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Enhanced Growth of Microalgae and Production of Lipids via Electrostatically Controlled Photosynthesis
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  • Xuyang Shi
    Xuyang Shi
    Department of Electrical and Computer Engineering, Cleveland State University, Cleveland, Ohio 44115, United States
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    Orcidhttps://orcid.org/0000-0002-9473-8692
  • Anup Sam Mathew
    Anup Sam Mathew
    Department of Electrical and Computer Engineering, Cleveland State University, Cleveland, Ohio 44115, United States
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  • Yan Xu
    Yan Xu
    Department of Chemistry, Cleveland State University, Cleveland, Ohio 44115, United States
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  • Siu-Tung Yau*
    Siu-Tung Yau
    Department of Electrical and Computer Engineering, Cleveland State University, Cleveland, Ohio 44115, United States
    Applied Bioengineering, Cleveland State University, Cleveland, Ohio 44115, United States
    *Email: [email protected]. Phone: (216) 875-9602. Fax: (216) 678-5405.
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    Orcidhttps://orcid.org/0000-0002-6566-4305
  • Gang Xu
    Gang Xu
    Department of Chemistry, Cleveland State University, Cleveland, Ohio 44115, United States
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ACS Sustainable Chemistry & Engineering

Cite this: ACS Sustainable Chem. Eng. 2022, 10, 35, 11459–11465
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https://doi.org/10.1021/acssuschemeng.1c08735
Published August 22, 2022

Copyright © 2022 The Authors. Published by American Chemical Society. This publication is licensed under

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Abstract

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Lipid accumulation in microalgae is a renewable resource for the synthesis of biodiesel. Two microalgae, Spirulina and S. dimorphus, were subjected to the electrostatic conditions imposed by applying a dc voltage to the algal growth mixtures under different light intensities without inducing electrical currents. The electrostatic conditions increased the growth rates of the microalgae well above those due to natural photosynthesis. The enhanced growth was dependent on the magnitude of the applied voltage and the contact area of the algal growth mixture to the electrodes. The voltage also induced the flocculation of the algae on the electrodes. The lipid contents of S. dimorphus were analyzed and found to be increased by the electrostatic effect. The observed enhanced algal growth could be due to accelerated electron transport rates in the cellular processes of photosynthesis. The results presented here indicate that, even with deficient light intensities, the electrostatic method is able to increase the overall production of the microalgae consistently and significantly beyond the algal level caused by natural photosynthesis with the normal light intensity.

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Synopsis

This article demonstrates a simple and economically viable way to produce lipids from microalgae as a renewable resource for the production of biodiesel, which is a biomass for alternative energy.

Introduction

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Microalgae are a viable resource for the production of biodiesel. (1,2) Photosynthesis plays a twofold role in the algae-based production of biodiesel. Photosynthesis is the principal process responsible for the reproduction of algae. Microalgae utilize inorganic carbon (CO2) and organic carbon (glucose and acetate) to produce lipids via photosynthesis. (3) Lipids are used to synthesize biodiesel through transesterification. (4) The growth of algae and plants requires sufficient light intensities. Deficient light intensities reduce the rate of photosynthesis causing the growth to slow down but do not affect the respiration process. The compensation point of metabolism occurs when light intensity is reduced so that the rate of photosynthesis is equal to the rate of respiration. (5) One cause of deficient light intensity is global dimming due to atmospheric pollution. (6)
The process of photosynthesis has been elucidated with detailed mechanisms. (7) It is well known that natural photosynthesis is inherently inefficient with an efficiency of 8–10%. (8) Strategies for enhancing photosynthesis have been formulated. Examples of the strategies are (a) increasing the CO2 level around Rubisco to increase the catalytic rate, (9) (b) increasing the electron transport rate in chloroplast, (10) (c) optimizing the antenna size to maximize photosynthetic efficiency, (11) and (d) increasing photosynthetic carbon assimilation in C3 plants. (12) In this study, we describe enhanced growth of two microalgae, namely, Spirulina and S. dimorphus, as a result of subjecting them to electrostatic conditions. Specifically, we show that the algal growth was significantly enhanced when the microalgae were disposed between two electrodes that were polarized by a dc voltage without inducing currents. Our results show that when full-light (FL), the normal light intensity responsible for natural photosynthesis, was used to perform photosynthesis of the microalgae, the application of the voltage caused a growth rate, which was faster than that solely due to FL. Under the half-light (HL) condition, in which light intensity was reduced by 50% below the FL level, the electrostatic effect significantly enhanced algal growth rates so that the algal concentration approached and exceeded the FL level. The lipid contents of S. dimorphus also showed increases above the FL and HL levels as a result of the electrostatic effect in the similar trend as the algal growth.

Experimental Section

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Electrostatic Growth Reactor

The schematic of the electrostatic growth reactor used to perform the enhanced algal growth is shown in Figure 1. The reactor consisted of a 250 mL glass container, which contained an algae growth mixture and an assembly of a pair of electrodes connected to a circuit. An electrode was formed by winding a piece of insulator-coated copper wire around a glass rod. Two wire-wound glass rods were used as a pair of electrodes. The copper wire was coated with a 1 mm thick layer of polyvinyl chloride to provide electrical insulation. Alternatively, an electrode pair that consisted of a piece of carbon cloth and a piece of the insulator-coated wire assembled on and within a rack of wood sticks were used for large quantity growth. The electrode pair was immersed in the growth mixture. The two electrodes were electrically connected to an external dc power supply Vappl and an ammeter A. Applying a dc voltage to the electrodes did not generate a current in the electrode-mixture system as confirmed by the ammeter, which was set at the micro-ampere scale. The dc voltage only polarized the algal mixture. A 15-W fluorescent lamp was used to irradiate light on the glass container and hence to facilitate photosynthesis in the microalgae. The spectrum of the lamp consists of significant wavelength components between 350 and 700 nm. (13) The light intensity of 3000 lumens measured at the surface of the reactor was referred to as the FL intensity. A lux meter was used to measure light intensity. The algal growth mixture was sparged with air through an air pump. Air sparging created circulation of the mixture and allowed continuous supply of ambient CO2 to avoid carbon dioxide limitation in the mixture.

Figure 1

Figure 1. Electrostatic growth reactor used to perform the enhanced growth of microalgae.

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Spirulina and S. dimorphus growth mixtures were prepared by inoculating microalgae cells from a culture into 200 mL of growth medium contained in the reactor. Experiments were performed at the room temperature. Optical density (OD) measurements at 600 nm (A600) were used to measure algal concentration. For each measurement, 1 mL of the growth mixture was taken from the reactor and was returned to the reactor after the measurement was completed.

Reagents and Materials

Algal growth mixtures were prepared by mixing live algae with a growth broth. Live Spirulina (Arthrospira platensis) was purchased from AlgaeLab (www.algaelab.org). The growth broth for Spirulina with an optimized metal ionic solution was purchased from Algae Lab. Live S. dimorphous was mixed with Bold’s basal medium (PhytoTech Labs; product no: B1650) and Bold Modified Basal Freshwater Nutrient Solution (Sigma Life Sciences; catalog no: B5282). Distilled water (18.2 MΩ-cm) was used in preparation. The pH of the growth mixture was maintained at 10.18 for Spirulina and 6.4 for S. dimorphous.

