Factors Affecting Growth of Various Microalgal Species

Abstract

The diversity of microalgal species is colossal; however, only a few species are better known and have been investigated relatively well. Lately, microalgae have been garnering great consideration because of their potential to serve as a feedstock for either biofuel or nutraceutical production. They have the capability of producing and storing desired products as cell metabolites, and adapting themselves when there is a change in the environmental conditions (pH, temperature, light, carbon dioxide, salinity, and nutrients). The current review focuses on how the environmental conditions, including mixing, affect the growth and biomass productivity of various species of microalgae. This baseline information is important to focus on research efforts for improving biomass productivity to enhance the use of algae as a feedstock for various industries and applications. Optimal environmental conditions for enhancing biomass productivity of various species of microalgae as well as screening and selection of microalgae species are also discussed.

Introduction

Potential shortages of food, energy, water, and fuel, as a result of extreme climatic events caused by climate change, pose a serious threat to society. These potential shortages directly affect the economic stability of the many facets of society (Stephens et al., 2013). According to the Food and Agricultural Organization (FAO), the number of malnourished people is presumed to be >815 million globally (FAO, 2017). To meet the food and fuel needs of a globally growing population, feedstocks obtained from sustainable sources will play a crucial role (Ruiz et al., 2016). Algaculture promises to be one such method, considered to be very economic and may satisfy many of the requirements of the population in a sustainable way (Starckx, 2012). Humans require food for their survival, whereas in the 1950s, fearing the scarcity of food resources in the future, some companies incorporated themselves with the purpose of checking the feasibility of microalgal technology in manufacturing food for human consumption (Burlew, 1953). The first industrial development of algal growth for food took place in the 1960s in Taiwan and Japan, where Chlorella's biomass was used as a supplemental human food. The biomass obtained from Chlorella was also processed in a variety of forms including tablets and powders and sold globally. Another development was the use of Spirulina biomass as a food supplement and for the extraction of its phycocyanin content. Certain algae were also further investigated for their medicinal properties of their metabolites. For instance, the microalgae Dunaliella and Haematococcus were found to be rich in antioxidants and were sold in the form of consumable products that could enhance human health through nutrition (Slocombe and Benemann, 2016).

Microalgae, especially diatoms and flagellates, established a niche in the aquaculture industry by serving as feedstock for animal and fish production (Slocombe and Benemann, 2016). An estimate from Pulz and Gross (2004) indicated that the retail value of products acquired from microalgae was about US$ 5–6.5 billion and this was generated by diverse sectors such as health and food (US$ 1.25–2.5 billion), aquaculture (700 million), and through DHA (docosahexaenoic acid) omega-3 production (US$ 1.5 billion) (Carlsson, 2007). Thus, in the past few decades, the production of microalgae has expanded commercially, producing products of relatively high value and volume. Until today, DHA omega-3 obtained from the microalga Crypthecodinium cohnii has been leading the sales as the most sold microalgal product. Biomass productivity is an important aspect when analyzing microalgae, and it is dependent on their gross photosynthetic activity, which, in succession, relies on the prevailing environmental conditions (Slocombe and Benemann, 2016). The optimization of the environmental conditions that favor microalgae growth would, therefore, support the potential of microalgae feedstock to source products that are sustainable, ranging from food to fuels in years to come (Chen et al., 2016). However, some of the toxins produced by microalgae may pose a serious threat to public health and the World Health Organization recommends countries to monitor this closely (Cardozo et al., 2007). This article aims to provide a critical overview of how environmental conditions, such as pH, temperature, light, carbon dioxide, and salinity, and other factors, such as mixing and selection and screening of microalgal strains, affect the growth and biomass productivity of algal species.

Environmental Factors Affecting Algal Growth

Temperature

Average temperature around the globe is increasing rapidly, owing to gaseous imbalances produced by human activities, creating a greenhouse effect on the planet. It is forecasted that before the end of the 21st century, the global average temperature of the sea surface would increase by 1.4°C–5.8°C (Tait and Schiel, 2013). Temperature plays a crucial role in the growth of algae and, to optimize growth, it is essential to control the temperature in experiments involving algae (Raven and Geider, 1988). Temperature affects the gross photosynthetic activity of microalgae by undergoing cellular division, which, in turn, affects the biomass productivity of microalgae. Cell division occurs due to the increase in enzymatic activities related to the Calvin cycle. Some studies have developed a model for relating growth rate with temperature and the most commonly used expression is the Arrhenius equation. According to this equation, for every 10°C increase in temperature, growth doubles until an optimum temperature is reached after which point there will be a decrease in growth. The decrease in growth is due to the heat stress that the algae undergo and this results in the denaturation of proteins and inactivation of enzymes that are involved in the photosynthesis process (Mayo, 1997; Ras et al., 2013). The maximum growth rate with respect to temperature can be estimated by the following Arrhenius expression (μ) (Mayo, 1997): \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\usepackage{upgreek}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} \mu = A^ \prime { e^ { - \left( { { \frac { El } { RT } } } \right) } } , \end{align*} \end{document}

where A′ is constant/(day), El is activation energy of the growth limiting reaction (J/mole), R is universal gas constant, and T is the absolute temperature (°K).

Depending on the prevailing temperature conditions, microalgal strains should be adequately selected as this enhances the growth of the strain under study (Slocombe and Benemann, 2016). The absorption of nutrients and the chemical composition of cells in microalgae are also influenced by changes in temperature. In certain cases, application of temperature stress restricts the nutrient interactions (Chen et al., 2012). In most cases, increasing temperature increases the growth of microalgae up to an optimum value, and then decreases with any further increase in temperature (Cassidy, 2011). Temperatures <16°C and >35°C are considered to be detrimental for microalgal growth (Pachiappan et al., 2015).

