Next Article in Journal
Simulation for the Effect of Singlet Fission Mechanism of Tetracene on Perovskite Solar Cell
Previous Article in Journal
Influence of Oxygen/Steam Addition on the Quality of Producer Gas during Direct (Air) Gasification of Residual Forest Biomass
Previous Article in Special Issue
Biofuel Production from Seaweeds: A Comprehensive Review
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Energies
Volume 16
Issue 5
10.3390/en16052429
energies-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Optimization of Microalgal Biomass Production in Vertical Tubular Photobioreactors

by
Małgorzata Hawrot-Paw
* and
Magdalena Sąsiadek
Department of Renewable Energy Engineering, West Pomeranian University of Technology in Szczecin, Pawla VI 1, 71-459 Szczecin, Poland
*
Author to whom correspondence should be addressed.
Energies 2023, 16(5), 2429; https://doi.org/10.3390/en16052429
Submission received: 20 January 2023 / Revised: 19 February 2023 / Accepted: 1 March 2023 / Published: 3 March 2023
(This article belongs to the Special Issue Sustainable Bioenergy Feedstock Production)
Browse Figures
Versions Notes

Abstract

:
Microalgal biomass is a promising alternative and renewable substrate for bioenergy production. The main problem for its commercial application is to obtain and keep a high level of production by providing microalgae with appropriate conditions for growth. The aim of this study was to determine optimal culture conditions such as temperature, photoperiod, and pH. The amount of biomass by gravimetry, optical density by spectrophotometry, and productivity were analyzed. Suitable values of cultivation parameters allowed for the increased growth and biomass productivity of Arthrospira platensis (4.24 g·L−1), Chlamydomonas reinchardtii (1.19 g·L−1), Chlorella vulgaris (2.37 g·L−1), and Dunaliella salina (4.50 g·L−1) and optical density for Ch. reinchardtii and C. vulgaris. These species had maximum biomass productivity of 0.72, 0.12, 0.36, and 0.77 g·L−1·d−1, respectively. Productivity was determined by cultivation temperature and for Ch. reinchardtii also by pH.

1. Introduction

Sustainable and renewable energy sources are an alternative to conventional energy derived from fossil fuels. An important and universal source of renewable energy that allows the production of bioenergy, whether in the form of heat, electricity, or transportation biofuels, is biomass [1]. Bioenergy production increases energy independence [2], and some associated technologies can reduce greenhouse gas emissions [3]. Some biomass sources are products and waste from the agricultural, forestry, municipal, or aquaculture industrial sectors [4]. Since certain biomass types also have non-energy uses and the available feedstock for the bioenergy sector can be limited [5], microalgae have been of interest again. Microalgae are microscopic organisms that have been used in a wide range of industries. Their biomass and cellular components are used in the production of food and supplements, feed, cosmeceuticals, nutraceuticals, and pharmaceuticals [6,7]. Among others, carbohydrates, lipids, and proteins can be obtained from their fast-growing biomass [8]. Biomass and those macromolecules are important for energy production and for biofuels [9,10,11], including biodiesel [12,13], biohydrogen [14,15], bio-oil [16], or bioethanol [17]. Some microalgal strains can produce liquid hydrocarbons [18] that can be converted into diesel or petrol [10]. The energy potential of algae is wide and the type of fuel produced from them depends on the biomass conversion method (biochemical, thermochemical, or physicochemical). The selection of the appropriate method depends on the amount and type of used biomass, the required form of final energy, and economic efficiency [19]. Biomass is a promising substrate also for biogas production during anaerobic digestion [20]. Compared to other fuels, not only raw biomass but also biomass residues, e.g., after oil pressing, can be used for biogas production [21]. Microalgal biomass for AD does not require drying, which is beneficial for the economic balance of this process [22]. Many authors confirm the significant potential of microalgae for methane production [23,24,25,26]. The efficiency of biogas extraction from microalgal biomass depends on the technology (single- or multi-stage processes and dry or wet, mesophilic or thermophilic fermentation) and the retention time (HRT), but above all on the type of algae, which is related to the chemical composition of their cells. Large amounts of carbohydrates increase the rate of methane fermentation. A higher content of lipids and proteins decreases the rate of biogas production but increases the methane content in the range of 75 to 90% [27]. The integration of bioprocessing pathways makes it possible to obtain not only electricity and different types of fuels, but also value-added chemicals such as lutein or astaxanthin [28].
Production of microalgal biomass on a large scale requires optimization of cultivation technologies [29]. These processes depend on the culture conditions as well as the type of microalgae species. Microalgae are most often grown in an autotrophic method [30] in open pond systems [31] or in photobioreactors [32]. During photosynthesis with light, microalgae convert carbon dioxide into biomass and valuable cellular components [33]. The spectrum of light influences the cell size, amount, and productivity of the biomass [34]. Optimal light intensity values for the growth of different algal species are between 26–400 µmol m−2 s−1 [35]. Microalgae are grown in an aquatic environment, which must be kept under appropriate conditions of illumination, temperature, pH, and CO2 concentration [36]. Suitable nutrients are also required for algal growth [37,38].
Under natural conditions, microalgae utilize sunlight, while under laboratory or industrial conditions, artificial lighting is most often used [39]. The intensity of light affects photosynthesis, resulting in biomass yield and its composition [40]. The use of artificial lighting allows to control not only the period of illumination and light intensity but also its spectrum [41]. Special attention is given to light-emitting diodes (LEDs) with their low energy consumption, narrow emission spectrum, long lifetime, and no mercury [42]. Not only the type of light and its intensity are important for the growth and development of microalgae, but also the time of illumination of the culture per day and the meaning photoperiod [43].
Microalgae can grow at temperatures between 5 and 40 °C; however, each species has its own optimal growth temperature. For most microalgae, this is between 20 °C and 30 °C [44]. Temperatures beyond this range can inhibit or completely stop their growth [45]. Temperature significantly affects their metabolism, including nutrient uptake and carbon dioxide fixing efficiency [46]. The production of biomass is inhibited by temperatures that are too low relative to the optimal, while temperatures above the optimum significantly reduce productivity. This can lead to a loss of culture as cell mortality increases [47,48].
For microalgae, the pH is one of the most critical environmental conditions [49]. They usually grow in a pH from 6 to 9 [37], despite the fact that many of them can tolerate wide pH ranges [50]. The pH increases during the light period and decreases in darkness due to respiration [51]. Furthermore, the pH changes can affect enzymes [52], the functions of cell membranes, and photosynthesis [53] since the pH of the culture medium affects the availability of CO2 [46].
Optimization of microalgae growth conditions is crucial for the intensification of biomass production for energy purposes, including biofuel production. The suitable abiotic conditions for this process should be appropriate to the type of photobioreactor. The aim of this study was to determine the optimal cultivation parameters affecting the growth of four selected microalgae species in vertical tubular photobioreactors. Photobioreactors with capacities similar to those used in this study represent the first stage of scale-up production. The effects of temperature, lighting time, and the pH of the growth medium were analyzed. All of the parameters were evaluated at the same time, and the results presented represent the interaction between those factors. We hypothesize that an appropriate configuration of optimal values for each parameter will positively affect the production of microalgal biomass. The aim of the optimization is to increase the amount of biomass as feedstock for anaerobic digestion.

2. Materials and Methods

2.1. Microalgae Strains

The presented study is a continuation of previously carried out experiments [54] on the production of microalgal biomass as a substrate for anaerobic digestion. In the preliminary study, 16 strains of microalgae were analyzed, and for the next stages, based on the results of biomass production efficiency, four of them were selected. The following species were used in this study: Chlorella vulgaris (BA 002) from the Culture Collection of Baltic Algae (CCBA, University of Gdansk, Gdansk, Poland) and Chlamydomonas reinhardtii (CHL 152), Arthrospira platensis (CYA 428), and Dunaliella salina from the culture collection of the Department of Renewable Energy Engineering at the West Pomeranian University of Technology in Szczecin, Poland.

