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Proceeding Paper

Biological Treatment of Second Cheese Whey Using Marine Microalgae/Cyanobacteria-Based Systems †

by
Stefania Patsialou
1,*,
Ioanna Aikaterini Tsakona
2,
Dimitris V. Vayenas
2,3 and
Athanasia G. Tekerlekopoulou
1
1
Department of Sustainable Agriculture, School of Agricultural Sciences, University of Patras, 30100 Agrinio, Greece
2
Department of Chemical Engineering, School of Engineering, University of Patras, 26500 Patras, Greece
3
Institute of Chemical Engineering Sciences (ICE-HT), Stadiou Str., Platani, 26504 Patras, Greece
*
Author to whom correspondence should be addressed.
†
Presented at the 1st International Online Conference on Bioengineering, 16–18 October 2024; https://sciforum.net/event/IOCBE2024.
Eng. Proc. 2024, 81(1), 4; https://doi.org/10.3390/engproc2024081004
Published: 16 January 2025
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Abstract

:
The biological treatment of second cheese whey (SCW) was investigated using two different marine cultures, the microalgae Picochlorum costavermella and the cyanobacterium Geitlerinema sp. Seawater from the coastal area of Rio, near Patras, was used for dilution of the SCW to achieve an initial concentration of about 2000 mg d-COD/L in both cases without any external additions of the inorganic nutrients N and P. The growth of the mixed biomass, the removal of nutrients and the simultaneous accumulation of bioproducts over time were studied, with d-COD removal reaching 65% and maximum lipid and protein contents, up to 24% and 41.7%, respectively.

1. Introduction

The wastewater produced by dairy industries, such as milk-processing factories and cheese, yogurt or pudding production plants, originates from both the manufacturing process and the washing waters. Mixed dairy wastewater is usually characterized by a high organic load, high nitrogen concentrations, unpleasant odors and intense turbidity. The main by-products of cheese manufacturing are the cheese whey (CW) and the second cheese whey (SCW) [1]. Cheese whey is the by-product derived from the cheesemaking process following the coagulation of casein. Employing a thermal process to achieve protein denaturation and convert the cheese whey into cottage cheese produces a yellowish, nutrient-rich liquid by-product known as secondary cheese whey. This secondary by-product accounts for over 90% of the original cheese whey utilized in the process. Specifically, SCW is characterized by high concentrations of organic load (43,000 mg/L d-COD) and total solids (49.3 g/L TS), with significant salinity values (up to 52‰) and acidic pH ranging from 4.5 to 6 [1].
The reckless disposal of untreated dairy wastewater into natural water ecosystems, like lakes, rivers and sea, raises a significant environmental problem. This practice is especially common in areas where small dairy plants are located. Consequences include a strong stench, especially during summer, and eutrophication caused by the high nitrogen and phosphorus content in wastewater. Additionally, to discharge dairy wastewater into sewer systems, specific physicochemical parameters must comply with legislative limits according to the Gazette of the Government (GR) 2011/354B of 8 March 2011 [2]. Specifically, COD and BOD5 values must not exceed thresholds of 1000 mg/L and 500 mg/L, respectively, while, for nitrates and phosphates, the limits are 20 mg/L and 10 mg/L, respectively. As a result, the treatment of dairy wastewater is considered necessary, and various treatment methods have been extensively studied, such as physicochemical [3,4], electrochemical [5,6] and biological [7,8], as well as combinations of these [9,10].
Although the biological treatment of dairy wastewater has been extensively studied, there are limited studies on the biological treatment of SCW, especially using microalgae/cyanobacteria cultures without pretreatment. Anaerobic biological treatment has been successfully used for cheese whey wastewater, resulting in high pollutant removal and significant biogas/biomethane production [11,12]. Aerobic methods have also been used for CW and SCW treatment over the years, demonstrating satisfactory organic matter removal rates [1,13,14]. An alternative biological treatment approach involves constructed wetlands, where wastewater supports plant growth, such as reeds, resulting in high organic load removal [15,16]. Given this context, using microalgae/cyanobacteria cultures represents an effective strategy for dairy wastewater biodegradation, as the inorganic compounds in the wastewater provide essential nutrients for the cultures’ growth. Several studies have investigated dairy wastewater as a substrate for microalgae/cyanobacteria growth. However, only a few of these have focused exclusively on SCW. These studies achieved high COD removal rates while also producing biomass and valuable bioproducts, such as lipids [17,18,19,20,21,22].
Marine microalgae/cyanobacteria have gained significant scientific interest due to their ability to produce high-added value bioproducts. Recently, Álvarez et al. [23] used marine Spirulina to treat dairy wastewater diluted with seawater, achieving the substantial removal of total nitrogen (TN) and total phosphorus (TP) while also obtaining intracellular proteins, carbohydrates, and pigments. Considering the above, the present study investigates the treatment of SCW using marine microalgae/cyanobacterial strains, without pretreating the SCW. Diluting SCW with seawater creates an ideal substrate for microalgal growth, as it provides a nutrient-rich environment with natural salinity conditions for marine strains, which in turn reduces the operating costs of the process.

2. Materials and Methods

2.1. Set Up of Biological Treatment Using Microalgae/Cyanobacteria Cultures

Experiments for the biological treatment of SCW were conducted using two different marine microalgae/cyanobacteria species, Geitlerinema sp. and Picochlorum costavermella, in separate bioreactors, under non-sterilized conditions, at temperature 24 ± 1 °C and pH 7.5–8. Cylindrical Duran glass flasks with a working volume of 1 L were used as laboratory-scale photobioreactors, under continuous stirring with a magnetic stirrer, with atmospheric CO2 as the external inorganic carbon source and biomass suspension maintained. Continuous illumination (2000 lux) was provided by LED lamps, measured by a Testo 540 light meter, and no other mechanical aeration was used.
These experiments were conducted without sterilization or any pretreatment of the dairy wastewater, allowing the establishment of a naturally occurring mixed microbial consortium comprising microalgae/cyanobacteria and the indigenous microbial populations present in the wastewater. This approach fosters a synergistic interaction between microalgae and bacteria, which enhances the functional robustness and ecological resilience of the system. Moreover, the mixotrophic metabolic activity, wherein microorganisms utilize both organic and inorganic carbon sources, facilitates elevated pollutant removal rates by efficiently exploiting available nutrients [22]. Finally, with the scope of applying the system on a larger scale, sterilization of the wastewater would not be practically feasible.
Freshly collected seawater from the coastal area of Rio, Patras, was used for the dilution of the SCW to achieve the desired concentration of about 2000 mg d-COD/L. The diluted wastewater was then filtered with filter paper to reduce the excess solids. A pH adjustment was necessary prior to inoculation, due to the low acidic pH value of the diluted wastewater. The addition of external inorganic nutrients such as N and P was not required.
The cyanobacterial strain Geitlerinema sp. was isolated and identified as described by Patsialou et al. [24], while the microalgal strain Picochlorum costavermella was isolated according to Dritsas et al. [25]. Both cultures are indigenous to coastal areas of the Ionia Sea and were maintained in an artificial seawater medium, prepared as described by Dritsas et al. [25]. The inoculum for all experiments was taken from the mid-exponential growth phase of each culture, at 20% v/v of the working volume. All experiments were performed in duplicate, and results are expressed as mean values (±standard deviation (SD)).

2.2. Analytical Methods and Procedures

During the experiments, the removal of organic and inorganic components was assessed. Precisely, organic compounds such as dissolved chemical oxygen demand (d-COD) and Total Kjeldahl Nitrogen (TKN) were measured following the methods described in ‘Standard Methods for the Examination of Water and Wastewater’ [26]. Inorganic analyses for nitrates (NO3− -N) and orthophosphates (PO43−) were carried out using Method 4500-ΝO3− Β and the Ascorbic acid method 4500-P E, respectively [26]. Total sugars were quantified using the DuBois method [27]. Biomass samples were collected every two days to determine the biomass concentration growth and the accumulation of intracellular bioproducts. Total mixed biomass concentration was expressed as total suspended solids (TSSs) according to Standard Methods [26], by filtration through a 0.45 μm membrane filter. Biomass productivity was determined as described by Patrinou et al. [28]. Protein content was evaluated through basic hydrolysis according to the Lowry method [29], and intracellular carbohydrate content was estimated using a modified DuBois method, as described by Patsialou et al. [24]. Considering the total lipid content, it was estimated according to Patrinou et al. [28] using the Folch method [30]. The composition of all bioproduct contents was expressed as a percentage (%) in dry weight (DW).

3. Results and Discussion

3.1. Removal of Nutrients

Figure 1 presents the kinetic studies on the removal of d-COD, sugars, nitrate nitrogen, and orthophosphates. As shown in Figure 1a, the organic load was successfully reduced by over 55% for both d-COD and sugars. Specifically, the two mixed cultures of marine cyanobacterium Geitlerinema sp. and microalgae P. costavermella, along with the indigenous microorganisms of the wastewater, degraded d-COD by the 8th day, with no further reduction observed afterward. Initial d-COD concentrations for Geitlerinema sp. and P. costavermella were 2129 and 1921 mg d-COD/L, achieving the maximum d-COD removal of 55.8% and 64.8%, respectively. A higher removal rate was recorded by Singh et al. [31], who achieved 90.54% COD removal that used the microalgae Monoraphidium sp. to treat artificial dairy wastewater with an initial concentration of 1920 mg COD/L after 11 days of cultivation. In a similar study, Hemalatha et al. [32] reported a 90% COD removal after 9 days with a mixed microalgal culture at an initial COD concentration of 1746 mg/L. Other studies using pretreated SCW as the substrate for microalgae Choricystis-dominated cultures by Tsolcha et al. [18] showed higher d-COD removal rates, up to 83.3% and 88.9%, for initial d-COD concentrations of about 2300 and 1800 mg/L, respectively. Tsolcha [19,20] also examined Leptolyngbya-based cyanobacteria systems with pretreated SCW, achieving similar COD removals to this study, at 65.5% and 54.4% for initial concentrations of about 2400 and 1600 mg d-COD/L, respectively. Mohanty and Mohanty [33] reported a COD reduction of 78% when using the microalgae Monoraphidium sp. KMC4 to treat synthetic wastewater with an initial COD concentration of 2000 mg /L. A similar COD reduction, up to 75%, was reported by Divya Kuravi and Venkata Mohan [34], employing Monoraphidium sp. to treat wastewater with an initial COD concentration of 1600 mg/L. The most significant COD removal across the studies was achieved by Ravi Kiran and Venkata Mohan [35], who reported a 95.5% COD reduction using Tetradesmus sp. SVMIICT4 for the treatment of synthetic dairy wastewater, which initially contained 3600 mg COD/L, following a 12-day cultivation period.
Simultaneously, sugar removal achieved higher levels (80.6–91.4%), with the concentration consistently decreasing until the 10th day of cultivation (Figure 1b). This higher removal may be due to sugars being simpler carbon compounds and thus more biodegradable by microalgae and bacteria. Singh et al. [31] observed similar glucose removal (90.93%). Tsolcha et al. [18,19,20] also reported a high removal of total sugars (85–91%) for all cases, closely aligning with this study. Although d-COD removal did not exceed 65% in both cases, the final concentration was below 1000 mg d-COD /L, which meets the disposal limit for treated wastewater in the sewerage system [2].
NO3− -N removal ranged from 53.3% for Geitlerinema sp. to 73.1% for P. costavermella, while orthophosphate (PO43−) removal was similar for both cultures, at around 75% (Figure 1c). Orthophosphate concentration decreased steadily over time, whereas NO3− -N removal followed a different pattern. Specifically, nitrate concentration dropped sharply in the first two days but then showed a slight, continuous increase, likely due to the lysis of part of the microalgae/cyanobacteria-bacteria population in the next days of the experiments or possibly due to a limitation in nitrate uptake. While nitrate may continue to be released through cell lysis, it may not be consumed at the same rate as initially observed. Hemalatha et al. [32] reported NO3− -N and PO43− removal rates 65.5% and 73%, respectively, providing a direct comparison with the current study. Divya Kuravi and Venkata Mohan [34] reported a nitrate removal efficiency of 85%, while Ravi Kiran and Venkata Mohan [35] observed similar nitrate removal rates of 65.2%. In contrast, the phosphate removal efficiency in both studies was lower than that observed in the current work, with values of 60% and 57.35%, respectively [34,35]. Singh et al. [31], however, a achieved higher NO3− -N removal (80%) and a slightly higher phosphate removal (84.1%) in their study. Nevertheless, it should be noted that the wastewater used in their experiments was artificially prepared. Similarly, Tsolcha et al. [19,20] observed a nitrate removal of 50–55% for Leptolyngbya-based systems, with higher rates of 66.3 and 82.0% achieved in microalgae-dominated experiments [18]. Corresponding PO43− removal rates in these studies ranged from 68.4 to as high as 99.7%, exceeding the values achieved in the present study. Total Kjeldahl Nitrogen (TKN) was measured at the start and end of the cultivation period, showing removal rates of 21.3% and 45.8% for Geitlerinema sp. and P. costavermella, respectively (Table 1). These TKN removal rates are lower than those reported in studies on TN and TKN removal [18,19,20,23,36].

3.2. Biomass Growth and Composition

The final biomass concentrations for both cultures were similar, reaching 710 mg/L for Geitlerinema sp. and 800 mg/L for P. costavermella after 10 days of cultivation (Figure 2a), resulting in biomass productivities of 47 and 57 mg/(L day), respectively (Table 2). A similar biomass productivity of 50.9 mg/(L day) was reported by Divya Kuravi and Venkata Mohan [34] for the microalgae Monoraphidium sp. SVMIICT6 in a synthetic dairy medium. These biomass productivity values are quite low compared to those reported in other studies, where typical biomass productivities range from 100 to 300 mg/(L day) [18,19,20,21]. Although the biomass productivity in this study was notably low, the final biomass concentrations were satisfactory. For example, Daneshvar et al. [37,38] investigated reported biomass concentrations of 360–650 mg/L for microalgae Scenedesmus and Tetraselmis grown in dairy wastewater, which are even lower than those in this study. Similarly, Ouhsassi et al. [36] reported biomass concentrations of about 500–600 mg/L for a Pseudanabaena culture used in dairy wastewater from yogurt production. By contrast, Hemalatha et al. [32] and Singh et al. [31] reported higher final biomass concentrations of 1.4 and 1.5 g/L, respectively, approximately twice those observed in this study.
The kinetics of intracellular bioproduct accumulation are shown in Figure 2b,c. In this study, the cyanobacteria-dominated culture exhibited a significant accumulation of protein (up to 42%) and carbohydrates (up to 25%). Specifically, for Geitlerinema sp. the maximum protein, carbohydrate, and lipid contents were 41.7, 25.4 and 14.4% DW, respectively. Cyanobacteria are known to preferentially accumulate carbohydrates over lipids, and the carbohydrate content observed in this study is consistent with values reported by Divya Kuravi and Venkata Mohan (2022) [34] and Ravi Kiran and Venkata Mohan [35], which were 22.88% and 21.48%, respectively. Although lipid content was lower in the later stage of the cultures (<10%), the maximum lipid accumulation observed (14.4%) aligns with reported values in the literature. For instance, Tsolcha et al., investigated the lipid accumulation of Leptolyngbya-dominated cultures and found similar lipid content, with reported values of 14.8 and 16.1% in their respective studies [19,20].
For the P. costavermella culture, the maximum protein, carbohydrate, and lipid contents were 28.0, 17.9, and 24.2% DW, respectively. Singh et al. [31] reported higher protein and carbohydrate contents of 48.5 and 28.73%, respectively, but a lower lipid content of 20.29% for a microalgae-dominated culture of Monoraphidium sp. Similarly, Divya Kuravi and Venkata Mohan [34] reported a total lipid content 25% for Monoraphidium sp. SVMIICT6 cultivated in a synthetic dairy medium. Hemalatha et al. [32] observed a different profile, with lower protein (15.6%), higher carbohydrate (38.9%), and similar lipid content (22%), at the end of a 6-day cultivation period. Tsolcha et al. [18] also recorded lower lipid contents, specifically 12.9% and 13.4%, for Choricystis-dominated cultures used in dairy wastewater treatment. Also, for the microalgae P. costavermella, Dritsas et al. [25] reported a lipid content of 19.1% under photoautotrophic conditions, which was 5% lower than observed in the current study, thereby confirming that mixotrophic metabolism enhances lipid production.
A clear inverse trend in the accumulation of lipids and carbohydrates is observed in the microalgae/cyanobacteria cultures. This can be attributed to the fact that, during the initial stages of the experiment, the removal of d-COD was particularly active, and the microalgae/cyanobacteria tended to produce carbon-rich lipid particles. The maximum lipid content was recorded on the fourth day, coinciding with the peak d-COD removal in both cases. However, in the last days of cultivation, the microalgae/cyanobacteria appeared to metabolize the lipids produced earlier as a carbon source, with lipid content decreasing to 5.0% for Geitlerinema sp. and 11.1% for P. costavermella, while carbohydrate accumulation increased in the absence of nitrogen. Ravi Kiran and Venkata Mohan [35] reported a similar lipid content of 10.33% using Tetradesmus sp. SVMIICT4, as well as comparable protein content of 19.52%, which is in line with the final protein contents observed in this study (19.8% and 21.3%, respectively).
The carbohydrate content observed in this study was lower than that reported in other studies, which could be attributed to residual nitrogen levels. It is well established that nitrogen starvation conditions promote the accumulation of carbohydrates. The maximum content of each bioproduct occurred on different cultivation days. Notably, the microalgae-dominated culture achieved significantly higher lipid content (24.2%), nearly double that of the cyanobacteria-dominated system, in addition to a high protein content (28.0%). This finding underscores the distinct bioproduct accumulation potentials of different microorganisms and highlights the fundamental differences between microalgae and cyanobacteria in terms of their metabolic capabilities and product synthesis.

4. Conclusions

Overall, the present study investigated the removal efficiency of mixed microalgae/cyanobacteria-indigenous bacteria cultivation systems using marine strains. The growth of marine Geitlerinema sp. and Picochlorum costavermella-dominated mixed cultures in diluted SCW (with seawater) resulted in high nutrient removal rates, with a final concentration of <1000 mg d-COD/L after 10 days of cultivation, meeting the legislation limit for the disposal of treated agro-industrial effluents. Additionally, maximum bioproduct contents were observed, with high levels of lipids (up to 24%), proteins (up to 41.7%) and carbohydrates (25.4%). The use of abundant natural seawater for wastewater dilution also contributes to both a cost-effective and environmentally sustainable process. By reducing the reliance on freshwater, which is typically required for dilution purposes, it minimizes resource consumption and lowers the overall operational costs. This approach presents a potentially viable scenario for large-scale applications. In addition, the absence of mechanical aeration or the addition of external nutrients further reduces operational expenses, enhancing the economic feasibility of the process. However, the proposed treatment system faces some challenges, particularly in the biomass harvesting stage. In this context, the specific filamentous cyanobacterium selected for this study is particularly advantageous, as it tends to form biofilms and aggregates, facilitating auto-settling and thereby simplifying biomass recovery. For microalgae-dominated cultures, the use of support media to encourage biomass attachment could further enhance the ease of harvesting.
While microalgae research is an expansive field, only a limited number of studies propose economically viable scenarios [39]. Consequently, a comprehensive techno-economic analysis of this system should be conducted in future research to explore further optimization potential. Optimizing these microalgae/cyanobacteria-based systems could involve the use of pilot-scale column bio-reactors (biofilters). Finally, these systems are proposed as a post-treatment step, in combination with methods, like anaerobic digestion, which could further reduce organic content and generate valuable biogas.

Author Contributions

Conceptualization, A.G.T. and D.V.V.; methodology, S.P., A.G.T. and D.V.V.; validation, S.P., A.G.T. and D.V.V.; formal analysis, S.P., I.A.T. and A.G.T.; investigation, S.P. and I.A.T.; data curation, S.P., A.G.T. and D.V.V.; writing—original draft preparation, S.P. and A.G.T.; writing—review and editing, A.G.T. and D.V.V.; supervision, A.G.T. and D.V.V.; project administration, A.G.T. and D.V.V. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within this article.

Acknowledgments

The authors would like to thank the management and staff of the cheese factory ‘Papathanasiou A.B.E.E.’ for their collaboration in providing the second cheese whey.

Conflicts of Interest

The authors declare no conflicts of interest.

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Engproc 81 00004 g001
Figure 1. Removal of (a) d-COD, (b) sugars, and (c) NO3−-N and PO43− over time for Geitlerinema sp. and Picochlorum costavermella.
Figure 1. Removal of (a) d-COD, (b) sugars, and (c) NO3−-N and PO43− over time for Geitlerinema sp. and Picochlorum costavermella.
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Figure 2. Changes in (a) biomass concentration and (b,c) the bioaccumulation of proteins, carbohydrates, and lipids (% DW) over time for Geitlerinema sp. and Picochlorum costavermella.
Figure 2. Changes in (a) biomass concentration and (b,c) the bioaccumulation of proteins, carbohydrates, and lipids (% DW) over time for Geitlerinema sp. and Picochlorum costavermella.
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Table 1. Removal (%) of inorganic and organic compounds at the end of experiments for Geitlerinema sp. and Picochlorum costavermella.
Table 1. Removal (%) of inorganic and organic compounds at the end of experiments for Geitlerinema sp. and Picochlorum costavermella.
Removal (%)
d-CODSugarsNO3− -NPO43−TKN
Geitlerinema sp.55.880.653.373.921.3
Picochlorum costavermella64.891.473.176.445.8
Table 2. Characterization of biomass concentration and content at the end of the cultivation period for Geitlerinema sp. and Picochlorum costavermella.
Table 2. Characterization of biomass concentration and content at the end of the cultivation period for Geitlerinema sp. and Picochlorum costavermella.
Biomass Concentration (mg/L)Biomass Productivity (mg/L day)Bioproducts (% DW)
ProteinsCarbohydratesLipids
Geitlerinema sp.7104719.825.45.0
Picochlorum costavermella8005721.310.711.1
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MDPI and ACS Style

Patsialou, S.; Tsakona, I.A.; Vayenas, D.V.; Tekerlekopoulou, A.G. Biological Treatment of Second Cheese Whey Using Marine Microalgae/Cyanobacteria-Based Systems. Eng. Proc. 2024, 81, 4. https://doi.org/10.3390/engproc2024081004

AMA Style

Patsialou S, Tsakona IA, Vayenas DV, Tekerlekopoulou AG. Biological Treatment of Second Cheese Whey Using Marine Microalgae/Cyanobacteria-Based Systems. Engineering Proceedings. 2024; 81(1):4. https://doi.org/10.3390/engproc2024081004

Chicago/Turabian Style

Patsialou, Stefania, Ioanna Aikaterini Tsakona, Dimitris V. Vayenas, and Athanasia G. Tekerlekopoulou. 2024. "Biological Treatment of Second Cheese Whey Using Marine Microalgae/Cyanobacteria-Based Systems" Engineering Proceedings 81, no. 1: 4. https://doi.org/10.3390/engproc2024081004

APA Style

Patsialou, S., Tsakona, I. A., Vayenas, D. V., & Tekerlekopoulou, A. G. (2024). Biological Treatment of Second Cheese Whey Using Marine Microalgae/Cyanobacteria-Based Systems. Engineering Proceedings, 81(1), 4. https://doi.org/10.3390/engproc2024081004

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