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Review

Unraveling the Potential of Microbial Flocculants: Preparation, Performance, and Applications in Wastewater Treatment

by
Yang Yang
1,2,
Cancan Jiang
2,3,*,
Xu Wang
2,3,
Lijing Fan
1,
Yawen Xie
2,3,
Danhua Wang
4,
Tiancheng Yang
2,3,
Jiang Peng
5,
Xinyuan Zhang
4 and
Xuliang Zhuang
2,3,6,*
1
Henan Institute of Advanced Technology, Zhengzhou University, Zhengzhou 450000, China
2
Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
3
College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China
4
School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230027, China
5
The Institute of International Rivers and Eco-Security, Yunnan University, Kunming 650500, China
6
State Key Laboratory of Tibetan Plateau Earth System, Environment and Resources (TPESER), Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100101, China
*
Authors to whom correspondence should be addressed.
Water 2024, 16(14), 1995; https://doi.org/10.3390/w16141995
Submission received: 14 June 2024 / Revised: 10 July 2024 / Accepted: 12 July 2024 / Published: 14 July 2024
(This article belongs to the Special Issue Water Quality Engineering and Wastewater Treatment III)
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Abstract

:
Microbial flocculants (MBFs), a class of eco-friendly and biodegradable biopolymers produced by various microorganisms, have gained increasing attention as promising alternatives to conventional chemical flocculants in wastewater treatment and pollutant removal. This review presents a comprehensive overview of the current state of MBF research, encompassing their diverse sources (bacteria, fungi, and algae), major categories (polysaccharides, proteins, and glycoproteins), production processes, and flocculation performance and mechanisms. The wide-ranging applications of MBFs in removing suspended solids, heavy metals, dyes, and other pollutants from industrial and municipal wastewater are critically examined, highlighting their superior efficiency, selectivity, and environmental compatibility compared to traditional flocculants. Nonetheless, bioflocculants face significant challenges including high substrate costs, low production yields, and intricate purification methodologies, factors that impede their industrial scalability. Moreover, the risk of microbial contamination and the attendant health implications associated with the use of microbial flocculants (MBFs) necessitate thorough evaluation. To address the challenges of high production costs and variable product quality, strategies such as waste valorization, strain improvement, process optimization, and biosafety evaluation are discussed. Moreover, the development of multifunctional MBF-based flocculants and their synergistic use with other treatment technologies are identified as emerging trends for enhanced wastewater treatment and resource recovery. Future research directions are outlined, emphasizing the need for in-depth mechanistic studies, advanced characterization techniques, pilot-scale demonstrations to accelerate the industrial adoption of MBF, and moreover, integration with novel wastewater treatment processes, such as partial nitrification and the anammox process. This review is intended to inspire and guide further research and development efforts aimed at unlocking the full potential of MBFs as sustainable, high-performance, and cost-effective bioflocculants for addressing the escalating challenges in wastewater management and environmental conservation.