Chlorophyll Extraction

Chlorophyll was extracted from Spirulina using the hot ethanol extraction technique. Ethanol (75% v/v) was heated to 80 °C. The algal growth mixture was centrifuged at 872 × g for 15 min. The supernatant was discarded. Then, hot ethanol was added to the centrifuge tube containing the wet algal pellet and then vortexed for 10 min to extract chlorophyll. After vortexing, the mixture was transferred to a hot water bath maintained at 80 °C and left in the bath for 2 h. Then, HCl was added to the mixture to acidify it. The acidification lasted for 90 s. Then, OD (A665) on the mixture was performed.

Lipid Extraction

The S. dimorphous growth mixture was centrifuged to form algal pellets, which were resuspended in distilled water and centrifuged again to remove any remaining soluble salts or unwanted substances. The wet pellets were then dried in an oven at 45–50 °C. The dried pellets were then pulverized manually using a mortar and pestle. This method of powdering algae recovers most of the lipids compared to other methods without cell disruption. (14) Lipids were extracted from the powdered algae using the modified Folch method (15) (see below), which has high efficiency toward glycerolipids.
The powdered S. dimorphous was transferred to a borosilicate glass tube. A volume of 600 μL of methanol/chloroform mixture (2:1 v/v) was added to the tube. Then, 30 μL of lipid standard mix (see below), which contained 25 μM of each lipid standard, was added to the tube. The sample underwent a three-step vortex process separately with HCl, chloroform, and deionized water. The vortexed sample was then centrifuged, which led to phase separation. The lower phase, which contained lipids, was transferred to a borosilicate tube. Chloroform (600 μL) was added to the upper phase, which was then vortexed. Then, the vortexed mixture was centrifuged, leading to phase separation. The lower phase was pipetted out and combined with the lower phase of first extraction. The combined total algal extract was then dried using nitrogen. A mixture of chloroform (300 μL), methanol, and ammonium acetate (30:66.5:3.5) was added to the algal extract, which was then vortexed twice and centrifuged at 4500 rpm for 5 min at 10 °C. Then, 200 μL of this mixture was transferred to aminopropyl cartridge tubes for liquid chromatography tandem mass spectrometry (LC–MS/MS) characterization.

LC–MS/MS Detection

The analysis of lipid contents was performed using an ultra-high performance liquid chromatography (UHPLC)–mass spectrometry (MS/MS) system. The UHPLC part (Agilent 1290 infinity UHPLC) was used to separate lipids, and the MS/MS part (Agilent 6540 QTOF mass spectrometer) was used to detect lipids. LC separation was performed on a Waters Acquity BEH C18 column operated in the gradient elution mode. The mass spectrometer was operated in both positive and negative electron spray ionization modes. LC–MS/MS data were acquired by Agilent MassHunter data acquisition software with auto MS/MS acquisition mode.
Six synthetic lipid standards were used for the semiquantitation of lipids. These were (1) 1,2-dipentadecanoyl-sn-glycero-3-phosphoethanolamine or [PE 30:0 (15:0/15:0)] (catalog no: 850704), (2) 1,2-dinonadecanoyl-sn-glycero-3-phosphocholine or [PC 38:0 (19:0/19:0)] (catalog no: 850367), (3) 1-myristoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine or [LPE 14:0 (14:0/0:0)] (catalog no: 856735), (4) 1-tridecanoyl-2-hydroxy-sn-glycero-3-phosphocholine or [LPC 13:0 (13:0/0:0)] (catalog No: 855476), which were purchased from Avanti Polar Lipids, Inc., (5) glyceryl triheptadecanoate or [TAG 51:0 (17:0/17:0/17:0)] (Catalog No: T2151), which was obtained from Sigma Aldrich, and (6) dinonadecanoin or [DAG 38:0 (19:0/19:0)] (catalog No: 26981), which was purchased from Larodan Fine Chemicals AB. The standard stock solutions (1000 μM) of PC 38:0 (19:0/19:0), PE 30:0 (15:0/15:0), LPC 13:0 (13:0/0:0), and LPE 14:0 (14:0/0:0) were prepared in chloroform/methanol (2:1, v/v) mixture and the standard stock solutions of DAG 38:0 (19:0/19:0) and TAG 51:0 (17:0/17:0/17:0) were prepared in chloroform. The standard stock solutions were stored in glass vials at −20 °C until use.
HPLC-grade chloroform (catalog no: A607SK) and methanol (catalog no: A454) were purchased from Fisher Scientific. HPLC-grade ammonium acetate (catalog no: A2149) was purchased from Spectrum Chemical MFG. Corp. HPLC-grade isopropanol (catalog no: 34863) was purchased form Sigma Aldrich.

Results

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Verification of Photosynthesis

We used the microalga Spirulina as a model microalga to demonstrate the electrostatically enhanced algal growth and its characteristics. The growth of Spirulina under atmospheric pressure in a growth mixture illuminated by 3000 lux, which is the light intensity of natural photosynthesis in algae (16) or FL, was monitored by recording the change in the algal concentration during a period of 5 days. Figure 2 shows the FL growth profile of Spirulina obtained using OD measurements. The profile shows an increasing trend in the algal concentration, indicating growth due to photosynthesis. To confirm that photosynthesis occurred in the growth mixture, the chlorophyll content and the pH of the mixture were also monitored over the same period. The amount of chlorophyll and the pH value are shown by vertical columns at each data point of the profile. Figure 2 shows that the increase in the algal concentration is accompanied by an increase in the chlorophyll content and an increase in pH. Chlorophyll is produced during photosynthesis. Because photosynthesis consumes CO2, that is, carbon fixation, dissolved in the growth mixture, (7) the decreasing acidity is an indication that CO2 was being consumed in the mixture. Together, these results qualitatively indicate the functioning of photosynthesis in the algal mixture.

Figure 2

Figure 2. FL growth profile (FL concentration) of Spirulina and changes in chlorophyll and pH. Volume of the algal growth mixture was 200 mL. Growth took place under the FL condition.

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Voltage-Dependent Growth

The electrostatically enhanced growth of microalgae was demonstrated by applying a dc voltage to a Spirulina growth mixture undergoing photosynthesis. Figure 1 shows the electrostatic growth system. A dc voltage Vappl was applied between two insulated electrodes dipped into the growth mixture to polarize the algal mixture. The algal growth was first demonstrated with the HL intensity. This intensity is close to the compensation point of algae. (17) Both the FL growth and the HL growth without applying voltage were used as references to show the effect of the electrostatically induced change in algal growth in the case of deficient light intensity. Figure 3 shows the effect of the applied voltage on the growth of Spirulina. The HL reference profile reflects a slow growth rate. The application of 0.5 V to the algal mixture causes a faster growth rate compared with that of the HL profile. The 1-V profile follows a similar trend as that of the 0.5-V profile albeit at an even faster rate. The 1.3 V profile shows an initial increase in the growth rate, which is similar to that of the previous two profiles. After 24 h, the growth rate slows down so that the algal concentration becomes lower than those indicated by the other two voltage-dependent profiles, and eventually, the concentration falls toward the HL reference. This anomaly is discussed in Discussion.