According to a study, the optimum temperature for growth of Chlorella vulgaris was reported to be between 25°C and 30°C (Chinnasamy et al., 2009). A study on unidentified Chlorella sp. and Chaetoceros calcitrans at temperatures of 20°C, 25°C, and 30°C revealed that the highest growth rate of the species was achieved at 25°C (0.35 ± 0.04/day) and at 30°C (0.27 ± 0.02/day), respectively (Adenan et al., 2013). An analysis was carried out on the growth rate of four species of microalgae (Phaeodactylum tricormutum, Tetraselmis gracilis, Chaetoceros sp., and Minutocellus polymorphus) at temperatures ranging from 11°C to 36°C. The study revealed that the growth rate of Phaeodactylum tricormutum was highest between 16°C and 26°C; Tetraselmis gracilis showed maximum growth between 11°C and 16°C; whereas Chaetoceros sp. and Minutocellus polymorphus showed the highest growth at 31°C (Sigaud and Aidar, 1993). A study by Ha (2000) revealed that the most conducive temperature was 28°C for the growth of Tetraselmis sp. and it attained the highest cell density of 196 × 10⁴ cells/mL on day 18. The suitable temperature range for the growth of this microalga was from 22°C to 31°C. The growth of the alga began to fall rapidly at 34°C after the first few days of culturing, indicating that higher temperatures were not suitable for its growth (Ha, 2000). A study showed that Chlorella zofingiensis thrived at an ambient temperature of 28°C (Travieso Córdoba, Domínguez Bocanegra et al., 2008). Kessler (1985) studied the growth rate versus optimal temperatures for 14 different strains of Chlorella sp. and revealed that they grew successfully between 26°C and 36°C.

An investigation disclosed that the optimal temperature for the growth of Scenedesmus almeriensis was 35°C and was capable of withstanding up to 48°C after which cell death occurred (Sánchez et al., 2008a). An analysis found that Scenedesmus sp. LX1 could grow within a temperature range of 10°C to 30°C (Xin et al., 2011). A study reported that the growth of three strains of Dunaliella salina isolated from 60 saline soil samples exhibited the highest growth at 22°C (Wu et al., 2016). It was found that Dunaliella was able to withstand a temperature range between 0°C and 45°C. An experiment involving the growth of Dunaliella antarctica disclosed that the microalga was able to survive at subzero temperatures. Although Dunaliella sp. still flourished at temperatures >40°C, it nonetheless led to a decrease in the microalgal growth, but, sequentially, also led to an increase in the carotenoid content. Hence, the ideal growth of Dunaliella sp. was determined at 32°C with a wide growth temperature span ranging between 25°C and 35°C (Hosseini Tafreshi and Shariati, 2009). A study revealed that Nannochloropsis salina flourished well at an optimal temperature of 26°C with no growth detected >35°C (Van Wagenen et al., 2012). Another study disclosed that Nannochloropsis oculata grew well at a temperature of 20°C, whereas there was a gradual decrease in growth as the temperature increased (Converti et al., 2009). A study on Nannochloropsis ocenaica exhibited that the growth of the species was highest at 20°C and was incapable of growing at high temperatures of 40°C–50°C (Rai and Rajashekhar, 2014). Experiments conducted on Nannochloropsis gaditana showed that the highest cell growth was obtained at a temperature of 25°C (Al-Adali et al., 2012).

A study on the microalga Tetraselmis subcordiformis cultured at 15°C, 20°C, 25°C, 30°C, and 35°C indicated that it grew best at 20°C (Wei et al., 2015). In the case of Haematococcus pluvalis cultivated under different temperature conditions of 20°C, 23.5°C, 27°C, and 30.5°C, it revealed that the culture growth rate and biomass productivity increased with an increase in temperature to 30.5°C (Giannelli et al., 2015). The growth of the unicellular microalga Isochrysis galbana was studied under laboratory conditions at different temperatures of 15°C, 17°C, 22°C, 27°C, 33°C and 35°C. The optimal temperature for obtaining maximum growth was 27°C. Temperatures >32°C or <19°C decreased the growth of the microalga remarkably (Kaplan et al., 1986). Growth responses for Pithophora oedogonia and Spirogyra sp. at different temperatures indicated that Pithophora oedogonia had a maximum growth rate at 35°C and experience an inhibited growth at 15°C, indicating that the species was warm stenothermal. Similarly, Spirogyra exhibited maximum growth at 25°C and showed moderate inhibition at 15°C and 35°C, suggesting that this species was eurythermal over the given temperature range (O'Neal and Lembi, 1995).

Light

Algae absorbs light energy in the presence of light and stores it in the form of adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide phosphate, which are used for biomass production during the dark cycle. During the light cycle, water gets hydrolyzed to form oxygen and during the dark cycle carbon dioxide is taken up by the cell components through the Calvin cycle. It is also in the dark cycle that the microalgae build up carbohydrates, proteins, and lipids (Al-Qasmi et al., 2012; Rastogi et al., 2017). Light impacts the growth of microalgae under any one of the three different light conditions, namely light limitation, light saturation, and light inhibition. When the condition is light limiting, the growth of algae increases with any increase in light intensity. At light saturation, the photosynthetic activity decreases as the photon absorption exceeds the amount of electron turnover, thereby inhibiting photosynthesis. When the light intensity is further increased, an irreversible damage occurs to the photosynthetic apparatus, and this process is termed as photoinhibition (Chang et al., 2017). In addition, certain studies have also shown that photoperiod has a significant effect on the growth of microalgae.

For instance, a study to investigate the effect of photoperiod on the growth of Dunaliella salina CCAP 19/30 revealed that longer photoperiods led to an increased growth of microalga with higher cell densities (Xu et al., 2016). Algae grow well under light conditions but tend to divide preferably under dark conditions by binary or multiple fission to produce daughter cells, and this seems to have a significant implication on the overall productivities of microalgal cultures (Bišová and Zachleder, 2014; Concas et al., 2016b). The duration and intensity of light, therefore, directly affect the growth and photosynthesis of microalgae. A research study disclosed that microalgae tend to flourish under either blue (λ∼420–470 nm) or red light (λ∼660 nm). It was also observed that red to far-red light accelerated the growth of microalgal cells (Schulze et al., 2014). The kinetic model for photosynthesis in microalgae in relation to light is given by the following equation (Rastogi et al., 2017): \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\usepackage{upgreek}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} { \frac { d { x_1 } } { dt } } = - \alpha I { x_1 } + \Upsilon { x_2 } + \delta { x_3 } , \end{align*} \end{document}

where I is incident light illumination (μE/m²·h), x_1, x₂, and x₃, are fraction of photosynthetic factory in the open, closed, and inhibited state (dimensionless), and α, ϒ, and δ, are kinetic constants (μE/m²·h).

