Integration of microalgae biomass in biomethanation systems

Renewable and Sustainable Energy Reviews 52 (2015) 1610–1622

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

Integration of microalgae biomass in biomethanation systems Hamzat Tijani a, Norhayati Abdullah b,n, Ali Yuzir c,nn a

Faculty of Biosciences and Medical Engineering, Universiti Teknologi Malaysia, 81310 Johor Bahru, Malaysia Palm Oil Research Center (UTM Palm), Faculty of Biosciences and Medical Engineering, Universiti Teknologi Malaysia, 81310 Johor Bahru, Malaysia Center for Environmental Sustainability and Water Security (IPASA), Faculty of Civil Engineering, Universiti Teknologi Malaysia, 81310 Johor Bahru, Malaysia b c

art ic l e i nf o

a b s t r a c t

Article history: Received 4 October 2014 Received in revised form 1 June 2015 Accepted 29 July 2015

Concerted efforts in the field of bioenergy are driving dynamic studies for the production of microalgaebased biogas systems. Its ability to recycle residual nutrients and carbon dioxide (CO2) products of the anaerobic effluent reflected anaerobic digestion as the most sustainable means for renewable energy generation in microalgae. These measures will aid to lessen the effect of greenhouse gas emissions and increase the prospects for the application of microalgae biomass in the field of food and agricultural technology, medicine, and bioengineering, contributing to the sustainability of the industries. To begin with, the experimental limitations associated with the cultivation of microalgae biomass need to be resolved. In spite of the extensive studies conducted in the field of bioengineering, problems related to culture optimization, high building and operation costs remained persistent. This review highlighted vital points of microalgae-based bioprocesses that require several advancements in order to improve the prospects of anaerobic digestion and discover novel renewable energy products. Coupled anaerobic digestion with microalgae cultivation systems requires intensive research as a distinct bioenergy generation process to uphold pilot-scale applications. & 2015 Elsevier Ltd. All rights reserved.

Keywords: Biomethanation Microalgae Anaerobic digestion Biomass cultivation

Contents 1. 2.

3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1611 Microalgae biomass for biomethanation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1611 2.1. Definition of microalgae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1611 2.2. Macromolecular constituents of microalgae biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1611 2.2.1. Carbohydrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1612 2.2.2. Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1612 2.2.3. Lipids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1612 2.3. Microalgae cultivation systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1612 2.3.1. Comparison of different microalgae cultivation systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1612 2.3.2. Factors affecting microalgae cultivation systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1613 2.3.3. Practical limits for photon excitation in microalgae cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1614 2.4. Microalgae strain selection for biomethanation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1614 2.4.1. Components of microalgae cell wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1614 2.4.2. Biodegradability of microalgae cell wall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1615 2.4.3. Pre-treatment of microalgae biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1615 2.4.4. Source of methane in microalgae biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1615 2.4.5. Downstream processing of microalgae biomass. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1615 Anaerobic digestion of microalgae biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1617 3.1. Microalgae: source of recyclable anaerobic digestate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1617 3.2. Microalgae: source of biomethane and syngas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1618

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Corresponding author. Tel.: þ 60 137036730; fax: þ 60 75557534. Corresponding author. Tel.: þ 60 19 7073567. E-mail addresses: [email protected] (N. Abdullah), [email protected] (A. Yuzir). nn

http://dx.doi.org/10.1016/j.rser.2015.07.179 1364-0321/& 2015 Elsevier Ltd. All rights reserved.

H. Tijani et al. / Renewable and Sustainable Energy Reviews 52 (2015) 1610–1622

3.3. Codigestion of microalgae biomass with carbon-rich substrates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Effect of operating parameters on the composition of biogas product . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Purification of biogas product . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Perspectives and further research. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction The increasing demand for energy fuels is placing massive pressure on fossil energy. As a consequence, there is a necessity to design alternative strategies in the chains of energy generation to concurrently reduce reliance on fossil exploration and mitigate the climatic influence of its fractionation. The rates of biomass proliferation and CO2 fixation potential of photosynthetic entities are receiving greater interests and may serve as sustainable substitutes to biofuel crops [1,2]. Microalgae are a distinct assembly of small microscopic aquatic photosynthetic prokaryotes and eukaryotes characterized for their proficient ability to transform solar energy into solid biomass. Because of its high carbon contents and biological CO2 fixation efficiencies, they serve as a viable feedstock for biofuel generation and expected to mitigate the increase in atmospheric CO2 [3]. With a wide array of 200,000 species existing in nature of which almost 50,000 species have been taxonomically defined, microalgae are reported to be the primary source of approximately 50% of the oxygen generated on earth by concurrently transforming CO2 into biomass during photosynthesis [4]. It can be cultured on non-arable fields such as marine habitats as well as deserts, thus decreasing competition with food production [5,6]. The ability of specific microalgae strains to exhibit defined structural growth under extreme saline conditions promotes its usage as primary feedstock for biogas generation, especially in the desert regions where freshwater resource is not feasible. One remarkable feature of some microalgae strains is the ability of their biological system to transverse between phototrophic and/or heterotrophic metabolism in order to remain resilient to shocking environmental impacts. This phenomenon of heterotrophic proliferation enables the viability of these strains in cultivators enriched with organic carbon (sugars, organic acids and alcohols) and results in the cultivation of denser cell mass due to the lack of photo-inhibition systems [7]. However, establishing a mixotrophic propagation of variegated cultures would contribute to the cultivation of a much denser cell mass than the exclusively phototrophic/heterotrophic systems [8]. Recently, anaerobic digestion of algal and microalgae biomass have been researched to include biogas upgrading (CO2 biosequestration) [4,74,75]. However, studies related to the co-digestion of microalgae biomass with other kinds of sludge residues are also possible. Anaerobic degradation process transiently evolves under natural aquatic environments in cases when the cell biomass is localized along the anoxic and aphotic zones. Even though the decomposition is slow and incomplete, nutrient remineralization is the strategic process responsible for recycling nutrients that leads to ammonium and phosphate release for sustainable growth. The kinetics of these processes is highly limited by the resistance of the cell walls, which tends to hinder cell digestibility. Besides their energetic value, different microalgae strains have been channelled for the synthesis of chemicals, feed nutrients and health products because of their capability to effectively capture solar energy and sequestrate CO2 to yield valuable organic products (carbohydrates, lipids, pigments, and fibres). The increasing need for anaerobic digestion can be linked to its ability to transform different organic wastes into renewable energy. Methane, one of the most commonly sourced biogas, is recognized as an ideal renewable energy and thus also as a