Figure 3

Figure 3. Voltage-dependent Spirulina growth profiles. Profiles were obtained with four pairs of wire-wound glass-rod electrodes (32 cm2). Each pair of electrodes had an area of 8 cm2 exposed to the growth mixture. Mixture volume was 200 mL. The initial concentration was 0.18 g/L.

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Effect of the Electrode Area

We found that the enhanced growth of Spirulina was also dependent on the surface area of the electrodes exposed to the algal growth mixture, as shown in Figure 4. The HL and FL growth profiles of Figure 3 are plotted in Figure 4 as references. Figure 4 shows that, with the voltage kept at 1V, increasing the electrode contact area to the algal mixture from 8 cm2 (one pair of wire-wound glass-rod electrodes) to 32 cm2 (four pairs of wire-wound glass-rod electrodes; see the red profile in Figure 3.) results in progressively increased algal growth toward the FL profile. The results indicate that the growth can be enhanced if more microalgae cells are included in the region between the two electrodes to be subjected to the polarization in the mixture induced by the voltage. This observation demonstrates the scaling up capability of the electrostatic method. Figure 4 shows that increasing the electrode area to 40 cm2 (5 pairs) slows down the growth below those of the 2,4-pair electrode cases. This unexpected decrease is similar to that observed in Figure 3 with further increasing voltage.

Figure 4

Figure 4. Electrode area dependence of Spirulina growth. Increasing the microalga-electrode contact area from 8 to 32 cm2 while keeping the voltage at 1 V results in progressively increased algal growth from the HL profile toward the FL profile. The growth mixture volume was 200 mL. The initial concentration was 0.20 g/L.

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Effect of Lower Initial Concentration

It is well known that the initial concentration of organisms in a culture determines the growth pattern. Figure 5 shows the voltage-dependent growth profiles of Spirulina with the initial algal concentration reduced from 0.18 g/L, which is the initial concentration used in Figure 3, to 0.105 g/mL. Compared to the high initial-concentration results shown in Figure 3, the low initial-concentration growth profiles shown in Figure 5 appear to be more susceptible to the applied voltage. With 1 V, the HL concentration increases above the FL concentration after the 100th hour. The entire profile is closer to the FL reference than the corresponding high-initial-concentration profile shown in Figure 3. On the contrary, increasing the voltage to 1.3 V makes the algal concentration fall faster below the FL level compared to the corresponding high initial-concentration profile. The 1.3 V profile falls even below the HL level starting at the 72nd hour. This anomaly will be discussed in the Discussion section in terms of algae flocculation.

Figure 5

Figure 5. Dependence of Spirulina growth on voltage with the initial concentration of 0.105 g/mL. Four pairs of electrodes (32 cm2) were used in 200 mL of the growth mixture.

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Voltage-Enhanced Production of Lipids

We have applied the electrostatic method to the growth of S. dimorphus, a microalga that has been found to be a promising feedstock for the production of biodiesel, (18) to demonstrate enhanced production of lipids in microalgae as a result of the enhanced algal growth. Figure 6a shows the growth profiles of S. dimorphus obtained during a period of 6 days under three different conditions: FL, HL, and HL + 1 V. The growth rate reflected in the HL profile is below that indicated by the FL profile. When 1 V is applied to the algal growth mixture under HL, the growth profile shows an upward deviation with an increased slope, indicating a faster rate of growth under the influence of the voltage. The algae concentration reaches the FL concentration at 120 h and 144 h. Figure 6b shows the effect of applying 0.15 V to a growth mixture under FL. The algal concentration shows an upward deviation from the normal FL concentration after the 24th hour. The voltage causes the microalga to enhance its growth as reflected in the increasing slope of the growth profile. At the 100th hour, the concentration is well above that of the normal FL concentration.

Figure 6

Figure 6. S. dimorphus growth profiles. (a) Effect of applying 1 V on HL growth. (b) Effect of applying 0.15 V on FL growth. Results in (a) and (b) were obtained with two separate growth mixtures. The volume of the growth mixture was 200 mL. Carbon-wire electrodes were used.

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We have performed LC–MS/MS on the lipids produced by S. dimorphus in order to show that the electrostatically enhanced algal growth also enhanced the production of lipids. Three classes of lipids, namely, phospholipids, glycolipids, and glycerolipids, are used by industry to produce biodiesel using the transesterification process. The most useful lipid is glycerolipid because it is the most abundant in green microalgae. (19)
The three types of lipids collected in the S. dimorphus produced from the three growth processes shown in Figure 6 are shown in Figure 7. The S. dimorphus growth profile of the lipids is similar to that shown in Figure 6a. The conditions used to produce the lipids are HL, HL + 1 V applied, and FL. The contents of phospholipid, glycolipid, glycerolipid, and the total lipid, which is the sum of the three lipids, are shown in Figure 7 a–d, respectively. Figure 7 shows that the applied voltage generally enhances the lipid content under HL during the 144 hour growth period. The HL lipid contents of S. dimorphus under the electrostatic effect shift toward the FL content. In the case of glycerolipids, the HL content under 1 V becomes greater than the FL content during the entire growth period.

Figure 7

Figure 7. Lipid contents of S. dimorphus. (a) Phospholipid, (b) glycolipid, (c) glycerolipid, and (d) total lipid. Lipid contents were measured under the HL, HL with 1 V, and FL conditions during a six-day growth period. S. dimorphus growth profiles of the results are similar to those shown in Figure 6a. The content of each lipid from the collected S. dimorphus was plotted. Lipid weights were measured relative to internal standards.

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Glycerolipds are divided into three classes: monoacylglycerols (MAG), diacylglycerols (DAG), and triacylglycerols (TAG). We have identified DAG and TAG in our samples. It should be noted that the concentration of MAG in microalgae is very low. Figure 8 shows the voltage-dependent contents of DAG and TAG from the glycerolipid content of S. dimorphus in Figure 7c. Growth patterns of DAG and TAG are consistent with that of glycerolipids shown in Figure 7c.

Figure 8

Figure 8. Contents of (a) DAG and (b) TAG produced by applying 1 V to the S. dimorphus growth mixture as in Figure 7.

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Discussion

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The study on the enhanced algal growth described here is phenomenological in nature. Although the exact mechanism of the observed electrostatic effect has not been elucidated yet, we discuss this effect from different perspectives in order to provide clues for future studies. The results presented in Figures 3–6 show the general features of the electrostatic effect on the growth of Spirulina and S. dimorphus: (1) increasing the electrostatic polarization causes faster growth, and (2) too much polarization due to higher voltages or larger algae-electrode contact area decreases growth.