2.2. Preincubation Conditions

Microalgae were kept in F/2 synthetic culture medium [55] with a composition of (g·L–1): NaNO3–75, NaH2PO4·2H2O–5, microelement solution (1 mL·L−1): Na2EDTA–4,16, FeCl3·6H2O–3,15, CuSO4·5H2O–0.01, ZnSO4·7H2O–0.022, CoCl2·6H2O–10, MnCl2·4H2O 0.18 and NaMoO4·2H2O–0.0063, vitamins solution (1 mL·L−1): cobalamin (vitamin B12)–0.01, thiamine (vitamin B1)–0.1, and biotin (vitamin H)–0.005. For the D. salina and A. platensis species, the growth medium was enriched by sodium chloride (NaCl) to a salinity of 8‰. In addition, 1 g·L–1 of sodium bicarbonate (NaHCO3) was added to A. platensis medium. Inoculum was prepared in 1 L photobioreactors, which were filled with 700 mL of sterile F/2 culture medium adjusted to pH 7, followed by the addition of 70 mL culture of each microalgae. These cultures were kept for 7 days at 23 ± 1 °C using sodium light (High Pressure Sodium, HPS; PHILIPS, Amsterdam, Netherlands) at 125 µmol m−2 s−1 and a photoperiod of 12/12 h (light/dark cycle). The photobioreactors were aerated with compressed air with an atmospheric concentration of carbon dioxide using a membrane pump at a flow rate of 10 L·min−1.

2.3. Experimental Setup

The microalgae were grown in vertical tubular photobioreactors (Aqua Medic, Bissendorf, Germany) with a capacity of 2.5 L (Figure 1). They were filled into 2 L of sterile F/2 culture medium and 200 mL of inoculum. The LED lighting (HOLDBOX, Żabia Wola, Poland) with white, red (wavelength from 600 to 700 nm), and blue (wavelength from 400 to 500 nm) diodes was used in the experiment. The light intensity was 130 µmol m−2 s−1. The carbon dioxide required for photosynthesis came from the compressed atmospheric air supplied to the photobioreactors using an Aqua Medic Mistral 2000 pump with a flow of 0.9 m3·h–1. This also allowed for the proper stirring of the culture medium and homogeneous conditions throughout the volume of the photobioreactor. A sterile 0.22 µm polytetrafluoroethylene (PTFE) filter was used for air filtration. The photobioreactors had air-filter-protected valves to remove the oxygen produced during photosynthesis. This experiment was carried out as a batch culture for 15 days. Optimization was conducted for photoperiods of (12/12, 18/6, and 24/0 h in the light/dark cycle), temperatures of (20, 25, and 30 °C), and for pH values of (7, 8, 9). The microalgae cultivation parameters are presented in Table 1.

2.4. Analytical Methods

Optimal conditions for microalgae cultivation were determined by measuring the amount of biomass and optical density (OD) in the culture.
The dry weight of the microalgae was determined by the gravimetric method. Their biomass was analyzed using a moisture analyzer (AXIS ATS60, Gdańsk, Poland). Each day, 30 mL samples were taken from particular photobioreactors and centrifuged (Eppendorf, Hamburg, Germany) at 4000× g for 20 min. After centrifugation, the biomass was transferred to aluminum dishes and dried at 105 °C until a constant mass was obtained. After this, the dishes with the biomass were cooled in the desiccators and then weighted. The amount of biomass was determined on the first day of culture start and every 24 h for the next 15 days. The results were given in g·L−1. Productivity (g·L·d−1) was determined based on the biomass yield using the following formula:
B i o m a s s   p r o d u c t i v i t y   ( B P ) = B f − B 0 d
where
Bf is the final amount of biomass (g), B0 is the initial amount of biomass (g), and d is the cultivation time (day).

2.5. Statistical Analysis

All measurements were carried out in triplicate and the data were expressed as mean value ± standard deviation (SD). The results were analyzed using a computer program (Statistica version 13.3; Dell Inc., Tulsa, OK, USA). Analysis of variance and a post-hoc Tukey’s tests were performed at statistical significance of p ≤ 0.05.