1. Introduction

Rapid industrialization and population growth have enabled the rapid increase in the generation of wastewater containing a variety of pollutants, including suspended solids, heavy metals, dyes, and both organic and inorganic contaminants. The inadequate treatment of such discharge poses serious dangers to aquatic environments, human health, and ecological safety [1]. Consequently, there is an urgent requirement for the advancement of effective and sustainable techniques for wastewater treatment and pollutant removal. Flocculation has been broadly employed as a primary wastewater treatment technique due to its simplicity, cost-effectiveness, and notable efficiency in the removal of suspended and colloidal particles [2,3]. Traditional flocculants utilized in the wastewater treatment sector can be categorized into inorganic flocculants (such as aluminum sulfate, ferric chloride, and polyaluminum chloride) and organic synthetic polymers (such as polyacrylamide and polyethylene imine) [4,5]. Although these chemical flocculants have been widely adopted, they are associated with drawbacks, including high cost, potential toxicity, low biodegradability, and secondary pollution resulting from the residual flocculants and their degradation products [6].
In recent years, there has been a notable surge in the development of eco-friendly and sustainable flocculants as alternatives to conventional chemical counterparts [7]. MBFs, in particular, have attracted significant attention due to their unique benefits, including high efficiency, selective action, minimal toxicity, and superior biodegradability [8,9]. These eco-friendly agents are essentially extracellular polymeric substances (EPSs) produced by microorganisms during their growth and metabolic processes [10]. Composed of polysaccharides, proteins, nucleic acids, and lipids, these EPSs are characterized by diverse functional groups (such as hydroxyl, carboxyl, amino, and phosphate) facilitating interactions with pollutants through mechanisms including charge neutralization, adsorption, and flocculation [11]. The utilization of MBFs in wastewater treatment and pollution remediation has gained considerable traction in recent times. Their application in treating diverse types of wastewaters, including municipal sewage and industrial effluents from sectors such as textiles, dyeing, pulp and paper, tanneries, agricultural runoff, and landfill leachate, has demonstrated their versatility and capability [12,13]. MBFs have proven effective in removing suspended solids, turbidity, chemical oxygen demand (COD), heavy metals, dyes, and other contaminants [14,15,16], often achieving removal efficiencies on par with or surpassing those of traditional chemical flocculants [17,18,19]. Moreover, the biodegradable and nontoxic nature of MBFs reduces environmental liabilities associated with the disposal of residuals and effluents, contributing to sustainable waste management practices [20].
Although MBFs offer numerous attractive advantages and hold significant promise for application, they still face several obstacles that impede their large-scale production and use. Major hurdles include high manufacturing costs, low yield, complex compositions, and the uncertain safety of MBF products [7]. To address these challenges and facilitate the industrial application of MBFs, considerable research has been directed towards identifying high-producing strains, optimizing fermentation processes, sourcing low-cost substrates, and enhancing downstream processing methods [21]. With the advancement of wastewater treatment technology, the benefits and potential of biological flocculants in wastewater treatment are increasingly evident. Furthermore, as science and technology progress, we have access to more advanced technologies for further developing the principles and applications of biological flocculants.
The objective of this review is to offer a comprehensive summary of the current research landscape on MBFs and their prospective applications in wastewater treatment and pollution control. This article starts by outlining the origins, classifications, and production process of MBFs. It then reviews the effectiveness and mechanisms of MBFs in flocculation. Following this, the application of MBFs in treating various types of wastewaters and removing different pollutants is critically reviewed and discussed. This review also highlights the existing challenges and future directions in MBF research and application. This review is anticipated to provide insightful knowledge and guidance for professionals involved in wastewater management and environmental restoration.

2. Sources and Categories of MBFs

MBFs are a diverse group of extracellular polymeric substances (EPSs) produced by various microorganisms, including bacteria, fungi, and algae [22]. These EPSs serve important biological functions, such as cell adhesion, protection, and nutrient uptake, and can also facilitate the aggregation and sedimentation of suspended particles in aqueous systems [23]. The composition, structure, and properties of MBFs vary depending on the microbial species, growth conditions, and extraction methods.