Electron Transfer

The observed electrostatic effect on algal growth can be attributed to increased rate of photosynthesis in the microalgae. The different metabolic pathways in algal cells all involve redox reactions catalyzed by enzymes. We propose that the voltage polarizes ionic charges in algal cells to induce localized electric fields, which lower the tunnel barrier experienced by transferring electrons. Photosynthesis has a light-dependent part and a respiration part, both of which include electron transfer processes . (5) This effect may speed up cellular electron transfer even in the lag phase to enhance metabolic rates to rapidly energize algal cells. We propose that the polarization created by the applied voltage in the algal cells between the electrodes speeds up the electron transfer processes, leading to enhanced growth rates.

Enhanced Photosynthesis

Figures 3–6 show that, when HL or FL was used to perform photosynthesis of Spirulina, the growth rate could be increased above the normal growth rate in the presence of the electrostatic effect. Although HL, the deficient light intensity, reduced the growth rate below that of FL, the electrostatic polarization might have enhanced electron transport activities in the light-dependent part of photosynthesis, counterbalancing the tendency to slow down the growth. At the same time, the electron transport activities in the light-independent part of photosynthesis were also enhanced, leading to even more enhanced algal growth that have reached or surpassed the FL algae concentration, as shown in Figures 5 and 6.
Interestingly, there are anomalies in the light-dependent growth of algae. Photoinhibition is the reduction of the photosynthesis rate of a plant or algae because of an increase in light intensity, which causes damage to PSII. (20) Also, it was found that, for certain algae, increasing light intensity, although enhances the growth of algae, reduces the lipid content. (21) These algae devote more synthesized energy to their reproduction at the expense of producing less lipids. Therefore, lower light intensities favor the accumulation of lipids in these algae. In these cases, the electrostatic effect demonstrated here could be used to maintain algae growth in the case of photoinhibition or enhance lipid production when the synthesized energy is used for algae reproduction.

Flocculation

Figures 3 and 5 show a seemingly detrimental effect of the applied voltage on algal growth. Initially, when the applied voltage is increased from 0.5 to 1 V, the growth profile shows a progressive increase above the HL reference. Above 1 V, the growth profile shows a decrease with increasing voltage. This observation suggests that the electrostatic effect produced by higher voltages reduces the algal concentration in the mixture. Figure 9 provides a visual explanation of this effect. Figure 9a shows the initial growth mixture of Spirulina with a greenish color, reflecting the high algal concentration of 2 g/L. After applying 15 V for 24 h, the mixture became almost clear, as shown in Figure 9b with a concentration 0.04 g/L. Figure 9c shows that Spirulina was adsorbed on the carbon cloth and wire electrodes, which explains the apparent decrease in the algal concentration in the mixture. The majority of the flocculated algae were found on the carbon cloth electrode, which was connected to the positive terminal of the dc power supply. The green color of the flocculated algae suggested that they were alive. This effect explains the decrease of algal concentration in the growth mixture when the voltage is high enough to bring about significant adsorption of microalgae on electrodes. This effect also suggests a convenient method to harvest algae from solutions.

Figure 9

Figure 9. Voltage-induced algal flocculation on electrodes. (a) Initial Spirulina growth mixture at 2 g/L. (b) Algal mixture after applying 15 V for 24 h. The concentration of the mixture was 0.04 g/L. (c) Spirulina adsorbed on the carbon cloth and wire electrodes. Similar adsorption also occurs on the pair of wire electrodes.

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The effect of increasing the electrode area while keeping voltage unchanged, as described in Figure 4, is also related to the voltage-induced flocculation. As the electrode area is increased from 8 cm2 through 16 to 32 cm2, the growth also increases at progressive higher rates. When the electrode area is increased to 40 cm2, the growth rate drops significantly. This observation suggests that although increasing electrode area allowed more alga cells to be subjected to the electrostatic effect, the voltage also induced flocculation. When the area was increased to 40 cm2, flocculation made more microalga cells adsorb on the electrodes than reproduced in the mixture. The observed flocculation implies that the concentration of the algae either at the FL or the HL level could be increased well above the FL level by increasing the applied voltage in the absence of the flocculation effect.
The cause of flocculation is not clear. Microalgae in cultural media exist in a suspension form due to the negative charges on their cell surface. A simple and efficient method to harvest microalgae is to introduce cationic flocculants to the algae suspension. (22) Microalgae cells, under the electrostatic effect of the flocculant, migrate to the flocculant to form flocs. The flocculation observed in our work could be caused by voltage-induced polarization of the algae suspension causing cells to migrate to the carbon cloth, where they flocculate.

Lipid Production

Figures 7 and 8 show the contents of different lipids produced by applying 1 V to a S. dimorphus growth mixture. The lipids produced under the HL + 1 V condition are greater than that due to HL only, and, in some cases, the lipid due to HL + 1 V is even higher that that due to FL only. This scenario is consistent with that shown in Figure 7a, which shows the algal concentrations due to the HL + 1 V, HL, and FL conditions. However, the actual amount of the lipids due to HL + 1 V should be higher than that shown in Figures 7 and 8. This is because certain amounts of S. dimorphus became adsorbed on the electrodes and was not included in the lipid extraction process.

Conclusions

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In this work, we show that the application of dc voltages to the growth mixtures of Sprulina and S. dimorphus exposed to different light intensities increases the growth rates of the microalgae above those under the condition of natural photosynthesis alone. Because electrical currents are not induced in the growth system, the observed effect on the microalgae is electrostatic in nature. Our results indicate that the enhanced growth is dependent on the magnitude of the electrostatic effect. Increasing the voltage or the contact area between the growth mixture and the electrodes increases the growth rate. However, the growth rates of the algae in the growth mixture starts to decrease with further increased voltages. We show the occurrence of flocculation of the algae on the electrodes caused by the voltage. With higher voltages, the flocculation appears to be significant and depletes the algal content in the mixture, resulting in the observed decrease in growth rates. The lipid contents in S. dimorphus produced by HL + voltage also follow similar patterns as in algal growth in that they are always greater than the HL contents and, in some cases, greater than the FL contents. The results presented here indicate that, even with deficient light intensity, the electrostatic method is able to increase the overall production of the microalgae consistently beyond the level caused by natural photosynthesis with the normal light intensity (FL without voltage) in the absence of flocculation. A possible mechanism of the electrostatic effect could be that the dc voltage induces polarization in algae cells to accelerate electron transport processes of photosynthesis. The electrostatic method presented here could also work on other microorganisms.

Author Information

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  • Corresponding Author
    • Siu-Tung Yau - Department of Electrical and Computer Engineering, Cleveland State University, Cleveland, Ohio 44115, United States;  Applied Bioengineering, Cleveland State University, Cleveland, Ohio 44115, United States;  Orcidhttps://orcid.org/0000-0002-6566-4305;  Email: [email protected]
  • Authors
    • Xuyang Shi - Department of Electrical and Computer Engineering, Cleveland State University, Cleveland, Ohio 44115, United States;  Orcidhttps://orcid.org/0000-0002-9473-8692
    • Anup Sam Mathew - Department of Electrical and Computer Engineering, Cleveland State University, Cleveland, Ohio 44115, United States
    • Yan Xu - Department of Chemistry, Cleveland State University, Cleveland, Ohio 44115, United States
    • Gang Xu - Department of Chemistry, Cleveland State University, Cleveland, Ohio 44115, United States
  • Author Contributions

    X.S. and A.S.M. contributed equally to this work.