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possible primary energy source. However, pilot generation of biomethane faces a number of technical hurdles that render the current development of the algal industry economically unfit. In addition, it is also necessary, but very difficult, to develop cost-effective technologies that would permit efficient biomass harvesting and biomethanation. Nevertheless, since microalgae production is regarded as a feasible approach to mitigate global warming, it is clear that producing methane from microalgal biomass would provide significant benefits, in addition to the fuel. Microalgae have thus been widely recognized as the feedstock for third-generation biofuels. Although, more than 15,000 novel compounds have been associated with algae biomass, most of the current studies aimed at transforming microalgae biomass for bioenergy generation are directed towards biodiesel production in view of their inherent ability to amass lipids under controlled reactor settings. Biogas production via anaerobic digestion system is a renowned advancement in the field of biofuel generation. It aims to employ varieties of sludge residues as substrate for the digesting microbial consortia and enhance the reduction of carbon emissions to generate a cleaner, eco-friendly, green energy process. In the anaerobic digestion process of microalgae biomass, the total organic macromolecules (proteins, carbohydrates and lipids) are converted into methane (CH4), carbon dioxide (CO2) and other gases, which results in higher energy yields that can be channelled for the production of heat and electricity via co-generation. This review identifies the biomass characteristics of the primary feedstock with reference to their growth, harvest, downstream processing and anaerobic degradation. Prospects in co-digestion processes that combine microalgae biomass with carbon-rich substrates were also highlighted.

2. Microalgae biomass for biomethanation 2.1. Definition of microalgae Microalgae are micrometre-sized single-cell aquatic organisms that exhibit photosynthetic metabolism and are less structurally complex to terrestrial plants. Based on their nutritional requirements, microalgae can be categorized into three classes: autotrophs, heterotrophs and mixotrophs [9]. The presence of chlorophylls and accessory pigments in autotrophic microalgae drives its light-harnessing and photosynthetic metabolism. Heterotrophic microalgae are independent of photosynthesis and consume organic carbons such as glycerol and glucose as the primary source of metabolic energy source. Mixotrophic microalgae exhibit versatile characteristics; they are capable of fixing CO2 via photosynthesis as well as consume organic nutrients [9,10]. According to their phylum classification, microalgae have been grouped into nine phyla, namely chlorophyta, cryptophyta, cyanobacteria, dinophyta, euglenophyta, glaucophyta, haptophyta, ochrophyta and rhodophyta [9]. 2.2. Macromolecular constituents of microalgae biomass Based on its average composition, microalgae are described as CO0.48H1.83N0.11P0.01 [11]. The residual-point for which an anaerobic digester carries out the recycling mineralization of organic nitrogen

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and phosphorus embedded in this biomass results in a flux of ammonium and phosphates [12,13]. Proteins (6–52%), carbohydrates (7–23%) and lipids (5–23%) constitute the vast majority of microalgae biomass, respectively. Besides these three main components, lesser concentration of nucleic acids and pigments such as carotenoids may also be included within the cells. Table 1 highlights the proportions of macromolecular components in microalgae cells. It is however important to note that the chemical composition of the substrate being fed to microalgae biomass strategically influences the macromolecular composition of the matured cells. For instance, nitrogen starvation within the range viable for specific microalgae tends to result in the accumulation of more lipids than carbohydrates [15]. Variations in these compositions may influence the performance stability of the anaerobic digestion. 2.2.1. Carbohydrates Cellular carbohydrates in microalgae may account for as high as 75% of the total cell mass with starch constituting approximately 60% [14]. The nature of these carbohydrates found in microalgae can be very dissimilar in their structural and functional characteristics. For instance, a number of green algae exhibit plant-based carbohydrates such as cellulose and starch, while diatomic algae prominently accumulate laminaran, fucoidin and mannitol [16]. The percentage starch content of the biomass is readily influenced by concentration of the macronutrient components including nitrogen, phosphorus and sulphur. Besides these elemental components, iron, cobalt and zinc have been described to also stimulate methanogenesis [11]. However, application of protein synthesis inhibitors such as cycloheximide has been employed as structural analogues that block protein generation and enhance the carbohydrate concentration [16]. Microalgae biomass has been examined and analysed for several nutraceutical products ranging from omega-3 fatty acids (boost the healthiness of the brain and heart), carotenoids (antioxidants; promote visual sense), sulphated polysaccharides (anticoagulant/anti-tumour/ antiviral), fucoxanthin (antioxidants; reduce obesity tendencies) and sterols (anti-diabetics) [17]. Microalgae biomass with high carbohydrate contents can be a suitable fermentative substrate for the production of ethanol. The carbohydrate component of the biomass is extracted from microalgae via cell disruptive mechanical techniques prior to its scarification with enzymes and fermentation with bacteria or yeasts and the quality of the ethanol product is upgraded by distillation [18]. 2.2.2. Proteins In microalgae, the cellular protein concentration significantly varies from species to species, accounting for 15–71% of its cell mass [14]. Algal proteins are characterized by an excellent amino acid profile which describes its compatibility with high-quality protein source as shown in Table 2. For a number of microalgae species, their protein fraction is defined by lower carbon/nitrogen ratio at averages of 10.2 for freshwater microalgae [19]. Table 1 Fractions of macromolecules in microalgae cells [14]. Macromolecular constituent

Function(s)

BIOMASS Carbohydrates Structure and energetic reservoir Proteins Structure and metabolism Lipids Structure and energetic reservoir Nucleic acids Genetic functions and cellular replication