2.1. MBF-Producing Microorganisms

A wide range of microorganisms have been reported to produce MBFs with different flocculating activities and characteristics. Table 1 presents some typical MBF-producing microorganisms and their MBF yield under experimental conditions. A major disadvantage of an MBF is its low yield, and the yield of some strains is less than 1 g/L. However, currently, through screening and genetic engineering methods, MBF-producing strains with high yields have been obtained, such as Lipomyces starkeyi in Table 1. The yield can reach about 62.1 ± 1.2 g/L. Of all the MBF-producing microorganisms, bacteria are the most common and extensively studied MBF producers, especially those belonging to the genera Bacillus, Pseudomonas, Klebsiella, Rhodococcus, and Paenibacillus [24]. These bacteria can be isolated from various sources, such as activated sludge, soil, wastewater, and marine environments, and are known for their high growth rate, easy cultivation, and adaptability to different substrates [25].
Fungi and yeasts are also significant producers of MBFs, with species from genera such as Aspergillus, Penicillium, Phanerochaete, Streptomyces, and Lipomyces being notable [40,41]. Fungal MBFs typically exhibit higher molecular weights and enhanced flocculating activity compared to their bacterial counterparts. However, their production cost can be relatively higher, due to the slower growth rate and more complex fermentation requirements characteristic of fungi.
Algae, including species such as Scenedesmus obliquus AS-6-1 and Chlorella vulgaris JSC-7, have also been investigated as potential sources for MBF production [42,43]. Algal MBFs are primarily composed of polysaccharides and can be produced through photosynthetic processes that require minimal energy and nutrients. However, typically, the yield of MBFs from algae is lower compared to bacteria and fungi.
In addition to the natural MBF producers, genetically engineered microorganisms have been developed to enhance MBF production or confer specific functionalities. For example, the overexpression of bcsB can stimulate an increase in EPS production and enhance the flocculation effect of Escherichia coli [44]. Genetic engineering approaches offer new opportunities to design and optimize MBFs with desired properties for specific applications [45].

2.2. Categories of MBFs

Based on their chemical composition and structure, MBFs can be broadly classified into three major categories: polysaccharides, proteins, and glycoproteins [46], as shown in Figure 1. Polysaccharide MBFs are the most common and extensively studied type of MBFs [47]. They are composed of repeating monosaccharide units (e.g., glucose, galactose, mannose) connected by glycosidic bonds, forming linear or branched polymers with high molecular weights (104–107 Da) [48]. Polysaccharide MBFs often contain functional groups (e.g., hydroxyl, carboxyl, amino, sulfate) that can interact with pollutants through hydrogen bonding, electrostatic attraction, and complexation mechanisms. Some examples of polysaccharide MBFs include xanthan, dextran, pullulan, and alginate-like exopolysaccharides. Protein MBFs are another important category of MBFs, which are composed of polypeptide chains with a high content of acidic (e.g., aspartic acid, glutamic acid) and hydrophobic (e.g., alanine, valine) amino acids. Protein MBFs usually have lower molecular weights (103–105 Da) than polysaccharide MBFs but exhibit higher charge density and flocculating activity. The flocculation mechanism of protein MBFs involves charge neutralization and bridging effects between the positively charged amino groups and negatively charged particles. Glycoprotein MBFs are a special type of MBF that contain both polysaccharide and protein moieties covalently linked together [49]. The polysaccharide component provides the backbone structure and hydrogen bonding sites, while the protein component confers the charge and hydrophobic interactions. Glycoprotein MBFs often have a complex and heterogeneous structure, with a molecular weight ranging from 105 to 107 Da. The synergistic effect of polysaccharide and protein components can enhance the flocculation performance and stability of glycoprotein MBFs.
In addition to these major categories, some MBFs may also contain other components, such as nucleic acids (e.g., DNA, RNA), lipids (e.g., fatty acids, phospholipids), and inorganic substances (e.g., metals, minerals) [50]. These minor components can modulate the physicochemical properties and flocculating activity of MBFs, depending on their content and interaction with the main components. The diversity and complexity of MBF composition and structure reflect the adaptation and optimization of microorganisms to different environmental conditions and substrates. Understanding the structure–function relationship of MBFs is crucial for selecting and designing MBFs with desirable properties for specific applications in wastewater treatment and pollutant removal. A wide variety of microorganisms have been discovered as MBF-producing strains, including bacteria, fungi, and algae. Table 1 summarizes some typical MBF-producing microorganisms reported in the literature. Among them, Bacillus, Pseudomonas, Klebsiella, Aspergillus, and Penicillium are the most common genera that can produce MBFs with high flocculating activity [51,52]. Most of the MBF-producing strains are isolated from activated sludge, soils, and wastewater, probably due to the natural selection of microorganisms under stress conditions. Some strains are also obtained through mutation or genetic engineering to enhance MBF production.

