Anaerobic digestion of microalgae for biomethane production

CHAPTER

Anaerobic digestion of microalgae for biomethane production

15

´ 2, Marcin De˛bowski2 Ewelina Jankowska1, Marcin Zielinski and Piotr Ole´skowicz-Popiel1 1

Institute of Environmental Engineering, Faculty of Civil and Environmental Engineering, Poznan University of Technology, Poznan, Poland 2Department of Environment Engineering, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland

15.1 INTRODUCTION Since the traditional biomass used for biofuel production has been considered to not be fully carbon-neutral, the research community is looking for a new, alternative, and completely sustainable source for biofuel and bioproduct production (Gerardo et al., 2015; Naik et al., 2010) that would be able to overcome the disadvantages of first- and second-generation biofuels. The third generation of biofuels, derived from microalgae biomass, could be the solution that the research community is looking for (Brennan and Owende, 2010). The potential of microalgae biomass and its competitiveness in comparison to terrestrial biomass derives from a higher photosynthetic efficiency (3 5 times higher), a shorter harvesting cycle (1 10 days) (Mobin and Alam, 2018), and a rapid growth rate (5 10 times faster in favorable conditions compared to terrestrial biomass) (Kro¨ger and Mu¨ller-Langer, 2012). All of this results in a higher oil production rate (by up to 91%) (Mobin and Alam, 2018). Moreover, the cultivation process is not in competition with human and animal food and feed production, mainly due to the use of barren areas (deserts or coastal land) (Saharan et al., 2013). To provide the nutrients necessary for growth and to avoid high costs of cultivation, wastewater could be used as a cultivation medium (with a reduction of the consumption of fresh water and nutrient supplementation) (Rusten and Sahu, 2011). These valuable properties of microalgae, together with their composition (lipids .60%, carbohydrates 64%, and proteins .71%; % in dry biomass) (Ravindran et al., 2016) and intracellular products [e.g., fatty acids (eicosapentaenoic acid, docosahexaenoic acid), carotenoids, antioxidants, enzyme polymers, toxins, and sterols] make them an extremely interesting subject of many studies (Maity et al., 2014; Zhu et al., 2014). According

Second and Third Generation of Feedstocks. DOI: https://doi.org/10.1016/B978-0-12-815162-4.00015-X Copyright © 2019 Angelo Basile and Francesco Dalena. Published by Elsevier Inc. All rights reserved.

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to these, microalgae have been widely studied for the production of biofuels. Through fermentation of microalgal carbohydrates it is possible to produce bioethanol (Harun et al., 2011, 2009; Harun and Danquah, 2011; Ho et al., 2013; Zhou et al., 2013b) or butanol (in acetone butanol ethanol fermentation) (Cheng et al., 2015). Biodiesel can be obtained through the transesterification of lipids (Converti et al., 2009; Lee et al., 2010; Li et al., 2007). On the other hand, the nontreated and pretreated microalgae biomass or the residues after lipid extraction could be used as a substrate in anaerobic digestion (AD) for methane (Gonza´lez-Ferna´ndez et al., 2012a,b; Mussgnug et al., 2010) and dark fermentation for hydrogen production (Yang et al., 2011, 2010). The results of previous works concerning microalgae-based biofuels have indicated that it would not be cost-effective to focus only on the strict generation of one product (Arashiro et al., 2018; Arias et al., 2018; Jankowska et al., 2017; Mobin and Alam, 2018). Today, most of the studies concerning biogas production are focused on integration with other algal-based production processes (e.g., biodiesel, bioethanol, high-value products, etc.) together with wastewater treatment (Chen et al., 2018a,b). The biorefinery concept could be the solution to increasing the opportunity for commercialization of microalgae processing and the answer to drawbacks and constraints in the up-scaling. In this chapter, biogas production from microalgae biomass is described. It consists of cultivation, harvesting, and processing it via AD. Furthermore, the limitations and possible solutions to overcome obstacles towards scaling-up are discussed.

15.2 MICROALGAE CULTIVATION SYSTEMS The types of systems for microalgae biomass production determine the profitability of using microalgae for energy production purposes. Microalgae cultivation can be carried out using a variety of methods, ranging from advanced technological solutions in which the process is strictly monitored and controlled, and ending with less predictable techniques based on the use of open tanks (Molina Grima et al., 2010). The examples of open systems are ground or concrete ponds, circular ponds with a rotating mixing arm, paddle-wheel mixed ponds, and cascade ponds (Borowitzka, 1999). Closed systems are mainly photobioreactors of various designs. In contrast to open systems, closed systems provide the possibility of constant control over the intensity and time of light exposure, temperature of the cultivation medium and, predominantly, limit the contamination of the medium by predators, parasites, or competing species of microalgae. The most commonly used photobioreactors are: plastic bags, tubular horizontal, vertical, or angled at any angle photobioreactors, biocoil reactors, and flat panels (Kaewpintong et al., 2007; Pulz, 2001; Tredici, 2002).

15.3 Technological Parameters of Microalgae Cultivation

Photobioreactors are the most universal devices, and can be used in different climatic zones. Under conditions in the reactor, cultures of specific species of microalgae, for example, with a high concentration of oil in the biomass, can be cultivated. Unfortunately, so far, it has not been possible to develop a system which is justified in terms of economic viability. The construction of photobioreactors is expensive, has high operating costs (lighting, supply of carbon dioxide), and causes operational difficulties, for example, by overgrowing and limiting light penetration (Janssen et al., 2003; Lee, 2001; Lo´pez et al., 2006; Sa´nchez Miro´n et al., 2002). However, the operation of open systems on a technical scale is, in many cases, justified in terms of investment and exploitation costs. The examples are a circular ground pond with an area of up to 250 ha and a depth of up to 0.5 m or a racetrack pond with paddle-wheel mixing (Mara et al., 1998; Tredici and Materassi, 1992). Cultivation medium usually includes properly composed chemical substances. Carbon dioxide is typically obtained from atmospheric air by the principle of diffusion (Tredici and Materassi, 1992). Operation of open systems is directly related to large water losses due to evaporation, relatively low efficiency of biomass growth, limitation of the possibility of cultivating of specific species of algae, and high susceptibility to infections, diseases, and parasites. Such systems are effective in areas with high solar radiation and unrestricted access to water, and thus mostly in coastal areas. Mainly microalgae from the genera Spirulina, Chlorella, and Scenedesmus (Mara et al., 1998) are cultivated in such systems. The effectiveness of algal biomass production in various technological systems is presented in Table 15.1.