% Biomass concentration 8–30 40–60 5–60 5–10

2.2.3. Lipids Previous studies linked to biodiesel generation have identified lipids as the predominant functional component of microalgae biomass that exhibit high energy densities which can be easily upgraded to biodiesel [20–22]. Cellular lipids are usually categorized based on the polarization potential of their functional moiety: (i) polar lipids (fatty acids þglycolipids þphospholipids); (ii) neutral lipids (tri/di/mono-acylglycerolþsterols). At optimally viable reaction environments, microalgae growth yields are predominantly polar lipids until stressed conditions are assumed before the synthesis of neutral lipids is expressed [15]. 2.3. Microalgae cultivation systems A vast majority of microalgae strains are strictly phototrophic with light being the transitional energizing parameter for cell proliferation. However, certain strains have been distinguished with specialized features, which include their utilization of organic substrates as energy source. Heterotrophic cultivation of microalgae is usually carried out via notable fermentation technologies that are not hindered by light limitations under a highly stabilized process control [23]. Closed observations have revealed that heterotrophically cultivated microalgae are prone to amass lipids than phototrophically grown microalgae of the same species. A typical example is the cells of Chlorella sp.; it heterotrophically amasses 55.2% lipids and only attains 14.6% under phototrophic environments [24]. Closed photobioreactors (PBR) have been described to establish a condition that resolves the main concerns associated with open pond cultures such as microbial contamination, fluid vaporization, lower cell counts and land requirements. Closed PBRs are more functionally flexible and can harness photosynthetic rays from artificial light and natural light. The most prominent reactor design for closed PBRs assumes the tubular configuration, which enables the light to be harnessed by the circulating cultivars at small surface area to volume ratio. 2.3.1. Comparison of different microalgae cultivation systems Even though biomethanation of microalgae biomass is straindependent, comparative analysis seems to indicate that heterotrophic cultivation could yield higher biomass productivity than autotrophic cultivation systems. Yet, heterotrophic cultures are negatively influenced via microbial contamination, especially in open reactor configuration designs, as a result causing problems in pilot-scale cultivation. In a similar trend, the cultivation cost associated with heterotrophic systems especially in relation to supplementing an organic carbon source for the microalgae cells has been the major limitation for its application in biomethanation process. Phototrophic cultivation is the most recurrently used cultivation approach for microalgae cultures due to its simple reactor setup and it can be easily piloted into industrial scales. It is less influenced by microbial contaminations except in open pond systems, and it provides a promising solution to filtering CO2 from industrial flue gas discharges. However, the biomass productivity of this system is significantly less than that of heterotrophic systems because of their reduced cell growth as well as gas–liquid mass transfer limitations of CO2. Contrariwise, the provision of lower cost for system scaling-up and production of microalgae biomass with less-rigid cell walls features phototrophic cultivation as the most sustainable and efficient approach to synthesize biomass for biomethanation. To date, experimental studies related to microalgae biomass synthesis in mixotrophic and photoheterotrophic systems still experience impending limitations caused by their high contamination tendencies and light requirements. These

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necessitate the requirement to design specialized photobioreactor units before piloting can be achieved at industrial scales, thereby increasing the operational cost for reactor maintenance and biomass synthesis. 2.3.2. Factors affecting microalgae cultivation systems The cultivation of microalgae in a bioengineered system is governed by several parameters including light intensity, nutrient composition, temperature and gaseous exchange rate. These factors influencing biomass growth of microalgae have been investigated and streamlined to specific operating parameters for the yielding-specific strains to produce methane. 2.3.2.1. Light intensity. Light is the central energy source that promotes the proliferation of phototrophic microalgae cells. The accessibility to light is very crucial as shortened intensities may result in lower growth rates. Even though the photosynthetic sensitivity of these cells increases with increasing light intensity, a threshold phase is attained when photosensitivity is saturated and photo-inhibition is expected. At this point, the light rays may cause an irreversible damage to the light receptors in the chloroplasts and instantaneously decrease their photosynthetic rates [25]. The complex oxygenic photosynthetic process that occurs in microalgae involves the anabolic processes of water splitting and CO2 fixation to drive the Calvin cycle. However, slight distinctions to this key process may exist in different strains, especially in relation to the form of pigments harvested by the photons before the excitons are routed to the photosynthetic reaction centres where it is transformed into chemical energy and conserved in the form of adenosine triphosphate (ATP) and reduced energy equivalents (NADPH/FADH2). These forms of metabolic energy are required in the Calvin cycle where CO2 is actively reduced to carbohydrates. One of the prominent problems associated with denser cell cultures arises when cells flanking the superficial areas in directional proximity to the light rays harness the mainstream of light. The inaccessibility of light to these cells at the interior fluid layers is referred to as Mutual Shading Effects. Mutual shading is a common growth-restraining factor that limits biomass propagation to attain high cell density. In view of this, facilitating the laminar mixing of the culture fluids promotes the even distribution of light rays and improves the substrate uptake of the cultivating cells in the culture media. Several studies have been conducted to ensure even distribution of light to the cell cultures

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via slight modification of control parameters such as fluid depth, viscosity and mixing frequency [14,26]. The maximum photon transformation efficiency was observed when light is limiting and maximum productivity appeared at levels below maximum growth rates. Thus, there is no relatively parallel correlation between the biomass productivity and the photon conversion efficiency [27]. 2.3.2.2. Nutrient constituents. Different concentrations of inorganic nutrients such as macronutrients, vitamins and trace elements are required for microalgae to attain high biomass productivity. Most microalgae cultivation systems have adopted macronutrients requirements of nitrogen and phosphorus at 16N:1P which can be supplemented in excess to avoid nutrient limitation [28]. In addition, trace metals including chelated salts of iron, nickel, manganese, selenium, cobalt and zinc have also been reported as micronutrient supplements [29]. These nutrients can be augmented into the feed influent independently. Metabolic energy is required to reduce the nitrate components of these micronutrients into ammonia. This energy demand decreases biomass productivity through ammonium inhibition by nearly 5%. Thus, microalgae strains that can utilize ammonia or urea will be required for optimal productivity. Ammonia should be added to the culture medium during CO2 injection and the lower pH caused by CO2 will decrease ammonia volatilization. A host of other nutrients such as phosphate (P), potassium (K), iron (Fe), manganese (Mn) and magnesium (Mg) are also required. Since algae have an extraordinarily high nutrient content (5–12% N and 0.3–0.5% P) compared to most crops, recycling the residual biomass nutrients after anaerobic digestion is a subject of great concern. 2.3.2.3. Temperature. Temperature is a key environmental factor that limits microalgae productivity. The growth profile of microalgae increases exponentially with increasing temperature. Due to the significance of this parameter, microalgae growth should be acclimatized to ambient temperatures and solar irradiance [30]. The optimal temperature regimes for mass cultivation of microalgae strains ranges from 20 1C to 35 1C and culturing outside this temperature bounds would be unsuitable for microalgae proliferation [31]. The culture temperatures below optimal settings do not exterminate the cells prior to fluid freezing, but temperatures above these optimal settings can be destructive because the cell's fragility at high temperatures result in loss of cellular contents

Table 2 Amino acid profile of microalgae species (g per 100 protein source) [15]. Source

Chlorella vulgaris

Dunaliella bardawil

Scenedesmus obliquus

Arthrospira maxima

Spirulina platensis

Aphanizomenon sp.