  • Notes
    The authors declare no competing financial interest.

Acknowledgments

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We thank Dr. Joanne M. Belovich for providing S. dimorphous. Drs. Xiang Zhou, Ruhan Wei and Aimin Zhou have helped us with LC–MS/MS. Their efforts are deeply appreciated. This work was supported by Cleveland State University.

References

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    Mata, Teresa M.; Martins, Antonio A.; Caetano, Nidia. S.
    Renewable & Sustainable Energy Reviews (2009), 14 (1), 217-232CODEN: RSERFH; ISSN:1364-0321. (Elsevier Ltd.)
    A review. Sustainable prodn. of renewable energy is being hotly debated globally since it is increasingly understood that first generation biofuels, primarily produced from food crops and mostly oil seeds are limited in their ability to achieve targets for biofuel prodn., climate change mitigation and economic growth. These concerns have increased the interest in developing second generation biofuels produced from non-food feedstocks such as microalgae, which potentially offer greatest opportunities in the longer term. This paper reviews the current status of microalgae use for biodiesel prodn., including their cultivation, harvesting, and processing. The microalgae species most used for biodiesel prodn. are presented and their main advantages described in comparison with other available biodiesel feedstocks. The various aspects assocd. with the design of microalgae prodn. units are described, giving an overview of the current state of development of algae cultivation systems (photo-bioreactors and open ponds). Other potential applications and products from microalgae are also presented such as for biol. sequestration of CO2, wastewater treatment, in human health, as food additive, and for aquaculture.
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    Biodiesel production by microalgal biotechnology
    Huang, Guan Hua; Chen, Feng; Wei, Dong; Zhang, Xue Wu; Chen, Gu
    Applied Energy (2009), 87 (1), 38-46CODEN: APENDX; ISSN:0306-2619. (Elsevier Ltd.)
    A review. Biodiesel has received much attention in recent years. Although numerous reports are available on the prodn. of biodiesel from vegetable oils of terraneous oil-plants, such as soybean, sunflower and palm oils, the prodn. of biodiesel from microalgae is a newly emerging field. Microalgal biotechnol. appears to possess high potential for biodiesel prodn. because a significant increase in lipid content of microalgae is now possible through heterotrophic cultivation and genetic engineering approaches. This paper provides an overview of the technologies in the prodn. of biodiesel from microalgae, including the various modes of cultivation for the prodn. of oil-rich microalgal biomass, as well as the subsequent downstream processing for biodiesel prodn. The advances and prospects of using microalgal biotechnol. for biodiesel prodn. are discussed.
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    Renewable & Sustainable Energy Reviews (2009), 13 (6-7), 1646-1651CODEN: RSERFH; ISSN:1364-0321. (Elsevier Ltd.)
    A review. Fuels are inevitable for industrial development and growth of any country. The life span of fossil fuel resources has always been terrifying. Biodiesel, a renewable source of energy seems to be an ideal soln. for global energy demands including India as well. The current review is addressed to various aspects of biodiesel prodn. Latest literature has been critically reviewed and consulted.
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    Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis
    Nelson, Nathan; Junge, Wolfgang
    Annual Review of Biochemistry (2015), 84 (), 659-683CODEN: ARBOAW; ISSN:0066-4154. (Annual Reviews)
    A review. Oxygenic photosynthesis is the principal converter of sunlight into chem. energy on Earth. Cyanobacteria and plants provide the oxygen, food, fuel, fibers, and platform chems. for life on Earth. The conversion of solar energy into chem. energy is catalyzed by two multisubunit membrane protein complexes, photosystem I (PSI) and photosystem II (PSII). Light is absorbed by the pigment cofactors, and excitation energy is transferred among the antennae pigments and converted into chem. energy at very high efficiency. Oxygenic photosynthesis has existed for more than three billion years, during which its mol. machinery was perfected to minimize wasteful reactions. Light excitation transfer and singlet trapping won over fluorescence, radiation-less decay, and triplet formation. Photosynthetic reaction centers operate in organisms ranging from bacteria to higher plants. They are all evolutionarily linked. The crystal structure detn. of photosynthetic protein complexes sheds light on the various partial reactions and explains how they are protected against wasteful pathways and why their function is robust. This review discusses the efficiency of photosynthetic solar energy conversion.
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    Improving photosynthetic efficiency for greater yield
    Zhu, Xin-Guang; Long, Stephen P.; Ort, Donald R.
    Annual Review of Plant Biology (2010), 61 (), 235-261CODEN: ARPBDW; ISSN:1543-5008. (Annual Reviews Inc.)
    A review. Increasing the yield potential of the major food grain crops has contributed very significantly to a rising food supply over the past 50 years, which has until recently more than kept pace with rising global demand. Whereas improved photosynthetic efficiency has played only a minor role in the remarkable increases in productivity achieved in the last half century, further increases in yield potential will rely in large part on improved photosynthesis. Here we examine inefficiencies in photosynthetic energy transduction in crops from light interception to carbohydrate synthesis, and how classical breeding, systems biol., and synthetic biol. are providing new opportunities to develop more productive germplasm. Near-term opportunities include improving the display of leaves in crop canopies to avoid light satn. of individual leaves and further investigation of a photorespiratory bypass that has already improved the productivity of model species. Longer-term opportunities include engineering into plants carboxylases that are better adapted to current and forthcoming CO2 concns., and the use of modeling to guide mol. optimization of resource investment among the components of the photosynthetic app., to maximize carbon gain without increasing crop inputs. Collectively, these changes have the potential to more than double the yield potential of our major crops.
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    Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm
    Zhu, Xin-Guang; de Sturler, Eric; Long, Stephen P.
    Plant Physiology (2007), 145 (2), 513-526CODEN: PLPHAY; ISSN:0032-0889. (American Society of Plant Biologists)
    The distribution of resources between enzymes of photosynthetic carbon metab. might be assumed to have been optimized by natural selection. However, natural selection for survival and fecundity does not necessarily select for maximal photosynthetic productivity. Further, the concn. of a key substrate, atm. CO2, has changed more over the past 100 years than the past 25 million years, with the likelihood that natural selection has had inadequate time to reoptimize resource partitioning for this change. Could photosynthetic rate be increased by altered partitioning of resources among the enzymes of carbon metab. This question is addressed using an "evolutionary" algorithm to progressively search for multiple alterations in partitioning that increase photosynthetic rate. To do this, we extended existing metabolic models of C3 photosynthesis by including the photorespiratory pathway (PCOP) and metab. to starch and sucrose to develop a complete dynamic model of photosynthetic carbon metab. The model consists of linked differential equations, each representing the change of concn. of one metabolite. Initial concns. of metabolites and maximal activities of enzymes were extd. from the literature. The dynamics of CO2 fixation and metabolite concns. were realistically simulated by numerical integration, such that the model could mimic well-established physiol. phenomena. For example, a realistic steady-state rate of CO2 uptake was attained and then reattained after perturbing O2 concn. Using an evolutionary algorithm, partitioning of a fixed total amt. of protein-nitrogen between enzymes was allowed to vary. The individual with the higher light-satd. photosynthetic rate was selected and used to seed the next generation. After 1,500 generations, photosynthesis was increased substantially. This suggests that the "typical" partitioning in C3 leaves might be suboptimal for maximizing the light-satd. rate of photosynthesis. An overinvestment in PCOP enzymes and under-investment in Rubisco, sedoheptulose-1,7-bisphosphatase, and fructose-1,6-bisphosphate aldolase were indicated. Increase in sink capacity, such as increase in ADP-glucose pyrophosphorylase, was also indicated to lead to increased CO2 uptake rate. These results suggest that manipulation of partitioning could greatly increase carbon gain without any increase in the total protein-nitrogen investment in the app. for photosynthetic carbon metab.
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    Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement
    Blankenship, Robert E.; Tiede, David M.; Barber, James; Brudvig, Gary W.; Fleming, Graham; Ghirardi, Maria; Gunner, M. R.; Junge, Wolfgang; Kramer, David M.; Melis, Anastasios; Moore, Thomas A.; Moser, Christopher C.; Nocera, Daniel G.; Nozik, Arthur J.; Ort, Donald R.; Parson, William W.; Prince, Roger C.; Sayre, Richard T.
    Science (Washington, DC, United States) (2011), 332 (6031), 805-809CODEN: SCIEAS; ISSN:0036-8075. (American Association for the Advancement of Science)