3. MBF Production, Flocculation Performance, and Mechanisms

3.1. MBF Production

MBFs are usually produced by microbial fermentation under optimized culture conditions. The growth medium for MBF production generally contains a carbon source, nitrogen source, mineral salts, and trace elements. Carbon sources are crucial for MBF biosynthesis, which are usually supplied as glucose, sucrose, starch, or agricultural wastes like rice straw, wheat bran, and molasses [53]. Nitrogen sources and the C/N ratio also play important roles in microbial growth and MBF accumulation. Inorganic nitrogen sources like ammonium salts are commonly used, while organic nitrogen sources like peptone, yeast extract, and corn steep liquor are sometimes added to improve MBF production [54]. Mineral salts (e.g., magnesium, calcium, potassium salts) are essential for maintaining microbial metabolism and enzyme activity. The optimal medium composition depends on the microbial species and should be optimized through experimental design. The cultivation conditions such as temperature, pH, aeration, and agitation speed also need to be optimized for efficient MBF production [55]. Most MBF-producing microorganisms favor temperatures between 25 and 37 °C and neutral pH (6.0–8.0). The aeration rate and agitation speed should provide sufficient oxygen supply while avoiding shear stress on microbial cells. Fed-batch fermentation is often adopted to achieve high cell density and MBF yield by preventing substrate inhibition [56]. Some inducers like ethanol, methanol, and organic acids can be added to stimulate MBF biosynthesis [57]. A two-stage fermentation strategy, where MBF production is separated from the cell growth stage, is also employed to enhance yield.
After fermentation, MBFs are present in the fermentation broth as soluble metabolites or in association with the microbial cell surface. Centrifugation or filtration is used to remove the microbial cells and obtain the cell-free supernatant. Alcohol (ethanol or acetone) precipitation is the most common method to extract MBFs from the supernatant, followed by centrifugation or filtration to collect the precipitates [7]. The crude MBF can be further purified by dialysis, ion exchange chromatography, size exclusion chromatography, or other purification techniques to obtain MBFs with higher purity [58]. Alternatively, MBFs can be recovered by directly treating the fermentation broth with an alkaline solution (e.g., NaOH) to dissolve and extract the MBF from the cell surface. Acid precipitation (e.g., HCl) is then used to precipitate MBFs from the alkaline extract [59]. Membrane filtration technology is also explored to simultaneously concentrate and purify MBFs from the fermentation broth [60,61]. The extraction efficiency and product purity may be affected by the extraction techniques and operating parameters, which should be optimized for each specific MBF. The extracted MBFs are usually dried by lyophilization or spray-drying to obtain a stable product for application.