In an experiment, the light for Chlorella vulgaris was regulated at 3,960, 7,920, and 11,920 lux with no control over pH. The light/dark period was 12/12 h. It was observed that the maximum growth of cells was observed under 3,960 lux (Gong et al., 2014). The effect of light illumination on Scenedesmus obliquus for intensities varying from 740 lux (10 μmol/[m²·s]) to 74,000 lux (1,000 μmol/[m²·s]) indicated that highest growth was detected at 11,100 lux after which the increase in light intensity did not improve the growth rate, confirming that the point of saturation for photosynthesis was reached (Sforza et al., 2014). In the case of Scenedesmus almeriensis, greater resistance to higher irradiances showed no signs of photoinhibition even at the maximum tested irradiance of 102,250 lux. The biomass productivities were the highest (0.66 g/L-day) at this light intensity (Sánchez et al., 2008a). Dunaliella salina CCAP 19/30 could modify their photo systems to achieve maximum photosynthesis even when they were exposed to higher light intensities. When the light intensity was increased >74,000 lux (1,000 μmol photons/[m²·s]), cells displayed photo damage. However, the growth rate increased with increase in light intensity (Xu et al., 2016). Dunaliella bardawil DCCBC 15 and Dunaliella salina CCAP 19/18 were inspected for their growth at light intensities of 3,700, 7,400, and 11,100 lux (50, 100, and 150 μmol photons/[m²·s]) and the results showed that the optimal growth of Dunaliella was obtained at 50 μmol photons/[m²·s] light intensity and the growth rate decreased with increasing light intensity (Vo and Tran, 2014).

Nannochloropsis salina was exposed to varying intensities of 370, 1,850, 3,700, 7,400, 18,500, and 62,900 lux (5, 25, 50, 100, 250, and 850 μmol/[m²·s]). The growth rate increased with light intensity and the highest growth rate was achieved at 18,500 lux; however, photon conversion efficiency decreased for light efficiencies >3,700 lux (Van Wagenen et al., 2012). The growth rate of Nannochloropsis ocenaica increased exponentially when exposed to light intensities in the range of 2,516–5,920 lux (34–80 μmol photons/[m²·s]), reaching a maximum at 5,920 lux (Sandnes et al., 2005). It is evident that light influences cultivation of algae and optimal exposure to light is required to achieve maximum productivity. In fact, sunlight provides the light required for supporting metabolism, but if present in excess, it leads to oxidative stress and photo inhibition, thereby reducing photosynthetic efficiency (Sforza et al., 2012). A study on the growth of Odontella aurita under two light intensities of 11,100 and 22,200 lux (150 and 300 μmol photons/[m²·s]) revealed that the microalga was able to grow under 11,100 lux; however, the alga grew faster at early stages under high light (22,000 lux). This was due to the low cell density at early stages, which enabled the cells to receive an additional amount of irradiance under high-light conditions (Xia et al., 2013). The biomass concentration of Neochloris oleoabudans HK-129 increased from 1.2 to 1.7 g/L when the light intensity was increased from 3,700 to 14,800 lux (50–200 μmol/[m²·s]) (Sun et al., 2014).

The growth of Chlamydomonas reinhardtii increased when the light intensities were varied from 4,440 to 22,200 lux (60–300 μE/[m²·s]). However, there was little difference in growth between 14,800 and 22,200 lux and it was concluded that the light intensity of 14,800 lux was conducive for the growth of the species (Pyo Kim et al., 2006). A study on the growth of Isochrysis sp. under exposure to varying illumination levels of 108,000, 79,488, 62,208, 31,320, and 0 lux (100%, 73.6%, 57.6%, 29%, and 0%) of natural sunlight revealed that the maximum growth rate was attained under the illumination exposure of 79,488 lux. This revealed that for an optimum photosynthetic process, cell growth rate and carbon fixation in microalgae could be achieved by altering both dark and light regimes. Direct exposure of the microalgae to sunlight could potentially damage the cells, whereas unavailability of light negatively impacts the growth of the microalgae (Harun et al., 2014). The growth of four microalgal strains namely Chlorella vulgaris, Pseudokirchneriella subcapitata, Synechocystis salina, and Microcystis aeruginosa was studied under various light irradiances of 2,664, 4,440, 8,880, and 13,320 lux (36, 60, 120, and 180 μE/[m²·s]) with varying light/dark ratios (10:14, 14:10, and 24:0). The results observed showed that highest growth rate and biomass productivity for all the species under study were achieved at an irradiance of 13,320 lux by continuous illumination for 24 h (Gonçalves et al., 2014). A study using LED lights (red, natural white, warm white, and blue) at different light intensities of 3,700, 5,920, and 8,140 lux (50, 80, and 110 μmol/[m²·s]) on the biomass productivity of Chlorella vulgaris revealed that warm white light (380–760 nm) with 80 μmol/[m²·s] was optimal for enhancing biomass productivity and photosynthetic rate (Khalili et al., 2015). Another study on marine microalgae Tetraselmis sp. and Nannochloropsis sp. under blue light (420–470 nm) and red light (660 nm) of 7,400 lux (100 μmol/[m²·s]) with a 24:0 light/dark cycle revealed that both the species grew well under blue light (Teoa et al., 2014). An experiment conducted on red alga Pyropia haitanesis under blue, red, green, and fluorescent light of 7,400 lux (100 μmol/[m²·s]) with 12:12 light/dark cycle revealed that the highest growth was achieved under fluorescent light (Wu, 2016).

pH

pH is believed to be one of the underlying parameters that controls the cell metabolism and formation of biomass in microalgae. The growth of a majority of microalgal species is known to flourish at neutral pH and all strains of microalgae seem to have a limited optimal range of pH (Lutzu, 2012). Algae respire carbon dioxide during photosynthesis, and at optimal pH, the bicarbonate present in the medium is converted into carbon dioxide by the action of algal enzyme carbonic anhydrase with the release of hydroxyl ions that tend to increase the pH (Gerardi, 2015). \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\usepackage{upgreek}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} {{{\rm{HCO}}_3}^ -} - - - - {\rm{Carbonic \ anhydrase}} --- - > {{\rm {CO}}_2} + { \rm{OH}}^ - \end{align*} \end{document}