    A review. Comparing photosynthetic and photovoltaic efficiencies is not a simple issue. Although both processes harvest the energy in sunlight, they operate in distinctly different ways and produce different types of products: biomass or chem. fuels in the case of natural photosynthesis and non-stored elec. current in the case of photovoltaics. To find common ground for evaluating energy-conversion efficiency, the authors compare natural photosynthesis with present technologies for photovoltaic-driven electrolysis of water to produce hydrogen. Photovoltaic-driven electrolysis is the more efficient process when measured on an annual basis, yet short-term yields for photosynthetic conversion under optimal conditions come within a factor of 2 or 3 of the photovoltaic benchmark. Opportunities in which the frontiers of synthetic biol. might be used to enhance natural photosynthesis for improved solar energy conversion efficiency are considered.
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    Optimizing antenna size to maximize photosynthetic efficiency
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    Plant Physiology (2011), 155 (1), 79-85CODEN: PLPHAY; ISSN:0032-0889. (American Society of Plant Biologists)
    A review.
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    Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: Current and future strategies
    Raines, Christine A.
    Plant Physiology (2011), 155 (1), 36-42CODEN: PLPHAY; ISSN:0032-0889. (American Society of Plant Biologists)
    A review.
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    Elvidge Christopher D; Keith David M; Tuttle Benjamin T; Baugh Kimberly E
    Sensors (Basel, Switzerland) (2010), 10 (4), 3961-88 ISSN:.
    We investigated the optimal spectral bands for the identification of lighting types and the estimation of four major indices used to measure the efficiency or character of lighting. To accomplish these objectives we collected high-resolution emission spectra (350 to 2,500 nm) for forty-three different lamps, encompassing nine of the major types of lamps used worldwide. The narrow band emission spectra were used to simulate radiances in eight spectral bands including the human eye photoreceptor bands (photopic, scotopic, and "meltopic") plus five spectral bands in the visible and near-infrared modeled on bands flown on the Landsat Thematic Mapper (TM). The high-resolution continuous spectra are superior to the broad band combinations for the identification of lighting type and are the standard for calculation of Luminous Efficacy of Radiation (LER), Correlated Color Temperature (CCT) and Color Rendering Index (CRI). Given the high cost that would be associated with building and flying a hyperspectral sensor with detection limits low enough to observe nighttime lights we conclude that it would be more feasible to fly an instrument with a limited number of broad spectral bands in the visible to near infrared. The best set of broad spectral bands among those tested is blue, green, red and NIR bands modeled on the band set flown on the Landsat Thematic Mapper. This set provides low errors on the identification of lighting types and reasonable estimates of LER and CCT when compared to the other broad band set tested. None of the broad band sets tested could make reasonable estimates of Luminous Efficacy (LE) or CRI. The photopic band proved useful for the estimation of LER. However, the three photoreceptor bands performed poorly in the identification of lighting types when compared to the bands modeled on the Landsat Thematic Mapper. Our conclusion is that it is feasible to identify lighting type and make reasonable estimates of LER and CCT using four or more spectral bands with minimal spectral overlap spanning the 0.4 to 1.0 um region.
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    Sostaric Maja; Klinar Dusan; Bricelj Mihael; Golob Janvit; Berovic Marin; Likozar Blaz
    New biotechnology (2012), 29 (3), 325-31 ISSN:.
    The microalga Chlorella vulgaris was cultured in a combined medium obtained by mixing standard Jaworski medium with a solution from the modified Solvay process that contained only NaHCO(3) and NH(4)Cl. Cell number, pH and nitrogen content were monitored throughout growth. Lipids were extracted from lyophilised biomass using CHCl(3)-MeOH. A combination of grinding, microwave treatment and sonication proved to give the best lipid extract yield. Freeze-dried algal biomass was also utilised for thermal degradation studies. The degradation exhibited three distinct regions - primary cell structure breakage paralleled by evaporation of water, followed by two predominant exothermic degradation processes. The latter were modelled using nth order apparent kinetics. The activation energies of the degradation processes were determined to be 120-126kJ/mol and 122-132kJ/mol, respectively. The degradation model may be readily applied to an assortment of thermal algal processes, especially those relating to renewable energy.
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    Journal of Biological Chemistry (1957), 226 (), 497-509CODEN: JBCHA3; ISSN:0021-9258.
    cf. C.A. 46, 159i. A simple method is described for the prepn. of total pure lipide exts. from various tissues: it consists of homogenizing the tissue with a 2:1 CHCl3-MeOH mixt. and washing the ext. by addn. of 0.2 its vol. of water or an appropriate salt soln. The resulting mixt. seps. into 2 phases; the lower phase is the total pure lipide ext. The washing removes essentially all the nonlipide contaminants from the ext. with a concomitant loss of about 0.3% of the tissue lipides in the case of white matter and about 0.6% in the case of gray matter. Even these small losses can be reduced by the addn. of a definite amt. of certain mineral salts. The efficiency of the washing depends upon the presence of mineral salts in the crude ext. These salts alter the distribution of the lipides and practically eliminate them from the upper phase. In the absence of salts, substantial amts. of acidic lipides are present in the upper phase and would be lost during the washing. The advantages and limitations of the procedure were established for brain gray and white matter, liver, and muscle.
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    Gour, Rakesh Singh; Chawla, Aseem; Singh, Harvinder; Chauhan, Rajinder Singh; Kant, Anil
    PLoS One (2016), 11 (5), e0155321/1-e0155321/16CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
    In current study isolates of two native microalgae species were screened on the basis of growth kinetics and lipid accumulation potential. On the basis of data obtained on growth parameters and lipid accumulation, it is concluded that Scenedesmus dimorphus has better potential as biofuel feedstock. Two of the isolates of Scenedesmus dimorphus performed better than other isolates with respect to important growth parameters with lipid content of ∼30% of dry biomass. Scenedesmus dimorphus was found to be more suitable as biodiesel feedstock candidate on the basis of cumulative occurrence of five important biodiesel fatty acids, relative occurrence of SFA (53.04%), MUFA (23.81%) and PUFA (19.69%), and more importantly that of oleic acid in its total lipids. The morphol. observations using light and Scanning Electron Microscope and mol. characterization using amplified 18S rRNA gene sequences of microalgae species under study were also performed. Amplified 18S rRNA gene fragments of the microalgae species were sequenced, annotated at the NCBI website and phylogenetic anal. was done. We have published eight 18S rRNA gene sequences of microalgae species in NCBI GenBank.
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    Degraeve-Guilbault, C. Glycerolipid Characterization and Nutrient Deprivation-Associated Changes in the Green PicoalgaOstreococcus tauri. Plant Physiol. 2017, 173, 2060– 2080,  DOI: 10.1104/pp.16.01467
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    Glycerolipid characterization and nutrient deprivation-associated changes in the green picoalga Ostreococcus tauri
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    Plant Physiology (2017), 173 (4), 2060-2080CODEN: PLPHAY; ISSN:1532-2548. (American Society of Plant Biologists)
    The picoalga Ostreococcus tauri is a minimal photosynthetic eukaryote that has been used as a model system. O. tauri is known to efficiently produce docosahexaenoic acid (DHA). We provide a comprehensive study of the glycerolipidome of O. tauri and validate this species as model for related picoeukaryotes. O. tauri lipids displayed unique features that combined traits from the green and the chromalveolate lineages. The betaine lipid diacylglyceryl-hydroxymethyl-trimethyl-β-alanine and phosphatidyldimethylpropanethiol, both hallmarks of chromalveolates, were identified as presumed extraplastidial lipids. DHA was confined to these lipids, while plastidial lipids of prokaryotic type were characterized by the overwhelming presence of ω-3 C18 polyunsatd. fatty acids (FAs), 18:5 being restricted to galactolipids. C16:4, an FA typical of green microalgae galactolipids, also was a major component of O. tauri extraplastidial lipids, while the 16:4-CoA (CoA) species was not detected. Triacylglycerols (TAGs) displayed the complete panel of FAs, and many species exhibited combinations of FAs diagnostic for plastidial and extraplastidial lipids. Importantly, under nutrient deprivation, 16:4 and ω-3 C18 polyunsatd. FAs accumulated into de novo synthesized TAGs while DHA-TAG species remained rather stable, indicating an increased contribution of FAs of plastidial origin to TAG synthesis. Nutrient deprivation further severely down-regulated the conversion of 18:3 to 18:4, resulting in obvious inversion of the 18:3/18:4 ratio in plastidial lipids, TAGs, as well as acyl-CoAs. The fine-tuned and dynamic regulation of the 18:3/18:4 ratio suggested an important physiol. role of these FAs in photosynthetic membranes. Acyl position in structural and storage lipids together with acyl-CoA anal. further help to det. mechanisms possibly involved in glycerolipid synthesis.
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Cite this: ACS Sustainable Chem. Eng. 2022, 10, 35, 11459–11465
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  • Abstract

