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Article

Biomass Fatty Acid Profile and Fuel Property Prediction of Bagasse Waste Grown Nannochloropsis oculata

by
Abo El-Khair B. El-Sayed
1,
Nashwa A. Fetyan
2,
Farahat S. Moghanm
3,
Mohssen Elbagory
4,5,
Fatma M. Ibrahim
6,
Mahmoud W. Sadik
7,8 and
Mohamed S. Shokr
9,*
1
Algal Biotechnology Unit, National Research Centre, Cairo 12622, Egypt
2
Soils, Water and Environment Research Institute, Agricultural Research Center, Giza 12619, Egypt
3
Soil and Water Department, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt
4
Department of Biology, Faculty of Science and Arts, King Khalid University, Abha 61321, Saudi Arabia
5
Department of Microbiology, Soils, Water and Environment Research Institute, Agricultural Research Center, Giza 12112, Egypt
6
Student Academy of Scientific Research & Technology, Cairo 4262104, Egypt
7
Department of Microbiology, Faculty of Agriculture, Cairo University, Giza 12613, Egypt
8
Department of Environmental Biotechnology, College of Biotechnology, Misr University for Science and Technology, Giza 3236101, Egypt
9
Soil and Water Department, Faculty of Agriculture, Tanta University, Tanta 31527, Egypt
*
Author to whom correspondence should be addressed.
Agriculture 2022, 12(8), 1201; https://doi.org/10.3390/agriculture12081201
Submission received: 18 June 2022 / Revised: 28 July 2022 / Accepted: 5 August 2022 / Published: 11 August 2022
(This article belongs to the Special Issue Utilization of Biomass Energy in Agriculture: Technology, Challenges and Opportunities)
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Abstract

:
The Chrythophyta alga Nannochloropsis oculata was mixotrophically grown in artificial media enriched with acid-prehydrolyzed bagasse waste as a source of organic carbon. The used growth medium was composed of F2 nutrients, sea salt (22.0 g L−1), and bagasse extract dissolved in sterile tap water. All of the determined growth parameters resulted in their maximums, as the alga was fed with 25% F2 growth medium enriched with 10% bagasse extract, while bagasse-extract-free medium engaged the total chlorophyll and carotenes at the expense of dry weight accumulation during the vegetative growth period. On the contrary, the dry weight under induction growth slightly differed among the different employed treatments; however, all the treatments surpassed the control one, and variation was obviously found in the cases of chlorophyll and carotene. A slight increase in oil content (6.19–11.89%) was observed, as the vegetative cells were grown under induction conditions. The fatty acids ranged between C16 and C20, and the proportions of SFA and MUFA increased from a sum of 63.57% to 88.31%, while the PUFA, including linoleic acid, α-linolenic acid, and arachidonic acid, declined from 36.3 to 11.69%. Concerning the fuel properties, the induction-produced oil surpassed the vegetative one.

1. Introduction

The increasing demand for energy and global warming are two major challenges facing modern society. Dependence on fossil fuels for meeting increasing energy demands is unsustainable due to increasing levels of consumption and the scarcity in discovery of new sources for these non-renewables. Microalgae are an extremely heterogeneous group of microorganisms that are potentially rich sources of important chemicals with potential applications in the feed, food, nutrition, cosmetic, pharmaceutical, and even fuel industries [1,2]. Most algae are capable of producing energy-rich oils, and many microalgae species have been isolated that naturally accumulate high oil levels [3]. Additionally, microalgae biofuels have the potential to become a renewable, cost-effective alternative for fossil fuels with reduced impact on the environment [4]. Algae hold tremendous potential to provide a nonfood, high-yield, nonarable land use source for renewable fuels, such as biodiesel, bioethanol, hydrogen, etc. [5]. They also represent an environmentally friendly alternative option for biological carbon capture and storage (CCS) technology. With high losing rates and the rise in carbon dioxide costs, the use of organic carbon seems to be more beneficial. A lot of organic sources for algae production have successfully been used, even for mass production purposes, including citrate, corn, okra, whey, potato peels, canola, cassava, olives, etc. Thus, a series of agricultural and food industrial wastes have already been used in algal mass production, mainly as unconventional carbon sources, including corn steam liquor [6,7], citrate waste [8,9], and okra [10,11]. Increasing the oil-yielding capacity of microalgae is one of the keys to reducing the production cost of microalgae biodiesel. There has been progress in increasing the lipid biosynthesis capability of microalgae through high biomass cultivation, metabolic engineering, and genetic engineering [12,13,14]. Unfortunately, some recent lifecycle assessment studies on microalgae biofuels have shown that the energy requirement for microalgal biodiesel is fairly high during the cultivation and refinery stages. In addition, the costs for carbon sources, nutrients (such as nitrogen or phosphorous), and the water supply for cell growth can contribute up to 80% of the total medium costs [15], indicating that further renovations are necessary for microalgal biodiesel production to enhance the sustainability in terms of energy balance and chemical consumption [16]. The accumulation of lipids increases when microalgal cells grow under high salinity because they change from active cell division to the storage of energy as an adaptation to the stress environment [17]. At the cellular level, microalgae exposed to a saline environment undergo a survival response that includes the restoration of turgor pressure, the accumulation of osmoprotective molecules (glycerol), and the induction of stress-related proteins. This stress then leads to increased production of lipids, an energy-rich substance that allows survival under extreme environmental conditions [18,19]. On the other hand, the response to salinity stress differs among species, and the growth of some species at high salt concentrations lowers the efficiency of photosynthesis and decreases biomass accumulation [20]. The average lipid content of algal cells varies between 1% and 70% but can reach 90% of the dry weight under certain conditions [21]. In spite of the oil content, the initial fatty acids markedly affect the produced fuel, as an indicator for biodiesel quality [22].
This work is carried out to improve the economic feasibility and environmental sustainability of microalgal biodiesel production. A nontoxic, copious agricultural waste, sugarcane bagasse aqueous extract (SBAE), is used for cultivating Nannochloropsis oculata microalga as a potential source of substitute for traditional nutrition to reduce the cost in cultivation. Secondly, we investigate the effects of malty stress factors, organic carbon (10% sugarcane bagasse aqueous extract), nitrogen starvation, and salinity stress on maximizing the production of biodiesel from the microalga Nannochloropsis oculate.