3.2. Flocculation Performance

The flocculation performance of MBFs is usually evaluated by a jar test, where a certain dosage of the MBF is added into the wastewater under stirring, followed by a slow mixing and sedimentation process. The supernatant is then analyzed for the residual contaminant concentration or turbidity to calculate the removal efficiency [62]. Flocculation capacity can also be assessed by measuring the turbidity, particle size distribution, and settling velocity of the flocs formed [63]. The dosage effect, pH tolerance, temperature stability, and selectivity of MBFs are important parameters to evaluate their flocculation performance under different conditions. Compared with conventional chemical flocculants, many MBFs exhibit higher or comparable flocculation efficiencies towards various wastewater contaminants. For example, the MBF produced by Bacillus agaradhaerens C9 could achieve over 99% removal of chemical oxygen demand (COD) and turbidity from textile wastewater, outperforming polyaluminum chloride [64]. The MBF from Klebsiella pneumoniae could remove 97% of Cu(II) and 94% Cr(VI) from electroplating wastewater, showing superior performance over polyacrylamide [65]. The MBFs isolated from Bacillus velezensis (40B), Bacillus mojavensis (32A), and Pseudomonas (38A) had excellent C.I 28 basic yellow dye removal capability, and their maximum decolorization efficiencies were 91%, 89%, and 88% [66]. MBFs can maintain high flocculation activity over a wide range of pH (3–11) and temperature (20–80 °C), probably owing to the stability of hydroxyl and carboxyl groups on MBFs [67,68]. The dosage of an MBF is typically lower than chemical flocculants, with the optimal dose being several mg/L compared to tens or hundreds of mg/L for the latter [69]. This is attributed to the higher charge density and molecular weight of MBFs that can facilitate bridge formation and charge neutralization [70]. MBFs sometimes show selectivity towards some contaminants, which may be related to the specific binding affinity between the functional groups on MBFs and the target pollutants [71]. Due to the significant impact of the environment on microorganisms, biological flocculants’ flocculation performance is easily influenced by factors such as temperature and pH, leading to poor environmental stability. Prior to application, flocculant-producing bacteria might require a period of acclimatization. Nonetheless, after a screening process, strains that can adapt to various conditions have been successfully identified. For instance, a strain of Klebsiella pneumoniae, which produces a flocculant, was isolated from H acid wastewater. This flocculant boasts a high molecular mass, thermal stability, and pH responsiveness, and exhibits notably high flocculation activity [72]. B. mojavensis strain 32A has high flocculation efficiency, high yield, and thermal stability in the temperature range of 5~60 °C, and is suitable for use in neutral, weakly acidic, and weakly alkaline environments [73].

3.3. Flocculation Mechanisms

The flocculation mechanisms of MBFs have been extensively studied, and several hypotheses are proposed, as shown in Figure 2. Charge neutralization is regarded as a key mechanism, where the negatively charged MBF can neutralize the positively charged particles or vice versa, resulting in the destabilization and aggregation of colloidal particles [74]. Adsorption bridging is another important mechanism, in which the long-chain MBF can adsorb onto the surface of multiple particles and form a three-dimensional network, thus bridging the particles into large flocs [75]. The hydroxyl and carboxylic groups in biological flocculants also enhance the flocculation effect because they bind strongly to particles and other chemical contaminants [76]. Sweeping flocculation may also occur, where the MBF can capture and enmesh the fine particles into the precipitates as the MBF settles down [77]. Other mechanisms such as hydrophobic interactions and hydrogen bonding are also proposed to play a role in MBF flocculation. The hydrophobic regions on MBFs (e.g., lipid fraction) can facilitate the aggregation of hydrophobic pollutants through hydrophobic interactions. The hydrogen bonds formed between hydroxyl groups on MBFs and water molecules or particles may aid the adsorption and stability of flocs [78]. In some cases, Ca2+ or other divalent cations are involved in the flocculation process by crosslinking the negatively charged MBF and particles, thus acting as bridging agents [79].
At present, the flocculation mechanism of MBFs has not been thoroughly studied, but the advancement of science and technology provides us with more opportunities to explore this mechanism. It is important to note that the actual flocculation mechanism of MBFs may involve a combination of multiple mechanisms, which can vary depending on the characteristics of the MBF and the wastewater substrate. Additionally, the dominant mechanism can differ under varying pH, concentration, and other conditions [80,81]. The types of biological flocculants can also influence the flocculation mechanism. For instance, bioflocculants can initiate the destabilization of kaolin suspension through charge neutralization, followed by enhancing the aggregation of suspended particles through adsorption and bridging [82]. The bioflocculant B4-PS, prepared by Arthrobacter B4, may primarily rely on ionization and charge neutralization as its main flocculation mechanism [83]. Therefore, when studying the mechanism of biological flocculants, it is crucial to consider the specific circumstances. The investigation of the flocculation mechanism of MBFs remains a key focus for future research. A deeper understanding of the underlying mechanism is essential for designing and optimizing MBF for specific wastewater treatment applications.