According to the physiology of microalgae, it is observed that either the thylakoid or chloroplasts carry out the vital functions at a specific pH range, since the medium's pH is known to influence the process of photosynthesis in microalgae. Indeed, extremes of pH, that is high as well as low pH, reduce the rate of photosynthesis. At high pH, the trend of absorption of the trace metals and nutrients might get altered. Similarly, at low pH, enzyme inhibition occurs in the photosynthetic process and there is a high possibility of the growth medium getting contaminated by micro-organisms (Bakuei et al., 2015). At medium pH, there is an affiliation to the carbon dioxide concentration, that is, the pH increases steadily as carbon dioxide is consumed. The pH also influences the availability of nutrients such as iron and organic acids (Lutzu, 2012). Hence, pH is considered to be a major environmental factor that is regulated by carbonate equilibrium in both oceans and inland waters. The optimal pH range for photosynthesis to occur in most of the microalgae is in between 6 and 10, wherein the bicarbonate form is considered to be dominant (Rastogi et al., 2017). The pH in oceans is 8 ± 0.5; however, it fluctuates from <2 to 12 in natural bodies of water. Low pH natural water often originates from volcanic regions that receive strong mineral acids, in general, sulfuric acid, and hence the pH is often found to be <4. High pH values can be attributed to lakes that belong to endorheic regions due to the presence of high concentrations of sodium carbonate or sodium bicarbonate (Weisse and Stadler, 2006). Algae have been found to survive at both alkaline and acidic pH (Ying et al., 2014). The effect of pH on Chlorella vulgaris species revealed that the microalga exhibited reduced growth at both acidic (3.0–6.2) and alkaline (8.3–9.0) pH. However, optimal growth was achieved when the pH was between 7.5 and 8.0 (Rachlin and Grosso, 1991). The optimum pH for the growth of Spirulina platensis was observed to be in between 7.0 and 9.0. The maximum growth rate for the microalga was observed at pH 8.0, suggesting that moderate alkalinity was necessary for the ideal growth of the microalga (Fagiri et al., 2013). Scenedesmus almeriensis grew effectively at a pH of 8.0 with a decrease in growth at higher pH and exhibited tolerance to neutral pH (Sánchez et al., 2008b). Scenedesmus obliquus grew well in neutral as well as in weakly alkaline conditions and the maximum growth was observed at a pH of 8.0 (Yang et al., 2016).

The growth of Scenedesmus sp. (ADIITEC-II and GUBIOTJT116) at various pH levels ranging from 5.0 to 9.0 showed that the maximum specific growth rate and biomass productivity for the species was achieved at a pH of 7.0. Acidic conditions (pH 5.0 and 6.0) did not alter the cell density and demonstrated lower biomass productivity (Difusa et al., 2015). The initial pH for Scenedesmus sp. strain R-16 was varied from 3.0 to 12.0 and it was observed that the alga had strong tolerance to varying pH and grew well at a pH varying between 4.0 and 11.0. At pH 3.0 and pH 12.0, the algal cells exhibited poor growth. The microalga exhibited the highest biomass productivity at a pH of 7.0 (Ren et al., 2013). A study on Dunaliella salina at different pH revealed that the maximum growth occurred at pH 9.18 (4.59 × 10⁶ cells/mL) (Abu-Rezq et al., 2010). The effect of pH on the growth of Dunaliella bardawil and Chlorella ellipsoidea for a wide range (pH 4.0 to pH 11.0) showed that the ideal pH for the growth of the species was 7.5 and 10.0, respectively. The growth of both Dunaliella bardawil and Chlorella ellipsoidea was retarded at a pH >10.0, as carbonate ion (an important source of inorganic carbon) was not available for the algae (Khalil et al., 2010).

The optimum growth of Nannochloropsis salina was observed at a pH of 7.5–8.0; however, the microalga could grow over a wide range of pH (5.0–10.5) (Boussiba et al., 1987). Another study on the growth of Nannochloropsis salina at six different pH levels (5, 6, 7, 8, 9, and 10) revealed that highest growth rate was achieved at a pH between 8 and 9 (Bartley et al., 2014). The optimum pH for growth of Nannochloropsis oculata was validated using response surface methodology and was found to be 8.4 (Spolaore et al., 2006). Influence of the medium's pH on Chlorococcum sp. revealed that the maximum growth of the microalga was observed at a pH of 8.0 and the growth rate was 0.066/h (Zhang et al., 1997). The ideal pH for the growth of Tetraselmis sp. was observed to be at 8.5 (Khatoon et al., 2014). A series of experiments to investigate the effect of pH on the growth of Nannochloris eucaryotum revealed that a maximum growth of 9.85 ± 0.54 × 10⁻⁴/h was achieved when the pH was controlled at 6.60 ± 0.67 (Lutzu, 2012). A study on the growth of Chlamydomonas applanata, within a pH range of 1.4–8.4, showed that no growth was observed at low pH between 1.4 and 3.4. Optimum growth was obtained for pH ranging from 5.4 to 8.4, whereas the maximum growth was observed at pH 7.4 (Visviki and Santikul, 2000). The growth response of Chlamydomonas acidophila was examined at pH ranging from 1.4 to 8.4. Analysis of variance showed that growth was maximum at pH 7.4 with no growth observed at pH between 1.4 and 2.4 (Visviki and Palladino, 2001). Euglena mutabilis exhibited the highest growth between pH 3.4 and pH 5.4 and it was able to survive over a wide range of pH between 0.9 and 8.2. At pH 0.9, there was reduced growth, and within 24 h, all the microalgal cells were dead (Dach, 1943).

Salinity

Each strain of microalgae displays differences in their capacity to adjust to salinity. Stress, from high concentrations of salt, affects the growth of cells and the formation of lipids. It was noted that as salinity increases, the expression of lipids increased but resulted in dwindling cell growth. Since the two important traits that researchers look for in selecting a microalgal strain for study is often the ability of the algae to produce both high biomass and lipids, considerable importance is given to microalgae that flourish in a saline environment (Asulabh et al., 2012). Marine microalgae are exceptionally tolerant to alterations in salinity when compared with freshwater species (Blinová et al., 2015).

Spirulina platensis exposed to different concentrations of sodium chloride ranging from 5.844 to 23.376 ppt (0.1–0.4 M) revealed that the growth of microalga was higher at lower concentrations of sodium chloride between 5.844 and 11.688 ppt and the growth reduced at higher concentrations ranging from 17.532 to 23.376 ppt (Sujatha and Nagarajan, 2014). Chlorella sp. was exposed to different salinities, namely 0, 30, 35, and 40 ppt of BG11 (blue-green medium) with a limited supply of sodium nitrate. The salinity was adjusted to the desired levels using sodium chloride. It was reported that as the salinity increased, the growth of the microalgae decreased. The biomass concentration was high (0.09 g/L) at 0 ppt when compared with 30 ppt (0.045 g/L), 35 ppt (0.038 g/L), and 40 ppt (0.04 g/L) (Andrulevičiūtė et al., 2011). The effect of salinity on growth of Scenedesmus almeriensis was studied with different salinities (brackish water (3 × 10⁶cells/mL), sea water (7 × 10⁶cells/mL), and fresh water. It was found that a higher number of cells were found in fresh water (9.8 × 10⁶ cells/mL), indicating that the lower the salinity the higher the growth of this microalga (Suyono et al., 2015). However, Scenedesmus almeriensis also showed higher tolerance to medium salt concentrations of 5.844 ppt (0.1 M) sodium chloride and showed higher biomass productivities at 5.844 sodium chloride when compared with productivities observed in freshwater medium (Benavente-Valdés et al., 2016).

Measurement of the effect of salinity on growth of Scenedesmus obliquus was made at various concentrations of sodium chloride 3, 17.5, 35, 58.44, 116.88, and 166.32 ppt (0.05, 0.3, 0.6, 1.0, 2.0, and 3.0 M). The growth of Scenedesmus obliquus was inhibited at sodium chloride concentrations >35 ppt, whereas there was reduced growth at 17.5 ppt. The highest growth of the microalga was observed at 3 ppt NaCl and it was equivalent to the growth that was obtained in fresh water. The results thus suggested that low salinities, between 0 and 0.05 M, were appropriate for the promotion of the growth rate of Scenedesmus obliquus (Kaewkannetra et al., 2012). Dunaliella bardawil was exposed to salinity levels ranging from 1 to 3 M. The results revealed that the maximum growth rate was observed at lowest salinity of 1 M (Gomez et al., 2003). A decrease in cell growth of Dunaliella tertiolecta ATCC 30929 was observed when the concentration of sodium chloride was increased from 58.44 to 116.88 ppt (1.0–2.0 M). Hence, sodium chloride concentration of <58.44 ppt was considered to be appropriate for achieving a high cell concentration (Takagi et al., 2006). Dunaliella salina is a marine microalga that has the ability to tolerate high salinity. Dunaliella salina CCAP 19/18 was inspected for its growth under different salinities of 58.44, 87.66, and 116.88 ppt (1, 1.5, and 2.0 M). The ideal growth for Dunaliella was obtained at 87.66 and 116.88 ppt salinities (Vo and Tran, 2014).

Nannochloropsis salina was exposed to different salinity levels of 10, 22, 34, 46, and 58 ppt practical salinity unit. Being a marine microalga, it exhibited highest growth rate at 22 ppt and highest biomass accumulation at salinities of 22 and 34 ppt. Nannochloropsis salina exhibited no growth at salinities of 58 ppt and <10 ppt (Bartley et al., 2013). The effect of salinity on growth of Nannochloropsis oculata CS 179 was carried out at various salinities of 150, 250, 350, 450, and 550 ppt. The results indicated that the highest biomass was obtained at a salinity of 250 ppt (Gu et al., 2012). The marine microalga Tetraselmis suecica was capable of tolerating a wider range of salt concentrations. The cultures were grown at 48 different salinity conditions from 0 to 350 ppt. The ideal growth was achieved between 250 and 350 ppt with a maximum cellular density of 1.3 × 10⁶ cells/mL (Fabregas et al., 1984). Four species of microalgae Desmodesmus armatus, Mesotaenium sp., Scenedesmus quadricauda, and Tetraedron sp. were cultured at 2, 8, 11, and 18 ppt salinity. Desmodesmus armatus showed maximum tolerance to salinity, growing actively at 18 ppt, whereas Mesotaenium sp. was less halotolerant (ability to survive in hypersaline conditions) with the growth rate decreasing from 11 ppt. Therefore, the ideal salinity level for the growth of Mesotaenium sp. was observed to be between 2 and 8 ppt. Both Scenedesmus quadricauda and Tetraedron sp. grew well at salinity levels of 2 and 8 ppt (Von Alvensleben et al., 2016).

The growth of Schizochytrium limacinum OUC88 at various salinities 0, 0.9, 1.8, 2.7, and 3.6 ppt (0, 0.9, 1.8, 2.7, and 3.6% w/v) was analyzed. The strain performed better and the biomass remained steady with salinity at 1.8, 2.7, and 3.6 ppt. When there was a decrease in salinity from 0.9 to 0 ppt, there was a significant reduction in the biomass productivity (Zhu et al., 2007). The growth of Botryococcus braunii under various salinities of 1, 2, 3, 4, and 5 ppt (17, 34, 51, 68, and 85 mM) revealed that although the microalga was able to grow at all salinity levels, the maximum growth rate was observed at the lowest salinity level of 1 ppt (Rao et al., 2007). A study on the effect of salinity on three microalgal strains, C. cohnii ATCC 30556, C. cohnii ATCC 50051, and C. cohnii RJH, revealed that C. cohnii ATCC 30556 had its maximum growth rate of 0.090/h at a sodium chloride concentration of 9.0 ppt (g/L), whereas C. cohnii ATCC 50051 and C. cohnii RJH had their maximum growth rates of 0.049 and 0.067/h, respectively, at a sodium chloride concentration of 5.0 ppt (g/L). When an optimum salinity was reached, the growth rate decreased with increasing salinity. Almost no growth was observed when the medium did not contain sodium chloride, and at extremely high sodium chloride concentrations, growth was inhibited, and the cells were elongated. The elongation of the cells was attributed to the increase in external ionic concentrations that tend to inhibit cell growth (Jiang and Chen, 1999).

Microalgae have the capability of maintaining a balanced cell composition even if there is a dramatic change in the external environment. When this happens, growth rate can be retarded to maintain smooth functioning of the cell structures without any changes in the cellular composition. This process is defined as homeostasis. However, there are certain microalgae that change their cellular composition due to changes in external environment through acclimatation. The conditions that stimulate homeostasis or acclimatation response are currently unknown (Montechiaro et al., 2006). Salinity is considered to be one such factor that will be able to maintain homeostasis in algal cells. For instance, in Tetraselmis viridis, the Na⁺ transporting ATPase played an important role in increasing the salt tolerance of this alga by maintaining the cytoplasmic ion homeostasis (Strizh et al., 2004). In short, maintenance of balance in the composition of the cell (homeostasis) holds the key when there is change in salinity or any other external factors (Montechiaro et al., 2006).

Carbon dioxide

Today about 85% of the world's energy demand is satisfied by burning fossil fuels that emit and concentrate greenhouse gases in our atmosphere. In recent decades, the levels of carbon dioxide in the air have risen from 260 to 380 ppm. Some suggestions have been made and studies have been conducted to minimize the effects of human activities on increasing greenhouse gases (Minillo et al., 2013). The sum of fossil fuels being ignited is directly proportional to the increase of carbon dioxide in the air. The increasing concentration of carbon dioxide in the air is considered to be one of the main causes of global warming. Therefore, fixing carbon dioxide biologically could be considered to help mitigate this problem (Salih, 2011), or the effective removal of carbon dioxide from the point source should be initiated (Li et al., 2012). Capturing carbon and sequestering it biologically are considered to be safe for reducing environmental carbon dioxide. Microalgae can fix carbon dioxide with efficiencies greater than that of terrestrial plants. The selection of microalgal species is important for attaining biological carbon dioxide systems that work, and the microalgal species selected depend on the strategy involved in carbon sequestration. The amount of carbon dioxide in the air plays a major role in the growth of microalgae, that is, the higher the concentration of carbon dioxide, the better the growth (Salih, 2011; Khairy et al., 2014). A study on the effect of varied carbon dioxide concentrations, namely a control (absence of carbon dioxide), 280, 385, 550, 750, and 1,050 ppm (control, 280, 385, 550, 750, and 1,050 μatm) on the growth of Chlorella gracilis showed that there was an increase in the number of cells up to the carbon dioxide concentration of 385 ppm, followed by a decrease in growth observed at 550 ppm as the microalga was not CO₂ tolerant above this limit (Khairy et al., 2014).

A study with Chlorella vulgaris ARC1 examined growth under different carbon dioxide concentrations ranging between 350 and 200,000 ppm (0.036% to 20%). The results obtained showed that Chlorella vulgaris had the ability to sequester 38.4 ppm (milligrams of CO₂ L/day) at elevated carbon dioxide concentration of 60,000 ppm (6%), thereby increasing the growth of biomass (Chinnasamy et al., 2009). Another study on Chlorella vulgaris showed that the alga had the capability of growing well (0.4 g/L after 300 h of cultivation) at carbon dioxide concentrations of 2,000,000 ppm in a semibatch photobioreactor while maintaining low pH values (Cao, 2013). An investigation on the growth rate of three species Chlamydomonas reinhardtii, Chlorella pyrenoidosa, and Scenedesmus obliquus disclosed that as the concentration of carbon dioxide increased, the growth of microalgae also increased, but attained saturation at 1,320 ppm (30 μM), 4,400 ppm (100 μM), and 2,640 ppm (60 μM) of carbon dioxide, respectively (Yang and Gao, 2003). Scenedesmus obliquus showed increased biomass (2.3 g/L) at 150,000 ppm (15%) carbon dioxide concentration (Singh and Singh, 2014). A study to improve the biomass productivity of filamentous microalgae using carbon dioxide concentrations of 7,480 ppm (170 μM) and 748 ppm (17 μM) was carried out in Denmark. It was found that the biomass productivity was higher in the enclosures containing 7,480 ppm of carbon dioxide (Andersen and Andersen, 2006).

The microalgal strain Botryococcus braunii LB-572 was exposed to various concentrations of carbon dioxide of 0, 5,000, 10,000, and 20,000 ppm (0%, 0.5%, 1%, and 2%, v/v) and the growth pattern was studied. The results revealed that at 20,000 ppm of carbon dioxide, the growth of the microalgal strain flourished the most, whereas the microalga also exhibited growth at the other concentrations studied (Ranga Rao et al., 2007). A study on Dunaliella salina disclosed that there were no alteration in growth for changes in carbon dioxide concentrations from <230 to 5,100 ppm, thus showing that carbon dioxide had no significant effect on the growth of Dunaliella salina over that range (King et al., 2015). Nannochloropsis oculata NCTU-3 exhibited decreased growth at elevated carbon dioxide concentrations when investigated for its growth at various carbon dioxide concentrations of 20,000, 50,000, 100,000, and 150,000 ppm (2%, 5%, 10%, and 15% v/v). Microalga exhibited reduced growth at 50,000, 100,000, and 150,000 ppm of carbon dioxide. However, the growth of microalga was enhanced when aerated with 20,000 ppm of carbon dioxide concentration (Chiu et al., 2009). Spirulina platensis was exposed to carbon dioxide concentrations of 0, 5,000, 10,000, and 20,000 ppm. The pH decreased with increasing carbon dioxide concentration. The results revealed that the alga grew well at carbon dioxide concentrations of up to 10,000 ppm, although the difference in growth was insignificantly small when compared with 20,000 ppm carbon dioxide. The productivity of the microalga was increased to 60% when it was exposed to 10,000 ppm of carbon dioxide (Ravelonandro et al., 2011). The effect of carbon dioxide concentration on Chlorocuccum littorale at concentrations of 50,000, 200,000, 350,000, and 500,000 ppm (5%, 20%, 35%, and 50%) revealed that the growth decreased with increasing carbon dioxide concentration (Ota et al., 2009).

Nutrients

Growth of algae is directly proportional to the uptake rate of the most limiting nutrients and is described by the Michaelis–Mentis equation as follows: \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\usepackage{upgreek}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} {{ \mu = }}{{{ \mu }}_{{ \rm{max}}}} \left[ {{ \rm{S / S + K}}} \right] , \end{align*} \end{document}

where μ is the growth rate, μ_max is the maximal growth rate, S is the concentration of the limiting nutrient, and K is the concentration that leads to half-maximal growth rate called the half-saturation constant (Titman, 1976). Nitrogen is considered to be a building block for proteins and nucleic acids, whereas phosphorus forms parts of phospholipids. If these macronutrients are limited, then it tends to shift the metabolic pathways (Juneja et al., 2013). Redfield (1963) had stated that when the ratio of N/P exceeds 16, then phosphorus was considered to be the limiting factor and nitrogen content needs to be controlled to optimize the growing condition of microalgae. The requirement of optimum level of phosphorus was considered to be conducive for the growth of microalgae. Phosphorus content <0.045 mg/L, or >1.65 mg/L, prohibits the growth of microalgae. The growth of microalgae is favored when the phosphorus content is equal to 0.02 mg/L (Redfield, 1963; Ren, 2014).

A study on Chlorella vulgaris and Nannochloropsis oculata disclosed that if the supply of nitrogen was decreased, the lipid synthesis had increased, whereas no effect on the growth pattern of microalgae was observed (Paes et al., 2016). Dunaliella sp. was able to build up a huge volume of carotenoids and astaxanthin when deprived of nitrogen. Unlike for nitrogen, phosphorus was considered to be the main limiting nutrient in the growth of microalga for the expression of value added products. Phosphorus limitation in Scenedesmus sp. (from 2.0 to 0.1 mg/L) led to the increase in lipid content from 23% to 53% (Juneja et al., 2013). For Scenedesmus species LX1, nitrogen and phosphorus limitation increased the lipid content but the growth was low (Xin et al., 2010). Reduction of nitrogen in the medium by 75% for Nannochloropsis salina resulted in an increase of lipid content from 34.6% to 59.3% with a significant decrease in growth (Fakhry and El Maghraby, 2015). During Calvin's cycle, inorganic carbon from the liquid medium is taken up by the microalgal cell and converted into glyceraldehydes 3-phosphate. The shift of metabolism toward production of storage or functional molecules depends on the ratio between internal carbon and nitrogen. At the initial stage of growth of microalgae, the internal carbon exceeds the C:N ratio due to high photosynthetic rate, thereby synthesizing proteins. However, as growth progresses, the nitrogen in the liquid medium gets consumed and there is a shift of production from proteins to lipids (Concas et al., 2016a). Trace metals such as iron, manganese, cobalt, zinc, nickel, and copper are some of the important trace metals that are required by algae for their metabolic functions. If absent, the growth of algae may be limited (Bruland et al., 1991). A study revealed that the growth of Nannochloropsis oculata increased with the addition of trace elements such as Fe³⁺, Zn²⁺, Mn²⁺, Cu²⁺, Co²⁺, and EDTA. Increase in concentration of these trace elements increased the photosynthetic activity of the algae by enhancing the carbon dioxide concentration (Dou et al., 2013).

Mixing

Effects of light and temperature on microalgae are two important growth parameters that are dependent on each other, and simultaneously controlling both can be difficult and costly. As a potential solution, mixing is one of the easiest methods to ensure uniform distribution of light and temperature to all the cells (Rocha et al., 2003). Problems of shading are commonly addressed by seeking mixing solutions, as shading prohibits the microalgae from absorbing light, and mixing is considered to be a cost-effective solution. Proper mixing can be provided to the microalgae effectively and at a low cost by gas mixing (Ren, 2014). A study on the effect of mixing on Spirulina platensis in three ways (mixing with a magnetic agitator inside the column, bubbling air into the column, and recirculating through a pump) showed that the growth of the microalga was highest when using a bubble column. However, almost similar values were observed for stirring and mixing as well (0.0122, 0.009, and 0.010/h) (Ravelonandro et al., 2011). Another study on the mixing of Chlorella sp. revealed that continuous mixing (airlift pump) of the culture increased the growth of microalga significantly (up to 30%) (Persoone et al., 1980). A study on the influence of mixing (using shaker) on Desmodesmus communis revealed that the growth and yield of the microalga significantly increased when mixed in comparison with unmixed cultures (Vanags et al., 2015). The effect of mixing on the biomass productivity of Scenedesmus obliquus using three modes namely stirring, aeration, and a combination of stirring and aeration revealed that the biomass productivity increased with stirring when compared with the other two methods (Mandal and Mallick, 2012). A study on Phaeodactylum tricornutum revealed that mixing, mass transfer, and carbon dioxide consumption could be the important factors that limit growth of the microalga. Mixing tends to improve when the gas flow rate is increased. Subsequently the availability of carbon dioxide increases and so does the growth. Depending on biomass concentration, the carbon dioxide consumption was controlled either by carbon dioxide gradients in the liquid phase or by carbon dioxide transfer from the gas phase (Contreras et al., 1998). However, additional research in this domain should be carried out to get a better understanding of the effect of dissolved gases on microalgal growth.