2. Materials and Methods

Marine microalga Nannochloropsis oculata belonging to Chrythophyta was obtained from the Algal Biotechnology Unit, National Research Center. Cultures were grown under conditions of F2 medium containing the following composition (g L−1): 0.075 NaNO3, 0.005 NaH2PO4 H2O, and 0.030 Na2SiO3.9H2O. Sea water was artificially formulated from 22.0 g L−1 of sea salt dissolved in presterilized tap water. Mixotrophic carbon nutrition was performed based on the examined volume of bagasse extract. Light intensity was adjusted to 120 µE m−2 s−1 from one side of a white light bank, and aeration was performed with free-oil-compressed air.

2.1. Preparation of Sugarcane Bagasse Aqueous Extract (SBAE)

Sugarcane bagasse was locally collected from the Giza Governorate, Egypt. The bagasse was dried at 105 °C for 24 h in a hot-air oven and homogenized using a blender. Dried bagasse was then subjected to acid hydrolysis at 30 °C for 24 h with 1.0 N HNO3, and suspended solids were removed using a sieve (0.2 mm); then, the sugarcane bagasse filtrate was vacuum-filtered using a 0.45 μm membrane filter. The chemical composition of the sugarcane bagasse aqueous extract (SBAE) is shown in Table 1.

2.2. Experimental Design

The trials were carried out in two steps. In the first step, the superior bagasse extract concentration (10%) was used as previously tested by [23] with different concentrations of F2 growth medium (0.0, 25, 50, 75, and 100 percent of the full medium). The second experiment was set up to see the effects of the combined stress factors of nitrogen starvation (0.0–100% F2) and salinity stress (2.0% NaCl). A control experiment was conducted using F2 medium only.
The growth period was 15 days in combination with 10% bagasse extract (the most effective one), as described by [23]. Scaling up was performed with a vertical tubular photobioreactor (15 tubes × 14 L volume) (Figure 1).

2.3. Microalgal Growth Rate and Analysis

The investigated parameters were dry weight, total chlorophyll, and total carotene. For dry weight, the OD of the microalgal suspension was measured at 680 nm using a spectrophotometer. The total chlorophyll was extracted with dimethyl sulfoxide (DMSO) [24]. The chlorophyll absorbance was measured at 666 nm. To recover carotenes, saponification was performed with 5% KOH/30% MeOH, and the residual was re-extracted with DMSO after the addition of 5 drops of concentrated acetic acid [25]. Carotene absorbance was measured at 468 nm [26].

2.4. Lipid Extraction and Fatty Acid Analysis

By the end of the induction period, as the dense culture was obtained, aeration was interrupted to allow gravity sedimentation. The upper clear solution was discarded, and the remainder slurry was then concentrated using centrifugation at 4000 rpm to contain about 70% moisture. The de-watered biomass was then refrigerated at 5 °C to allow cell wall cracking. One day later, the obtained biomass was dried in a 45 °C circulated oven, finely ground, and then subjected to oil extraction. Fine algal powder was filled into 100 g cellulose extraction thimbles (4 × 123 mm) and soaked overnight with solvent mixture of 3:2 (v/v) n-hexane:isopropanol in dim light at room temperature (25 °C). Thimbles were picked up and put into a Soxhelt Jacket, covered with an ex-soaking mixture, and then subjected to extraction for 24 h. The oil fraction was then separated using a rotary evaporator. The solvents were evaporated, and the oil content was then calculated. The identification and determination of the fatty acids were carried out using gas chromatography (GC).

2.5. Prediction of Biodiesel Properties

To predict the properties of microalgal biodiesel, physical properties such as the saponification value (SV; mg KOH), iodine value (IV; gI2/100 g), cetane number (CN), degree of unsaturation (DU; % wt), long-chain saturation factor (LCSF; % wt), cold filter plugging point (CFPP; °C), and high heating value (HHV; MJ/kg) were estimated according to the following empirical formulas [27]:
SV = Σ(560 ∗ Fi)/MWi
IV = Σ(254 ∗ Fi ∗ D)/MWi; CN = (46.3 + 5458/SV) − (0.225 ∗ IV);
HHV = 49.43 − (0.041 ∗ S.N) − (0.015 ∗ IV); DU = (MUFA%) + 2 ∗ (PUFA%)
and LCSF = (0.1 ∗ C16) + (0.5 ∗ C18) + (1 ∗ C20) + (1.5 ∗ C22) + (2 ∗ C24)
CFPP = (3.1417 ∗ LCSF) − 16.477.

2.6. Statistical Analysis

The statistical analysis was conducted with an ANOVA test using Microsoft Excel. The difference in values was indicated in the form of probability (p < 0.05) values.

3. Results

3.1. Effect of SBAE on N. oculata Growth under N Deficiency

The early growth of Nannochloropsis oculata was examined under a wide range of bagasse concentrations that, in turn, defined the proper concentration to be used [23]. It was concluded that full F2 growth medium enriched with 10% bagasse extract of the growth volume resulted in the maximum growth dry weight, while the excess of bagasse extract had no inhibitory effect. When the superior bagasse concentration (10%) was used corresponding to different concentrations of F2 growth medium, the growth parameters possessed a linear increase due to the decrease in the growth medium concentration used (Figure 2). For dry weight accumulation, the maximum was 1.36 g L−1 when F2 medium was used at 75% percent of the full growth medium (Figure 2a). Most of the used concentrations were found to give a markedly enhancing effect. Thus, reducing the initial nutrient concentration saved the proper growth as a result of the bagasse enriching the algal growth medium. Chlorophyll accumulation (Figure 2b) exposed the same pattern, but free F2 growth medium (0.427%) followed the 75%-free F2 medium (0.419%) and all of the others (Figure 2).
We concluded that using organic carbon as an essential additive to the algal growth medium could solve the issue by providing essential carbon and providing a buffering effect, resulting in the stimulation of growth and lipid accumulation. It could be mentioned here that N. oculata grown in F2 medium required lower quantities of nutrients, mainly nitrogen, and the addition of bagasse extract resulted in an extra load of nutrients. This could be observed from the data concerning dry weight accumulation, which maximized at 25% F2 growth medium with 10% bagasse extract. Under such conditions, the enhancing effect on chlorophyll accumulation could be ascribed to a high growth rate and the mixotrophic growth of alga, as organic carbon seemed to be insufficient, and the cells required more chlorophyll to perform photosynthesis. Extremely F2-deficient grown cultures resulted in high carotene content, which could be attributed to high nitrogen depletion or mixotrophic growth. The high chlorophyll content masked the presence of the visual yellow color of relatively high carotene content. It was observed that 10% SBAE enriching the growth media (25% and 0.0%) increased the total chlorophyll of the examined alga, while other nitrogen concentrations growing alga and enriched with the same SBAE concentration (10%) resulted in a marked decrease in the total chlorophyll content compared to control cultures. The highest chlorophyll productivity under low nitrogen content could be ascribed to the decreasing function of chlorophyll under stress or carotenogensis conditions. Otherwise, under high nitrogen and bagasse concentrations, algal growth and metabolism tended to shift toward heterotrophic growth at the expense of chlorophyll accumulation. Under such conditions, a massive accumulation of non-green pigments, as well as chlorophyll, and protein decomposition were expected.
Cultures grown under 10% bagasse-extract-enriched growth medium showed that increasing the bagasse content could be accompanied by a high nutritional load concerning macro- and micro-elements, which require more carbon skeleton for further cell metabolism. This finding can be confirmed by the results obtained when such cultures were incubated with bagasse extract and enriched with a different growth medium [23].