3. Results and Discussion

3.1. Microalgal Biomass Concentration and Productivity

The effectiveness of microalgal biomass production was dependent on the time of culture lighting, temperature, and the pH of the culture medium, and it varied between strains (Figure 2). Under the same cultivation conditions, the highest values were observed for A. platensis and D. salina. For A. platensis, the amount of biomass ranged from 3.08 g·L−1 to 4.24 g·L−1. The maximum value was found at 20 °C, 12/12 h in the light/dark, cycle and at pH 8. According to Li et al. [56], most Arthrospira strains prefer an alkaline pH of around 9.0–9.5; however, in this study, the optimum pH was lower. A range of variables determines the growth of microalgae. It is possible that in an optimal combination of temperature and photoperiod, maximum biomass values can be observed at lower pH values. Chaiklahan et al. [57] noted 1.42 ± 0.11 g·L−1 for a photoperiod of 24/0 h and a PAR light intensity of 2300 µmol m−2 s−1. The efficiency of microalgal biomass production can be increased by optimizing environmental factors or the composition of the culture medium. If the biomass is destined for energy purposes, then the costs associated with nutrient supply are important. Madkour et al. [58] substituted all of the components of Zarrouk’s growing medium with lower cost and commonly available fertilizers and chemicals. The authors obtained a maximum biomass yield of 0.813 ± 0.018 mg·L−1 with 0.840 ± 0.008 mg·L−1 when the microalgae were grown on an optimal medium. De Castro et al. [59] in a study on the effect of sodium bicarbonate and sodium nitrate on the biomass production of this strain obtained 3270 mg·L−1. Based on these results, it can be concluded that, for A. platensis, modification of the abiotic factors allows for more favorable results.
The use of microalgae in commercial applications requires a large amount of biomass, but the yield of Ch. reinchardtii in this study was rather low, ranging from 0.90–1.19 g·L−1. Lower temperatures resulted in less suitable conditions for the growth and development of these microalgae. The average biomass at 20 °C was 1.01 g·L−1, while at 30 °C, it was 1.12 g·L−1. The optimum pH for this strain was 7–8, while the photoperiod was 18/6 h (light/dark). Vargas et al. [60] also obtained 1073.33 ± 23.09 g·L−1 of biomass, although under different conditions (32 °C, pH 6.2). Abd El Baky and El Baroty [61] carried out a larger scale study (400 L photobioreactor) and, under limited availability of N, P, and S and with 6% CO2 introduced into the culture, obtained a biomass yield of as much as 3.11 g·L−1. This suggests how important suitable carbon dioxide levels could be for some microalgal strains [62].
The average amount of C. vulgaris biomass in particular photobioreactors ranged from 1.02 g·L−1 to 2.37 g·L−1. Biomass decrease was observed at extreme temperatures, as well as at extreme pH values. The optimal conditions for C. vulgaris cultivation, considering all of the analyzed parameters, were a temperature of 25 °C, a photoperiod of 18/6 h in the light/dark cycle, and a pH of 8. A suitable pH provides an optimum ratio of HCO3− and CO2 for carbon assimilation [63]. In a previous study [64], biomass production was optimized for the type of light used in cultivation (high-pressure sodium light or light-emitting diode), photoperiod, and pH, and a maximum of 546 ± 7.88 mg·L−1 dry weight of biomass was obtained, which confirms that temperature is an important factor determining the growth of microalgae and the increase in biomass production.
The average biomass content for D. salina in the present study, where only the combinations of selected cultivation parameters were used, ranged from 3.36 g·L−1 to 4.50 g·L−1. It was noted that the amount of biomass decreased with the increasing temperature. Similar changes were observed when the lighting time of the culture increased. As indicated by Xu et al. [65], intracellular starch content increases during periods of light, while it decreases in the dark. This may have significance for energy production from microalgal biomass. According to the maximum values observed in the presented study, beneficial conditions for D. salina cultivation are 20 °C, pH 8, and a photoperiod of 12/12 h (light/dark), although the optimal temperature may change depending on the cultivation parameters [66]. Gastelum-Franco et al. [67] kept cultures of D. salina in F/2 medium at a temperature of 24 ± 2 °C, a pH 8.2, and for a 12/12 h photoperiod and obtained 2.93 ± 0.40 g·L−1. Statistical analysis of the presented results did not confirm significant changes in biomass productivity as an interaction between temperature and pH. Several studies have been carried out to increase the biomass productivity of D. salina by modifying the composition of culture media or by modifying culture conditions [68]. Morowvat and Ghasemi [69] optimized the composition of the culture medium for glucose content and nitrate and phosphate concentration and obtained a biomass concentration of 1.015 g·L−1. Ahmed et al. [70] optimized biomass production by changing the salinity level and, after 21 days of culture, obtained at 2 M NaCl 1231.66 ± 1. 26 mg·L−1. In this study, the biomass yields were higher than those presented by other authors, indicating that optimizing the environmental parameters for D. salina had a more beneficial effect than modifying the composition of the culture medium.
In different types of photobioreactors, the optimum growth conditions for the same strains may differ (Table 2). Additionally, a change in the scale of biomass production, with varying volumes, alters cultivation conditions. Optimizing cell culture conditions is essential to improve microalgae’s industrial productivity [71].
The productivity of microalgal biomass is presented in Table 3. The average values varied according to the temperature, time of culture lighting, and pH. For A. platensis, productivity ranged from 0.49 g·L−1·d−1 to 0.72 g·L−1·d−1. Similar values (maximum 0.62 ± 0.05 g·L−1·d−1) were reported by Chaiklahan et al. [57]. In the present study, high productivity was promoted by cultivation under controlled conditions in photobioreactors. Guidi et al. [82] cultivated this strain under a greenhouse in an 8000 L raceway and determined biomass productivity of 0.08 g·L−1·d−1.
Significantly lower values were observed for Ch. reinchardtii, with a maximum of 0.12 g·L−1·d−1 at 25 °C for a photoperiod of 18/6 h in the light/dark cycle and pH 8 and for a photoperiod of 24/0 and a pH range of 7–8. By optimizing the physicochemical parameters (pH 6.5–7.0 and 30 °C), Banerjee et al. [83] improved biomass productivity to 512 mg·L−1·d−1. Research by Kong et al. [84] indicates that the optimal pH for C. reinhardtii is 7.5. Under such conditions in Biocoil photobioreactors, these authors obtained 2.00 ± 0.03 g·L−1·d−1.
In this study, the biomass productivity of C. vulgaris was at a relatively low level. A maximum value of 0.36 g·L−1·d−1 was observed at 25 °C for a photoperiod of 18/6 h (light/dark) and pH 8. Kim et al. [71] reported increases in the productivity of the Chlorella sp. genus from a level of 0.28 g·L−1·d−1 to 0.51 g·L−1·d−1 in mixotrophic cultivation with glucose. Anyanwu et al. [85] analyzed the effects of introducing dark periods and different types of LEDs to lighting photobioreactors (red, white, and green) and without a dark period, and using white light, they obtained significantly higher biomass productivity of 2.438 g·L−1·d−1. A suitable light type and light intensity and an appropriate photoperiod affect the chemical composition of cells [86] which is important if microalgae are used as a substrate for bioenergy production.
The productivity for D. salina was high and ranged from 0.56–0.81 g·L−1·d−1. Values decreased with increasing culture lighting time, while the effect of pH was unclear. There were no statistically significant differences in biomass productivity at different pH values. Abarna et al. [87] analyzed the enhancement of biomass productivity through the application of liquid seaweed fertilizers in cultivation and obtained a maximum of 0.038 g·L−1·d−1. The evaluation of biomass productivity was the first stage of the analyses of D. salina’s commercial suitability carried out by Borovkov et al. [88]. These authors cultivated D salina for 14 days. In the mid-incubation time, they reduced the temperature from 27–28 °C to 23–24 °C and increased the average intensity of light from 40 W·m−2 to 80 W·m−2 and obtained for one of the three tested strains 0.18 g·L−1·d−1.
The optimum growth temperatures for the different microalgal species ranged from 20 to 30 °C. Setting an optimum value for this parameter avoids cellular stress [89] and increases biomass production. Our studies indicate that this parameter is related to other environmental factors. The light/dark cycle influences the rate of photosynthesis, so extending the light phase can significantly increase biomass yield [90]. Such a correlation was not observed in this study, suggesting that the optimum for this parameter depends on the microalgal species. This has also been confirmed by studies carried out by other authors [91,92]. An important parameter affecting microalgal growth, where the optimum and tolerance also depend on the microalgal species [46], is pH. This factor influences the solubility of inorganic carbon in culture [93] and can significantly modify the physicochemical properties of the cells [94], so it is crucial to determine and keep optimal values during cultivation. Most of the microalgae tested preferred slightly alkaline conditions, even A. platensis. In this strain, this consideration may have resulted from interaction between the applied factors.

3.2. Optical Density in Microalgal Culture

The average OD680 values determined in the study are presented in Figure 3. For A. platensis, a significant effect was determined only for the temperature and photoperiod; the effect of the pH of the culture medium and the interaction between the factors studied were not significant. At 20 °C, the highest OD680 value (0.421) was recorded for the 24/0 h photoperiod in the light/dark cycle. At 25 °C, the OD680 increased to 0.509 for the 12/12 h photoperiod, while at 35 °C a value of 0.455 was recorded for the 18/6 h light/dark cycle. Hussin et al. [73] analyzed the effect of aeration rate, pH, and light intensity for two morphological forms of A. platensis and obtained a cell density (OD680) of 1.287 ± 0.019 for helical forms and 1.318 ± 0.059 for straight forms. Due to the difference in light dispersion during the measurement associated with different cell sizes according to Shagerl et al. [95], OD values cannot be used to compare different species.
For Ch. reinchardtii, all analyzed of the factors and their interactions had a significant effect on optical density. The highest OD680 was recorded at 30 °C for 18/6 h (light/dark cycle) and pH 8 (0.468). Ivanov et al. [96] cultivated Ch. reinchardtii for 6 days at 30 °C, and then, after dilution of the growth medium, they set up two combinations and continued incubation at 30 °C and 39 °C. These authors observed advantageous changes in optical density at 30 °C.
Additionally for the C. vulgaris strain there was a significant interaction effect of the analyzed growth parameters. The highest values for optical density were observed at the temperature of 25 °C and for pH 8 and ranged from 0.349 for the 12/12 h photoperiod to 0.557 for 24/0 h of continuous lighting. Sharma et al. [97] analyzed the effect of light type (fluorescent or natural) and temperature in two ranges, 25–30 °C and 30–35 °C, and the maximum OD670 value for this microalgae species (0.42) was observed during cultivation under natural light at lower temperatures.
For D. salina, there was no significant interaction effect between the temperature, the pH of the growth medium, and the photoperiod. At 20 °C, the OD680 was 0.630 for the 18/6 h photoperiod and pH 8, while at 25 °C and 35 °C, it was 0.659 and 0.650, respectively, for 18/6 h lighting and for pH 7. The absence of cell walls in this strain is an unquestionable advantage [70]. It simplifies the pretreatment of such substrates and the hydrolysis of components accumulated in the microalgal cells.
The amount of biomass was correlated with the optical density for all of the microalgae; however, the correlation coefficient had a relatively low value between r = 0.35 for D. salina to r = 0.62 for C. vulgaris. Determination of optimal growing conditions is one of the most important steps in starting large-scale biomass production. Direct weight measurement is a reliable indicator of biomass growth efficiency; however, it is a long-term and time-consuming procedure. In many studies, spectrophotometric measurements of optical density are carried out as an alternative, although the use of this parameter is not evident. Earlier studies [98] on C. vulgaris confirmed the correlation between gravimetric and spectrophotometric measurements, but optical density is based on cellular pigment, and its content varies with culture age and culture conditions, which can lead to incorrect results [99]. Algal cell size varies within the growth cycle [100] and can increase with the increasing temperature of cultivation [101]. Thus, OD measurements can be used for online monitoring of biomass production [102] and as a complement to gravimetric methods [95].