Isoleucine Leucine Valine Lysine Phenylalanine Tyrosine Methionine Cysteine Tryptophan Threonine Alanine Arginine Aspartate Glutamate Glycine Histidine Proline Serine

3.8 8.8 5.5 8.4 5 3.4 2.2 1.4 2.1 4.8 7.9 6.4 9 12 5.8 2 4.8 4.1

4.2 11 5.8 7 5.8 3.7 2.3 1.2 0.7 5.4 7.3 7.3 10 13 5.5 1.8 3.3 4.6

3.6 7.3 6 5.6 4.8 3.2 1.5 0.6 0.3 5.1 9 7.1 8.4 11 7.1 2.1 3.9 3.8

6 8 6.5 4.6 4.9 3.9 1.4 0.4 1.4 4.6 6.8 6.5 8.6 13 4.8 1.8 3.9 4.2

6.7 9.8 7.1 4.8 5.3 5.3 2.5 0.9 0.3 6.2 9.5 7.3 12 10 5.7 2.2 4.2 5.1

2.9 5.2 3.2 3.5 2.5 – 0.7 0.2 0.7 3.3 4.7 3.8 4.7 7.8 2.9 0.9 2.9 2.9

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[32]. One of the key solutions to overcoming these temperature limitations is by employing selective strains capable of attaining high biomass yield over a larger temperature range, thus acclimatizing more swiftly to change in temperature settings. This form of temperature resiliency in specific microalgae strains is yet to be fully examined.

in the mutagenesis of these strains could be highlighted, it is unlikely that the structural genes regulating the photo-sensory antenna size would undergo genetic alterations without causing an irreversible defect that would render it functionally inactive.

2.3.2.4. Gaseous exchange rate. Microalgae have the capability to remove CO2. It has been featured to consume CO2 from flue gases more efficiently than other lithotrophs [33]. The pilot-scale cultivation of microalgae may be regarded as advanced technology for CO2 sequestration. During photosynthesis, there is a concurrent CO2 fixation and O2 released into the biomass fluids. Photo-oxidative damage usually occurs to the chlorophyll when the O2 flux attains higher concentrate, leading to the inhibition of photosynthesis and lower productivity [34]. In closed reactor systems, there exist an additional compartments termed the gas exchange unit that facilitates gaseous exchange. It reduces the dissolved O2 concentrate of the media via CO2 influx, which drives the anabolic processes of transforming carbonic acids into biomass and stabilizes the pH of the cultivation system. As the most significant gradient for attaining fast proliferation, carbon supplemented in the form of CO2 accounts for approximately 50% of the biomass dry weight. Even though the degree at which CO2 diffuses in the fluid media is limited and influences the pH of the fluid system, CO2 must be supplemented in recurrent and precise concentrates. Thus, the fluid media is re-carbonated at specific time intervals, with its pH in close proximity to neutral (for freshwater microalgae strains) ensuring that the cultivating environments stabilize growth for maximum productivity.

For all biofuel production processes, productivity is of paramount importance. Regulating the biological physiognomies and bacteria/fungi/virus infections for efficient proliferation is the most complex and challenging subject in the mass production of microalgae biomass. At present, it remains unknown as to how much degree of biotic environmental control is practicable for microalgae cells [41]. Pilot-scale processes have cultivated monocultures of Spirulina and Dunaliella using minute amounts or no inoculum, but the composition of their growth media is selectively alkaline/saline. Such extremophiles are prone to propagate slowly and may not be a good target for researches aimed for high biomass yield. In contrast, Chlorella and Haematococcus do not require a selective media for its growth, but essentially needs extensive inoculum and recurrent reactor start-ups; this feature makes them a poor guide for large microalgae cultivation. Nannochloropsis and Cyclotella (diatom) biomass stably amassed at lab scale for extensive periods have appeared to exhibit high yield, but the cells are prone to infections. Thus, the identification of stable strains capable of generating large volumes of methane gas via anaerobic digestion is a fundamental need. Owing to its cell wall features, the anaerobic digestion efficiency of microalgae is often strain-specific. The ideal microalgae specie for maximum biogas production are characterized with thin or no cell wall, large cytoplasmic content, high growth rate in nonsterile media, high resistivity against natural contaminants and carbohydrate-based cell wall. Thus, the structural organization of its cell wall is crucial for anaerobic digestion; this is because cell walls are rigid, resistant to biological degradation and their presence avoids cell  cell contact of anaerobic bacteria to disintegrate the biomass.

2.3.3. Practical limits for photon excitation in microalgae cells The most important factor that limits photon excitation during photosynthesis is the light saturation effect, which causes photoinhibition and inhibits the photosynthetic productivity of microalgae biomass. The elementary process of reducing light saturation is to evenly expose the individual cells at lower light intensity. This can be achieved when microalgae cells transverse in and out of the sectional light area at a high frequency, which would be ideal for one photon to be excited during the light and dark reactions. However, the millisecond time intervals for these photosynthetic processes may be too short for practical applications except in cases where the light–dark cycle is achieved by fluid turbulence. This phenomenon limits biomass shading, and this rapid mixing needs high-energy inputs and parasitic losses. Another prevalent model that has proved impractical due to costs and design complexities involve the application of optical fibres and light prisms for dispersing light rays into the core layers of the culture media. However, PBRs could be oriented vertically, instead of horizontal designs to enable efficient light capture; modifications in the engineering approaches do not seem to be the key factor in resolving the limitations associated with light saturation and photo-inhibition. According to Kok [35], the choice of the strains to be propagated should selectively feature lower content of photo-sensory antenna pigments, which would enable more dispersion of light into the deeper layers of the culture. However, such microalgae strains have not been acknowledged because they possess more photosensitive antennas which enables them to grow in low light environments except under severe stress that halts photosynthesis [36]. Based on these limitations, extensive genetic studies on the photo-sensory antenna size reduction have been examined [27,37–40]; however, a practical model of microalgae strains with constantly amplified photon excitation efficiencies remained unproven. Even though the applications of genetic engineering

2.4. Microalgae strain selection for biomethanation

2.4.1. Components of microalgae cell wall Microalgae cell wall is predominantly made up of 30–75% carbohydrates and 1–37% proteins, which accounts for approximately 12–36% of its total cell mass. Table 3 highlights the macromolecular composition of cell wall in different microalgae strains. Neutral sugars, cellulose and hemicelluloses are the main components of the carbohydrate composition in microalgae cell wall. Studies in relation to cell wall carbohydrate composition of Table 3 Cell wall composition of microalgae. Microalgae