3.2. Effect of Induction on N. oculata Growth

Stress growth, meaning the growing of algae under certain conditions, occurs in both nutritional and environmental conditions. A nutritional condition is mainly to reduce the nitrogen in the growth medium to be 0.0 or 10% [28], and the other is to increase the salinity and iron ions [29,30,31]. When N. oculata was incubated under 2.0% NaCl, 25% F2, and 10% bagasse extract, noticeable growth differences were observed. The differences were varied due to different given factors, including high salt concentration and medium deficiency (Figure 3). In general, the salinity increased the growth dry weight and productivity of N. oculata, and all of the examined levels of the growth medium resulted in different acceleratory effects, especially the moderate level of nutrients (50% F2 plus 10% bagasse extract), which reached the maximum dry weigh accumulation (1.067 g L−1) within the same defined time (Figure 3a). The total chlorophyll (Figure 3b) represented a more positive response in a sigmoid curve due to the given conditions, and this response could be ascribed to the multiple factors affecting the grown alga since the treatments included both a vegetative factor (organic carbon) and stress factors (salinity and nutrient depletion). On the other hand, carotene represented a linear response, but it was lower than that of chlorophyll, meaning that the stress degree was lowest and needed more stress. The data also indicated a promising condition to produce high oil content in addition to proper growth meeting high dry weight accumulation (Figure 3c). The reduction in the used F2 volume decreased the initial nitrogen content, leading to severe injury of the algal cells. Such an effect was obviously noticed in the presence of other related stress factors, including salinity and high light intensity. It was reported that a 75% reduction in the nitrogen concentration in the medium led to about a 100% increase in the total lipid content in N. oculata [32,33]. Furthermore [30], reported that at least 10% nitrogen was required for proper growth under stress conditions.
In spite of the initial mineral content of bagasse extract, the main reason concerning the dry weight accumulation enhancement could be attributed to the presence of a high quantity of organic carbon. The physiological and nutritional aspects of algae nutrition claim that about 50% of an algal cell’s composition is carbon, and one kilogram of dried algal biomass requires about 1.8 kg of carbon, regardless of the carbon source [3]. Carbon dioxide is considered the most traditional carbon source; however, its utilization rate by algal cells in a closed system was very low, and such a value was minimized when used in open-air production [34]. Thus, with a high losing rate and the rise in carbon dioxide costs, the use of organic carbon seems to be more beneficial. A lot of organic sources in algae production have successfully been used, even for mass production purposes, including citrate, corn, okra, whey, potato peesls, canola, cassava, olive, bagasse extract, etc. [23,35]. Nannochloropsis is a promising source of commercially valuable pigment [36]. Its pigment composition is mostly chlorophyll a, with a small amount of carotenoids under favorable conditions. The adjustment of pigment composition is a mechanism for microalgae to adapt to environmental stresses [37,38]. Factors affecting the bioaccumulation of such pigments have been fully understood. Carotenoid accumulation by microalgae depends on the nutritional status [39,40], in addition to the shifting of photosynthetic metabolism to carotenoid accumulation by lipids. The maximum chlorophyll yield was obtained in cultures that were fed with 10% SBAE in the zero medium concentration, followed by 10% SBAE and 25% growth medium (Figure 3b). It is well-known that chlorophyll accumulation has been found to be closely related to nutritional status, and in the absence or lack of atmospheric CO2, chlorophyll increase to meet the required carbon harvesting for photosynthesis. In the present of organic carbon, the chlorophyll content is expected to decrease, where algal cells tended to accumulate oils at the expense of chlorophyll and protein. In this case, the chlorophyll seemed to be functionless.