15.3 TECHNOLOGICAL PARAMETERS OF MICROALGAE CULTIVATION The nutrients essential for the efficient growth of microalgae are nitrogen, phosphorus, and iron (Liu et al., 2008). High concentrations of nitrogen in the culture medium usually stimulate and intensify the growth of microalgae biomass. The limiting character resulting from the presence of this element is observed only in specific situations, for example, in conditions of high concentration of ammonium ions in the environment (De˛bowski et al., 2013). Nitrogen deficiency significantly reduces the growth rate of biomass and influences the final effects of cultivation. The technological efficiency of systems for the intensive production of microalgae biomass can also be significantly inhibited by a low concentration of phosphorus compounds. It is assumed that from 1 kg of phosphorus it is possible to produce nearly 50 kg of microalgae dry matter. The availability of organic carbon, in contrast to nitrogen and phosphorus, rarely limits the growth of autotrophic microalgae, while it might be a factor decreasing the efficiency of cultivation in heterotrophic or mixotrophic systems. In photobioreactors, the high concentration of organic carbon stimulates the growth of competitive

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Table 15.1 Comparison of Systems for Microalgae Biomass Production Cultivation System

Biomass Concentration (g/L)

Biomass Productivity (g/m2 days)

References

Open Systems Open ponds reactors

0.35 0.1 0.4 0.25 1.0

11.0 10 20 10.0 20.0

0.5 1 1.8

4.1 21.0 10 25 11.4

Ozkan et al. (2012) Wiley et al. (2011) Christenson and Sims (2011) Doucha et al. (2005) Jonker and Faaij (2013) Wiley et al. (2011) DeÎbowski et al. (2011)

Closed Systems Tubular photobioreactors

1.5 1.7

Biofilm photobioreactor

1.5 2.0 1.02 2.7 1 2 89.6 103.2 70.0

Biocoil reactor Alveolar Airlift

1.45 1.20

Flat-plate photobioreactor

15.0 20.0 30.0 25 50 25.0 27.0 25 50 0.65 0.77

2.0 20.0

Christenson and Sims (2011) Jonker and Faaij (2013) Wiley et al. (2011) Ozkan et al. (2012) Ozkan et al. (2012) Wiley et al. (2011) Ozkan et al. (2012) Christenson and Sims (2011) Pittman et al. (2011) Tredici et al. (1997) Acién Fernández et al. (2001)

microorganism species, including bacteria that increase the turbidity of the medium and thus reduce the efficiency of light penetration and finally reduce microalgae biomass growth. Many species of microalgae for intensive growth require an external source of vitamins, such as thiamine, biotin, B12 (Miyamoto et al., 2002), and riboflavin, purines, pyrimidines, and other growth factors. The ratio of basic nutrients in the medium often used for microalgae biomass growth, for example, in wastewater is 20:8:1 (C:N:P), while the optimal ratio from a technological point of view should be 106:15:1 (De˛bowski et al., 2013). Thus, carbon compounds, mainly inorganic, should be supplemented, which can be obtained by increasing the intensity of CO2 saturation or introducing into the culture effluents from fermentation chambers (De˛bowski et al., 2013). During intensive biomass growth it is necessary to provide about 2 kg CO2 for cultivation of 1 kg of microalgae dry mass. Carbon dioxide assimilation and oxygen

15.3 Technological Parameters of Microalgae Cultivation

production by microalgae during photosynthesis might increase potential of hydrogen (pH) to values of 10 11 in both open and closed systems. An increase in pH value is beneficial due to a reduction in the number of pathogenic organisms present in wastewater. However, a high pH value might decrease the efficiency of a wastewater treatment by reduction of microalgae growth and limitation of nutrient utilization (Oswald, 1995; Schumacher et al., 2003). Therefore, it is necessary to monitor and control the pH value in cultivation systems and maintain this parameter at a level ranging from pH 6 8. Some of the eurobiontic strains tolerate pH changes in a wider range. The activity of microalgae from the genus Chlorella is significantly reduced when the pH value decreases below 5 or increases above 9. The optimum temperature for most species of microalgae is maintained at 20 C 35 C. These conditions are often difficult to ensure, especially when microalgae biomass production systems are integrated with wastewater treatment processes carried out in open systems in a temperate climate. The outdoor operation of the photobioreactors in climate at lower temperatures forces the use of heating, which affects the economic efficiency of production. In addition, a temperate climate is characterized by high variability depending on the season. An increase in temperature of the medium from 25 C to 30 C caused a twofold increase in growth rate of microalgae and effective removal of pollutions from wastewater (Mun˜oz et al., 2004). Chevalier et al. (2000) observed that strains isolated from Arctic and Antarctic environments can grow effectively in wastewater treatment systems at a temperature of 15 C. Sunlight is undoubtedly the best possible type of light source for microalgae cultivation. However, solar energy is available only during cloudless days. In temperate climates, the intensity of natural sunlight varies significantly depending on the season. The photosynthetic activity of most microalgae species increases with the intensity of the supplied light energy in the range of 200 400 μmol E/(m2 s) (Ogbonna and Tanaka, 2000), which corresponds to about 10% of the amount of light that can be obtained directly from the Sun. In the case of microalgae, the requirements for the amount of light are slightly smaller than those of terrestrial plants. For example, Chlorella vulgaris grows at a light exposure of 50 100 W/m2, which corresponds to values from 232 465 μmol E/(m2 s) of photosynthetically active radiation values (in photometric units it is from 13,000 to 26,000 lx). For many microalgae species optimal lightening is in the range from 5000 lx [90 μmol/(m2 s)] to 13,000 lx [230 μmol/(m2 s)] and temperature between 17 C and 20 C. Recently, daylighting technology has been developed equipped with modern fiberoptic systems. This technology might be applied for intensive CO2 biosequestration and wastewater treatment by microalgae. Due to the fact that access to sunlight is only during the day, the best method of cultivation is utilization of hybrid systems in conjunction with light-emitting diodes (LEDs) (Szwaja et al., 2016), because most devices for intensive biosequestration and wastewater treatment are designed for continuous operation. A high level of dissolved oxygen (in connection with high intensity of lightening) might cause