4. Conclusions

Microalgae are a promising renewable source for bioenergy production. Biomass and components accumulated in the microalgal cells can be converted to heat, electricity, and different types of biofuels. A simple and low-cost method to convert microalgal biomass into a sustainable renewable energy source is anaerobic digestion. This process allows for the utilization of wet biomass, which has a positive effect on the balance of energy obtained compared with that invested, including for biomass production and harvesting. Production of large amounts of biomass requires optimization of cultivation conditions. There are many factors that affect microalgae growth. Besides nutrient availability, critical environmental parameters for cultivation include light, temperature, and pH. Providing optimal growth conditions increases biomass yield and productivity. Therefore, microalgae were cultured under different temperatures, pH values, and light/dark times over a 24-h cycle. The results show that the interaction between these essential abiotic factors for cell growth had a positive effect on A. platensis and D. salina and resulted in over 4 g·L−1 of dry weight for both strains. For the other strains, it is necessary to extend the study to other environmental factors or to modify the growth media to obtain more positive results. For all of the tested species, the most important determinant of biomass productivity was temperature.

Author Contributions

Conceptualization, M.H.-P.; methodology, M.H.-P.; validation, M.H.-P.; formal analysis, M.H.-P. and M.S.; investigation, M.H.-P. and M.S.; data curation, M.H.-P. and M.S.; writing—original draft preparation, M.H.-P. and M.S.; writing—review and editing, M.H.-P. and M.S.; visualization, M.H.-P.; supervision, M.H.-P. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Rector of the West Pomeranian University of Technology in Szczecin for Ph.D. students at the Doctoral School, grant number ZUT/28/2022 (540/071 WKŚiR).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Luo, Z.; Zhou, J. Thermal Conversion of Biomass. In Handbook of Climate Change Mitigation; Chen, W.Y., Seiner, J., Suzuki, T., Lackner, M., Eds.; Springer: New York, NY, USA, 2012. [Google Scholar] [CrossRef]
  2. Driver, T.; Bajhaiya, A.; Pittman, J.K. Potential of Bioenergy Production from Microalgae. Curr. Sustain. Renew. Energy Rep. 2014, 1, 94–103. [Google Scholar] [CrossRef] [Green Version]
  3. Baležentis, T.; Streimikiene, D.; Zhang, T.; Liobikiene, G. The role of bioenergy in greenhouse gas emission reduction in EU countries: An Environmental Kuznets Curve modelling. Resour. Conserv. Recycl. 2019, 142, 225–231. [Google Scholar] [CrossRef]
  4. Garba, A. Biomass Conversion Technologies for Bioenergy Generation: An Introduction. In Biotechnological Applications of Biomass; Basso, T.P., Basso, T.O., Basso, L.C., Eds.; IntechOpen: London, UK, 2020; Available online: https://www.intechopen.com/chapters/73832 (accessed on 18 February 2023). [CrossRef]
  5. Hoang, D.L.; Davis, C.; Moll, H.C.; Nonhebel, S. Can Multiple Uses of Biomass Limit the Feedstock Availability for Future Biogas Production? An Overview of Biogas Feedstocks and Their Alternative Uses. Energies 2020, 13, 2747. [Google Scholar] [CrossRef]
  6. Nethravathy, M.U.; Mehar, J.G.; Mudliar, S.N.; Shekh, A.Y. Recent Advances in Microalgal Bioactives for Food, Feed, and Healthcare Products: Commercial Potential, Market Space, and Sustainability. Compr. Rev. Food Sci. Food Saf. 2019, 18, 1882–1897. [Google Scholar] [CrossRef] [Green Version]
  7. Lucakova, S.; Branyikova, I.; Hayes, M. Microalgal Proteins and Bioactives for Food, Feed, and Other Applications. Appl. Sci. 2022, 12, 4402. [Google Scholar] [CrossRef]
  8. Vyas, S.; Patel, A.; Risse, E.N.; Krikigianni, E.; Rova, U.; Christakopoulos, P.; Matsakas, L. Biosynthesis of microalgal lipids, proteins, lutein, and carbohydrates using fish farming wastewater and forest biomass under photoautotrophic and heterotrophic cultivation. Bioresour. Technol. 2022, 359, 127494. [Google Scholar] [CrossRef]
  9. Sharma, P.K.; Saharia, M.; Srivstava, R.; Kumar, S.; Sahoo, L. Tailoring Microalgae for Efficient Biofuel Production. Front. Mar. Sci. 2018, 5, 382. [Google Scholar] [CrossRef]
  10. Tiwari, A.; Kiran, T. Biofuels from Microalgae. In Advances in Biofuels and Bioenergy; Nageswara-Rao, M., Soneji, J.R., Eds.; IntechOpen: London, UK, 2018; Available online: https://www.intechopen.com/chapters/59007 (accessed on 18 February 2023). [CrossRef] [Green Version]
  11. Zewdie, D.T.; Ali, A.Y. Cultivation of microalgae for biofuel production: Coupling with sugarcane-processing factories. Energ. Sustain. Soc. 2020, 10, 27. [Google Scholar] [CrossRef]
  12. Hawrot-Paw, M.; Ratomski, P.; Koniuszy, A.; Golimowski, W.; Teleszko, M.; Grygier, A. Fatty Acid Profile of Microalgal Oils as a Criterion for Selection of the Best Feedstock for Biodiesel Production. Energies 2021, 14, 7334. [Google Scholar] [CrossRef]
  13. Zhang, S.; Zhang, L.; Xu, G.; Li, F.; Li, X. A review on biodiesel production from microalgae: Influencing parameters and recent advanced technologies. Front. Microbiol. 2022, 13, 970028. [Google Scholar] [CrossRef]
  14. Limongi, A.R.; Viviano, E.; De Luca, M.; Radice, R.P.; Bianco, G.; Martelli, G. Biohydrogen from Microalgae: Production and Applications. Appl. Sci. 2021, 11, 1616. [Google Scholar] [CrossRef]
  15. Li, S.; Li, F.; Zhu, X.; Liao, Q.; Chang, J.-S.; Ho, S.-H. Biohydrogen production from microalgae for environmental sustainability. Chemosphere 2022, 291, 132717. [Google Scholar] [CrossRef] [PubMed]
  16. Shahi, T.; Beheshti, B.; Zenouzi, A.; Almasi, M. Bio-oil production from residual biomass of microalgae after lipid extraction: The case of Dunaliella sp. Biocatal. Agric. Biotechnol. 2020, 23, 101494. [Google Scholar] [CrossRef]
  17. Lakatos, G.E.; Ranglová, K.; Manoel, J.C.; Grivalský, T.; Kopecký, J.; Masojídek, J. Bioethanol production from microalgae polysaccharides. Folia Microbiol. 2019, 64, 627–644. [Google Scholar] [CrossRef]
  18. Ranga Rao, A.; Sarada, R.; Ravishankar, G.A. Influence of CO2 on growth and hydrocarbon production in Botryococcus braunii. J. Microbiol. Biotechnol. 2007, 17, 414–419. [Google Scholar]