Chlorella vulgaris (F) Chlorella vulgaris (S) Kirchneriella lunaris Klebsormidium flaccidum Ulothrix belkae Pleurastrum terrestre Pseudendoclonium basiliense Chlorella fusca Chlorella pirenoidosa Chlorella fusca Chlorella Saccharophila Monoraphidium braunii Ankistrodesmus densus Scenedesmus obliquos

Cell wall composition (%) Carbohydrates

Proteins

30.0 35.0 75.0 38.0 39.0 31.5 30.0 80.0 45.0 68.0 54.0 47.0 32.0 39.0

2.46 1.73 3.96 22.60 24.00 37.30 20.00 7.00 – 11.00 1.70 16.00 14.00 15.00

References

[43]

[44]

[46] [45] [42]

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five different microalgae strains were related to obtaining a prominent neutral sugar component [42]. Composition of cellulose and hemicelluloses has ranged between 6–17% and 18–32% for microalgae studies carried out by Abo-Shady et al. [43] and Domozych et al. [44], respectively. For Chlorella pirenoidosa, cellulose amounts to approximately 45% of its cell wall [45], while the cell wall of Chlorella fusca lacks cellulose [46]. The proteinaceous components of microalgae cell wall exist primarily in peptides, proline and hydroxyproline forms. According to Punnett and Derrenbacker [47], the microalgae cell wall constituents were made up of peptide chains of amino acids and structurally lacks tertiary protein folding configuration; proline was more predominant in the cell wall of Chlorella vulgaris while hydroxyproline was found in ample amounts in the cell wall of Scenedesmus obliquos and Chlorella pyrenoidosa. 2.4.2. Biodegradability of microalgae cell wall Although the macromolecular composition of microalgae biomass has been reported as the basic feature that predefines methane productivity [48], the resilient nature of its cell wall to biodegradability is known as the limiting function in the kinetics of anaerobic microalgae digestion [48,49]. These biomass exhibits recalcitrant cells that are resilient to hydrolysis. Studies aimed at describing the recalcitrant nature of microalgae biomass have observed intact cellular entities in the anaerobic digester even after 30 days HRT [50,51] and the chlorophyll concentration of the biomass increased during the first two weeks of anaerobic digestion, and was still detected after 64 days [52]. According to Mussgnug et al. [5], the methane yields of the six (6) microalgae species studied range from 287 to 587 mL CH4/g VS and less methane productivities were linked to lower cellular degradation, which results in the accumulation of indigestible residues. Thus, the oxygen in the biogas was identified as the result of inherent photosynthetic functions of these cells with recalcitrant cellulosic cell wall; such microalgae cells include Scenedesmus sp. and Chlorella sp. [53]. With these observations, microalgae strains characterized by no cell wall or a protein-based cell wall (without cellulose/ hemicellulose) are readily biodegradable and most preferable for anaerobic digestion. The presence of a protective shield, which constitutes the tri-laminar sheath of the cell wall, prevents the efficient digestion of the biomass and makes the intracellular contents inaccessible [7]. This form of hydrolytic resistance has been identified in the outer cell wall structures of Botryococcus braunii and linked with the presence of sporopollenin-like biopolymers [54]. Algaenans, another indigestible residue in microalgae cell wall, has been reported as a non-hydrolysable-resistant biopolymer composed of polyether-linked n-alkyl units [55,56]. 2.4.3. Pre-treatment of microalgae biomass Biomass pre-treatment can be considered as a vital tool to lower the recalcitrant organic fraction of the biomass and increase methane generation. The pre-treatment of the feed substrate prior to anaerobic digestion significantly modifies the physicochemical features of the biomass, which increases the anaerobic microflora biodegradability of the cell wall and accessibility to its intracellular organic contents. Cellular disruption has been highlighted as the primary factor capable of enhancing anaerobic digestion productivity. The pre-treatment approaches applicable for cellular disruption of microalgae to mobilize the fraction of organic matter during digestion can be categorized as mechanical (homogenization, autoclaving and sonication), chemical (acid or alkaline treatment/ozonation) and enzymatic pre-treatments. Mechanical and chemical pre-treatments cause enhanced structural fragmentation to enable accessibility to the recalcitrant

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organic fractions that are resilient to anaerobic hydrolysis [28,57,58]. Ultrasonication as well as high-pressure homogenization techniques have been reported to increase the digestibility of Chlorella vulgaris and have proven to be an efficient means for enhancing methane yields [49,59,60]. The influences of pH, temperature, substrate concentration, and treatment duration have been studied for microalgae biomass cultivated in sewage treatment ponds [49]. Chemical degradation of microalgae biomass would be appropriate when the components of the cell wall are rich in hemicelluloses which can be solubilized via alkaline pre-treatment [43]. Enzymatic method of pre-treatment employs amylo-glucosidase, immobilized cellulase, and α-amylase for cell wall disintegration and 62% increase in cell wall hydrolysis was reported for Chlorella sp. pre-treated with immobilized cellulase [61,62]. The outcome of the biomass pretreatment enriches the methanogens in the anaerobic digester, increases the solubility of organic matter and enhances biogas yield. Imposing thermal pre-treatment up to 100 1C for a period of 8 h exerts significant effect on the cell wall disruption process, promoting 33% additional methane yield; pre-treatment of microalgae strains such as Spirulina maxima exhibits similar proficiency at 150 1C and a pH ¼11 [63]. Thus, thermal hydrolysis would not only demonstrate increase in methane yields but also energetically stabilize the sustainability of the system outputs.

2.4.4. Source of methane in microalgae biomass Several studies have linked the component ratio of carbohydrates/proteins/lipids of microalgae biomass to methane generation [15,48,64–67]. The research observations made by these authors depict zero correlation in the analysed experimental data between the carbohydrates/proteins/lipids composition of different microalgae biomass and methane productivity. Angelidaki and Sanders [68] calculated the latent methane productivity based on the carbohydrates/proteins/lipids composition of different microalgae biomass. According to their analysis, the lipid content plays a key role in methane generation even though they are not the sole source of methane in the biomass. Thus, the lipids content–methane yield correlation remains undefined and no relative correlation can be defined for carbohydrates/ proteins-methane generation in the twelve microalgae species analysed. These results demonstrate that methane generation via anaerobic digestion of microalgae is not predominantly influenced by the proportion of macromolecules present in the biomass. However, the biomass productivity as well as the biodegradability of the inert organic content of its cell wall is more significant in the selection of microalgae strains for enhanced methane yields [66]. Fig. 2 describes the latent methane productivity based on the carbohydrates/proteins/lipids composition of different microalgae biomass as calculated by Angelidaki and Sanders [68]. These results obviously demonstrate that methane generation via anaerobic digestion of microalgae is not predominantly influenced by the proportion of macromolecules present in the biomass. However, the biomass productivity as well as the biodegradability of the inert organic content of its cell wall is more significant in the selection of microalgae strains for enhanced methane yields [66].