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photoinhibition that results in damage to microalgae cells and reduces the efficiency of wastewater treatment (Suh and Lee, 2003). An increase in oxygen concentration in cultivation medium to a level of 29 mg/dm3 caused a decrease in photosynthesis efficiency of 98% (Lee and Lee, 2003). Infections by parasitic fungi such as Chytridium sp. or the development of trophic chains in the photobioreactors can cause an unexpected decrease in the efficiency of microalgae biomass production. This type of technological difficulty can be limited by periodically lowering the oxygen level in the system in order to inhibit the growth of higher aerobic organisms in the photobioreactors.

15.4 HARVESTING Harvesting of microalgae biomass is one of the major bottlenecks in the largescale production of biofuels. The costs of harvesting contributes 30% of the total production costs, mainly because of the relatively low concentration in culture media (0.5 5 g/L), small size of cells (3 50 μm), and density compared to that of the medium (Roselet et al., 2017; Vandamme et al., 2010). The effective harvesting strategy should provide efficient capacity to process very large volumes of culture broth together with extensive water removal (from 0.05% to 20% of dry matter content), complete harvesting (without selective pressures on the culture), and recirculation of the culture medium. Simultaneously, the process need to be energy-efficient, cost-effective, and harmless for the quality microalgal biomass (to avoid valuable materials being lost into the medium) (Gerardo et al., 2015). Currently, harvesting is achieved by centrifugation, filtration, flotation, flocculation, and sedimentation, but not all of these methods are suitable for implementation in commercial systems (Gonza´lezGonza´lez et al., 2018). The selection of appropriate harvesting technology is related to the type, density, and size of microalgae cells, the requirements of downstream processing, and the value of the end product (Brennan and Owende, 2010). For example, a wide range of cell sizes (0.5 200 μm) could impact the filtration process (Gerardo et al., 2015). Gravity filtration is an efficient method for harvesting of relatively large microalgae. The smaller ones could theoretically be harvested using ultrafiltration, but the risk of rapid fouling caused by extracellular organic matter (EOM) is possible. The application of fouling-reduction strategies increases the costs of separation, which makes the filtration methods not attractive for use in a full-scale system (Vandamme et al., 2010). The second key physical property is the shape and form of the microalgae cells. The flagellated cells (e.g., Scenedesmus, Chlamydomonas reinhardtii) can be mobile in the medium and avoid flocculation or even swim out of the flocs. Furthermore, cell structure and spine integrity can be damaged during mechanical harvesting (Gerardo et al., 2015). Another property is the cell surface charge, that is, zeta potential. The zeta

15.4 Harvesting

potential depends on the chemical functional groups (e.g., carboxyl and aminogroups) presented in the surface. These groups can change with cell age and culture conditions which could result in charge fluctuation from 2 to 75 mV (Greenwell et al., 2010; Zhang et al., 2012) and influence the dose of flocculants used in the chemical flocculation. The next key parameter is the cell density, for green microalgae it was determined as 1070 kg/m3 ton (Henderson et al., 2008). Consequently, the differences in solid liquid densities have a strong influence on the gravity-based methods for separation (i.e., gravity filtration, sedimentation) (Gerardo et al., 2015). The EOM causes severe fouling in the membrane filtration process and affects the surface chemistry of mineral particles (inhibition or promotion of floc formation and chelating metal cations) during the sedimentation flocculation separation. The EOM consists of proteins, polysaccharides, or polysaccharide-like substances the overall concentrations of which increase with the age of the microalgae culture (Greenwell et al., 2010). The physical and chemical characteristics of microalgae cells should be carried out before determining the separation method. Moreover, the harvesting process chain should be considered. In onestage harvesting, a high degree of concentration has to be achieved, whereas in two-stage harvesting the concentration can be split into two steps, resulting in energy saving and better cost efficiency (Vandamme et al., 2015a). The two-stage harvesting process consists of primary or bulk harvesting [concentration of total suspended solids (TSS) up to 2% 7%] and dewatering (concentration of TSS up to 15% 25%) (Gerardo et al., 2015). The first stage could be carried out as flocculation combined with gravity sedimentation or flotation. In the second stage, mechanical methods (e.g., centrifugation, filtration) are used for final water removal (Bilad et al., 2013; Vandamme et al., 2015a). Not all the harvesting methods are suitable for implementation in full-scale systems, for instance, expensive filtration or energy-intensive centrifugation are not likely to be chosen. Currently, the most promising low-cost technologies to harvest microalgae are flocculation and sedimentation (Gonza´lez-Gonza´lez et al., 2018; Roselet et al., 2017; Vandamme et al., 2015a) and these are described in more detail below. The description of several natural technologies for harvesting of microalgae which could possibly be implemented in a full-scale system are summarized in Table 15.2.

15.4.1 SEDIMENTATION The sedimentation process is one of the simplest methods for harvesting microalgae biomass. The suspended microalgal cells, that have a density greater than water, can be separated by gravitational settling. The process is carried out in conventional sedimentation systems (e.g., lamella-type sedimentation tanks or clarification tanks), where the level of TSS in preconcentrated slurry ranges from 1% to 3% (Uduman et al., 2010). The key advantages over the other harvesting methods are: the lower capital and operating costs, low energy demand, no influence on

411

Table 15.2 Comparison of Several Harvesting Methods Suitable for Full-Scale Systems—Chemical Flocculant

Separation Efficiency (%)

Advantages

Limitations

References

5

100

Nontoxic, natural

Dependent on pH

Roselet et al. (2017)

70 mg/L 15 mg/L

9 5

100

70 mg/L 20 mg/L

9

0.15 g/L

Low cost, nontoxic, independent of pH

Inefficient for flocculating marine microalgae

Vandamme et al. (2010)