  19. Milano, J.; Ong, H.C.; Masjuki, H.H.; Chong, W.T.; Lam, M.K.; Loh, P.K.; Vellayan, V. Microalgae biofuels as an alternative to fossil fuel for power generation. Renew. Sustain. Energy Rev. 2016, 58, 180–197. [Google Scholar] [CrossRef]
  20. Torres, A.; Padrino, S.; Brito, A.; Díaz, L. Biogas production from anaerobic digestion of solid microalgae residues generated on different processes of microalgae-to-biofuel production. Biomass Conv. Bioref. 2021. [Google Scholar] [CrossRef]
  21. Costa, J.A.V.; Bezerra, P.Q.M.; Moreira, J.B.; Molina, A.N.; de Morais, M.G. Biogas from Microalgae: Production Approaches and Strategies for Process Optimization. In Role of Microbes in Industrial Products and Processes; Kumar, S., Kumar, N., Shahid-ul-Islam, Eds.; Scrivener Publishing: Beverly, MA, USA, 2022. [Google Scholar] [CrossRef]
  22. Wu, N.; Moreira, C.M.; Zhang, Y.; Doan, N.; Yang, S.; Phlips, E.J.; Svoronos, S.A.; Pullammanappallil, P.C. Techno-Economic Analysis of Biogas Production from Microalgae through Anaerobic Digestion. In Anaerobic Digestion; Rajesh, B.J., Ed.; IntechOpen: London, UK, 2019. [Google Scholar] [CrossRef] [Green Version]
  23. Mussgnug, J.H.; Klassen, V.; Schlüter, A.; Kruse, O. Microalgae as substrates for fermentative biogas production in a combined biorefinery concept. J. Biotechnol. 2010, 150, 51–56. [Google Scholar] [CrossRef]
  24. Ward, A.J.; Lewis, D.M.; Green, F.B. Anaerobic digestion of algae biomass: A review. Algal Res. 2014, 5, 204–214. [Google Scholar] [CrossRef]
  25. Klassen, V.; Blifernez-Klassen, O.; Wibberg, D.; Winkler, A.; Kalinowski, J.; Posten, C.; Kruse, O. Highly efficient methane generation from untreated microalgae biomass. Biotechnol. Biofuels 2017, 10, 186. [Google Scholar] [CrossRef] [Green Version]
  26. Veerabadhran, M.; Gnanasekaran, D.; Wei, J.; Yang, F. Anaerobic digestion of microalgal biomass for bioenergy production, removal of nutrients and microcystin: Current status. J. Appl. Microbiol. 2021, 131, 1639–1651. [Google Scholar] [CrossRef] [PubMed]
  27. Baltrėnas, P.; Misevičius, A. Biogas production experimental research using algae. J. Environ. Health Sci. Eng. 2015, 13, 18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Figueroa-Torres, G.M.; Pittman, J.K.; Theodoropoulos, C. Optimisation of microalgal cultivation via nutrient-enhanced strategies: The biorefinery paradigm. Biotechnol. Biofuels 2021, 14, 64. [Google Scholar] [CrossRef] [PubMed]
  29. Benedetti, M.; Vecchi, V.; Barera, S.; Dall’Osto, L. Biomass from microalgae: The potential of domestication towards sustainable biofactories. Microb. Cell Fact. 2018, 17, 173. [Google Scholar] [CrossRef] [Green Version]
  30. Skorupskaite, V.; Makareviciene, V.; Levisauskas, D. Optimization of mixotrophic cultivation of microalgae Chlorella sp. for biofuel production using response surface methodology. Algal Res. 2015, 7, 45–50. [Google Scholar] [CrossRef]
  31. Costa, J.A.V.; Freitas, B.C.B.; Santos, T.D.; Mitchell, B.G.; Morais, M.G. Chapter 9—Open pond systems for microalgal culture. In Biomass, Biofuels, Biochemicals, Biofuels from Algae, 2nd ed.; Pandey, A., Chang, J.-S., Soccol, C.R., Lee, D.-J., Chisti, Y., Eds.; Elsevier: Amsterdam, The Netherlands, 2019; pp. 199–223. [Google Scholar] [CrossRef]
  32. Al-Dailami, A.; Koji, I.; Ahmad, I.; Goto, M. Potential of Photobioreactors (PBRs) in Cultivation of Microalgae. J. Adv. Res. App. Sc. Eng. Tech. 2022, 27, 32–44. [Google Scholar] [CrossRef]
  33. Ozkurt, I. Qualifying of safflower and algae for energy. Energy Educ. Sci. Technol. Part A 2009, 23, 145–151. [Google Scholar]
  34. Izadpanah, M.; Gheshlaghi, R.; Mahdavi, M.A.; Elkamel, A. Effect of light spectrum on isolation of microalgae from urban wastewater and growth characteristics of subsequent cultivation of the isolated species. Algal Res. 2018, 29, 154–158. [Google Scholar] [CrossRef]
  35. Maltsev, Y.; Maltseva, K.; Kulikovskiy, M.; Maltseva, S. Influence of Light Conditions on Microalgae Growth and Content of Lipids, Carotenoids, and Fatty Acid Composition. Biology 2021, 10, 1060. [Google Scholar] [CrossRef]
  36. Baer, S.; Heining, M.; Schwerna, P.; Buchholz, R.; Hübner, H. Optimization of spectral light quality for growth and product formation in different microalgae using a continuous photobioreactor. Algal Res. 2016, 14, 109–115. [Google Scholar] [CrossRef]
  37. Khan, M.I.; Shin, J.H.; Kim, J.D. The promising future of microalgae: Current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb. Cell Fact. 2018, 17, 36. [Google Scholar] [CrossRef] [PubMed]
  38. Grobbelaar, J.U. Algal nutrition. In Handbook of Microalgal Culture: Biotechnology and Applied Phycology; Richmond, A., Ed.; Blackwell: Oxford, UK, 2004; pp. 97–115. [Google Scholar]
  39. Carvalho, A.P.; Silva, S.O.; Baptista, J.M.; Malcata, F.X. Light requirements in microalgal photobioreactors: An overview of biophotonic aspects. Appl. Microbiol. Biotechnol. 2011, 89, 1275–1288. [Google Scholar] [CrossRef]
  40. Krzemińska, I.; Pawlik-Skowrońska, B.; Trzcińska, M.; Tys, J. Influence of photoperiods on the growth rate and biomass productivity of green microalgae. Bioprocess Biosyst. Eng. 2014, 37, 735–741. [Google Scholar] [CrossRef] [Green Version]
  41. Blanken, W.; Cuaresma, M.; Wijffels, R.H.; Janssen, M. Cultivation of microalgae on artificial light comes at a cost. Algal Res. 2013, 2, 333–340. [Google Scholar] [CrossRef]
  42. Radzun, K.A.; Wolf, J.; Jakob, G.; Zhang, E.; Stephens, E.; Ross, I.; Hankamer, B. Automated nutrient screening system enables high-throughput optimisation of microalgae production conditions. Biotechnol. Biofuels 2015, 8, 65. [Google Scholar] [CrossRef] [Green Version]
  43. Gao, K.; Xue, C.; Yang, M.; Li, L.; Qian, P.; Gao, Z.; Gao, Z.; Deng, X. Optimization of light intensity and photoperiod for growing Chlorella sorokiniana on cooking cocoon wastewater in a bubble-column bioreactor. Algal Res. 2022, 62, 102612. [Google Scholar] [CrossRef]
  44. Singh, S.P.; Singh, P. Effect of temperature and light on the growth of algae species: A review. Renew. Sust. Energy Rev. 2015, 50, 431–444. [Google Scholar] [CrossRef]
  45. Bechet, Q.; Laviale, M.; Arsapin, N.; Bonnefond, H.; Bernard, O. Modeling the impact of high temperatures on microalgal viability and photosynthetic activity. Biotechnol. Biofuels 2017, 10, 136. [Google Scholar] [CrossRef] [Green Version]
