reticulum at the first carbon of glycerol-3-phosphate (G3P) by glycerol-3-phosphate acyltransferases (GPAT). Afterward, the lysophosphatidic acid (Lyso-PA) is acylated to the second carbon by lysophosphatidate acyltranferase (LPAAT) forming phosphatidic acid (PA). The later is dephosphorylated to produce diacylglycerol (DAG), then it is used as primary precursor for biosynthesis of structural lipids (phospholipids), or for storage lipids (triacylglycerol, TAG) which deposit in the cytosol as ER-derived lipid droplets [100]. In addition, chloroplast specific TAG biosynthesis was observed from its DAG precursor by chloroplast specific acyltransferases. Fan et al. [101] confirmed the biosynthesis of chloroplast specific TAG containing exclusively C16 fatty acids in Chlamydomonas reinhardtii, which accumulated as lipid droplets inside the chloroplasts. Similar to those of higher plants, microalgae commonly synthesized C16 to C18 chain length fatty acids [98]. However, greater variation in fatty acid composition was found in different taxonomic algal groups. Some algae are able to synthesize medium-chain fatty acids (e.g. C10, C12 and C14) as predominant fatty acids, whereas others produce very long chain fatty acids (4 C20). In addition, the fatty acid composition of the same microalga can vary both qualitatively and quantitatively according to the culture conditions and its physiological status. The most important fuel properties that evaluate the potential of biodiesel as a substitute of diesel fuel are kinematic viscosity, specific gravity, cetane number, cold filter plugging point (CFPP) and iodine value [102,103]. High cetane number is one of the most important fuel indicators of better combustion, easier engine startup and low nitrous oxide emissions [104,105]. On the other hand, higher iodine values may result in the polymerization of glycerides and deposition of lubricant in the engine [106]. The melting point

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Fig. 6. Pathways of de novo synthesis of fatty acids in chloroplasts (dashed line) and TAG accumulation pathways in chloroplast and endoplasmic reticulum. CoA: coenzyme A, ACC: acetyl CoA carboxylase, MCAT: malonyl CoA:ACP transferase, ACP: acyl carrier protein, KAS: 3-ketoacyl ACP synthase, KAR: 3-ketoacyl ACP reductase, HAD: 3-hydroxyacyl ACP dehydrase, EAR: enoyl ACP reductase, GPAT: glycerol-3-phosphate acyltransferase, G3P: glycerol-3-phosphate, Lyso-PA: lysophosphatidic acid, LPAAT: lysophosphatidic acid acyltransferase, PA: phosphatidic acid, PAP: phosphatidic acid phoaphatase, DAG: diacylglycerol, DAGAT: diacylglyceryl hydroxymethyl trimethyl-β-alanine, TAG: triacylglycerol, FATE: fatty acid thioesterase and ACS: acetyl-CoA synthetase.

Table 6 Comparison of microalgal biodiesel properties and the international biodiesel standards [109]. Properties







US (ASTM D6751-08)

Europe (EN 14214)

Kinematic viscosity at 40 °C (mm2 s  1) Specific gravity (kg  1) Cloud point (°C) Cetane number Iodine value (g I2/100 g CDW) HHV (MJ kg  1) Average Unsaturation Cold Filter Plugging Point (CFPP)

4.67 0.877 8.78 57.27 75.18 40.01 0.84  6.51

4.90 0.875 13.58 59.68 48.41 39.38 0.48 6.91

4.91 0.875 13.85 59.81 46.92 39.34 0.46  3.31

5.04 0.874 16.66 61.21 31.30 38.97 0.25  2.91

5.07 0.873 17.19 61.48 28.33 38.90 0.20 1.69

4.95 0.875 14.65 60.21 42.46 39.24 0.40  4.38

1.9–6.0 0.85–0.9 – Minimum 47 – – – –

3.5–5.0 – – 51–120 Maximum 120 – –  13 to  5

LC8 showed 100% similarity with Chlorella vulgaris SAG 211-11b, RP1 showed 100% similarity with Chlorella sorokiniana CCAP 211/8K, IL2 showed 100% similarity with Dictyosphaerium ehrenbergianum CCAP 222/10, IL3 showed 99.89% similarity with Micractinium sp., LC3 showed 99.78% similarity with Micractinium pusillum CCAP 248/3 and LC11 showed 99.66% similarity with Micractinium pusillum CCAP 248/3 (and 248/1).