0.15 g/L

.10 mg/L

80

0.25 g/L

.10 mg/L

.90

Nontoxic, natural

Inefficient for flocculating marine microalgae, costinefficient

Lama et al. (2016)

0.42 g/L

.20 mg/L

80

0.37 g/L 0.43 g/L

35 mg/L 40 80 mg/L

.90 .80

0.45 g/L

80 mg/L

Low-cost, flocculant reversible in 95%, nontoxic

Additional cost of flocculant recovery, dependent on pH

Vandamme et al. (2015a)

Microalgae Species

Initial Biomass Concentration

Dose

Chlorella vulgaris

0.315 g/L

15 mg/L

Nannochloropsis oculata

0.315 g/L

Parachloerlla kessleri Scenedesmus obliquus Chlamydomonas reinhardtii

pH

Flocculation Tannin-based biopolymer (Tanfloc SG/ Tanfloc SL)

Cationic starch (Greenfloc 120)

Chitosan

Tetraselmis suecica Chlorella vulgaris Scenesedmus obliquus Pseudanabaena

80

.90

Autoflocculation Magnesium hydroxide

Chlorella vulgaris

0.1 g/L

Phaeodactylum tricornutum

0.5 g/L

1.0 4.0 mM of 0.5 M NaoHa

10.7

90

10.3

73

Magnesium hydroxide

Chlorella vulgaris

0.25 g/L

Magnesium hydroxide

Phaeodactylum tricornutum

0.4 g/L

Calcium carbonate Stress conditions (N limitation)

Arthrospira pletensis

0.66 6 0.04 g/L

0.5 M NaOH, addition of 0.3 1.0 mM of magnesium sulfate .7.5 mM magnesium sulfate

10.5 12

.95

Low-cost, nontoxic

pH and magnesium dependent

GarcíaPérez et al. (2014)

10.5

.80

Low-cost, nontoxic

Calcium chloride flocculation is hard to control, pH dependent, biomass dependent

Vandamme, Pohl, et al. (2015b)

0.5 NaOH, 2.5 mM calcium chloride 20 mg NaNO3-N/L and 0 mg NaNO3N/L after 5 days of cultivation

10.5

.80 Low-cost, accumulation of carbohydrates, low energy demand

Sufficiently high settling velocity

Depraetere et al. (2015)

Natural, more efficient than chemical flocculants, pH independent

Additional process of polysaccharides extraction, cost of additional cultivation

Alam et al. (2014)

Natural, sustainable, nontoxic Natural, sustainable, nontoxic

Additional process of infochemicals extraction pH and time dependent, additional costs of extraction

Taylor et al. (2012)

94

Bioflocculation Algal algal Chlorella vulgaris JSC-7

Chlorella vulgaris CNW 11

Scenedesmus obliquus FSP

0.9 OD690

0.9 OD690

Skeletonema marinoi

Nannochloropsis oculata

1 3 107 cells/mL

Scenedesmus obliquus AS-6-1

Scenedesmus obliquus FSP-3

6 3 106 cells/mL

0.5 mL of crude extract

.80

1:5(v/v) JSC-7/ CNW11 0.5 mL of crude extract 1:2 (v/v) JSC-7/ FSP 40 μL of crude extracts

68.3

0.6 mg/L of purified flocculating agent

.80 62.7 95

6 8

88

Guo et al. (2013)

(Continued)

Table 15.2 Comparison of Several Harvesting Methods Suitable for Full-Scale Systems—Chemical Continued Microalgae Species

Initial Biomass Concentration

Klebsiella pneumoniae

Synecosystis

20 mL

2.5 mg of extracted agent

B. subtilis (γ-PGA)

Chlorella vulgaris

1.2 g/L

20 mg/L

Cunninghamella echinulata

Chlorella vulgaris

B4.0 g/L

1:2 fungi/algae

Aspergillus oryzab

Chlorella vulgaris UMN235

Flocculant

Dose

pH

Separation Efficiency (%)

Advantages

Limitations

References

95

Thermal stable, pH independent, natural, biodegradable

Additional costs of extraction

Nie et al. (2011)

90

Natural, no cell integrity damage

Additional costs of extraction

Zheng et al. (2012)

99

Cocultivation, increased lipid yield, cost effective Natural, nontoxic, complex used for wastewater treatment

Demand on species, poorly understand

Xie et al. (2013)

Lab-scale, pH demand from many parameters

Zhou et al. (2013a)

Algal bacterial

7.5

Algal fungal

1.1 3 104 spores/ mL

pH, Potential of hydrogen. a Spore concentration on the solution consisting of microalgae and culture medium. b 20 m/L glucose added to growth medium, heterotrophic growth mode.

4 5

B100

15.4 Harvesting

the microalgae structure, and no contamination from chemicals (i.e., flocculants) (Gerardo et al., 2015). However, the drawbacks are: high land area requirement and local environment conditions (e.g., temperature, contaminants, predators) (Greenwell et al., 2010; Singh et al., 2011). The sedimentation process is commonly used as a preconcentration step followed by other harvesting methods, that is, coagulation-flocculation, dissolved air flotation (DAF), or centrifugation (Collet et al., 2011). However, sedimentation without coagulants and flocculants is impractical for most species of microalgae due to the long harvesting time (Gerardo et al., 2015).