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    Figure 1

    Figure 1. Electrostatic growth reactor used to perform the enhanced growth of microalgae.

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    Figure 2

    Figure 2. FL growth profile (FL concentration) of Spirulina and changes in chlorophyll and pH. Volume of the algal growth mixture was 200 mL. Growth took place under the FL condition.

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    Figure 3

    Figure 3. Voltage-dependent Spirulina growth profiles. Profiles were obtained with four pairs of wire-wound glass-rod electrodes (32 cm2). Each pair of electrodes had an area of 8 cm2 exposed to the growth mixture. Mixture volume was 200 mL. The initial concentration was 0.18 g/L.

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    Figure 4

    Figure 4. Electrode area dependence of Spirulina growth. Increasing the microalga-electrode contact area from 8 to 32 cm2 while keeping the voltage at 1 V results in progressively increased algal growth from the HL profile toward the FL profile. The growth mixture volume was 200 mL. The initial concentration was 0.20 g/L.

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    Figure 5

    Figure 5. Dependence of Spirulina growth on voltage with the initial concentration of 0.105 g/mL. Four pairs of electrodes (32 cm2) were used in 200 mL of the growth mixture.

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    Figure 6

    Figure 6. S. dimorphus growth profiles. (a) Effect of applying 1 V on HL growth. (b) Effect of applying 0.15 V on FL growth. Results in (a) and (b) were obtained with two separate growth mixtures. The volume of the growth mixture was 200 mL. Carbon-wire electrodes were used.

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    Figure 7

    Figure 7. Lipid contents of S. dimorphus. (a) Phospholipid, (b) glycolipid, (c) glycerolipid, and (d) total lipid. Lipid contents were measured under the HL, HL with 1 V, and FL conditions during a six-day growth period. S. dimorphus growth profiles of the results are similar to those shown in Figure 6a. The content of each lipid from the collected S. dimorphus was plotted. Lipid weights were measured relative to internal standards.

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    Figure 8

    Figure 8. Contents of (a) DAG and (b) TAG produced by applying 1 V to the S. dimorphus growth mixture as in Figure 7.

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    Figure 9

    Figure 9. Voltage-induced algal flocculation on electrodes. (a) Initial Spirulina growth mixture at 2 g/L. (b) Algal mixture after applying 15 V for 24 h. The concentration of the mixture was 0.04 g/L. (c) Spirulina adsorbed on the carbon cloth and wire electrodes. Similar adsorption also occurs on the pair of wire electrodes.