  46. Morales, M.; Sánchez, L.; Revah, S. The impact of environmental factors on carbon dioxide fixation by microalgae. FEMS Microbiol. Lett. 2018, 365, fnx262. [Google Scholar] [CrossRef] [Green Version]
  47. Bleeke, F.; Rwehumbiza, V.M.; Winckelmann, D.; Klöck, G. Isolation and Characterization of New Temperature Tolerant Microalgal Strains for Biomass Production. Energies 2014, 7, 7847–7856. [Google Scholar] [CrossRef] [Green Version]
  48. Serra-Maia, R.; Bernard, O.; Gonçalves, A.; Bensalem, S.; Lopes, F. Influence of temperature on Chlorella vulgaris growth and mortality rates in a photobioreactor. Algal Res. 2016, 18, 352–359. [Google Scholar] [CrossRef]
  49. Lam, M.K.; Lee, K.T. Potential of using organic fertilizer to cultivate Chlorella vulgaris for biodiesel production. Appl. Energy 2012, 94, 303–308. [Google Scholar] [CrossRef]
  50. Chowdury, K.; Nahar, N.; Deb, U. The Growth Factors Involved in Microalgae Cultivation for Biofuel Production: A Review. Comput. Water Energy Environ. Eng. 2020, 9, 185–215. [Google Scholar] [CrossRef]
  51. Gao, K. Approaches and involved principles to control pH/pCO2 stability in algal cultures. J. Appl. Phycol. 2021, 33, 3497–3505. [Google Scholar] [CrossRef]
  52. Shekh, A.; Sharma, A.; Schenk, P.M.; Kumar, G.; Mudliar, S. Microalgae cultivation: Photobioreactors, CO2 utilization, and value-added products of industrial importance. J. Chem. Technol. Biotechnol. 2022, 97, 1064–1085. [Google Scholar] [CrossRef]
  53. Ismaiel, M.M.S.; El-Ayouty, Y.M.; Piercey-Normore, M. Role of pH on antioxidants production by Spirulina (Arthrospira) platensis. Braz. J. Microbiol. 2016, 47, 298–304. [Google Scholar] [CrossRef] [Green Version]
  54. Sąsiadek, M.; Hawrot-Paw, M. Microalgae biomass production in vertical tubular photobioreactors. In Improvement of Technologies Agricultural Production, Including Renewable Energy, Taking into Account the Requirements of Sustainable Development; Romaniuk, W., Ed.; ITP: Warszawa-Falenty, Poland, 2021. (In Polish) [Google Scholar]
  55. Guillard, R.R.L.; Ryther, J.J. Studies of marine planktonic diatoms, I. Cyclotella nana Hustedt and Detonula confervacea (cleve) Gran. Can. J. Microbiol. 1962, 8, 229–239. [Google Scholar] [CrossRef]
  56. Li, Z.; Liu, Y.; Zhou, T.; Cao, L.; Cai, Y.; Wang, Y.; Cui, X.; Yan, H.; Ruan, R.; Zhang, Q. Effects of Culture Conditions on the Performance of Arthrospira platensis and Its Production of Exopolysaccharides. Foods 2022, 11, 2020. [Google Scholar] [CrossRef]
  57. Chaiklahan, R.; Chirasuwan, N.; Srinorasing, T.; Attasat, S.; Nopharatana, A.; Bunnag, B. Enhanced biomass and phycocyanin production of Arthrospira (Spirulina) platensis by a cultivation management strategy: Light intensity and cell concentration. Bioresour. Technol. 2022, 343, 126077. [Google Scholar] [CrossRef]
  58. Madkour, F.F.; Kamil, A.E.-W.; Nasr, H.S. Production and nutritive value of Spirulina platensis in reduced cost media. Egypt. J. Aquat. Res. 2012, 38, 51–57. [Google Scholar] [CrossRef] [Green Version]
  59. De Castro, G.F.P.S.; Rizzo, R.F.; Passos, T.S.; dos Santos, B.N.C.; Dias, D.S.; Domingues, J.R.; Araújo, K.G.L. Biomass production by Arthrospira platensis under different culture conditions. Food Science and Technology Biomass production by Arthrospira platensis under different culture conditions. Food Sci. Technol. 2015, 35, 18–24. [Google Scholar] [CrossRef] [Green Version]
  60. Vargas, S.R.; Zaiat, M.; Calijuri, M.d. Influence of Sulfur and Light Intensity in Nutrient Removal, and Hydrogen and Ethanol Production by Improved Biomass of Chlamydomonas reinhardtii in Batch Anaerobic Photobioreactors. Bioenerg. Res. 2022, 15, 218–229. [Google Scholar] [CrossRef]
  61. Abd El Baky, H.; El Baroty, G.S. Optimization cultivation of Chlamydomonas reinhardtii in a tubular photobioreactor (2000 Liter) for biomass and green bioenergy (biodiesel) production. Not. Bot. Horti Agrobot. 2020, 48, 1439–1457. [Google Scholar] [CrossRef]
  62. Singh, S.P.; Singh, P. Effect of CO2 concentration on algal growth: A review. Renew. Sust. Energ. Rev. 2014, 38, 172–179. [Google Scholar] [CrossRef]
  63. Filali, R.; Tian, H.; Micheils, E.; Taidi, B. Evaluation of the Growth Performance of Microalgae Based on Fine pH Changes. Austin J. Biotechnol. Bioeng. 2021, 8, 1109. [Google Scholar]
  64. Ratomski, P.; Hawrot-Paw, M. Production of Chlorella vulgaris Biomass in Tubular Photobioreactors during Different Culture Conditions. Appl. Sci. 2021, 11, 3106. [Google Scholar] [CrossRef]
  65. Xu, Y.; Ibrahim, I.M.; Harvey, P.J. The influence of photoperiod and light intensity on the growth and photosynthesis of Dunaliella salina (chlorophyta) CCAP 19/30. Plant Physiol. Biochem. 2016, 106, 305–315. [Google Scholar] [CrossRef] [Green Version]
  66. Ras, M.; Steyer, J.P.; Bernard, O. Temperature effect on microalgae: A crucial factor for outdoor production. Rev. Environ. Sci. Biotechnol. 2013, 12, 153–164. [Google Scholar] [CrossRef] [Green Version]
  67. Gastelum-Franco, J.; Esparza-Leal, H.; García-Ulloa, M.; López-Álvarez, E.; Muy-Rangel, M.; Pérez-Rubio, V.; Ulloa-Mercado, R.; Montiel-Montoya, J. Preliminary evaluation of the green microalga Dunaliella salina as a potential feedstock for biodiesel: Effect of molasses on growth and lipid profile. Lat. Am. J. Aquat. Res. 2021, 49, 763–772. [Google Scholar] [CrossRef]
  68. Lv, H.; Wang, Q.E.; Wang, S.; Qi, B.; He, J.; Jia, S. Enhancing biomass production of Dunaliella salina via optimized combinational application of phytohormones. Aquaculture 2019, 503, 146–155. [Google Scholar] [CrossRef]
  69. Morowvat, M.H.; Ghasemi, Y. Culture medium optimization for enhanced β-carotene and biomass production by Dunaliella salina in mixotrophic culture. Biocatal. Agric. Biotechnol. 2016, 7, 217–223. [Google Scholar] [CrossRef]
  70. Ahmed, R.A.; He, M.; Aftab, R.A.; Zheng, S.; Nagi, M.; Bakri, R.; Wang, C. Bioenergy application of Dunaliella salina SA 134 grown at various salinity levels for lipid production. Sci. Rep. 2017, 7, 8118. [Google Scholar] [CrossRef] [Green Version]
  71. Kim, W.; Park, J.M.; Gim, G.H.; Jeong, S.H.; Kang, C.M.; Kim, D.J.; Kim, S.W. Optimization of culture conditions and comparison of biomass productivity of three green algae. Bioprocess Biosyst. Eng. 2012, 35, 19–27. [Google Scholar] [CrossRef]