3.3. Effects of SBAE on Fatty Acid Profile of N. oculata

The biomass productivity and lipid productivity of N. oculata were estimated to evaluate the potential for biodiesel production. Under ambient growth conditions (nutrition on SBA and collaborative stresses, i.e., 2.0% NaCl and nitrogen deficiency), most of the Nannochloropsis oculata fatty acids ranged between C14 and C20 (Table 2), with mainly C14:0, C16:0, C16:1, C18:0, C18:1n9,18:2n6, and C20:4n6 (arachidonic acid, ARA), similar to the majority of the species of Eustigmatophyceae [41]. The fatty acid distribution varies across Nannochloropsis strains, with C16, C18, and C20 being the most common. Of the six known species, N. oculata, N. gaditana, and N. salina contain mainly the C16 fatty acid, while N. limnetica contains mainly the C18 fatty acid [42]. Comparing the control along with the stresses, the proportions of saturated FA (SFA) and monounsaturated FA (MUFA) (% total FA) increased from a sum of 63.57% to 88.31%, while the polyunsaturated FA (PUFA, including linoleic acid, α-linolenic acid (ALA), and arachidonic acid (ARA), proportion declined from 36.3% to 11.69%. In particular, the proportion (% total FA, Table 2) of 16:0 increased, as well as that of 18:1n9, which suggests that they played a conspicuous role in the course of TAG reserve. Almost all of our results are similar to the findings of [43] for the fatty acid profile of N. oculata under stressed conditions (high irradiation, nitrogen deficiency, and elevated iron supplementation). They reported that, under stressed conditions, the SFA and MUFA proportions increased accordingly, with their sum increasing from 63.56% to 92.18%. Furthermore, organic carbon sources greatly affect the fatty acid composition. With change in the nature of the supplemented organic carbon sources, Chlorella kessleri cells displayed different values of both the percentage of individual fatty acid and the degree of fatty acid unsaturation [44]. Glucose was the preferred organic carbon source for C. kessleri growth and fatty acids accumulation, supporting the highest total fatty acid production at 300 mM with the value of 54.67%, or 7.11 g L−1 [45].
The SFAs of a chain length from C10 to C18 induce an increase in properties, such as the cetane number, and a decline in viscosity, as well as lower emission of pollutants, which makes them eminent for biodiesel production. Lipid profiles with mixtures of SFAs and MUFAs also are recommended for use in biodiesel production when compared to long-chain polyunsaturated fatty acids [46]. The fatty acid profile has been used as a potential indicator of biodiesel quality [47,48,49]. The C16 and C18 series contents (as percentages of the total FAMEs) of microalgae have been used to evaluate oil and biodiesel productivity [48], which corresponds to a low degree of unsaturation and is ideal for biodiesel production [50,51,52]. In that context [53], pointed out that, under such conditions, photosynthesis and carbon dioxide fixation declined greatly, and the dry weight increased due to the increase in accumulated sugars and oils (energy reservoir). Because sugars produced during photosynthesis affect the osmotic potential, cells store carbon in another form to avoid the deregulation of osmolality. The most common storage products are lipids and starch, although the preferred storage product is species-specific [54,55]. It is well-known that microalgal cell composition and growth are very sensitive to nutritional status and multiple environmental factors. Thus, extreme growth conditions can often drastically affect the algal biomass production. However, the factors that affect dry weight accumulation, including nutritional and environmental factors, are well-understood. In addition, growth patterns can also be changed due to changes in ambient conditions. Nitrogen content, salinity, carbon availability, light level, and pH are among the major factors affecting the growth patterns of microalgae. However, instead of considering growth pH as a factor that affects growth, pH can also be considered an indicator for algal growth. This is because microalgal growth is accompanied by the excretion of certain cell metabolites and the uptake of acidic compounds, such as amino acids and nitrogenous compounds, leading to increasing alkalinity of the growth medium over time. Thus, a moderate increase in alkalinity is a good indicator for normal microalgal growth.
An additional consideration is that microalgal growth is accompanied by processes affecting the pH, such as the excretion of certain cell metabolites and the absorption of acidic compounds (e.g., amino acids and nitrogenous compounds). Thus, the growth medium tends to become more alkaline over time. Thus, pH is not simply a static factor that affects growth, but rather it is also an indicator for healthy algal growth. Thus, the natural decline in the acid reaction of the algal growth medium gives rise to a decline in algal growth, indicating a high death rate [56].

3.4. Prediction of Biodiesel Properties

According to previous studies, there exist mathematically relational models between the molecular structure, the profile of fatty acid methyl ester (FAME), and biodiesel properties. Therefore, we could predict the properties of microalgal biodiesel (i.e., viscosity, iodine value, cetane number, and cold filter plugging point) with the relevant empirical equations below, helpful for evaluating whether it was an alternative to fossil fuel [57].
Based on the pertinent empirical equations, as described in the experimental procedures, the variation in the biodiesel properties of N. oculata under stress conditions could be predicted (Table 3). The viscosity (3.400 mm2 s−1), CFPP (−2.794 °C), IV (71.04354 g 100 g−1), and CN (54.789) could meet the biodiesel standards of the USA and the European Union throughout the culture period. Biodiesel feedstock with a high quality should have a high MUFA content, especially straight-chain C16 or C18 MUFA [58]. The results in Table 3 revealed that, under the organic carbon source (SBAE) and multifactor collaborative stresses (2.0% NaCl and nitrogen deficiency costress conditions), the proportions of SFA and MUFA increased, while the PUFA proportion decreased. Therefore, significant improvements in IV and CN, which are considered true indicators of high biodiesel quality, were reflected. Culture conditions have traditionally been investigated with a one-at-a-time strategy in early studies, meaning varying one factor while keeping all the others constant. Compared to one single stress factor, lipid synthesis was further improved by exposing the algal cells to moderately high light in a nitrogen-depleted medium with a higher level of Fe3+ concentration in Botryococcus, indicating the necessity in investigating the interactive effects of environmental factors on cell growth and the biosynthesis of lipids [58]. The response surface method was employed to optimize the culture conditions of Nannochloropsis, and the results suggested that the maximum growth rate was achieved under 21 °C, 52 µmol m−1 s−1, pH 8.4, and a 14.7 VVH aeration rate [59]. It was reported that a combination of high salinity and high light induced an increase in the total fatty acid in N. oceanica [60].

4. Conclusions

Carbon represents the main nutrient element forming algal cell skeletons (about 50%), and carbon nutrition realizes the most expensive figure of algae nutrition. The use of an organic carbon source suggests a dual objective: the first as a cheap carbon source, while the second reduces the external feeding of other micro- and macronutrients that are naturally chelated and more available.