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      https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2MXhsVyrt73O&md5=3256ead9adb71ed755c5242876397afc
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      >> More from SciFinder ®
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      We investigated the optimal spectral bands for the identification of lighting types and the estimation of four major indices used to measure the efficiency or character of lighting. To accomplish these objectives we collected high-resolution emission spectra (350 to 2,500 nm) for forty-three different lamps, encompassing nine of the major types of lamps used worldwide. The narrow band emission spectra were used to simulate radiances in eight spectral bands including the human eye photoreceptor bands (photopic, scotopic, and "meltopic") plus five spectral bands in the visible and near-infrared modeled on bands flown on the Landsat Thematic Mapper (TM). The high-resolution continuous spectra are superior to the broad band combinations for the identification of lighting type and are the standard for calculation of Luminous Efficacy of Radiation (LER), Correlated Color Temperature (CCT) and Color Rendering Index (CRI). Given the high cost that would be associated with building and flying a hyperspectral sensor with detection limits low enough to observe nighttime lights we conclude that it would be more feasible to fly an instrument with a limited number of broad spectral bands in the visible to near infrared. The best set of broad spectral bands among those tested is blue, green, red and NIR bands modeled on the band set flown on the Landsat Thematic Mapper. This set provides low errors on the identification of lighting types and reasonable estimates of LER and CCT when compared to the other broad band set tested. None of the broad band sets tested could make reasonable estimates of Luminous Efficacy (LE) or CRI. The photopic band proved useful for the estimation of LER. However, the three photoreceptor bands performed poorly in the identification of lighting types when compared to the bands modeled on the Landsat Thematic Mapper. Our conclusion is that it is feasible to identify lighting type and make reasonable estimates of LER and CCT using four or more spectral bands with minimal spectral overlap spanning the 0.4 to 1.0 um region.
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      Characterization and screening of native Scenedesmus sp. isolates suitable for biofuel feedstock
      Gour, Rakesh Singh; Chawla, Aseem; Singh, Harvinder; Chauhan, Rajinder Singh; Kant, Anil
      PLoS One (2016), 11 (5), e0155321/1-e0155321/16CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
      In current study isolates of two native microalgae species were screened on the basis of growth kinetics and lipid accumulation potential. On the basis of data obtained on growth parameters and lipid accumulation, it is concluded that Scenedesmus dimorphus has better potential as biofuel feedstock. Two of the isolates of Scenedesmus dimorphus performed better than other isolates with respect to important growth parameters with lipid content of ∼30% of dry biomass. Scenedesmus dimorphus was found to be more suitable as biodiesel feedstock candidate on the basis of cumulative occurrence of five important biodiesel fatty acids, relative occurrence of SFA (53.04%), MUFA (23.81%) and PUFA (19.69%), and more importantly that of oleic acid in its total lipids. The morphol. observations using light and Scanning Electron Microscope and mol. characterization using amplified 18S rRNA gene sequences of microalgae species under study were also performed. Amplified 18S rRNA gene fragments of the microalgae species were sequenced, annotated at the NCBI website and phylogenetic anal. was done. We have published eight 18S rRNA gene sequences of microalgae species in NCBI GenBank.
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    19. 19
      Degraeve-Guilbault, C. Glycerolipid Characterization and Nutrient Deprivation-Associated Changes in the Green PicoalgaOstreococcus tauri. Plant Physiol. 2017, 173, 2060– 2080,  DOI: 10.1104/pp.16.01467
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      Glycerolipid characterization and nutrient deprivation-associated changes in the green picoalga Ostreococcus tauri
      Degraeve-Guilbault, Charlotte; Brehelin, Claire; Haslam, Richard; Sayanova, Olga; Marie-Luce, Glawdys; Jouhet, Juliette; Corellou, Florence
      Plant Physiology (2017), 173 (4), 2060-2080CODEN: PLPHAY; ISSN:1532-2548. (American Society of Plant Biologists)
      The picoalga Ostreococcus tauri is a minimal photosynthetic eukaryote that has been used as a model system. O. tauri is known to efficiently produce docosahexaenoic acid (DHA). We provide a comprehensive study of the glycerolipidome of O. tauri and validate this species as model for related picoeukaryotes. O. tauri lipids displayed unique features that combined traits from the green and the chromalveolate lineages. The betaine lipid diacylglyceryl-hydroxymethyl-trimethyl-β-alanine and phosphatidyldimethylpropanethiol, both hallmarks of chromalveolates, were identified as presumed extraplastidial lipids. DHA was confined to these lipids, while plastidial lipids of prokaryotic type were characterized by the overwhelming presence of ω-3 C18 polyunsatd. fatty acids (FAs), 18:5 being restricted to galactolipids. C16:4, an FA typical of green microalgae galactolipids, also was a major component of O. tauri extraplastidial lipids, while the 16:4-CoA (CoA) species was not detected. Triacylglycerols (TAGs) displayed the complete panel of FAs, and many species exhibited combinations of FAs diagnostic for plastidial and extraplastidial lipids. Importantly, under nutrient deprivation, 16:4 and ω-3 C18 polyunsatd. FAs accumulated into de novo synthesized TAGs while DHA-TAG species remained rather stable, indicating an increased contribution of FAs of plastidial origin to TAG synthesis. Nutrient deprivation further severely down-regulated the conversion of 18:3 to 18:4, resulting in obvious inversion of the 18:3/18:4 ratio in plastidial lipids, TAGs, as well as acyl-CoAs. The fine-tuned and dynamic regulation of the 18:3/18:4 ratio suggested an important physiol. role of these FAs in photosynthetic membranes. Acyl position in structural and storage lipids together with acyl-CoA anal. further help to det. mechanisms possibly involved in glycerolipid synthesis.
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    20. 20
      Long, S. P.; Humphries, S.; Falkowski, P. G. Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1994, 45, 633– 662,  DOI: 10.1146/annurev.pp.45.060194.003221
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      Photoinhibition of photosynthesis in nature
      Long, S. P.; Humphries, S.; Falkowski, P. G.
      Annual Review of Plant Physiology and Plant Molecular Biology (1994), 45 (), 633-62CODEN: ARPBEX; ISSN:1040-2519.
      A review with 142 refs., discussing photosystem II inactivation, avoidance of PS II damage, photoinhibition in the filed and open ocean, terrestrial vegetation, phytoplankton, significance to prodn., and photoinhibition and plant distributions.
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    21. 21
      Cheirsilp, B.; Torpee, S. Enhanced growth and lipid production of microalgae under mixotrophic culture condition: Effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour. Technol. 2012, 110, 510– 516,  DOI: 10.1016/j.biortech.2012.01.125
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      Enhanced growth and lipid production of microalgae under mixotrophic culture condition: Effect of light intensity, glucose concentration and fed-batch cultivation
      Cheirsilp, Benjamas; Torpee, Salwa
      Bioresource Technology (2012), 110 (), 510-516CODEN: BIRTEB; ISSN:0960-8524. (Elsevier Ltd.)
      Microalgae capable of accumulating high lipid content were screened in photoautotrophic, heterotrophic and mixotrophic cultures. The biomass and lipid prodn. of all tested strains in mixotrophic culture were notably enhanced in comparison with photoautotrophic and heterotrophic cultures. Among the tested strains, marine Chlorella sp. and Nannochloropsis sp. were ideal candidates for biodiesel prodn. because of their high lipid prodn. The influence of light intensity and initial glucose concn. on growth and lipid content of both strains were investigated. Although increasing light intensity and initial glucose concn. enhanced the growth of both strains, it reduced their lipid content. To produce a high amt. of biomass with high lipid content, a fed-batch cultivation with stepwise increasing light intensity was performed. The lipid prodn. by this strategy was approx. twice that of conventional batch cultivation. The main fatty acid compns. of the two microalgae were C16-C18 (>80%) which are appropriate for biodiesel prodn.
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    22. 22
      Pugazhendhi, A. A review on chemical mechanism of microalgae flocculation via polymers. Biotechnol. Rep. 2018, 20, e00302  DOI: 10.1016/j.btre.2018.e00302
      There is no corresponding record for this reference.