  72. Saxena, R.; Rodríguez-Jasso, R.M.; Chávez-Gonzalez, M.L.; Aguilar, C.N.; Quijano, G.; Ruiz, H.A. Strategy Development for Microalgae Spirulina platensis Biomass Cultivation in a Bubble Photobioreactor to Promote High Carbohydrate Content. Fermentation 2022, 8, 374. [Google Scholar] [CrossRef]
  73. Hussin, A.A.; To, S.W.; Sani, M.H.; Amin, M.F.M.; Kamaroddin, M.F. Optimisation and growth kinetic analysis of Microalgae, Arthrospira platensis in 2-L Photobioreactors. In Proceedings of the 3rd International Conference on Tropical Resources and Sustainable Sciences, Kelantan, Malezja, 14–15 July 2021; Volume 842, p. 012036. [Google Scholar] [CrossRef]
  74. Bao, Y.; Wen, S.; Cong, W.; Wu, X.; Ning, Z. An Optical-Density-Based Feedback Feeding Method for Ammonium Concentration Control in Spirulina platensis Cultivation. J. Microbiol. Biotechnol. 2012, 22, 967–974. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Li, X.; Slavens, S.; Crunkleton, D.W.; Johannes, T.W. Interactive effect of light quality and temperature on Chlamydomonas reinhardtii growth kinetics and lipid synthesis. Algal Res. 2021, 53, 102127. [Google Scholar] [CrossRef]
  76. Zhu, Z.; Cao, H.; Li, X.; Rong, J.; Cao, X.; Tian, J. A Carbon Fixation Enhanced Chlamydomonas reinhardtii Strain for Achieving the Double-Win Between Growth and Biofuel Production Under Non-stressed Conditions. Front. Bioeng. Biotechnol. 2021, 8, 603513. [Google Scholar] [CrossRef]
  77. Ammar, S.H. Cultivation of Microalgae Chlorella vulgaris in Airlift photobioreactor for Biomass Production using commercial NPK Nutrients. Al-Khawarizmi Eng. J. 2016, 12, 90–99. [Google Scholar]
  78. Deniz, I. Determination of growth conditions for Chlorella vulgaris. Mar. Sci. Tech. Bull. 2020, 9, 114–117. [Google Scholar] [CrossRef]
  79. Akter, R.; Hossain, S.M.M.; Zhe, W.; Kermanee, P.; Juntawong, N. Enhanced lipid production in Dunaliella salina grown under high light intensity by shifting the culture from high to low nitrogen concentration. Adv. Environ. Biol. 2016, 10, 18–29. [Google Scholar]
  80. Demirel, Z. Monitoring of growth and biochemical composition of Dunaliella salina and Dunaliella polymorpha in different photobioreactors. Aquat. Res. 2022, 5, 136–145. [Google Scholar] [CrossRef]
  81. Saha, S.K.; Kazipet, N.; Murray, P. The Carotenogenic Dunaliella salina CCAP 19/20 Produces Enhanced Levels of Carotenoid under Specific Nutrients Limitation. Biomed Res. Int. 2018, 2018, 7532897. [Google Scholar] [CrossRef] [Green Version]
  82. Guidi, F.; Gojkovic, Z.; Venuleo, M.; Assunçao, P.A.C.J.; Portillo, E. Long-Term Cultivation of a Native Arthrospira platensis (Spirulina) Strain in Pozo Izquierdo (Gran Canaria, Spain): Technical Evidence for a Viable Production of Food-Grade Biomass. Processes 2021, 9, 1333. [Google Scholar] [CrossRef]
  83. Banerjee, S.; Ray, A.; Das, D. Optimization of Chlamydomonas reinhardtii cultivation with simultaneous CO2 sequestration and biofuels production in a biorefinery framework. Sci. Total Environ. 2021, 762, 143080. [Google Scholar] [CrossRef]
  84. Kong, Q.X.; Li, L.; Martinez, B.; Chen, P.; Ruan, R. Culture of Microalgae Chlamydomonas reinhardtii in Wastewater for Biomass Feedstock Production. Appl. Biochem. Biotechnol. 2010, 160, 9. [Google Scholar] [CrossRef] [PubMed]
  85. Anyanwu, R.C.; Rodriguez, C.; Durrant, A.; Olabi, A.G. Evaluation of Growth Rate and Biomass Productivity of Scenedesmus quadricauda and Chlorella vulgaris under Different LED Wavelengths and Photoperiods. Sustainability 2022, 14, 6108. [Google Scholar] [CrossRef]
  86. Amini Khoeyi, Z.; Seyfabadi, J.; Ramezanpour, Z. Effect of light intensity and photoperiod on biomass and fatty acid composition of the microalgae, Chlorella vulgaris. Aquacult. Int. 2012, 20, 41–49. [Google Scholar] [CrossRef]
  87. Abarna, K.M.; Velu, R.; Padmavathy, P.; Jawahar, P.; Uma, A.; Kalidas, C.; Shukla, S.P. Effect of seaweed-based liquid extracts on biomass production and lipid accumulation in Nannochloropsis oculata and Dunaliella salina. Turk. J. Bot. 2022, 46, 4. [Google Scholar] [CrossRef]
  88. Borovkov, A.B.; Gudvilovich, I.N.; Avsiyan, A.L. Scale-up of Dunaliella salina cultivation: From strain selection to open ponds. J. Appl. Phycol. 2020, 32, 1545–1558. [Google Scholar] [CrossRef]
  89. Barten, R.; Djohan, Y.; Evers, W.; Wijffels, R.; Barbosa, M. Towards industrial production of microalgae without temperature control: The effect of diel temperature fluctuations on microalgal physiology. J. Biotechnol. 2021, 336, 56–63. [Google Scholar] [CrossRef]
  90. Maroneze, M.M.; Siqueira, S.F.; Vendruscolo, R.G.; Wagner, R.; de Menezes, C.R.; Zepka, L.Q.; Jacob-Lopes, E. The role of photoperiods on photobioreactors—A potential strategy to reduce costs. Bioresour. Technol. 2016, 219, 493–499. [Google Scholar] [CrossRef] [PubMed]
  91. Atta, M.; Idris, A.; Bukhari, A.; Wahidin, S. Intensity of blue LED light: A potential stimulus for biomass and lipid content in fresh water microalgae Chlorella vulgaris. Bioresour. Technol. 2013, 148, 373–378. [Google Scholar] [CrossRef] [PubMed]
  92. Kato, Y.; Fujihara, Y.; Vavricka, C.J.; Chang, J.-S.; Hasunuma, T.; Kondo, A. Light/dark cycling causes delayed lipid accumulation and increased photoperiod-based biomass yield by altering metabolic flux in oleaginous Chlamydomonas sp. Biotechnol. Biofuels 2019, 12, 39. [Google Scholar] [CrossRef]
  93. Moazami-Goudarzi, M.; Colman, B. Changes in carbon uptake mechanisms in two green marine algae by reduced seawater pH. J. Exp. Mar. Biol. Ecol. 2012, 413, 94–99. [Google Scholar] [CrossRef]
  94. Elalami, D.; Oukarroum, A.; Barakat, A. Anaerobic digestion and agronomic applications of microalgae for its sustainable valorization. RSC Adv. 2021, 11, 26444–26462. [Google Scholar] [CrossRef]
  95. Schagerl, M.; Siedler, R.; Konopáčová, E.; Ali, S.S. Estimating Biomass and Vitality of Microalgae for Monitoring Cultures: A Roadmap for Reliable Measurements. Cells 2022, 11, 2455. [Google Scholar] [CrossRef] [PubMed]
  96. Ivanov, I.N.; Zachleder, V.; Vítová, M.; Barbosa, M.J.; Bišová, K. Starch Production in Chlamydomonas reinhardtii through Supraoptimal Temperature in a Pilot-Scale Photobioreactor. Cells 2021, 10, 1084. [Google Scholar] [CrossRef] [PubMed]