Author Contributions

Conceptualization, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; methodology, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; software, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I., M.S.S. and M.W.S.; validation, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; formal analysis, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I., M.S.S. and M.W.S.; investigation, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; resources, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; data curation, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; writing—original draft preparation, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; writing—review and editing, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I., M.S.S. and M.W.S.; visualization, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; supervision, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; project administration, A.E.-K.B.E.-S., N.A.F., F.S.M., M.E., F.M.I. and M.W.S.; funding acquisition, M.E. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Deanship of Scientific Research at King Khalid University (grant number RGP.2/138/43).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors extend their appreciation to the Deanship of Scientific Research at King Khalid University for funding this work through Large Groups (Project under grant number R.G.P. 2/138/43). This research work was carried out as a part of activities of the Algal Biotechnology Unit, National Research Center, Dokki, Cairo, Egypt, (Abo El-Khair B. El-Sayed). The authors express thanks to all other staff members (The Academy of Scientific Research and Technology).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hassan, F.M.; Hayder, N.H.; Hammadi, S.S.F. Enhancement of Biodiesel Production from Local Isolates of Microalgae. Mesop. Environ. J. 2015, 1, 66–81. [Google Scholar]
  2. Rivera-Jaimes, J.A.; Postigo, C.; Melgoza, A.R.M.; Aceñ, A.; Barceló, D.; Ópez de Alda, M. Study of pharmaceuticals in surface and wastewater from Cuernavaca, Morelos, Mexico. Occurrence and environmental risk assessment. Sci. Total Environ. 2018, 613, 1263–1274. [Google Scholar] [CrossRef] [PubMed]
  3. Ren, X.; Liu, Y.; Fan, C.; Hong, H.; Wu, W.; Zhang, W.; Wang, Y. Production, Processing, and Protection of Microalgal n-3 PUFA-Rich Oil. Foods 2022, 11, 1215. [Google Scholar] [CrossRef] [PubMed]
  4. Han, P.; Lu, Q.; Fan, L.; Zhou, W. A Review on the Use of Microalgae for Sustainable Aquaculture. Appl. Sci. 2019, 9, 2377. [Google Scholar] [CrossRef]
  5. Jones, C.S.; Mayfield, S.P. Algae Biofuels: Versatility for the Future of Bioenergy. Curr. Opin. Biotech. 2012, 23, 346–351. [Google Scholar] [CrossRef]
  6. Battah, M.G.; El-Sayed, A.B.; El-Sayed, E.W. Growth of the green alga Chlorella vulgaris as affected by different carbon sources. Life Sci. J. 2013, 10, 2075–2081. [Google Scholar]
  7. El-Sayed, A.B.; Battah, M.G.; El-Sayed, E.W. Utilization efficiency of artificial carbon dioxide and corn steam liquor by Chlorella vulgaris. Biolife 2015, 3, 391–403. [Google Scholar] [CrossRef]
  8. El-Sayed, A.B. Carotenoids accumulation in the green alga Scenedesmus sp. incubated with industrial citrate waste and different inductions stress. Nat. Sci. 2010, 8, 34–40. [Google Scholar]
  9. El-Sayed, A.B.; Hoballah, E.M.; Khalafallah, M.A. Utilization of citrate wastes by Scenedesmus sp. I-Enhancement of Vegetative Growth. J. Appl. Sci. Res. 2012, 8, 739–745. [Google Scholar]
  10. Sheraz, M.K.; El-Sayed, A.B.; Hassan, A.A.; El-Shazly, H.A.M.; Ibrahim, M.T. Use of okara waste for algae nutrition. Arab. Univ. J. Agric. Sci. 2017, 25, 271–279. [Google Scholar]
  11. Fetyan, N.A.H.; El-Sayed, A.B.; Ibrahim, F.M.; Sadik, M.W.; Attia, A.Y. Bioethanol production from defatted biomass of Nannochloropsis oculata microalgae grown under mixotrophic conditions. Environ. Sci. Pollut. Res. 2021, 29, 2588–2597. [Google Scholar] [CrossRef]
  12. Gimpel, A.; Stelzenmuller, V.; Grote, B.; Buck, B.H.; Floeter, J.; Núñez-Riboni, I. A GIS modelling framework to evaluate marine spatial planning scenarios: Co-location of offshore wind farms and aquaculture in the German EEZ. Mar. Policy 2015, 55, 102–115. [Google Scholar] [CrossRef]
  13. Merchant, S.S.; Kropat, J.; Liu, B.; Shaw, J.; Warakanont, J. TAG, you are it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr. Opin. Biotech. 2012, 23, 352–363. [Google Scholar] [CrossRef]
  14. Muthukrishnan, L. Bio-engineering of microalgae: Challenges and future prospects toward industrial and environmental applications. J. Basic Microbiol. 2022, 62, 310–329. [Google Scholar] [CrossRef]
  15. Li, X.; Xu, H.; Wu, Q. Large-scale biodiesel production from microalga Chlorella protothecoides through heterotrophic cultivation in bioreactors. Biotechnol. Bioeng. 2007, 98, 764–771. [Google Scholar] [CrossRef]
  16. Lam, M.K.; Lee, K.T. Microalgae biofuels: A critical review of issues, problems and the way forward. Biotech. Adv. 2012, 30, 673–690. [Google Scholar] [CrossRef]
  17. Ben Moussa-Dahmen, I.; Chtourou, H.; Rezgui, F.; Sayadi, S.; Dhouib, A. Salinity stress increases lipid, secondary metabolites and enzyme activity in Amphora subtropica and Dunaliella sp. for biodiesel production. Bioresour. Technol. 2016, 218, 816–825. [Google Scholar] [CrossRef]