of unsaturated fatty acids is always lower than that of saturated fatty acids. Therefore, when the oil contains mostly saturated FAMEs (very low iodine value), crystallization may occur at the engine operation temperature [106] leading to poor CFPP properties. In general, most of these parameters are within established limits by European (EN) and American Society for Testing and Materials (ASTM) biodiesel standards [9,107–109]. Table 6 summarizes the biodiesel properties from the oil of microalgae isolated from soda lakes and freshwater by Selvarajan et al. [109]. All isolated species showed a value of cetane number ranged from 57 to 61, which is in accordance with the ASTM and EN standards reported as a minimum cetane number of 47 and 51, respectively (Table 6). The reported high kinetic viscosity has lubricant properties which enhances the engine performance. Iodine value of the studied microalgae was found to be less than 76 g I2/100 g CDW, which meets the European biodiesel standards reported a maximum iodine value of 120 g I2/100 g CDW. The low degree of unsaturation found in the studied microalgae is crucial for the overall performance of the engines. As general statement, regardless of CFPP, all other studied biodiesel properties of the six strains shown in Table 6 were in accordance with the American and/or European standards, revealing the efficiency of microalgal oil as a feedstock for biodiesel. Furthermore, Table 7 shows a comparison of typical

Table 7 Comparison of typical properties of biodiesel from microalgae and wood feedstocks. Properties



C (%) O (%) N (%) H (%) S (%) Heating value (MJ kg  1) Density (kg/l) Viscosity at 40 °C (Pa s)

61.52 20.19 9.79 8.50 0 29 1.16 0.10

56.4 37.3 0.1 6.2 0 21 1.2 0.04

a Data presented here are the mean of two microalgae, Chlorella protothecoides and Microcystis aeruginosa [111]. b Data of pyrolysis of Pine (Pinus brutia) according to Şensöz and Can [110].

properties of bio-oils obtained from fast pyrolysis of wood [110] and microalgae [111]. It was indicated that microalgal oil has a higher carbon content, which results in higher heating value, and higher viscosity compared to Pinus brutia oil, revealing the superiority of microalgal oil as a feedstock for biodiesel over the plant oils.


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Acceptable price of biomass ( US$/ton)=Ppetroleum/M

Fig. 7. The accepted price of algal biomass depending on algal lipid content and petroleum price. Data were recalculated from Chisti [117].

4.2. Economic feasibility Microalgae, in comparison with macroalgae, have a much more rapid growth rate and higher lipid content under optimal conditions. Moreover, they alter their metabolic products to accumulate natural oils (triaclyglycerols) as storage compounds under stress conditions. These characteristics add to their increased appeal for utilization in biodiesel production. In addition, they show high biodiesel conversion efficiency which was estimated by 95.9% from the oil extracted from Schizochytrium limacinum containing 57% oil [112]. Stephenson et al. [113] reported that C. vulgaris can produce a total biodiesel of 8.2 t ha  1 y  1. However, Abomohra et al. [9] reported about 12 t ha  1 y  1 biodiesel productivity of S. obliquus cultivated outdoor in transparent plastic sleeves. Moreover, in a running study at Harbin Institute of Technology, the estimated lipid productivity of S. obliquus outdoor cultivated in municipal wastewater was 18 t h  1 y  1 (unpublished data). Chisti [37] illustrated that in order to reach an economical balance, the residual biomass after lipid extraction can be transformed into methane via anaerobic digestion which can also recycle back nitrogen and phosphorus. In a previous study, using of 0.4 g L  1 of residual oil-free algal biomass increased the survival percent and average fresh weight of Artemia by 86% and 24%, respectively, over the control [9]. Moreover, the glycerol produced from the transesterification process can also be converted to several chemical products or fermented to produce biogas or bioethanol. From the economic point of view, microalgal biodiesel must be competitive with petroleum diesel which is, at present, less expensive. The net outcome of microalgae-based biodiesel production technology varies with the used microalga, different culture systems and different methods used for biomass harvest and algal refinery [114,115]. However, the competitiveness of biodiesel with petroleum diesel depends mainly on the cost of algal biomass production. One way to approach the competitiveness issue is to estimate the maximum price of algal biomass, which can then be compared with the current production cost. Chisti [116] reported that the quantity of algal biomass equivalent to the energy of a barrel of crude petroleum can be estimated by Eq. (5);