15.4.2 FLOCCULATION The coagulation-flocculation process is carried out with the addition of metal coagulants (e.g., aluminum sulfate, ferric chloride) or biopolymers (e.g., chitosan, tannins, cationic starch) that neutralize the surface charge of microalgae cells. This results in particle aggregation in flocs (Gerardo et al., 2015). The use of metal coagulants is not recommended for microalgae harvesting due to contamination of harvested biomass with metal residues (Alam et al., 2016). The efficiency of chemical flocculants is strongly dependent on the process parameters such as pH, water salinity, microalgae characteristics, and biomass concentration. This all affects the optimal dosage of flocculant (Gerardo et al., 2015). On the other hand, the bioflocculants do not contaminate microalgal biomass and they are required only in small dosages; unfortunately, they are currently too expensive to be applied for products of low market value such as biofuels (Alam et al., 2016). Autoflocculation could be another method for cost-efficient harvesting. The process is induced at high pH (above 9) and later, it is followed by sedimentation. In those conditions the precipitation of calcium or magnesium salts occurs and this causes the flocculation through a sweeping mechanism or neutralization of negative-charged microalgae cells (Vandamme et al., 2015a). The application of separation based on calcium phosphate precipitation is limited due to the high demand of phosphate concentration (Beuckels et al., 2013). More promising seems to be the use of magnesium hydroxide. The cost of the process is lowered as the concentration of magnesium in most wastewaters is sufficient and a lowcost base is used (e.g., lime base) (Vandamme et al., 2012). According to Vandamme et al. (2015a), the magnesium contents in harvested biomass of C. vulgaris and Phaeodactylum tricornutum can reach 5% and 18%, respectively. Due to the fact that it is a reversible flocculant, 95% of precipitated magnesium hydroxide can be removed during acidification. Moreover, pH fluctuation between precipitation (pH 10 and 10.5) and dissolution of magnesium hydroxide (pH 7 and 8) does not affect microalgae composition (mineral content, proteins, carbohydrates, total nitrogen, total phosphorus, and fatty acids methyl ester). Nevertheless, this approach is not feasible if the required pH is too low and/or the process takes too long.

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Bioflocculation based on microalgal microalgal, microalgal bacterial, or microalgal fungal interactions seems to be the most promising low-cost separation method that is suitable for application in full-scale operations. In microalgal bacterial bioflocculation, the aggregation of microalgae cells is induced by compounds produced by bacteria or due to direct integration between microalgae and bacteria (Alam et al., 2016). The main mechanism of microalgal bacterial bioflocculation is the charge neutralization due to ion attachment by cells or by extracellular polymeric substances (EPS) (e.g., polysaccharides, proteins, or other bioflocculant agents) (Lee et al., 2009; Powell and Hill, 2014). During microalgal bacterial bioflocculation the microalgae cells are not damaged. Moreover, in the full-scale system application, medium separated from harvested biomass could be recirculated, reducing the nutrient and water demands (Lee et al., 2009; Ndikubwimana et al., 2016). The microalgal bacteria bioflocculation process was used for harvesting of microalgae biomass in a pilot plant and it was applied for the production of shrimp feed, biogas, and fertilizer (Van Den Hende et al., 2011). The main obstacles are related to supporting of bacterial growth (supplementary substrates and an additional energy source are needed) and unwanted bacterial contamination. Moreover, it is necessary to characterize bioflocculant, especially the size of biomolecules (if too small they are not suitable for cell aggregation) (Wang et al., 2012) and functional groups (these determine the charge type, its distribution, and type of interaction) (Alam et al., 2016). Another type of bioflocculation is based on the microalgal fungal interaction (Alam et al., 2016). In the coculture of nonfilamentous microalgae and filamentous fungi, the microalgae fix CO2 and produce organic compounds that promote fungal growth, while the fungi immobilize microalgae by hyphae. Simultaneously, the process of aggregation is induced by formation of cell pellets. This process was observed in both autotrophic and heterotrophic conditions. Contrary to microalgae, all filamentous fungal strains form pellets during their growth. The main mechanism that induces an interaction between microalgae and fungi is the difference between surface charges. The hyphae of several fungi are positively charged and interact with the negatively charged surface of microalgae cells, causing flocculation (Zhang and Hu, 2012; Zhou et al., 2013a). Moreover, the fungal hyphae and mycelia that are charged and provide surface adsorption, contain polysaccharides, which have good bioflocculant properties, that is, high molecular weight and many functional groups (Alam et al., 2016; Zhang and Hu, 2012). The microalgae harvesting process induced by integration between microalgae and fungi is a promising approach. This method is unsuitable for microalgae-based food or pharmaceutical production due to the difficulty in separation of microalgal cells from fungi. However, it could be applied in the production of biofuels. In the process of microalgal microalgal bioflocculation, faster flocculation and sedimentation of nonflocculating microalgae is induced by addition of selfflocculating microalgae (Alam et al., 2014; Salim et al., 2011). Those two

15.4 Harvesting

mechanisms are involved in the bioflocculation process. The first is bridging, where specialized polymers stabilize the electronegative charge of algal cells by polymer adsorption onto the cell surface. This links and binds cells together (Barany and Szepesszentgyo¨rgyi, 2004). However, when the microalgae cells are more closely attached, the flocculation mechanism is induced by patching through the excreted EPS (Alam et al., 2016). The phenomenon of spontaneous flocculation of some microalgae is the result of bioflocculant synthesis. It was reported that flocculation triggered by polysaccharides or proteins/glycoproteins reached an efficiency of 75% 85% (Alam et al., 2014; Dı´az-Santos et al., 2016; Guo et al., 2013; Salim et al., 2011). On the other hand, the flocculation process can be controlled easily by addition of purified biological infochemicals and extractives produced by microalgae (Ianora et al., 2011; Poulson et al., 2009). Microalgal microalgal bioflocculation is a promising, low-energy demand harvesting technology for commercial production of microalgae-based products. The main drawback is the additional cultivation of self-flocculating microalgae.

15.4.3 FLOTATION The low density of microalgae biomass is advantageous for the flotation process. The microalgae particles can float upwards much faster than they can sediment downwards. The flotation process is natural for some microalgae species and is caused by the presence of gas vesicles (e.g., cyanobacteria Microcystis, Anabaena, Spirulina) (Kim et al., 2005). For the flotation of other microalgae species, air, supersaturated water, or ozone is required (Gerardo et al., 2015). When air bubbles attach to the microalgae particle, the mechanisms is dependent on the hydrophobicity of the algae cell, size of the particle, and the probability of collision and adhesion (Gerardo et al., 2015). The efficiency of separation can be enhanced by flocculation or addition of surfactants. Coagulants (i.e., cationic metal coagulants) increase the size of microalgal aggregates, simultaneously increasing the likelihood of collision between bubbles and the microalgal cells (Edzwald, 2010; Guillard, 1975). The combination of flocculation and flotation is challenging due to the increasing density caused by too large flocs. To prevent this, more bubbles need to be attached to detach the large flocs (Edzwald, 2010). On the other hand, the surfactants increase the contact angle between the air and the solid particle, which increases the probability of air-to-solid adhesion (Shelef et al., 1984; Uduman et al., 2010). Furthermore, positively charged air bubbles produced by the addition of cationic surfactants improve the separation by electrostatic attraction between the cell surface and the bubbles (Henderson et al., 2008). The latter method is more cost-effective than the combination of flotation with flocculation (i.e., reduction of coagulant dosage), and there is no need for metal contamination and removal of residual surfactants by ozone treatment or granular activated carbon (Henderson et al., 2008). The methods for creation of micron-sized bubbles are: a DAF, a microflotation, a froth flotation, or an exploitation of dispersed air and vacuum gas. During