Selection and Screening of Microalgal Strains

Selection of algal strains is carried out through a number of steps. The first step is isolation, which is commonly carried out to acquire pure cultures. The customary isolation technique involves the use of a micropipette and a microscope. The single cell isolation is the most commonly used method today because of its low cost and the applicability of this method to a broad range of samples. The advancement made in this technique as it is used today is called flow cytometry. Flow cytometry is a technique that employs the principle of fluorescence for cell sorting of desired algal strains from different algal strains present in water. A novel approach using bioinformatics provides a gateway for exploring new algal isolates. The steps commonly involved are DNA/RNA extraction, polymerase chain reaction amplification, and sequencing (Duong et al., 2012). After isolation, the first level of screening is generally done using Nile Red lipophilic fluorescent dye, for the stability of its fluorescence intensity, and its added benefit of remaining unaffected by changes in dye concentration, duration of staining, and organic solvent (Cirulis et al., 2012). The strains that successfully surpass the first level undergo a second level of screening to decide on the medium that should be used for the sustained growth of the microalgae. BG11, bold basal medium, and C-medium are used as common medium for growing freshwater strains, whereas F/2 medium is commonly used for marine strains. The second level of screening is mainly done to zero down on the most suitable growth medium for the algal strain under study. After selecting the growth medium, the algal strain undergoes the third level of screening, which assesses the growth of the strain when subjected to carbon dioxide, constant pH, and inhibited oxygen level. Strains that successfully excel in all three levels of screening are considered to be potential candidates for scale-up. Therefore, for future successful commercial employment of microalgal techniques, implementing strain bioprospecting will be crucial (Slocombe and Benemann, 2016).

Discussion and Conclusion

Based on the literature reviewed, it is evident that temperature and light are the two most important parameters that influence microalgal growth and are dependent on each other. The optimum temperature for the growth of the majority of the algal species should be between 15°C and 35°C, although some exceptions exist. The optimal light illumination required for the growth of microalgal species should be between 1,850 and 14,800 lux except for Scenedesmus almeriensis that has the capability to withstand higher irradiances. It can also be seen that altering the light–dark cycles and the color of light also positively or negatively impacts the growth of microalgae but only to a certain extent (Harun et al., 2014). The optimal pH for growth of most of the algal species should be between 7.0 and 9.0, although some species that dwell in both acidic and basic environments are also existent (Blinová et al., 2015). Besides this, the amount of major and minor nutrients present in the medium also plays a crucial role in the growth of microalgae. The importance of the effect of change in pH, salinity, and carbon dioxide on microalgal growth solely depends on the species (freshwater or marine) under study. Biomass productivity is the major challenge that microalgal industries face for the manufacturing of products of high commercial value.

In conclusion, microalgae are considered to be a valuable bioresource and are recently receiving great attention. A lot of progress has been made in understanding the growth of microalgae for the past few decades. The present review underlines the different environmental conditions that affect the growth of a number of microalgal species and also discusses how mixing and selection of microalgal strains can prove crucial for making microalgal technologies a reality in the future. The microalgal species discussed in this review provide a scope for future studies as these species have garnered great interest among researchers. Evidence in this review suggests that microalgal growth is directly proportional to the environmental conditions in which the algae are grown. Therefore, it becomes important to maintain optimum conditions for microalgae to grow as it directly influences the biomass productivity and, in turn, the amount and type of valuable products that can be obtained from the produced biomass. Currently algae that belong to the group Cyanophyceae, Chlorophyceae, and Bacillariophyceae are pondered more as they are considered to exhibit one or more desirable characteristics (wastewater treatment, carbon dioxide fixation, and biofuel production) and are frequently cited by researchers. Discovery of new strains of microalgae, by bioprospecting in habitats that have not been explored, may provide a gateway for identifying microalgae that may possess new industrial applications. Optimizing environmental conditions for acquiring maximum growth and biomass productivity from microalgae should be the focus of much research in the future. A summary of the biomass productivity and growth of commonly used microalgae according to varying environmental conditions is provided in Table 1. An area that has to be explored more in depth is the conditions of mixing of microalgal strains and the optimal control of nutrients and environmental conditions. Therefore, innovative research for the optimized production of microalgae will make the exploitation of microalgae economically feasible and in rising demand.

Table 1.

Summary of Impact of Environmental Factors on Growth and Biomass Productivity of Microalgae

Factor	Organism	Conditions	Biomass productivity (μ) (g/[L ·day])	Refs.
Temperature	Chlorella vulgaris	30°C (at elevated carbon dioxide concentration)	0.222	Chinnasamy et al. (2009)
	Chaetoceros calcitrans	30°C	0.270	Adenan et al., (2013)
	Tetraselmis sp.	28°C	—	Ha (2000)
	Scenedesmus almeriensis	35°C	0.730	Sánchez et al. (2008)
	Dunaliella salina	22°C	—	Wu et al. (2016)
	Nannochloropsis salina	26°C	—	Van Wagenen et al. (2012)
Light	Chlorella vulgaris	3,960 lux (with no pH control)	—	Gong et al. (2014)
	Scenedesmus obliquus	11,100 lux	0.863	Sforza et al. (2014)
	Dunaliella salina	3,700 lux	—	Vo and Tran (2014)
	Nannochloropsis salina	18,500 lux	1.300	Van Wagenen et al. (2012)
	Chlamydomonas reinhardtii	14,800 lux	—	Pyo Kim et al. (2006)
	Scenedesmus almeriensis	102,250 lux	0.660	Sánchez et al. (2008)
pH	Chlorella vulgaris	7.5–8.0	—	Rachlin and Grosso (1991)
	Scenedesmus almeriensis	8.0	—	Sánchez et al. (2008)
	Scenedesmus obliquus	8.0	—	Yang et al. (2016)
	Dunaliella salina	9.0	—	Abu-Rezq et al. (2010)
	Nannochloropsis salina	7.5–8.0	—	Boussiba et al. (1987)
Salinity	Chlorella sp.	0 ppt	0.09	Andrulevičiūtė et al. (2011)
	Scenedesmus almeriensis	Fresh water	—	Suyono et al. (2015)
	Scenedesmus obliquus	3 ppt	—	Kaewkannetra et al. (2012)
	Dunaliella salina	88–117 ppt	—	Vo and Tran (2014)
	Nannochloropsis salina	34 ppt	—	Bartley et al. (2013)
Carbon dioxide	Chlorella vulgaris	6%	—	Chinnasamy et al. (2009)
	Scenedesmus obliquus	15%	—	Singh and Singh (2014)
	Dunaliella salina	No significant effect on growth	—	King et al. (2015)
Mixing	Chlorella sp.	Continuous mixing	Increased growth by 30%	Persoone et al. (2000)
	Scenedesmus obliquus	Continuous stirring	—	(Mandal and Mallick (2012)
	Spirulina platensis	Bubble column	0.293	Ravelonandro et al. (2011)

Footnotes

Author Disclosure Statement

No competing financial interests exist.

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