2.4.5. Downstream processing of microalgae biomass The downstream processing of cultivated microalgae biomass is referred to as harvesting and dewatering. This process is crucial and can be primarily carried out by flocculation. The remnant cells in suspension are further concentrated via a simultaneous filtration and centrifugation process.

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2.4.5.1. Flocculation. The clustering of microalgae cells rarely occurs during the biomass cultivation prior to the harvesting phase; however, observatory studies have noted that the neutralization of the negatively charged ionic surface of microalgae cells tends to promote floc formation [42]. Different aggregation processes have been employed in previous studies to induce flocculation of microalgae cells; these include chemical flocculation, electroflocculation and bioflocculation. (a) Chemoflocculation Inorganic compounds such as aluminium sulphate, ferric sulphide and/or lime have been proven to neutralize cells charge and promote the formation of cell clusters [69]. The residual toxic effect of chemical applications to cells has been linked to the detrimental accumulation of composite compounds in the harvested cells. Therefore, highly charged organic molecules are supplanted as polyelectrolytes to neutralize the surface charges of these cells and interlink their structural networks to form stable flocs [1]. (b) Electroflocculation The introduction of electrical charges in the form of flocculating metal ions capable of generating an ionic gradient at thresholds that enables clustering of microalgae biomass is called electroflocculation. The generated cohesive forces enable the flocculating metal ions to cling to microalgae biomass, decrease their densities and hover them to the fluid surface. The behaviour of coagulation with these ions is similar to the effects observed when coagulating chemicals such as alum and ferric chloride are supplemented. This process of biomass floc formation can establish differential solid–liquid separation of microalgae cells via pH adjustment to near neutral without the need for chemicals or filters. Fig. 1 describes the mechanisms involved in electroflocculation under polymeric bridging and patching modes. The

application of electrolytic ions has several advantages over chemical flocculation; (i) No increase in salinity of the biomass is experienced; (ii) Increased flocculation efficiencies can be established with less concentration of metal ions; (iii) Biomass flocculation is independent of strain type. In electroflocculation, microalgae cells are discharged by the bubbles generated during the process, harnessing the flocculated biomass by floatation. A single flocculation unit can be employed for this process and efficiencies in excess of 98% have been reported from a single stage process [70]. (c) Bioflocculation The high-energy input for harvesting biomass makes the pilotscale anaerobic digestion of microalgae cells economically impractical. Bioflocculation employs the inherent ability of self-flocculating microalgae strains to amass non-flocculating strains. This form of aggregation does not require the additional cost for flocculants such as the supplementation of inorganic/organic compounds as well as the electrocution of the cells. It is, however, stimulated by limiting the influx concentration of nitrogen in the feed substrate while altering the pH and dissolved O2 concentrate [61]. The additional advantage of this method is that the flocculating and nonflocculating microalgae strains can be cultivated as sympatric cultures with similar growth conditions. Three flocculating microalgae strains – A. falcatus, S. obliquus and T. suecica – have been experimented for enhancing the sedimentation rate and biomass recovery of complementary microalgae cells such as C. vulgaris and N. oleoabundans from different habitats [61,71].

2.4.5.2. Filtration. Several filtration techniques can be employed for separating solid particles from suspensions. The basic principle

Fig. 1. Coupled process of microalgae cultivation systems with anaerobic digestion.

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of this process involves the channelling of fluid suspensions onto a screen filter with smaller pore size. This technique can be effectively employed for harvesting different microalgae strains, although the screen filter is prone to a major defect of fouling and clogging. 2.4.5.3. Centrifugation. Centrifugation is a commonly used solid– liquid separation technique that exerts centrifugal forces on the fluid suspensions to create a differential separation of particles based on their individual densities. Despite being regarded as one of the most effective separation techniques, centrifugation is characterized by high operational costs and thus is considered unfeasible for harvesting microalgae biomass at a pilot scale.

3. Anaerobic digestion of microalgae biomass Anaerobic digestion is a form of microbial process carried out by heterogeneous consortia with diverse biological and substrate affinities to digest organic biomass into biogas and digestate (effluent sludge). Microalgae biomass is made up substantial amounts of carbohydrates and proteins, which could undergo anaerobic digestion to generate biogas [25]. Severe ammonia inhibitions have been observed during the digestion of lipidextracted microalgae biomass and this limiting phenomenon has been linked to the elevated protein concentrates in the residues [72]. Fig. 1 also describes the different stages of coupling microalgae cultivation with the anaerobic digestion of its biomass (Fig. 2). Earlier studies on the anaerobic digestion of algae biomass can be dated back to the mid-twentieth century when the understanding of sunlight energy conversion to methane and biomass anaerobic fermentation was still primitive [50]. This primary study reported a biogas yield of 500 mL per volatile solid gram of biomass in which methane accounts for 63%. Subsequent studies carried out by Nair et al. [73] observed lower methane generation

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of approximately 220 mL per volatile solid gram of microalgae biomass at an organic loading rate of 1.7 kg m  3 d  1. The residual nutrients within the digester effluent can be reprocessed into the microalgae cultivating PBRs to enhance the overall product yields and limit cultivating costs. Because of the high biological oxygen demand (BOD) of digester effluents, the nutrient recycling efficiency may be as high as 90% [4,5,74,75].

3.1. Microalgae: source of recyclable anaerobic digestate The anaerobic digestion processes of organic substrate produce effluent discharges (liquor and sludge) predominantly composed of organic nitrogen and phosphorus derivatives. These discharges can be processed for maximum utilization of the nutrient components in agricultural applications such as organic fertilizers. Nutrient extraction techniques such as nitrogen removal via ammonia shedding for the production of ammonium sulphate and phosphorus precipitation via struvite formation have been employed to improve the quality of organic fertilizers [76,77]. Other extraction processes includes the addition of organic/mineral flocculants to produce liquid fractions (enriched with mineralized nutrients) and solid fractions (rich in organic residues) [78,79]. The degree of nutrient absorption from digestate varies according to the physicochemical characteristics of its organic matter, which account for approximately 40–86% constituting up to 75% phosphorus readily forms complexes with calcium and magnesium [80]. The amount of pathogens and heavy metals in the digestate must be characterized prior to nutrient recycling. According to Godfree and Farrell [81], the significant decrease in pathogenic microbes within the anaerobic digestate is attributed to the concentration of microflora applied as inoculum for digestion, the physicochemical properties of the digester, and the hydraulic retention time, respectively. Table 4 highlights the influence of reprocessing anaerobic digestates on microalgae biomass productivity. Several authors have proposed the recycling of digestates produced from the

Fig. 2. Latent methane productivity from the carbohydrates/proteins/lipids composition of different microalgae biomass.