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DAF, the water supersaturated with air is released into a flotation tank, where, in the atmospheric pressure, the dissolved air precipitates out of the water forming small bubbles. Unfortunately, the high pressure requirement induces a high energy demand (7.6 kWh/m3) (Wiley et al., 2009). On the other hand, in microflotation no high pressure is used. The bubbles are detached from the exiting pores in the diffuser by a fluidic oscillation at a specific frequency (Hanotu et al., 2012). This method has a high separation efficiency (up to 99%), but the energy demand has not been determined (Hanotu et al., 2012). The method based on dispersed air is energy-efficient (3 kWh/m3) (Wiley et al., 2009) due to the generation of bubbles and foam with the addition of surfactants and the use of a low-pressure sparger or an agitator (Wiley et al., 2011, 2009). Another low-pressure process is foam flotation, where the bubbles are generated by spargers. This process can be combined with fluid oscillation causing an increase in the biomass concentration (Coward et al., 2015, 2013). The microalgae flotation processes has a low energy demand (except DAF) and the operating and capital costs are also relatively low. Henceforth, these separation methods can be applied for low or medium market value commodity chemicals. To enhance the commercialization of microalgae processing, it is necessary to use economically and energy-efficient harvesting methods. Novel technologies such as harvesting by ultrasound, application of magnetic nanoparticles or charged cellulose-based nanocrystals (Rubio et al., 2002; Vandamme et al., 2015b; Xu et al., 2011) are still only in the laboratory scale and their energy demands need to be lowered. The selection of an optimal microalgae harvesting technology that would be applied in an industrial scale depends on the energy demand and the downstream processing requirements, that is, quality and concentration of microalgal biomass. Moreover, all harvesting methods described above have some merits and limitations and it is not possible to expect that one technology would be suitable for all the different scenarios.

15.5 BIOGAS PRODUCTION Anaerobic respiration is cellular respiration, during which organic compounds are oxidized, and the final electron acceptors are inorganic compounds. When electron acceptors and protons are organic compounds, the process is called fermentation. Depending on the final products of transformation, different types of fermentation are distinguished. A special case of fermentation is methane fermentation or AD, which consists of complex, biochemical transformations, combining the absence of oxygen in the environment and the use of products of one phase as substrates in another. Even though, in most cases, AD is carried out in one bioreactor, each process stage is conducted by different groups of microorganisms, creating an ecosystem of different trophic levels in the microbial food chain. An

15.5 Biogas Production

excess of products from one trophic level disturbs the balance of the entire system, resulting in accumulation of intermediates, change in pH value, and a reduction of process efficiency (Ferna´ndez et al., 1999). In the last stage, the products of the previous one are fermented to methane by methanogenic archaea (Lange and Ahring, 2001). The particular steps of AD are hydrolysis of highmolecular-weight organic compounds, acidogenesis (decomposition of hydrolyzed substances to organic acids), acetateogenesis (decomposition of organic acids to acetic acid), and methanogenesis. Depending on the stage, facultative and obligatory anaerobic microorganisms are involved in the reactions. The cascade of transformations leading to anaerobic decomposition of organic matter and production of biogas is an example of syntrophy (mutual nutrition). The efficiency of the entire process is ultimately determined by the efficiency of the most sensitive element in the chain of transformations (Liu and Tay, 2004). The microalgae AD have been investigated since the 1950s (Golueke et al., 1957; Meier, 1955). Microalgae are rich in lipids which can be converted into methane with high efficiency. However, the methane yield depends on several factors, such as microalgae specie, pretreatment of microalgal biomass (hence availability of the macromolecules for anaerobic microorganisms), process operating parameters, as well as the presence or absence of inhibitors of methanogenesis (Jones and Mayfield, 2012; Mussgnug et al., 2010).

15.5.1 PROCESS CONDITIONS AD consists of complex, subsequent biochemical transformations and depends to a different degree on the external physical and chemical factors according to the stage of the process. From physical factors affecting the efficiency of methane fermentation, temperature and intensity of biomass mixing are of decisive importance. Among the chemical factors, pH, type and availability of nutrients (especially C:N ratio), and the presence of toxic substances are important.

15.5.1.1 Temperature The biochemical reactions during acidogenesis, acetatogenesis, or methanogenesis are subjected to thermodynamic laws. On the one hand, the increase in temperature accelerates the rate of biochemical reactions catalyzed by enzymes in accordance with Arrhenius theory, but, on the other hand, due to the protein nature of enzymes, too high temperature causes denaturation and inhibition of the process. Depending on the optimum temperature of the highest metabolic activity, three groups of microorganisms are distinguished: psychrophilic (less than 25 C), mesophilic (30 C 40 C), and thermophilic (50 C 60 C). Among the AD microorganisms, methanogens are the most sensitive to temperature changes (Cha and Noike, 1997), high or frequent changes of temperatures are particularly disadvantageous. During digestion of microalgae, thermophilic conditions might enhance the hydrolysis, however the advantages and disadvantages of thermophilic versus mesophilic microalgae AD are the same as for other organic substrates.