M = Epetroleum/⎡⎣ q ( 1 − w) Ebiogas + ywEbiodiesel ⎤⎦


where Epetroleum is  6100 MJ, q is  400 m3 of biogas per ton of residual algal biomass; Ebiogas is  23.4 MJ per m3 of generated biogas; and Ebiodiesel is  37800 MJ per ton of algal oil [37]. According to Chisti [116], the maximum acceptable price of microalgal biomass would be the same as the price of a barrel of crude petroleum; thus


Using Eq. (6), the expected acceptable price of microalgal biomass containing various levels of oil (10–60% by weight) could be calculated as shown in Fig. 7 for crude petroleum prices of up to US$1000 per barrel [116]. Kang et al. [117] concluded that the cost of biomass production in the open raceway pond could be US$ 2710 per ton, and concluded that there was provision to reduce the cost further. Using the previous calculations at the price of petroleum diesel in March 2014 of US$ 124 per barrel (data obtained from US Energy Information Administration, 17 March 2014, http://www.eia.gov/ petroleum/gasdiesel), microalgal biomass production with an oil content of 40% will need to be produced at cost of less than US$ 360 t  1 to compete with petroleum diesel. However, at the present decline in diesel price (US$ 61.7 per barrel, US Energy Information Administration, in March 2016), microalgal biomass production with oil content of 40% should cost less than US$ 179 t  1. On the other hand, Satyanarayana et al. [8] estimated the cost of 1 L of biofuel produced by algal biomass to be US$ 2.8. In order to potentially replace petroleum, microalgal oils production costs need to be related to the current price of petroleum diesel according to the following equation;

ACalgae ( US$ per liter of algae oil)=Ppetroleum x85.22 × 10−4


However, the previous equation disregards the possible additional income from biomass residues and other refining processes of microalgae. Nevertheless, at the price of petroleum diesel of US$ 124/barrel, microalgal oil should not cost more than US$ 1.057 L  1. However, at the current price of petroleum diesel (US$ 61.7 per barrel, March 2016), microalgal oil should not cost more than US$ 0.526 L  1. Regardless the current temporary decline in the price of petroleum diesel, Department of Energy and Climate Change report [118] concluded that the price of petroleum diesel is predicted to rises to US$ 190/barrel by 2030. Therefore, microalgal oil costing US$ 1.619 L  1 will be likely to economically substitute for crude petroleum. Supposing the price of petroleum diesel raised to US$ 329/barrel, the current production cost of algal diesel ( EUS$ 2.8/ L) will be acceptable to substitute petroleum diesel.

5. Conclusion The search for beneficial biodiesel sources should focus on feedstocks that do not compete with food crops, do not lead to landclearing and provide GHG reductions. In addition, coherent biofuel policies must address the social context of agricultural production. Although, microalgae have been shown to be a potential source for that purpose, their cost is still high comparing to petroleum-derived diesel. Extensive efforts, all over the world, are already underway to achieve competitive large scale microalgal oil production, but for the moment it is still very limited approach. So that, large interest and focus from many governments and private funding bodies is taking place to address these challenges in the near future.

Acknowledgement The authors would like to acknowledge Shenzhen Government, China for financial support (Project ID JCYJ20150529114024234).

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