  97. Sharma, R.; Singh, G.P.; Sharma, V.K. Effects of Culture Conditions on Growth and Biochemical Profile of Chlorella Vulgaris. J. Plant Pathol. Microb. 2012, 3, 1000131. [Google Scholar] [CrossRef] [Green Version]
  98. Ratomski, P.; Hawrot-Paw, M. Influence of Nutrient-Stress Conditions on Chlorella vulgaris Biomass Production and Lipid Content. Catalysts 2021, 11, 573. [Google Scholar] [CrossRef]
  99. Griffiths, M.J.; Garcin, C.; van Hille, R.P.; Harrison, S.T.L. Interference by pigment in the estimation of microalgal biomass concentration by optical density. J. Microbiol. Methods 2011, 85, 119–123. [Google Scholar] [CrossRef]
  100. Chioccioli, M.; Hankamer, B.; Ross, I.L. Flow Cytometry Pulse Width Data Enables Rapid and Sensitive Estimation of Biomass Dry Weight in the Microalgae Chlamydomonas reinhardtii and Chlorella vulgaris. PLoS ONE 2014, 9, e97269. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  101. Srirangan, S.; Sauer, M.L.; Howard, B.; Dvora, M.; Dums, J.; Backman, P.; Sederoff, H. Interaction of Temperature and Photoperiod Increases Growth and Oil Content in the Marine Microalgae Dunaliella viridis. PLoS ONE 2015, 10, e0127562. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  102. Havlik, I.; Beutel, S.; Scheper, T.; Reardon, K.F. On-Line Monitoring of Biological Parameters in Microalgal Bioprocesses Using Optical Methods. Energies 2022, 15, 875. [Google Scholar] [CrossRef]
Energies 16 02429 g001 550
Figure 1. Microalgae cultivation system.
Figure 1. Microalgae cultivation system.
Energies 16 02429 g001
Energies 16 02429 g002 550
Figure 2. The average amount of microalgal biomass during different cultivation conditions. Different letters above the error bars (i.e., ±SD) indicate significant differences (p < 0.05) between the means; means followed by the same letter do not statistically differ from each other (Tukey’s post-hoc test).
Figure 2. The average amount of microalgal biomass during different cultivation conditions. Different letters above the error bars (i.e., ±SD) indicate significant differences (p < 0.05) between the means; means followed by the same letter do not statistically differ from each other (Tukey’s post-hoc test).
Energies 16 02429 g002
Energies 16 02429 g003a 550Energies 16 02429 g003b 550
Figure 3. The average optical density during different cultivation conditions. Different letters above the error bars (i.e., ±SD) indicate significant differences (p < 0.05) between the means; means followed by the same letter do not statistically differ from each other (Tukey’s post-hoc test).
Figure 3. The average optical density during different cultivation conditions. Different letters above the error bars (i.e., ±SD) indicate significant differences (p < 0.05) between the means; means followed by the same letter do not statistically differ from each other (Tukey’s post-hoc test).
Energies 16 02429 g003aEnergies 16 02429 g003b
Table
Table 1. Microalgal biomass production parameters.
Table 1. Microalgal biomass production parameters.
Photobioreactor
Capacity [L]		CO2
Dose		Light Intensity
[µmol m−2 s−1]		Temperature
[°C]		Photoperiod
[h; Light/Dark]		pH
2.5atmospheric concentration1302012/127
2516/88
3024/09
Table
Table 2. Comparison of microalgal biomass production during different cultivation conditions.
Table 2. Comparison of microalgal biomass production during different cultivation conditions.
MicroalgaeCultivation ConditionsAmount of Biomass [g·L−1]Photobioreactor
Type/Capacity [L]		References
Temperature [°C]Photoperiod [h/h Light/Dark]pH
A. platensis2012/1284.24Tubular: 2.5This study
Not controlled13/119–100.93Bubble 10.1[72]
Room temp.24/091.50Bubble: 2[73]
3024/09.63.06Airlift: 2.5[74]
Ch. reinchardtii3018/67–81.19Tubular; 2.5This study
24–32n.r 1n.r0.5–0.7Flask; 0.25[75]
3224/06.21.07Flask; 0.5[60]
2514/10n.r.1.74Flat plate; 1.5[76]
C. vulgaris2518/682.37Tubular; 2.5This study
25n.r70.824Baffled; 5[63]
20–2520/44–70.317Airlift; 6.6[77]
2524/090.150–0.205Flask; 0.25[78]
D. salina2012/1284.50Tubular; 2.5This study
25n.rn.r2.13Bubble; 0.25[79]
2018/6n.r0.801Bubble; 2[80]
2216/87.70.025Flask; 0.25[81]
1 n.r–not reported.
Table
Table 3. Comparison of microalgal biomass productivity.
Table 3. Comparison of microalgal biomass productivity.
Temperature
[°C]		Photoperiod
[Light/Dark]		pHBiomass Productivity
[g·L−1·d−1]
Arthrospira
platensis		Chlamydomonas
reinchardtii		Chlorella
vulgaris		Dunaliella
salina
70.69 ± 0.030.06 ± 0.010.10 ± 0.000.77 ± 0.03
12/1280.72 ± 0.040.07 ± 0.000.11 ± 0.010.81 ± 0.04
90.68 ± 0.030.06 ± 0.010.12 ± 0.030.74 ± 0.03
70.66 ± 0.030.08± 0.010.29 ± 0.020.72 ± 0.03
2018/680.63 ± 0.030.08 ± 0.010.30 ± 0.020.69 ± 0.02
90.66 ± 0.030.08 ± 0.010.26 ± 0.010.71 ± 0.03
70.50 ± 0.030.10 ± 0.020.20 ± 0.000.59 ± 0.03
24/080.50 ± 0.020.11± 0.010.19 ± 0.000.60 ± 0.03
90.53 ± 0.020.11 ± 0.010.20 ± 0.000.64 ± 0.02
70.67 ± 0.030.08 ± 0.010.10 ± 0.010.75 ± 0.04
12/1280.66 ± 0.020.08 ± 0.010.10 ± 0.010.71 ± 0.03
90.65 ± 0.030.08 ± 0.010.10 ± 0.010.72 ± 0.03
70.65 ± 0.020.11 ± 0.010.27 ± 0.010.71 ± 0.03
2518/680.65 ± 0.020.12 ± 0.010.36 ± 0.010.71 ± 0.03
90.59 ± 0.020.10 ± 0.010.31 ± 0.010.65 ± 0.02
70.51 ± 0.020.12 ± 0.020.19 ± 0.000.61 ± 0.03
24/080.56 ± 0.030.12 ± 0.010.20 ± 0.000.67 ± 0.03
90.49 ± 0.030.10 ± 0.010.20 ± 0.000.58 ± 0.04
70.69 ± 0.020.08 ± 0.010.10 ± 0.010.77 ± 0.03
12/1280.62 ± 0.020.11 ± 0.010.11 ± 0.020.69 ± 0.03
90.64 ± 0.030.09 ± 0.000.11 ± 0.000.71 ± 0.03
70.60 ± 0.020.08 ± 0.010.27 ± 0.010.65 ± 0.02
3018/680.63 ± 0.030.10 ± 0.010.28 ± 0.010.68 ± 0.03
90.61 ± 0.020.10 ± 0.010.29 ± 0.010.65 ± 0.02
70.47 ± 0.020.10 ± 0.010.20 ± 0.010.56 ± 0.02
24/080.49 ± 0.030.10 ± 0.010.19 ± 0.000.59 ± 0.03
90.47 ± 0.020.08 ± 0.010.20 ± 0.010.56 ± 0.02
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Hawrot-Paw, M.; Sąsiadek, M. Optimization of Microalgal Biomass Production in Vertical Tubular Photobioreactors. Energies 2023, 16, 2429. https://doi.org/10.3390/en16052429

AMA Style

Hawrot-Paw M, Sąsiadek M. Optimization of Microalgal Biomass Production in Vertical Tubular Photobioreactors. Energies. 2023; 16(5):2429. https://doi.org/10.3390/en16052429

Chicago/Turabian Style

Hawrot-Paw, Małgorzata, and Magdalena Sąsiadek. 2023. "Optimization of Microalgal Biomass Production in Vertical Tubular Photobioreactors" Energies 16, no. 5: 2429. https://doi.org/10.3390/en16052429

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop