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Review

A Critical Review of Growth Media Recycling to Enhance the Economics and Sustainability of Algae Cultivation

by
Neha Arora
,
Enlin Lo
,
Noah Legall
and
George P. Philippidis
*
Patel College of Global Sustainability, University of South Florida, Tampa, FL 33620, USA
*
Author to whom correspondence should be addressed.
Energies 2023, 16(14), 5378; https://doi.org/10.3390/en16145378
Submission received: 28 June 2023 / Revised: 11 July 2023 / Accepted: 13 July 2023 / Published: 14 July 2023
(This article belongs to the Special Issue Advances in Bioenergy)
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Abstract

:
Microalgae hold promise as a sustainable source of biofuels and bioproducts but their commercial development is impeded by high cultivation costs, primarily for growth nutrients, and concerns about the water-intensive nature of algae cultivation. As a result, minimizing water and nutrient input is imperative to reducing algal operating costs, while enhancing the sustainability of future algal biorefineries. However, spent media recycling often results in the accumulation of growth inhibitors, such as free fatty acids, polysaccharides, polyunsaturated aldehydes, and humic acid, which negatively affect algal growth and productivity. In this review, we critically assess media recycling research findings to assess the advantages and disadvantages of spent media reuse for a wide range of algae strains. Particular emphasis is placed on strategies to overcome growth inhibition through spent media treatment processes, such as ultraviolet oxidation, activated carbon, ultrasonication, microfiltration, crop rotation, and nutrient replenishment.

1. Introduction

Photosynthetic microalgae as a source of biofuels and bioproducts are a promising alternative to non-renewable fossil-based materials. Advancements in technology, including enhanced cultivation systems, engineered strains for higher productivity, media development, and specialized downstream processing techniques have paved the way for a sustainable bioeconomy facilitated by algae. The global biofuels and bioproducts market, where algae can compete, is estimated at USD 3.4 billion and expected to increase at a compound annual growth rate (CAGR) of 4.3% [1]. However, only a few algae-based materials, particularly carotene, astaxanthin, and omega-3-fatty acids, have been commercialized to date [2]. The significant amounts of water associated with algae farming is one of the key issues impeding the commercialization of algae biorefineries, so effective water use is critical to reducing the environmental impact [3]. Water usage in algal cultivation is typically estimated in terms of water demand required for operating the algal production process [4]. The volume of freshwater required to manufacture the desired product per functional unit (such as algal biomass, biofuel, or bioproduct) is referred to as the water footprint (WF) [5]. It includes both direct (process) and indirect (nutrient- and energy-related) water consumption in the algal process [3]. The total WF comprises both consumptive and degradative freshwater use [6]. The consumptive WF consists of green water, which is freshwater lost due to evaporation and gained through precipitation, and blue water, which is surface and ground freshwater used, while the degradative WF is gray water, which is water containing pollutants generated during the manufacturing process that needs to meet certain water disposal quality standards [7]. Notably, the blue water footprint can vary depending on the algal process, while the gray water footprint changes based on the local water disposal standards [8]. Water is used in algae biomass production during cultivation in an open raceway pond or a photobioreactor, harvesting, and product extraction, so all individual water uses across the algal process are added up to compute the total WF of the biorefinery [9]. A recent study compared the blue WF of algae biomass cultivated in southwestern regions of the United States to be from 127–256 m3 water/ton (metric), which is two times lower than other biofuel crops, such as corn (492–879 m3 water/ton), barley (955–1054 m3 water/ton), and sorghum (598–1063 m3 water/ton) [10]. However, the WF of algal biofuels (11.2 m3/GJ) is five times higher than petroleum-based fuels (1.54 m3/GJ), although it is significantly lower than biodiesel feedstocks, such as soybean (216 m3/GJ) and rapeseed (298 m3/GJ) [10]. Previous research on measuring the direct WF of algal biofuels reported values ranging from 33.0 m3 GJ−1 in a Mediterranean environment to 36.7 m3 GJ−1 in tropical settings [4]. More importantly, a significant drop was reported in WF, when 90% recycled water was used (20.7 m3 GJ−1) in tropical climates. Another study found that when 90% of the water used for PBR cultivation was reused, the WF decreased by 1.7-fold [3]. Furthermore, when water was recycled back to a Chlorella PBR culture, water usage was reduced by 93% [11].
Algae production in photobioreactors (PBRs) typically requires 200–500 kg of water per kg of dry biomass, which increases by an additional 200 kg, when algae are grown outdoors in open raceway ponds [12]. Moreover, the cultivation, harvesting, and extraction steps collectively account for 97.6% of the total blue WF of the algal process [5]. Even if marine algae are utilized for cultivation, hence replacing freshwater with seawater, large amounts of freshwater are still required to compensate for evaporation losses. Although the exact volume of water required for algal cultivation varies depending on the type/geometry of the cultivation system and the local climate conditions influencing evaporative losses, it is widely recognized that water use for algae cultivation is high. To reduce the WF of an algae biorefinery, it is critical to recycle and reuse the water released after cultivation/harvesting, which is often referred to as spent media. Following algal harvesting, around 84% of the water is discharged, while the remainder is lost to evaporation [13]. Media recycling helps reduce water use and also enables nutrient recycling, as significant amounts of residual nutrients are still present in spent media, but growth inhibition is often reported in recycled media and needs to be addressed [14,15]. According to life cycle assessment (LCA) research, reusing media could minimize freshwater and nutrient use by 84% and 55%, respectively [13]. Furthermore, employing wastewater can minimize freshwater use by 93.7%, with as little as 219 kg water consumed per kg of algal biodiesel produced [11]. It is important to note that, although the unutilized nutrients can be recycled back, it is still necessary to replenish used nutrients with fresh ones. To further cut down the cost of nutrients, food waste and other non-toxic residue streams can be employed to make the algal cultivation more sustainable and cost competitive. Techno-economic analysis (TEA) of food waste valorization (hydrolysate) for docosahexaenoic acid (DHA) from Aurantiochytrium sp. showed a reduction in operating cost of 35% [16]. Another study also reported a reduction in algal cultivation costs, when food waste hydrolysate was used [17].
The objective of this review is to assess the opportunities and challenges for media recycling during algae cultivation by cataloguing the benefits and drawbacks spent media represent for the growth and biochemical composition of various algal species of commercial interest (Figure 1). Particular emphasis is placed on investigating the allelopathic mechanism of growth inhibitors and identifying potential strategies for improving the recycling of spent media.

2. Effect of Media Recycling on Algal Growth and Biochemical Composition

The impact of recycled media on algae growth and productivity depends on the algal species, growth conditions, and treatment of water (if any) before recycling [18]. Indeed, employment of media recycling has been reported to affect the growth and biochemical composition of numerous algal species, thus influencing the quality and economics of the target end product, as summarized in Table 1.
Chlorella is an industrial strain extensively investigated for media recycling due to its rapid growth and ability to assimilate both ammonium and nitrate as nitrogen sources [29]. C. vulgaris 221/19SAG biomass productivity experienced no negative effect, when cultivated in recycled high assimilable minimal growth medium (HAMGM) (Table 1), where ions (such as Na+, K+, Ca2+, and NH4+) were found to accumulate intracellularly when the strain was continuously cultivated in recycled media for 56 days [29]. Similarly, C. vulgaris UTEX265 was able to maintain its biomass yield at 2 g L−1 for the first two cycles of recycling in BG-11 media over 12 days with an initial nitrate concentration of 6 mM (Table 1). However, the accumulation of total organic carbon (TOC) increased to 642 mg L−1, which inhibited growth during the third cycle, causing biomass production to decrease by a significant 75% [30]. In another study, when the cultivation media for Chlorella zofingiensis were harvested using a centrifuge and 100% or 50% of the media were recycled, fresh nutrient supplementation was required to enable two growth cycles without compromising productivity [42]. A marine Nannochloropsis sp., a promising source of polyunsaturated fatty acids, was used to study media recycling at outdoor pilot scale of 24,000 L, maintaining its growth rate during long-term cultivation (167 days) in 80% continuously recycled media after centrifugation and sand filtration pretreatment [48]. Ankistrodesmus sp., when harvested via centrifugation after 14 days of cultivation and recultivated in recycled media twice in a row, reached a biomass yield of approximately 1.0 g L−1, which was 34% higher than that in fresh media and 30% higher in the second cycle than in the first one [20]. These findings, however, seemed to be the result of initial nutrient levels (nitrogen and phosphorus) being excessively high, thus negatively affecting algal growth in fresh media compared to the subsequent cultivation is spent media. Tetradesmus obliquus was also subjected to media recycling, where the cultivation media were separated from the biomass by gravity sedimentation at 4 °C, and 50% spent media were used in each new cycle (Table 1). No negative effects were reported, which can be attributed to successful adaptation of the cells to the spent media environment [57].
Flocculation is one of the harvesting methods considered to be cost-effective by reducing high energy consumption compared to centrifugation [58]. Flocculation based on pH changes was applied to three freshwater algae (C. vulgaris, Scenedesmus sp., Chlorococcum sp.) and two marine algae (Nannochloropsis oculata, Phaeodactylum tricornutum) (Table 1). Even though magnesium hydroxide formation reduced flocculation efficiency, nutrient supplementation and pH neutralization enabled the recycled medium to maintain the algal growth (dry cell weight of 2.0–3.8 g L−1) at levels comparable to that of a fresh medium [28]. Bacterial flocculation was also investigated as a means of harvesting C. vulgaris, where bacterial proteins contributed to the flocculation effect (Table 1). During the first 15 days of cultivation, the growth rate in recycled BG-11 media was higher than that in fresh media, due to one of the bacterial communities having a growth-promoting effect on algae by reducing the stress level caused when reactive oxygen species (ROS) accumulate in algal cells at the early stage of cultivation [32]. However, in the second cycle of cultivation, a 50% decrease in growth was observed due to high ROS concentration. Algae are known to accumulate ROS as a result of environmental stressors, such as variations in cultivation conditions, exposure to high exopolysaccharides concentrations due to media recycling, and presence of heavy metals [33,59]. ROS build-up in algae may affect carbon partitioning and autophagy processes, ultimately leading to enhanced lipid accumulation [60]. The involvement of nitric oxide (NO) in the signal transduction pathway is facilitated by its ability to modulate the signaling of ROS. This modulation leads to the activation of the antioxidant system, which is achieved by increasing the content of glutathione (GSH). The primary purpose of this activation is to counteract the oxidative damage caused by environmental stress [60]. It has also been noted that algae exhibit the capacity to synthesize antioxidants, thereby mitigating the effects of ROS and safeguarding against oxidative damage of the cellular membrane [33,60]. In another study, using a combination of electro-flocculation and centrifugation, Tetraselmis sp. was harvested from a 3600-L outdoor open raceway pond (Table 1). Although salinity climbed to 12% during continuous recycling, ash-free dried weight increased in dissolved organic carbon (DOC) -enriched media under mixotrophic conditions [56]. When recycled media were used to cultivate C. vulgaris after biomass harvesting with the magnetic flocculant Fe3O4-chitosan, biomass yield of 1.05 g L−1 was achieved in 50% spent media. The results also demonstrated a higher biomass production when the algae were grown in 100% recycled media compared to fresh media, indicating that Fe3O4-chitosan had no negative effect on growth and that the culture medium could be reused for recultivation [39].
Although the above-mentioned studies reported no negative effect of media recycling, numerous other studies have shown that recycling cultivation media inhibit algal growth because of: (1) Accumulation of extracellular substances released during cultivation; (2) Bacterial accumulation [15,33]. More specifically, Staurosira sp. biomass production decreased by more than 50% in recycled media compared to fresh media [15]. Interestingly, Auxenochlorella protothecoides, an auxotroph that requires thiamine supplementation, was able to utilize the spent media generated by Chlorella sorokiniana, which contains thiamine metabolites that alleviated thiamine deficiency [61].
During cultivation in recycled media, algae modify their metabolism in order to regulate their biochemical composition based on the composition of the medium and the growth conditions [33]. Lipids and carbohydrates are primary forms of energy storage in algal cells, and their biosynthesis tends to increase in response to environmental stress in order to maintain homeostasis and metabolic functions [62]. That effect was observed in C. vulgaris UTEX 395, where carbohydrate content increased 11% during cultivation in 100% spent media as a result of stress attributed to limited access to nutrients caused by accumulating extracellular polymeric substances in the recycled media [33]. Compared to fresh media, the lipid content of Ankistrodesmus sp. was found to be 23% and 13% higher in the first and second reuse cycles, respectively, indicating that recycled media exerted greater nutrient stress than fresh media [20]. Similar results were observed in Tetradesmus obliquus and Chlorella zofingiensis, where higher lipid content was recorded in recycled media than in fresh media [42,57]. Interestingly, the fatty acid profile of Aurantiochytrium sp. shifted towards saturated fatty acids, when grown in spent media wastewater under salinity stress, which proves to be advantageous for biodiesel production [23]. The protein content of algae is also impacted by environmental and nutritional conditions in the culture medium, as nitrogen assimilation is directly associated with protein synthesis [21,33]. A study reported that 55% of the nutrients in fresh media were not utilized and could potentially be recycled for subsequent cultivation, where a 20% increase in the protein content of C. vulgaris was observed during the third recycling cycle [36]. However, further cycles experienced a decline in nitrogen accessibility, eventually leading to a reduction in protein content [36]. A comparable finding was reported in Arthrospira platensis, where the protein content increased 11%, when cultivated in spent media after flocculation and adsorption, compared to fresh media [21]. Certain algae species have been reported to increase biosynthesis of pigments and valuable bioactive substances, such as carotenoids, in spent media [63]. Under stressful cultivation conditions, C. vulgaris exhibited a 4% increase in carotenoid levels, which served as an antioxidant protecting the cells from the stress experienced in spent media [33]. A similar outcome was also found in Dunaliella salina that was grown in an outdoor open pond and subjected to media recycling [44].

3. Impact of Auto-Inhibitors on Algal Growth

Algae growing at high densities accumulate and release chemicals that restrict growth, resulting in allelopathy that limits productivity and, hence, the number of times growth media can be recycled [64]. Such auto-inhibitory compounds are released by cellular debris or via algogenic organic matter (AOM), such as free fatty acids (FFA), polysaccharides, proteins, and other nitrogenous substances [29]. In closed PBRs, algae can release up to 17% of AOM in the media with each cultivation cycle contributing 60–80 mg L−1 [65]. AOM secretion can limit growth, promote cell aggregation, and alter biochemical composition, thus resulting in lower algal productivity [51]. Furthermore, AOM accumulation increases the dissolved organic matter (DOM) in recycled media, increasing the likelihood of bacterial contamination and culture crashes. Additionally, culturing algae in recycled media alters population dynamics, resulting in a larger load of ciliates, amoebae, and rotifers in spent media because higher DOM may support more microzooplankton [66]. Such changes in the dynamics of the culture microbiota cause recurrent culture crashes.
Initial identification of the auto-inhibitory compound chlorellin was reported many years ago in cultures of C. vulgaris [67]. Auto-inhibitors were later discovered in Haematococcus pluvialis and Skeletonrma costatum cultures [68,69,70]. Similarly, 1-[hydroxyl-diethyl malonate]-isopropyl dodecenoic acid was discovered in cultures of Isochrysis galbana, hindering its growth and the growth of eight other algal species in a dose-dependent manner [71]. The main auto-inhibitory compounds present in recycled media include humic acid/fluvic acid-like substances, aromatic proteins (N-acyl-homoserine lactone), free fatty acids, such as palmitic, oleic, linoleic, and α-linolenic acid, polyunsaturated aldehydes, cyclic peptides (microcystins and nodularins), and exopolysaccharides (EPS) [33,72]. These auto-inhibitory chemicals can interfere with protein/enzyme activity and photosynthesis, cause cell membrane damage and cell lysis, or reduce nutrient uptake [73].
Humic acid/fluvic acid-like substances are produced during cell rupture and degradation and can form complexes with trace metals, thereby limiting their bioavailability to growing cells, impeding algal growth, and causing cellular aggregation [47]. Humic acid has been shown to limit the growth of Anabena circinalis at concentrations as low as 1 mg L−1 [74]. Furthermore, humic compounds in culture media can release free radicals, which inactivate catalases inside algal cells, resulting in H2O2 build-up that causes oxidative damage and cell death [75]. The concentration of humic compounds has been shown to increase with algal growth, peaking in the stationary and decline stages [76]. In the same study, adding humic compounds (5–50 mg L−1) to Scenedesmus acuminatus cultures reduced growth rates by 4.3% to 70.3%. Thus, harvesting algal biomass before the culture enters the stationary phase could be one strategy to limit the accumulation of humic acid.
The presence of free fatty acids (FFA) in recycled media inhibits algal development by disrupting the electron transport system of photosynthesis, causing plasma membrane instability, and leading to K+ leakage and subsequent cellular organization breakdown [73]. The addition of palmitic acid and oleic acid to fresh media at concentrations similar to those measured in spent media decreased the growth in S. acuminatus by 6.05% and 14.66%, respectively [14]. Similarly, a recent study evaluated the allelopathy effects of the FFAs oleic and linolenic acid on five different algal strains [64]. Notably, the authors reported that sensitivity to FFAs varied among the investigated algal species with Botrycoccus braunii showing the least growth inhibition in the presence of oleic acid, whereas S. acuminatus showed the least growth inhibition in the presence of linolenic acid.
The polyunsaturated aldehydes (PUA) 2E,4E/Z-heptadienal, 2E,4E/Z-octadienal, 2E,4E/Z,7Z-octatrienal, 2E,4E/Z-decadienal, and 2E,4E/Z,7Z decatrienal have been reported to be the most toxic oxylipins with auto-inhibitory effects on several algal species belonging to various taxonomic groups, including Prasinophyceae (unicellular green algae), Prymnesiophyceae (Haptophyta), Dinophyceae (Dinoflagellates), Chlorophyceae (green algae), and Bacillariophyceae (diatoms) [77]. Algal cell exposure to PUAs causes programmed cell death and cell lysis [78]. On the other hand, cell aggregation is caused by EPS synthesis, as it inhibits mass transfer, reducing nutrient uptake, gas exchange, and light penetration into algal cells. Our own previous research found that C. vulgaris uptake of macronutrients (nitrate and phosphate) decreases, when the alga is grown in spent media compared to fresh media [33]. Cellular aggregation was also found in Nannochloropsis oceanica cultures grown in recycled media, trapping the cells in cell wall debris and limiting light penetration, thus resulting in lower growth and lipid synthesis [47]. Furthermore, with each successive recycling cycle, counter ions such as NH4+, CO3−2, and PO4−3 accumulate, inhibiting cell development [29]. Another inhibiting factor in recycled media is an increase in salinity, which can be hazardous to cells, particularly those normally growing in fresh and brackish water.

4. Strategies to Increase Growth Media Recycling

While the use of recycled media leads to the accumulation of growth-inhibitory molecules that impede algal proliferation, the economic benefits of reusing media are an attractive motivator for developing strategies to increase spent media usability. Use of water and nutrients for cultivation is costly and unsustainable at large scale. Recent years have witnessed the rise of new and innovative strategies to deal with the adverse effects of spent media recycling, some of which come from advances in water treatment technologies, while others utilize methodologies that alter the chemical composition of recycled media. Figure 2 depicts a framework of methods that can extend recycled media use, while recognizing that process design may vary depending on the employed algal strain, cultivation system, and operating conditions.

4.1. Ultraviolet Advanced Oxidation

Advanced oxidation processes (AOP) are used in water treatment to deal with damaging chemicals that could linger after introduction, especially contaminants that are biologically toxic. AOPs utilize highly reactive hydroxyl and/or sulfate radicals that can oxidize organic materials [79]. UV-based AOPs generate oxidants, such as UV/H2O2, UV/peroxodisulfate (UV/PDS), and UV/NH2Cl that have been successfully applied in wastewater and drinking water treatment as environmentally friendly methods to remove destructive organics, whereas UV-A is used in combination with titanium dioxide, a well-established material for photodegradation of macromolecules. When UV AOP was employed to pretreat recycled media to assess its impact on algal cultivation, UV/PDS and UV/H2O2 were shown to degrade inhibitory molecules in recycled media used to grow S. acuminatus GT-2 [51]. However, not all UV AOP schemes tested were able to lead to significant degradation of growth inhibitors, with UV and UV/NH2Cl having some effect on the attenuation of inhibitory molecules, but failing to achieve full degradation [51]. In the case of D. salina, recycled media that were first ultrafiltered and subsequently treated with UV/H2O2 were lower in nitrate and organic glycerol that could inhibit algal growth [43]. Additionally, D. salina grown in AOP-treated recycled media showed higher growth rate, consistent ratios between chlorophyll and carotenoids, and a lower bacterial load [43]. However, AOP scale up to treat recycled media in large-scale bioreactors may incur significant additional operating and maintenance costs [80].

4.2. Activated Carbon

In water treatment, activated carbon in its various forms provides a porous large surface area to allow various chemical reactions to take place, thus providing benefits to the removal of inhibitory molecules. Powdered Activated Carbon (PAC), for example, results in strong adsorption, mild reaction conditions, and fewer by-products to achieve efficient and low-cost micropollutant removal [81]. Treatment of recycled growth media with PAC combined with flocculants was not only able to enhance spent media recyclability, but also accounted for a 13.5% enhanced growth of A. platensis compared to standard media [21]. Similarly, treatment with PAC resulted in 1.83 g L−1 of biomass yield for N. oceanica [47] and 21.9% higher yield for Monoraphidium sp. KMC4 alongside 30% water savings [82]. Granular Activated Carbon (GAC) has also been used for spent media treatment. GAC-treated BG11 spent media for cultivation of S. acuminatus showed no negative effect on growth, whereas untreated spent media led to a 14.3% growth decrease [76]. When using GAC in the cultivation of Spirulina maxima FACHB 438, researchers saw no discernable loss of growth compared to fresh media even after four recycling rounds [83]. Relying on activated carbon appears to be cost effective, but not all molecules can be removed from the recycled media, so pairing with other types of treatment schemes might be necessary. Additionally, the efficiency of activated carbon decreases over time, with one study reporting that the removal of certain non-degradable compounds decreased from 50% to 10% in the course of 100 days [84].