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15.5.1.2 Potential of hydrogen The pH of the environment significantly influences the efficiency of AD. Along with the change in pH, the solubility and forms of the organic and inorganic compounds change as well. Microorganisms involved in the particular stages of AD have different optimum ranges of pH values for their growth. The optimal pH of hydrolysis and acid-forming bacteria is between 4.5 and 6.3. In the case of methanogenic archaea, the optimal for their growth is a neutral pH (6.8 7.5). The pH values in an effective single-stage reactor are usually neutral and are a result of the presence of alkaline or acidic metabolic products formed during AD. Low pH values in the effluent from the digester indicate the disturbance of methanogenesis and the accumulation of acidic transformation products (Chinnaraj and Venkoba Rao, 2006). Therefore, in practice, the addition of alkalizing substances (e.g., sodium hydroxide) to the digesters is often used to maintain high methane production efficiency. The influence of the pH values on the degree of dissociation of individual metabolites and their toxicity is also related to temperature. In higher temperatures, the degree of dissociation decreases, and thus increases the harmful effects of metabolites. However, it should be noted that this phenomenon occurs only in the case of abrupt temperature changes. When the temperature increases gradually, microorganisms will gradually adapt to the new equilibrium. In the case of microalgae AD, pH levels are often adjusted to a range between 7 and 8 to meet the optimum conditions for methanogens (Gonza´lez-Ferna´ndez et al., 2012a,b; Mendez et al., 2013).

15.5.1.3 Carbon to nitrogen ratio The concentration of organic compounds also affects the efficiency of AD; effective methane production requires an optimal C:N ratio. The mutual balancing of the subsequent stages of AD is crucial for the effective functioning of the entire system. The excessive content of organic compounds in the substrate might cause acidification of the fermentation reactor. It is associated with higher activity and shorter generation time of hydrolyzing and acid-forming bacteria. When the amount of volatile fatty acids formed from the decomposition of complex organic compounds exceeds the buffer capacity of the system, and their excess is not processed in methanogenesis, a rapid lowering of pH value occurs and finally inhibition of the process. In practice, pH values below 6.5 indicate that the operation of the system is already disturbed. The C:N ratio in the substrate determines the stable methane fermentation operation. A high C:N ratio indicates that carbon cannot be completely transformed, and thus the methane potential of substrate is not achieved. With a low C:N ratio, ammonia (NH3) might be formed, which even in small concentrations inhibits the growth of bacteria. The optimal C:N ratio should be from 20:1 to 30:1. In order to overcome a low C:N ratio of microalgae, codigestion with carbon-rich substrates is recommended. Typically, those are primary and secondary sludge, waste paper, or the organic fraction of municipal solid waste (Demirbas, 2010; Wang et al., 2013; Yen and Brune, 2007).

15.5 Biogas Production

15.5.1.4 Organic loading rate and hydraulic retention time Typically, AD of microalgae biomass is carried out in a continuous-flow stirred tank reactor (CSTR). In these reactors, an organic loading rate from 2 kg/(m3 days) to 4 kg/(m3 days) results in maintaining the desired ratio of volatile fatty acids to alkalinity and ensures stable operation of the fermentation reactor. In the CSTR, a long solids retention time is applied, which corresponds to the hydraulic retention time (HRT) (Boe et al., 2009). This is particularly important in maintaining methanogens due to their long generation time (Fuchs et al., 2003). In order to ensure proper conditions for their growth, HRT in the system should be at least 15 20 days—a shorter time might result in the leaching of methanogens (De˛bowski et al., 2013). For microalgae AD, the optimal HRT is similar to wasteactivated sludge AD, that is, 15 30 days (Diltz and Pullammanappallil, 2013; Ehimen et al., 2011). Operating difficulties of microalgae AD might be caused by biochemical composition of microalgae biomass that is dominated by proteins, which lower the C:N ratio. High protein content in microalgae biomass can lead to increased production of free ammonia, which is toxic to the microorganisms responsible for methane formation. In addition, sodium ions present in the biomass of microalgae from saltwater-based cultivation systems can inhibit methanogenesis. However, there are scientific reports describing the possibility of adapting microorganisms of anaerobic sludge for efficient fermentation of marine algae biomass (Schlu¨ter et al., 2008).

15.5.1.5 Pretreatment Microalgal biomass digestibility is limited due to the cell wall resistance to degrading bacteria and is dependent on the microalgae species. The digestibility can be improved by a variety of pretreatments including physical, chemical, or biological methods (Ganesh Saratale et al., 2018). The microalgae cell wall characteristic determines which pretreatment method should be applied. The cell wall is composed of glycolipids, glycoproteins, and polysaccharides, and it also contains cellulose, hemicellulose, and pectin (Gonza´lez-Ferna´ndez et al., 2012a,b). In the studies of Mussgnug et al. (2010), it was shown that the cell wall composition had a direct impact on methane potential. State-of-the-art pretreatment technologies include: ultrasound (Park et al., 2013), high-pressure homogenization (Schwede et al., 2011), size reduction and sonication (Ehimen et al., 2013), thermal hydrolysis (Park et al., 2013), enzymatic hydrolysis (Ehimen et al., 2013; Park et al., 2013), oxidation, alkali treatments (Park et al., 2013), and addition of acids (Sukias and Craggs, 2007) or ionic liquids (Kaatze, 1995). A summary of different methods for microalgae pretreatment is given in Jankowska et al. (2017).

15.5.2 MICROALGAE SPECIES USED FOR BIOGAS PRODUCTION Many researchers hold that the use of methane fermentation is one of the most promising methods for energetic use of microalgae biomass. Sialve et al. (2009)

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stated that the use of this process determines a higher economic effect in relation to the integrated lipid extraction system and anaerobic processing of extraction residues. Other studies suggest that the balance of unit operations conducted in AD is the most effective, both in terms of economic analysis as well as environmental emissions (Campbell et al., 2009). An additional product of the process, apart from biogas, is the postfermentation sludge, which can be used directly as a fertilizer (Olguin, 2000; Phang et al., 2000). The methane potentials of different microalgae species are summarized in Table 15.3. Mussgnug et al. (2010) noted that the production of biogas was neither dependent on the alga taxonomic group of microalgae nor on the basis of systematic classification; the potential effectiveness of AD could not be predicted. In order to precisely determine the methane potential, batch or continuous tests should be conducted for each of the tested species. The literature reports a correlation between the cell walls of microalgae and the susceptibility to biomass decomposition under anaerobic conditions. High methane yield was possible to achieve in microalgae species, which were characterized by the lack of a cell wall, as in the case of Dunaliella salina (Sheffer et al., 1986), or the cell wall did not contained hardly decomposable cellulose and hemicellulose components, and its structure Table 15.3 Methane Production From the Anaerobic Digestion of Different Microalgae Biomass Species