  18. Venkata Mohan, S.; Devi, M.P. Salinity stress induced lipid synthesis toharness biodiesel during dual mode cultivation of mixotrophic microalgae. Bioresour. Technol. 2014, 165, 288–294. [Google Scholar] [CrossRef]
  19. Ishika, T.; Moheimani, N.R.; Laird, D.W.; Bahri, P.A. Stepwise culture approach optimizes the biomass productivity of microalgae cultivated using an incremental salinity increase strategy. Biomass Bioenergy 2019, 127, 105274. [Google Scholar] [CrossRef]
  20. Chen, H.; Zheng, Y.L.; Zhan, J.; He, C.L.; Wang, Q. Comparative metabolic profiling of the lipid-producing green microalga Chlorella reveals that nitrogen and carbon metabolic pathways contribute to lipid metabolism. Biotechnol. Biofuels 2017, 10, 10153. [Google Scholar] [CrossRef]
  21. Metting, F.B. Biodiversity and application of microalgae. J. Ind. Microbiol. Biotechnol. 1996, 17, 477–489. [Google Scholar] [CrossRef]
  22. Knothe, G. “Designer” biodiesel: Optimizing fatty ester composition to improve fuel properties. Energy Fuels 2008, 22, 1358–1364. [Google Scholar] [CrossRef]
  23. El-Sayed, A.B.; Fetyan, N.A.; Ibrahim, F.; AFayed, S.; Sadik, M.W. Application of bagasse extract in economic Nannochloropsis oculata mass production. Egypt. J. Chem. 2020, 63, 5183–5192. [Google Scholar]
  24. Burnison, K. Modified dimethyl sulfoxide (DMSO) extraction for chlorophyll analysis of phytoplankton. Can. J. Fish. Aquat. Sci. 1980, 37, 729–733. [Google Scholar] [CrossRef]
  25. Boussiba, S.; Fan, L.; Vonshak, A. Enhancement and determination of astaxanthin accumulation in green alga Haematococcus pluvialis. In Methods in Enzymology, Carotenoids Part A; Packer, L., Ed.; Academic Press: Cambridge, MA, USA, 1992; Volume 213, pp. 386–391. [Google Scholar]
  26. Davies, H. Carotenoids. In Chemistry and Biochemistry of Plant Pigments, 2nd ed.; Goodwin, T.W., Ed.; Academic Press: New York, NY, USA, 1976; Volume 2, pp. 38–165. [Google Scholar]
  27. Arora, N.; Patel, A.; Pruthi, P.A.; Pruthi, V. Boosting TAG Accumulation with Improved Biodiesel Production from Novel Oleaginous Microalgae Scenedesmus sp. IITRIND2 Utilizing Waste Sugarcane Bagasse Aqueous Extract (SBAE). Appl. Bioch. Biotech. 2016, 180, 109–121. [Google Scholar] [CrossRef]
  28. El-Sayed, A.B. Some Physiological Studies on Green Algae. Ph.D. Thesis, Plant Physiology Department, Faculty of Agriculture Cairo University, Cairo, Egypt, 1999. [Google Scholar]
  29. Almutairi, A.W.; El-sayed, A.B.; Reda, M.M. Combined effect of salinity and pH on lipid content and fatty acid composition of Tisochrysis lutea. Saudi J. Biol. Sci. 2020, 27, 3553–3558. [Google Scholar] [CrossRef]
  30. El-Shafey, Y.H.; El-Fouly, M.M.; Khalil, M.M.; Abdallah, F.E.; El-Sayed, A.B. Secondary carotenoids accumulation by some green algae species. In Proceedings of the First Congress on the Recent Technologies in Agriculture, Faculty of Agriculture, Cairo University, Cairo, Egypt, 27–29 November 1999. [Google Scholar]
  31. Talebi, A.F.; Tabatabaei, M.; Mohtashami, S.K.; Tohidfar, M.; Moradi, F. Comparative salt stress study on intracellular ion concentration in marine and saltadapted freshwater strains of microalgae. Not. Sci. Biol. 2013, 5, 309–315. [Google Scholar] [CrossRef]
  32. El-Sheekh, M.M.; Gheda, S.F.; El-Sayed, A.E.-K.B.; Shady, A.M.A.; El-Sheikh, M.E.; Schagerl, M. Outdoor cultivation of the green microalga Chlorella vulgaris under stress conditions as a feedstock for biofuel. Environ. Sci. Pollut. Res. 2019, 26, 18520–18532. [Google Scholar] [CrossRef]
  33. Converti, A.; Casazza, A.A.; Ortiz, E.Y.; Perego, P.; Borghi, M.D. Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem. Eng. Process. Process Intensif. 2009, 48, 1146–1151. [Google Scholar] [CrossRef]
  34. Chisti, Y. Biodiesel from microalgae. Biotechnol. Adv. 2007, 25, 294–306. [Google Scholar] [CrossRef]
  35. Dang, N.M.; Lee, K. Decolorization of organic fertilizer using advanced oxidation process and its application for microalgae cultivation. J. Ind. Eng. Chem. 2018, 59, 297–303. [Google Scholar] [CrossRef]
  36. Lubián, M.L.; Montero, O.; Moreno-Garrido, I.; Huertas, E.; Sobrino, C.; del Valle, M.G.; Parés, G. Nannochloropsis (Eustigmatophyceae) as source of commercially pigments. J. Appl. Phycol. 2000, 12, 249–255. [Google Scholar] [CrossRef]
  37. Shtaida, N.; Khozin-Goldberg, I.; Solovchenko, A.; Chekanov, K.; Didi-Cohen, S.; Leu, S.; Cohen, Z.; Boussiba, S. Down regulation of a putative plastid PDC E1α subunit impairs photosynthetic activity and triacylglycerol accumulation in nitrogen-starved photoautotrophic Chlamydomonas reinhardtii. J. Exp. Bot. 2014, 65, 6563–6576. [Google Scholar] [CrossRef] [PubMed]
  38. Dong, H.P.; Williams, E.; Wang, D.Z.; Xie, Z.X.; Hsia, R.C.; Jenck, A.; Halden, R.; Li, J.; Chen, F.; Place, A.R. Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Plant Physiol. 2013, 162, 1110–1126. [Google Scholar] [CrossRef]
  39. Cerón Garcıía, M.C.; Mirón, A.S.; Sevilla, J.F.; Grima, E.M.; Camacho, F.G. Mixotrophic growth of the microalga Phaeodactylum tricornutum. Influence of diferent nitrogen and organic carbon source on productivity and biomass composition. Proc. Biochem. 2005, 40, 297–305. [Google Scholar] [CrossRef]
  40. Tittel, J.; Bissinger, V.; Gaedke, U.; Kamjunke, N. Inorganic carbon limitation and mixotrophic growth in Chlamydomonas from an acidic mining lake. Protist 2005, 156, 63–750. [Google Scholar] [CrossRef]