4.3. Ultrasonication

Another approach that is effective at mitigating the threat posed by growth contaminants, like 4-chlorophenol, azo dye, oil, and various other organic compounds present in recycled media, is the use of ultrasound frequencies that degrade these molecules [26,85,86,87]. Degradation of contaminants is facilitated by the generation and eventual collapse of tiny bubbles in the water through cavitation. The collapse of the bubbles leads to energy release that breaks the interactions of larger organic molecules. A key advantage of integrating ultrasonication for improving the reusability of spent media is that this method has already been demonstrated in water treatment practices, so the potential to benefit media recycling is high. When applied on spent media of Scenedesmus sp. and Chlorella sp., ultrasonication resulted in better growing capacity than in control settings after four consecutive rounds of cultivation using untreated recycled media [26]. However, more research into the specific benefits of ultrasonication, when applied to spent media, needs to be conducted, to complement its use as a method of cell disruption and lipid extraction.

4.4. Microfiltration

Filtering prior to reuse appears as a rudimentary, yet ubiquitous, step that is often applied when treating recycled media. During filtration, spent media flow through semipermeable materials with certain size restrictions, such as 0.02 microns, removing larger organic matter from the spent media. When microfiltration separators were used as an energy-saving method to assist in reusing spent media to grow Synechocystis sp. PCC 6803, the algae grew well in 50% recycled media [88]. Filtration is often paired with other spent media pretreatment approaches to increase the reusability of recycled media. Filtration of reused media for cultivation of Nannochloropsis sp. and T. lutea led to significant cost savings in terms of water usage (77%) and nutrient supplementation (71%) [49], while Nannochloropsis sp. were able to grow in 80% recycled media over 167 continuous days of cultivation [48]. The combination of filtration with AOP was used to help D. salina grow at large scale, but it was also shown to grow equally well with only filtration applied [43]. Out of the methods explored, filtration is mechanically one of the simplest methods as it merely directs the media through a membrane. Over time, however, the filter will need to be changed due to the build-up of materials that limit flow [89].

4.5. Crop Rotation

A natural strategy that can be utilized to extend the use of media without having to use pretreatment is algae strain rotation, much like terrestrial crop rotation. This method takes into consideration that the inhibitory effect of spent media on a certain strain may be specific to that strain and not to other strains, so spent media of one strain may sustain well the growth of another strain. Additionally, doing so may provide additional benefits, such as reducing the possibility of strain-specific pathogen/predator build-up over time in the cultivation system and reducing the impact of self-inhibitory molecules that are excreted by algae. Recycled media from Staurosira sp. allowed uninhibited growth of Chlorella sp. and Navicula sp. [15]. Crop rotation using Nannochloropsis sp. and T. lutea, when combined with filtration and minimal nutrient replenishment, can lead to significant cost savings [49]. Algal crop rotation is still in its early stages, so additional research into its feasibility will be required to fully understand how promising it is.

4.6. Nutrient Replenishment

One of the challenges of using spent media is replenishment of nutrients that were depleted during algal cultivation. As reported in an earlier section, researchers crafted a highly assimilable minimal growth medium (HAMGM) for C. vulgaris and tested it using continuous long-term cultivation [29]. The HAMGM was crafted by replacing nutrients whose ions exhibited poor assimilation by algae with more available molecules, namely replacing ammonium chloride (NH4Cl) with ammonium bicarbonate (NH4HCO3). The replenishment of recycled medium with HAMGM supported biomass productivity similar to that in fresh media, while offering a 77% reduction in water consumption and 50% decrease in nutrient costs [29]. It should be noted that nutrient replenishment can be optimized when used in conjunction with other spent media treatment methods. Purely adding nutrients that are used up in the process of cultivation does little to curtail the accumulation of auto-inhibitory molecules excreted by growing algae. As an example, Nannochloropsis sp. grown in replenished spent media reported over a two-fold decrease in biomass production, when compared with growing in fresh media [90].