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digestion of organic wastewater, sewage sludge, diary/poultry manure or food wastes for microalgae growth [81–85]. Microbial-screened digestates with approximately 50% nitrogen (nutrient source) and water may be used as a substrate for microalgae growth to reduce the process inputs of coupling microalgae cultivation with anaerobic digestion. In this context, nutrient recycling is achieved by extracting the liquid phase of the digestate, which features lower levels of phosphorus and organic residues and offsets the high nitrogen (  80% ammonium) and potassium nutrient requirements of microalgae cultivation [83]. Douskova et al. [16] carried out combined studies on biogas production in a 50L mesophilic reactor with pure stillage and microalgae cultivation at pilot scale. It was reported that the microalgae growth kinetics observed with urea as substrate were similar to those obtained for acclimatized digestate. Though ammonia can be a remarkable nitrogen source, the presence of elevated levels of unionized ammonia causes uncoupling effect on the photosynthetic function of the chloroplasts in most microalgae strains [2,89,90]. The inhibitory roles of anaerobic digestate on the proliferation of microalgae cells are summarized in Table 5. The inhibitory effects highlighted in Table 5 can be resolved using several techniques: (i) Digestate dilution to lower substrate turbidity, (ii) CO2 augmentation to offset pH levels and ammonia concentration, (iii) Intermittent biomass harvest to avoid high microalgae concentrations [85]. Moreover, the differences in the nutrients composition of various anaerobic digestates requires further research. 3.2. Microalgae: source of biomethane and syngas Anaerobic digestion is a fundamental process that generates bioenergy from a variety of carbonaceous feedstock. This form of bioenergy is referred to as biogas, which predominantly comprises of CH4 and CO2. Methane can be harnessed for heat and electricity

generation while CO2 is recycled as carbonation source into the microalgae cultivation system. The application of unprocessed microalgae biomass for biogas production can significantly circumvent the production costs associated with biomass processing during harvests and oil extraction phases employed in microalgae biodiesel production even though the anaerobic digestion of these cell residues after lipid extraction is feasible. Microalgae biomass can also be degraded via a thermochemical process known as gasification to yield a gaseous mix called syngas [96,97]. The main component of syngas includes CH4, CO2, carbon monoxide (CO), hydrogen (H2) and small hydrocarbons, which can be combusted to either generate heat/electricity or biologically upgraded via syngas fermentation or catalytically upgraded via the Fischer–Tropsch process into several liquid biofuels. The gasification process is monitored at 750–900 1C under oxygen-starved conditions. 3.3. Codigestion of microalgae biomass with carbon-rich substrates The coupling of different substrates as feed influent for anaerobic digestion is a technique employed to improve the performance stability of the anaerobic digester. This process of codigestion has been described to exhibit steady correlations with the biogas output [113]. The carbon/nitrogen (C/N) ratio of the substrates is a significant factor for monitoring the performance stability of the anaerobic digestion. At lower C/N ratios of less than 20, there is a partial nutrient starvation for anaerobic microflora causing excessive discharge of nitrogen into the metabolic pool [114]. According to Yen and Brune, [115], optimal C/N profile of cosubstrates (waste paper sludgeþmicroalgae biomass) within the range of 20–25 was observed to significantly boost methane production via increase in the functional output of cellulase activity. This enhanced performance reported for the codigestion method is in agreement with studies carried out by Chen [116] in which protein-extracted microalgae were coupled with industrial canning effluents as co-substrates for anaerobic digestion. This experiment indicates an optimal methane-specific

Table 4 Influence of reprocessing digestates on microalgae biomass productivity. Reprocessing anaerobic digestates

Influence on microalgae biomass productivity

ABATTOIR DIGESTATE MANURE EFFLUENTS

High biomass yield of 5.29  106 cells/mL with 65.32 mg/L increase in the chlorophyll concentrations after 42 days of digestate recycling [86]. Long-term microalgae cultivation in freshwater showed that these two strains undergo cellular proliferation in the presence of high nutrient loads (40, 100, and 200 g/L TN) [87]. Magnesium limitation observed when biomass was propagated on manure digestate [88].

Spongiochloris sp. Chlorella sp. Scenedesmus sp.

Table 5 Inhibitory functions of anaerobic digestate on microalgae cultivation. Component parameters

Inhibitory functions

Anaerobic microflora

Viable to disrupt the ecological organization of the cells due to competition in nutrients and the sterility of the culture media significantly declines [91]. Mutual shading, coagulation and clogging effects resulting in biomass sedimentation, mixing problems, and inaccessibility to growth nutrients [92]. Partial immersion of light energy resulting in shading effects. Digestate requires dilution [90]. Toxicity of the unionized ammonia causes instability in the media pH, which can lead to osmolysis [90]. Promotes the proliferation of heterotrophic microbes and the sterility of the culture media significantly; long-chain fatty acids ( 4C14) can be inhibitory for microalgae growth [93]. Cellular toxicity, disrupts the membranes transfusion and may lead to osmolysis [94]. Latent cellular toxicity [95]. Mutual shading caused by a high biomass density [85].

Flocculants Turbidity Nitrogen concentration Volatile fatty acids concentration Heavy metals Organic trace elements Light limitation