  41. Kaye, Y.; Grundman, O.; Leu, S.; Zarka, A.; Zorin, B.; Didi-Cohen, S.; Goldberg, K.I.; Sammy, B. Metabolic engineering toward enhanced LC-PUFA biosynthesis in Nannochloropsis oceanica: Overexpression of endogenous 12 desaturase driven by stress-inducible promoter leads to enhanced deposition of polyunsaturated fatty acids in TAG. Algal Res. 2015, 2, 387–398. [Google Scholar] [CrossRef]
  42. Ma, X.N.; Liu, J.; Liu, B.; Chen, T.P.; Yang, B.; Chen, F. Physiological and biochemical changes reveal stress-associated photosynthetic carbon partitioning into triacylglycerol in the oleaginous marine alga Nannochloropsis oculata. Algal Res. 2016, 16, 18–35. [Google Scholar] [CrossRef]
  43. Wei, L.; Huang, X. Long-duration effect of multi-factor stresses on the cellular biochemistry, oil-yielding performance and morphology of Nannochloropsis oculata. PLoS ONE 2017, 12, e0174646. [Google Scholar] [CrossRef]
  44. Hamza, H.A.; Hamouda, R.A.; Husein, M.H.; Abd-Elwahid, S.S. The characteristics of biomass production and lipid accumulation of Chlorella kessleri growth under mixotrophic and heterotrophic conditions. Egypt. J. Exp. Biol. (Bot.) 2013, 9, 19–26. [Google Scholar]
  45. Wang, Y.; Chen, T.; Qin, S. Differential fatty acid profiles of Chlorella kessleri grown with organic materials. J. Chem. Technol. Biotechnol. 2012, 88, 651–657. [Google Scholar] [CrossRef]
  46. Francisco, E.C.; Neves, D.B.; Jacob-Lopes, E.; Franco, T.T. Microalgae as feedstock for biodiesel production: Carbon dioxide sequestration, lipid production and biofuel quality. J. Chem. Technol. Biotech. 2010, 85, 395–403. [Google Scholar] [CrossRef]
  47. Bhatia, S.K.; Gurav, R.; Choi, T.-R.; Kim, H.J.; Yang, S.-Y.; Song, H.-S.; Park, J.Y.; Park, Y.-L.; Han, Y.-H.; Choi, Y.-K.; et al. Conversion of waste cooking oil into biodiesel using heterogenous catalyst derived from cork biochar. Bioresour. Technol. 2020, 302, 122872. [Google Scholar] [CrossRef]
  48. Banani, R.; Youssef, S.; Bezzarga, M.; Abderrabba, M. Waste frying oil with high levels of free fatty acids as one of the prominent sources of biodiesel production. J. Mater. Environ. Sci. 2015, 6, 1178–1185. [Google Scholar]
  49. Nascimento, I.A.; Izabel-Marques, S.S.; Dominguez-Cabanelas, I.T. Screening microalgae strains for biodiesel production: Lipid productivity an estimation of fuel quality base on fatty acids profiles as selective criteria. Bioenergy Res. 2013, 6, 1–13. [Google Scholar] [CrossRef]
  50. Tang, H.; Chen, M.; Garcia, M.E.D.; Abunasser, N.; Ng, K.S.; Salley, S.O. Culture of microalgae Chlorella minutissima for biodiesel feedstock production. Biotechnol. Bioeng. 2011, 108, 2280–2287. [Google Scholar] [CrossRef]
  51. Xu, H.; Miao, X.; Wu, Q. High quality biodiesel production from a microalga Chlorella protothecoides by heterotrophic growth in fermenters. J. Biotech. 2006, 126, 499–507. [Google Scholar] [CrossRef]
  52. Francisco, E.C.; Jacob-Lopes, E.; Vieira, K.R.; Franco, T.T. Nitrogen Starvation of Assessment in the Production of Single Cell Oils and Biodiesel Quality in Heterotrophic Cultures of Cyanobacteria Phormidium autumnale. J. Adv. Chem. Eng. 2019, 9, 192. [Google Scholar] [CrossRef]
  53. Masojidek, J.; Koblizek, M.; Torzillo, G. Photosynthesis in Microalgae. In Handbook of Microalgal Culture: Biotechnology and Applied Phycology; John Wiley & Sons: Hoboken, NJ, USA, 2013; pp. 20–39. [Google Scholar]
  54. Rai, H. The influence of photon flux density (PFD) on short term 14 C incorporation into proteins, carbohydrates and lipids in freshwater algae. Hydrobiologia 1995, 308, 51–59. [Google Scholar] [CrossRef]
  55. Rai, H.; ARTS, M.; Wainman, B.; Dockal, N.; Krambeck, H. Lipid production innatural phytoplankton communities in a small freshwater Baltic Lake, LakeSchöhsee, Germany. Freshw. Biol. 1997, 38, 581–590. [Google Scholar] [CrossRef]
  56. Al-Mutairi, A.W.; Toulibah, H.E. Effect of Salinity and pH on Fatty Acid Profile of the Green Algae Tetraselmis suecica. J. Pet. Environ. Biotech. 2017, 8, 333. [Google Scholar]
  57. Stansell, G.R.; Gray, V.M.; Sym, S.D. Microalgal fatty acid composition: Implications for biodiesel quality. J. Appl. Phycol. 2012, 24, 791–801. [Google Scholar] [CrossRef]
  58. Yeesang, C.; Cheirsilp, B. Effect of nitrogen, salt, and iron content in the growth medium and light intensity on lipid production by microalgae isolated from freshwater sources in Thailand. Bioresour. Technol. 2011, 102, 3034–3040. [Google Scholar] [CrossRef] [PubMed]
  59. Spolaore, P.; Joannis, C.C.; Duran, E.; Isambert, A. Commercial applications of microalgae. J. Biosci. Bioengin. 2006, 101, 87–96. [Google Scholar] [CrossRef]
  60. Li, Z.-R.; Wakao, S.; Fischer, B.B.; Niyogi, K.K. Sensing and responding to excess light. Annu. Rev. Plant Biol. 2009, 60, 239–260. [Google Scholar] [CrossRef]
Agriculture 12 01201 g001 550
Figure 1. (a) A 2.5 L vertical tubular photobioreactor and (b) a vertical tubular photobioreactor (14 L).
Figure 1. (a) A 2.5 L vertical tubular photobioreactor and (b) a vertical tubular photobioreactor (14 L).
Agriculture 12 01201 g001
Agriculture 12 01201 g002 550
Figure 2. (a) Dry weight (g L−1), (b) total chlorophyll (%), and (c) total carotenes (%) of N. oculata grown under different nutrient concentrations and 10% bagasse extract. C: control (medium); T1: 100% medium with 10% bagasse extract; T2: 75% medium with 10% bagasse extract; T3: 50% medium with 10% bagasse extract; T4: 25% medium with 10% bagasse extract; and T5: 0.0% medium with 10% bagasse extract. Groups with different letters in the legends of each graph indicate significant differences (Linear-Mixed Model Repeated Measures ANOVA, sig. p < 0.05).
Figure 2. (a) Dry weight (g L−1), (b) total chlorophyll (%), and (c) total carotenes (%) of N. oculata grown under different nutrient concentrations and 10% bagasse extract. C: control (medium); T1: 100% medium with 10% bagasse extract; T2: 75% medium with 10% bagasse extract; T3: 50% medium with 10% bagasse extract; T4: 25% medium with 10% bagasse extract; and T5: 0.0% medium with 10% bagasse extract. Groups with different letters in the legends of each graph indicate significant differences (Linear-Mixed Model Repeated Measures ANOVA, sig. p < 0.05).
Agriculture 12 01201 g002
Agriculture 12 01201 g003 550
Figure 3. (a) Dry weight (g L−1), (b) total chlorophyll (%), and (c) total carotenes (%) of N. oculata grown under stress of 2.0% salinity, nitrogen deficiency, 25% F2 medium, and 10% bagasse extract. C: control (medium); T1: 100% medium with 10% bagasse extract; T2: 75% medium with 10% bagasse extract; T3: 50% medium with 10% bagasse extract; T4: 25% medium with 10% bagasse extract; and T5: 0.0% medium with 10% bagasse extract. Groups with different letters in the legends of each graph indicate significant differences (Linear-Mixed Model Repeated Measures ANOVA, sig. p < 0.05).
Figure 3. (a) Dry weight (g L−1), (b) total chlorophyll (%), and (c) total carotenes (%) of N. oculata grown under stress of 2.0% salinity, nitrogen deficiency, 25% F2 medium, and 10% bagasse extract. C: control (medium); T1: 100% medium with 10% bagasse extract; T2: 75% medium with 10% bagasse extract; T3: 50% medium with 10% bagasse extract; T4: 25% medium with 10% bagasse extract; and T5: 0.0% medium with 10% bagasse extract. Groups with different letters in the legends of each graph indicate significant differences (Linear-Mixed Model Repeated Measures ANOVA, sig. p < 0.05).
Agriculture 12 01201 g003
Table
Table 1. Some chemical analyses of sugarcane bagasse aqueous extract (SBAE).
Table 1. Some chemical analyses of sugarcane bagasse aqueous extract (SBAE).
CuMnZnFeNaMgCaKPNO.C
ppm%
0.03 ± 0.0210.42 ± 0.0331.02 ± 0.3711.15 ± 0.4632.5 ± 2.65733.75 ± 1.24744 ± 1.42151 ± 2.3017.0 ± 1.0210.04 ± 0.001298.9 ± 3.221
Data of elemental analysis of sugarcane bagasse; data are means ± SD.
Table
Table 2. GC/MS chromatogram of fatty acid methyl ester of Nannochloropsis oculata grown under vegetative and multifactor stress conditions (BSA, NaCl, and nitrogen deficiency).
Table 2. GC/MS chromatogram of fatty acid methyl ester of Nannochloropsis oculata grown under vegetative and multifactor stress conditions (BSA, NaCl, and nitrogen deficiency).
Fatty Acid (% Total FA)Control* Vegetative** MFS
Caprylic acid (C8:0)3.83 a3.98 a0.894 b
Capric acid (C10:0)7.30 a7.150 a1.876 b
Lauric (C12:0)5.91 a5.500 a2.650 b
Myristic acid (C14:0)1.96 b3.0400 b11.095 a
Myristoleic acid (C14:1)5.37 a4.410 a1.226 b
Palmitic (C16:0)14.91 b17.270 b31.300 a
Palmitolecic (C16:1)3.08 b3.470 b10.064 a
Stearic (C18:0)6.88 a5.570 a2.505 b
Oleic (C18:1)10.33 c13.32 b26.700 a
Linoleic (C18:2)18.12 a17.490 a3.70 b
Linolenic (C18:3)12.11 a9.7 b1.05 c
Arachidonic acid (C20:4)10.21 a9.110 a6.94 b
Σ C1617.39 c20.74 b41.368 a
Σ C1847.44 a46.08 a34.01 b
Σ C2010.21 c9.11 c6.94 c
Σ MUSFA18.78 c21.2 b37.99 a
Σ PUSFA40.44 a36.3 a b11.69 c
TUSFA59.22 a57.5 a49.68 a
TSFA40.78 a42.5 a50.32 a
* Vegetative means organic carbon (10% SBAE with 25% F2 medium); ** MFS means multifactor collaborative stresses, i.e., SBAE, 2.0% NaCl, and nitrogen deficiency; ARA: arachidonic acid C20:4n6; MUF: monounsaturated FA; PUFA: polyunsaturated FA; TUSFA: total unsaturated FA; and TSFA, total saturated FA. Any means in the same column followed by different letters (a, b, c) are significantly (p < 0.05) different), as analyzed by one-way ANOVA.
Table
Table 3. Some fuel properties of N. oculata grown under vegetative and multifactor stress conditions (BSAE, as well as NaCl and nitrogen deficiency).
Table 3. Some fuel properties of N. oculata grown under vegetative and multifactor stress conditions (BSAE, as well as NaCl and nitrogen deficiency).
ParameterDUSVIVCNLCSFCEPPVisOil%
Vegetative93.8248.29111.0543.274.51−2.303.316.19
MFS63.37223.0271.0454.793.31−2.793.4011.89
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El-Sayed, A.E.-K.B.; Fetyan, N.A.; Moghanm, F.S.; Elbagory, M.; Ibrahim, F.M.; Sadik, M.W.; Shokr, M.S. Biomass Fatty Acid Profile and Fuel Property Prediction of Bagasse Waste Grown Nannochloropsis oculata. Agriculture 2022, 12, 1201. https://doi.org/10.3390/agriculture12081201

AMA Style

El-Sayed AE-KB, Fetyan NA, Moghanm FS, Elbagory M, Ibrahim FM, Sadik MW, Shokr MS. Biomass Fatty Acid Profile and Fuel Property Prediction of Bagasse Waste Grown Nannochloropsis oculata. Agriculture. 2022; 12(8):1201. https://doi.org/10.3390/agriculture12081201

Chicago/Turabian Style

El-Sayed, Abo El-Khair B., Nashwa A. Fetyan, Farahat S. Moghanm, Mohssen Elbagory, Fatma M. Ibrahim, Mahmoud W. Sadik, and Mohamed S. Shokr. 2022. "Biomass Fatty Acid Profile and Fuel Property Prediction of Bagasse Waste Grown Nannochloropsis oculata" Agriculture 12, no. 8: 1201. https://doi.org/10.3390/agriculture12081201

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