CH4 (mL/g VS)

References

Isochrysis spp. Scenedesmus dimorphus Chlorella vulgaris Porphyridium aeruginosa Neochloris oleoabundans Chlorella sorokiniana Chlorococcus sp. Thalassiosira weissflogii Chlorella pyrenoidosa Nannochloropsis gaditana Glossomastix chrysoplasta Chlorella vulgaris Chlorella minutissima Chlorella sorokiniana Phaeodactylum tricornutum Chlorella sorokiniana Scenedesmus obliquus Chlorella vulgaris

408 6 4 397 6 10 361 6 11 352 6 3 308 6 1 283 6 4 267.36 265 6 15 264.71 228 6 4 227 6 8 195.64 166.12 220 280 350 6 0.03 212 210 6 0.03 189

Frigon et al. (2013) Frigon et al. (2013) Frigon et al. (2013) Frigon et al. (2013) Frigon et al. (2013) Frigon et al. (2013) Prajapati et al. (2013) Frigon et al. (2013) Prajapati et al. (2014) Frigon et al. (2013) Frigon et al. (2013) Prajapati et al. (2014) Prajapati et al. (2014) Ayala-Parra et al. (2017) Zamalloa et al. (2012) ˇ Polakovicová et al. (2012) Zamalloa et al. (2012) ˇ Polakovicová et al. (2012)

15.6 Microalgae Biorefinery

was based on the protein substances, for instance, as in the case of Chlamydomonas reinwardtii (Miller et al., 1972), Arthrospira platensis (Van Eykelenburg et al., 1980), and Euglena graciles (Nakano et al., 1987). In contrast to the above-mentioned species, Chlorella kessleri and Scenedesmus obliquus have a cell wall built from hemicellulose (Takeda, 1991, 1996). The cell wall of S. obliquus is hardly decomposable due to the presence of biopolimer sporopollenin. Even more complex is the cell wall of Bacillariophyceae, which is made of silica (Hildebrand et al., 2012).

15.6 MICROALGAE BIOREFINERY—A WAY TO COMMERCIALIZE MICROALGAE-BASED BIOGAS PRODUCTION The main constrains in commercialization of microalgae AD are high costs of biomass cultivation, harvesting and pretreatment, limited productivity in open reactors, high costs of closed photobioreactors, and finally high operation costs related to water and nutrient demands (Jankowska et al., 2017). The biorefinery approach, through multistep utilization of microalgae biomass to a wide range of biofuels and chemicals, seems to be a sustainable and economic solution for all the drawbacks and limitations (Table 15.4). The concept of biorefinery should be developed precisely for a specific location (Fig. 15.1). Several factors should be considered, such as the climate parameters (average temperature, high solar radiation), available area land (especially land availability for open reactors), water and nutrient sources (municipal, agricultural or industrial wastewaters, and organic wastes), and market value of algae-based products Table 15.4 Microalgae-Based Products Products From Biomass or Extracted Biomass

Substances Produced by Microalgae

Biohydrogen Biomethane Syngas Biocrude Pyrolysis oil Biochar Biodiesel Ethanol Acetone Butanol

Polyunsaturated fatty acids Proteins B-carotene Astaxanthin Canthaxanthin Lycopene Lutein Chlorophyll a and b

423

FIGURE 15.1 Two-step biorefinery concept for microalgae biomass processing to low- and high-value product.

List of Abbreviations

(linked to cultivation and harvesting methods). To lower the cultivation costs and to enhance the biomass productivity, the additional carbon sources could be provided from: flue gases (CO2) (Chen et al., 2018a,b; Raslaviˇcius et al., 2018), volatile fatty acids from acidogenic fermentation, or CO2 from produced biogas (after biogas upgrading and separating CH4 from CO2). Moreover, if the climate parameters are not suitable for cultivation in open reactors, closed photobioreactors equipped with LED lights should be considered (Raslaviˇcius et al., 2018). Moreover, the operational costs can be lowered by utilization of heat and electricity from biogas-run combined heat and power units. The harvesting process should be as natural and nontoxic as possible (i.e., bioflocculation, autoflocculation) to not decrease the quality of the microalgae biomass. To decrease the harvesting costs, the process should be two-step and flocculant regeneration should be assured. Biomass residues from the first production step could be further used for codigestion with other substrates (e.g., organic wastes) to enhance overall biogas production. Through such improvements the cost of microalgae biomass can be reduced significantly (Acie´n et al., 2012; Norsker et al., 2011). The most promising examples of multifuel production based on microalgae biomass seems to be biodiesel biomethane (Collet et al., 2011; Ehimen et al., 2011; Sialve et al., 2009) and biohydrogen biomethane biorefineries (Mussgnug et al., 2010; Wirth et al., 2015).

15.7 CONCLUSIONS AND FUTURE TRENDS Due to the high costs of cultivation, harvesting, and processing, the biomethane obtained during AD of microalgae is not yet competitive with commercial fossil fuels. The development of sustainable integrated system of multiproduction could not only provide biofuels and biochemicals with a minimal environmental footprint, but it would also allow nutrients and water recycling, CO2 sequestration, wastewater remediation, and organic waste reuse and recycling. In the future, research should focus on designing and establishing effective and economically viable microalgae-based biorefineries with multiple commodity products.

LIST OF ABBREVIATIONS AD CHP CSTR DAF DHA EOM EPA EPS

anaerobic digestion combined heat and power continuous-flow stirred tank reactor dissolved air flotation docosahexaenoic acid extracellular organic matter eicosapentaenoic acid extracellular polymeric substances

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HRT LED OLR PAR SRT TSS

hydraulic retention time light-emitting diodes organic loading rate photosynthetically active radiation solids retention time total suspended solids

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