5. Conclusions and Future Outlook

The most significant resource used in the production of algal biomass and algal materials is freshwater. Even if algae are cultured in wastewater or seawater, significant quantities of freshwater are still necessary to dilute the wastewater/seawater residual effluent to meet disposal specifications and to compensate for evaporative losses. Recycling spent media is viewed as a sustainable and cost-effective method for reducing the water footprint of algal biorefineries and also an effective means of recycling unutilized nutrients. However, recycled media often contain auto-inhibitors, cell debris, toxic ions, and high levels of salinity. These accumulated compounds impede the growth of algae and reduce the recyclability of the medium. The present review highlighted the varied effects of spent media on the growth and biochemical composition of numerous algal taxonomic groups. The reported findings place an emphasis on the selection and identification of robust algae species that have a higher tolerance to auto-inhibitors, hence allowing more extensive recycling of spent media. Moreover, the identification of auto-inhibitors, such as humic acid, FFAs, and PUAs, through advanced biophysical and metabolomics research has paved the way for the engineering of algal strains with increased tolerance to such growth inhibitors. Another important aspect is analyzing the microbiome of the algae cultivated in recycled media as compared to fresh media, which can unravel potential algal-bacterial interactions that may be beneficial for developing a symbiotic co-culture model, thus preventing costly culture crashes in large-scale production systems. Importantly, the selection of an effective method to reduce or eliminate auto-inhibitors in spent media will be essential to improve their reuse. The use of membrane filtration appears to be an appealing means for eliminating DOM and other auto-inhibitors from spent media. However, before adopting it into large-scale algae production systems, its capital cost and energy usage need to be considered. The use of metal and organic polymers for flocculation is another effective method for removing auto-inhibitors, but their impact on the quality of biomass and bioproducts needs to be investigated further. Finally, LCA and techno-economic analysis (TEA) are required to screen sustainable and cost-effective techniques for treating and reusing spent media.

Author Contributions

N.A. and G.P.P.: conceptualization. N.A., E.L. and N.L.: writing—original draft, data curation. G.P.P.: review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This work was partially supported by an award from the Intelligence Community (IC) Postdoctoral Research Fellowship Program, which is administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement between the IC and the U.S. Department of Energy.

Data Availability Statement

All data are available without restriction and are included in the manuscript file.

Acknowledgments

Figure 1 was made using Biorender.com.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Schematic of growth media recycling for algal cultivation. AOM: algogenic organic matter; FFA: free fatty acids; HA/FA: humic acid/fluvic acid-like substances; ROS: reactive oxygen species; PBR: photobioreactor; ORP: open raceway pond; N: nitrogen; P: phosphorous; K: potassium.
Figure 1. Schematic of growth media recycling for algal cultivation. AOM: algogenic organic matter; FFA: free fatty acids; HA/FA: humic acid/fluvic acid-like substances; ROS: reactive oxygen species; PBR: photobioreactor; ORP: open raceway pond; N: nitrogen; P: phosphorous; K: potassium.
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Figure 2. A framework of strategies for extending the reusability of recycled media. The black arrow signifies the flow of treatments using: (A) Microfiltration; (B) Activated Carbon; (C) Advanced Oxidation Processes; (D) Ultrasonication; (E) Nutrient Replenishment; (F) Algal Crop Rotation. These methods can be used singularly or in various combinations depending on the cultivation context and algae species.
Figure 2. A framework of strategies for extending the reusability of recycled media. The black arrow signifies the flow of treatments using: (A) Microfiltration; (B) Activated Carbon; (C) Advanced Oxidation Processes; (D) Ultrasonication; (E) Nutrient Replenishment; (F) Algal Crop Rotation. These methods can be used singularly or in various combinations depending on the cultivation context and algae species.
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Table
Table 1. Spent media recycling reported for several algal species and a variety of harvesting and media pretreatment methods *.
Table 1. Spent media recycling reported for several algal species and a variety of harvesting and media pretreatment methods *.
Algae strainCultivation MediaGrowth Cultivation ConditionsBiomass
Harvesting Method		Pretreatment of Media before RecyclingPercentage of Recycled Media
(%)		Number of Recycling CyclesReference
Temp. (°C)pHLight Cycle
Amphidinium carterae Dn241EHUMediterranean seawater218.512:12centrifugation0.2 μm filtration and autoclave754[19]
Ankistrodesmus sp.BG11 media30NRnatural lightNR1002[20]
Arthrospira
platensis UTEX1296		Modified Schlösser medium329.5continuousflocculation and absorptionWhatman filter paper no.31[21]
Arthrospira
platensis 21.99		Modified Zarrouk medium20NR16:8micro-strainerNR4[22]
Aurantiochytrium
sp. ICTFD5		Glucose and Yeast media256.8NRcentrifugation503[23]
Chaetoceros muelleri Modified
F/2 medium		8.016:8 flocculation (chitosan) 1001[24]
Chlamydomonas reinhardtii DW15Minimal medium7.2continuousflocculation0.2 μm filtration1[25]
Chlorella SDEC-18BG11 mediaNRcentrifugationultrasonication4[26]
Chlorella sorokiniana MSUModified TAP medium6.2NR50-[27]
Chlorella vulgarisBG11 media7.5pH Flocculation1001[28]
Chlorella vulgaris 221/19SAGHAMGM mediacentrifugation16[29]
Chlorella vulgaris UTEX265BG11 media7.03[30]
Chlorella vulgaris 211/19
SAG		HAMGM media7.516[31]
Chlorella vulgarisBG11 mediaNR12:12bacterial flocculationsterile media washesNR2[32]
Chlorella vulgaris UTEX 395BBM media7.5continuouscentrifugationNR100 and 502[33]
Chlorella vulgaris UTEX 265BG11 media25NRcentrifugation or flocculation0.2 μm filtration1003[34]
Chlorella vulgaris28-12:12fungi flocculationautoclave1[35]
BBM media253continuousgravity sedimentationNR3[36]
Parachlorella kesslerif/2
medium		7.516:8chemo magnetic flocculation0.2 μm filtration1[37]
Chlorella pyrenoidosaNanoemulsion media-12:12centrifugationNR502[38]
Chlorella vulgarisBBM media287.212:12magnetic flocculant100 and 501[39]
Modified BBM media236.8continuousflocculation1001[40]
Chlorella sorokinianaTAP media (mixotrophic growth)277.018:6centrifugation2[41]
Chlorella zofingiensisBG11 media256.8continuous100 and 503[42]
Chlorococcum sp.7.5pH flocculation1001[28]
Dunaliella salina DF40A4F industrial media218-membrane processingintegrative membrane filtration502[43]
Dunaliella salina (MUR 8)Modified F-mediumoutdoor-outdoorcentrifugationNaClO treatment1006[44]
Ettlia texensis SAG79.80Modified freshwater medium266.5continuousflocculationNR2[45]
Nannochloropsis salinaModified f/2
medium		258.0–8.8continuousflocculation [46]
Nannochloropsis oceanica23–287.6–8.2ultrafiltration membrane3[47]
Nannochloropsis
sp. CCAP278		Artificial seawateroutdoor cultivationcentrifugationsand filtration10[48]
Nannochloropsis sp. CCAP221228.716:8centrifugation0.22 μm filtration1[49]
Nannochloropsis oculataModified artificial seawater257.6continuouspH flocculationNR1[28]
Neochloris oleoabundans UTEX 1185 Brackish
medium		24-16:8 centrifugation 1[50]
Phaeodactylum tricornutumModified artificial seawater257.8continuouspH flocculation1[28]
Scenedesmus acuminatus GT-2BG11 media26–286.5–7.0ultrafiltration membraneUV-based AOP1001[51]
Scenedesmus acuminatus256.5–7.0NR3[14]
Scenedesmus subspicatus UTEX 2594 BBM media266.9centrifugation 0.30 μm filtration 50, 20, 10 [52]
Scenedesmus SDEC-8BG11 media25-ultrasonication1004[26]
Scenedesmus sp.7.5pH flocculationNR1[28]
Scenedesmus sp. 307.0continuous electro–coagulation–flocculation 0.2 μm filtration5[53]
256.5–8.012:12flocculation and centrifugationNR2[54]
Scenedesmus quadricauda FWAC 276 LC Oligo medium 207.0centrifugation2[55]
Tisochrysis lutea CCAP927Artificial seawater259.122:2centrifugation0.22 μm filtration1[49]
Tetraselmis sp. MUR 233Seawater-based mediaoutdoor cultivationelectro-flocculation, and centrifugationNR50continuous[56]
Tetradesmus obliquusChu synthetic medium20-12:12gravity sedimentation3[57]
* NR: Not reported; BG11: Blue green media; BBM: Bold’s Basal media; TAP: tris acetate phosphate.
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Arora, N.; Lo, E.; Legall, N.; Philippidis, G.P. A Critical Review of Growth Media Recycling to Enhance the Economics and Sustainability of Algae Cultivation. Energies 2023, 16, 5378. https://doi.org/10.3390/en16145378

AMA Style

Arora N, Lo E, Legall N, Philippidis GP. A Critical Review of Growth Media Recycling to Enhance the Economics and Sustainability of Algae Cultivation. Energies. 2023; 16(14):5378. https://doi.org/10.3390/en16145378

Chicago/Turabian Style

Arora, Neha, Enlin Lo, Noah Legall, and George P. Philippidis. 2023. "A Critical Review of Growth Media Recycling to Enhance the Economics and Sustainability of Algae Cultivation" Energies 16, no. 14: 5378. https://doi.org/10.3390/en16145378

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