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gas production at a C/N ratio between 20 and 35 – the distinct range acknowledged to exhibit positive influence on methane yield [68]. It is significant to note that lower C/N profiles result in latent inhibition due to increase in free ammonia released while the risk of excessively higher C/N ratios not needed for biomass synthesis causes nitrogen deficiency and becomes inhibitory. Therefore, codigestion with secondary substrates that complement limiting nutrients can be regarded as a viable alternative to enhance the process stability of anaerobic digestion. Substrate pairing could generate a synergistic effect to lessen the influence of nutrient imbalance and mitigate substrate inhibition. Since microalgae biomass is characterized with high nitrogen content, a carbonrich co-substrate could be supplemented to accelerate the methane generation process. For instance, the augmentation of carbon-rich paper waste sludge to a mixture of Chlorella spp. and Scenedesmus spp. biomass-enhanced cellulase activity and methane productivity [115]. Significant improvements in methane generation were also observed during the codigestion of microalgae biomass with swine manure [66]. 3.4. Effect of operating parameters on the composition of biogas product The fraction of methane in the biogas generated from the anaerobic digestion of microalgae biomass ranges from 69–75%, irrespective of the strain and reactor settings. This makes the organic components of its biomass to attain efficient transformation into methane. The key factor that influences the fraction yield of CH4 in the biogas is the reactor pH, which drives the carbonate system to liberate CO2. At elevated pH levels, the digesting media assumes increased alkalinity due to NH3 release and the biogas concentrate inclines to CH4. Since the protein constituents of microalgae are limited in sulphurated amino acids (Becker, 1988), the anaerobic digestion of their biomass transiently generates lower levels of hydrogen sulphide in the biogas product. However, generation of ammonia in the biogas is relatively enhanced with increase in the protein concentrates [50]. Mandeno et al. [107] established more than 8-fold reduction in the CO2 content of synthetic biogas and detected a slight transfer of oxygen to the biogas but explosive methane  oxygen amalgam was not formed. Microalgae species such as Scenedesmus obliquus, Chlorococcum littorale, Botryococcus braunii, Chlorella kessleri, Chlorella sp., Chlorella vulgaris, Spirulina sp. and Haematococcus pluvialis have demonstrated resiliency to fractional pressures of CO2; Nannochloropsis gaditana cultures experienced no inhibition effects when exposed to gas mix containing up to 100% methane [117,118].

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observed when the CO2 content of the flue gas is less than 30%, it appears the presence of methane does not induce any form of toxicity on the proliferation of the microalgae cells [104–107]. Thus, microalgae cultures can be very efficient in biogas purification. Several studies have reported the successful development of microalgae with flue gases to achieve productivities similar to those using pure CO2, depicting that proliferation remains uninfluenced by SOX and NOX concentrates [103,108]. However, hydrogen sulphide (H2S) concentrates in flue gases have been reported to decline after biogas upgrade was established in microalgae cultivation systems [48,104]. This phenomenon is indicative of the relatively high solubility of H2S in the fluid media as solubilized H2S is readily oxidized into sulphates in the presence of oxygen [48]. Thus, the treatment of H2S component present in biogas product should be considered. According to Travieso et al. [105], Arthrospira sp. cultures demonstrated strong affinities in screening biogas product resulting from the digestion of molasses, a viscous by-product of sugar refinery. With approximately 55–71% methane, the biogas product was purified to attain 88–97% CH4 while CO2 was depleted to 2.5–11.5% as the concentration of H2S reduced from 1% to 0.3–0.4%. Similarly, a 90% CO2 depletion was reported during the purification of synthetic biogas (60% N2 and 40% CO2) with microalgae cultures. In this case, less than 6% oxygen was liberated while the nitrogen content raised to 95% [107]. The biogas product from the anaerobic digestion of organic residues is predominantly made up of CH4 and CO2 with smaller fractions of H2S, N2, NH3, H2 and other volatile gases [109,110]. Several microalgae strains have been described as resilient to increasing soluble NOx and SOx thresholds despite slight changes in the acidity of the culture media [102,111]. Gas cleaning is a prospective application of microalgae cells. There have not been literatures that describe in details the different product gas cleaning techniques of microalgae cells. Present studies have been limited to the application of flue gas for biomass cultivation and CO2 filtering. However, the mass transfer of CO2 from gaseous to liquid phase may be influenced by the chemical composition of the culture media as well as the influx setting of the photobioreactor [112]. Even though current studies have identified no negative effect on high fraction of methane biogas mix over microalgae growth, there exist no industrial scale installations operating under this model. If biogas product can be fully adapted to microalgae recycling, the biothermic process of transforming methane into bioenergy would be sustainable and efficiently productive in reducing costs associated with biogas filtration [104]. However, the inability of microalgae cells to absorb volatile gases other than CO2 may necessitate the purification of the residual biogas products after microalgae filtration.

3.5. Purification of biogas product 4. Perspectives and further research For industrial applications, methane generated from anaerobic digestion of microalgae biomass may require to be upgraded to improve its biogas quality. The removal of CO2 significantly promotes the attainment of higher calorific value for biogas products. Different gas exclusion techniques such as solvent absorption, activated carbon adsorption and membrane filtration have been described for CO2 removal [98–100]. The possibility of mitigating flue gas discharges from power plant engines with high-rate microalgae cultivation systems was first described by Oswald and Golueke [101]. It was demonstrated that microalgae cells have inherent ability to screen for CO2 in the flue gases and enhanced its growth provided that pH of the culture media is closely monitored at lower levels to reduce the ammonia emission [102–104]. Although cell toxicity and growth limitations have been

Microalgae biomass is a promising substrate for bioenergy generation. The anaerobic digestion of unprocessed biomass is the most feasible approach for efficient and productive energy generation from microalgae. Although the lipid component of the biomass can be extracted for biodiesel production, it would be more actively efficient for the whole unprocessed microalgae to be digested by the anaerobic microbes because the transformation products of cellular lipids are rich in biogas. The ability of anaerobic digestion to produce higher yields of methane from microalgae biomass could be enhanced by employing advanced pre-treatment techniques or codigestion processes combined with suitable reactor configurations and operational strategies. Another remarkable feature that requires more consideration during the downstream processing is the

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characterization of anaerobic digestate to be recycled as fed substrate for microalgae growth. The process of coupling microalgae cultivation and anaerobic digestion configurations integrating varying installation designs that could establish complete utilization of all biomass components should be further explored. In line with the promising outcomes observed in laboratory research, a scaling-up technology of microalgae-based biomethanation to pilot scale and industrial plants is required to validate the sustainability of the process. The production of greenhouse gases such as nitrous dioxide (NO2) and methane (CH4) during microalgae cultivation has been discounted and these excluded experimental data is essential to understand the life cycle assessment (LCA) of developing a coupled anaerobic digestion with microalgae cultivation system. The growing concerns in this form of biomethanation technology require a comprehensive detailed cost evaluation and environmental impact assessments of the process chain from biomass cultivation to methane combustion to be described. The limitations that destabilize anaerobic digestion are linked to the presence of unionized ammonia. Microalgae co-digestion with a nitrogen-poor substrate can be employed. The feasibility of introducing sympatric microalgae strains with a higher C/N ratio as substrates for anaerobic digestion could be adopted without a preliminary lipid recovery stage. Further studies should focus on pilot-scale implementation of coupling automated process control microalgae cultivation systems with the application of inexpensive CO2 (such as a flue gas), nutrient-rich sludge and recyclable digestates to increase microalgae productivity.

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