4. Applications in Wastewater Treatment

4.1. Removal of Suspended Solids

MBFs play a crucial role in the treatment of wastewater, particularly in the removal of suspended solids (SSs). An SS refers to small solid particles that remain suspended in water, such as clay particles, inorganic sediments, organic sediments, organic scale, corrosion products, and other similar substances. These suspended solids can cause turbidity and give rise to aesthetic and safety concerns [84]. Due to their large surface area and charge density, MBFs can efficiently adsorb and flocculate SSs, leading to the rapid sedimentation of particles. For instance, the Aspergillus flavus-produced MBF achieved 92% SS removal from paper-making wastewater under ideal conditions [30]. Similarly, the bioflocculant IC-1 from Isaria cicadae GZU6722 was highly effective in treating coal-washing wastewater, achieving a maximum SS removal rate of 91.81% [85]. Furthermore, a protein-based MBF from Rhizopus sp. was capable of removing over 90% of SSs from domestic wastewater [86]. Similarly, a bioflocculant prepared via Serratia marcescens was observed to eliminate 83.95% of turbidity and 78.82% of suspended solids [4]. These findings underscore the promising potential of MBFs as bioflocculants for the control of SSs and turbidity in wastewater management.

4.2. Removal of Heavy Metals

The removal of toxic heavy metals from industrial effluents is another promising application of MBFs. Heavy metals like lead, chromium, cadmium, and mercury are highly toxic and can accumulate in the food chain, posing severe health risks [87]. Conventional treatment methods like chemical precipitation and ion exchange are costly and may cause secondary pollution [88]. MBFs offer an eco-friendly and cost-effective alternative for heavy metal removal owing to their strong affinity and selectivity towards metal ions. The hydroxyl, carboxyl, phosphate, and amino groups on MBFs can serve as binding sites for metal ions through electrostatic interaction or complexation. Sathiyanarayanan et al. reported that the MBF generated by Bacillus subtilis could adsorb 97% of Cr(VI) from tannery effluents [89]. Gomaa investigated the potential of MBFs from Pseudomonas aeruginosa for heavy metal removal, achieving an 85%, 80%, and 79% removal efficiency for Pb(II), Cu(II), and Cd(II) respectively [90]. By using MBFs as flocculation aids together with traditional alkaline precipitation, over 99% removal of Zn(II), Pb(II), Cu(II) and Cd(II) was obtained from electroplating wastewater [91]. The removal rates of Zn(II), Cd(II), Cu(II), and Hg by biological flocculants can reach 82.63 ± 1.20, 72.076 ± 0.42, 57.36 ± 1.05, and 44.7 ± 1.053% [92]. The metal-laden MBF flocs could be easily separated from water, and the heavy metals could be further recovered from the flocs by desorption or an incineration process. At present, some cation-dependent biological flocculants require the addition of Fe(II), Ca(II), and Al(III) ions to enhance their flocculation effect, and although this practice can reduce the dosage of inorganic flocculants and has certain advantages, it will introduce certain metal ions in the water body, weakening the green non-toxic advantage of biological flocculants. Therefore, the screening of biological flocculants with strong flocculation effects and the ability to remove metal ions such as Al(III) and Fe(II) is also a place worthy of attention in future research.

4.3. Removal of Dyes

Dyes are a major class of pollutants in the textile, leather, printing, and dyeing industries. The presence of dyes in water bodies can reduce light penetration, inhibit photosynthesis, and may cause carcinogenic and mutagenic effects [93]. Due to the complex structure and poor biodegradability of synthetic dyes, they are difficult to remove by conventional biological treatment methods. MBFs have shown excellent performance in decolorizing various synthetic dyes from wastewater. The mechanisms of dye removal by MBFs include adsorption, charge neutralization, and bridging effect. The functional groups (e.g., amino, hydroxyl, carboxyl) on MBFs can bind with dye molecules through hydrogen bonding, electrostatic attraction, and π-π stacking interaction [5]. Moreover, some MBFs exhibit enzyme-like activities (e.g., peroxidase, laccase) that can degrade the dye molecules into smaller fragments [94]. A moderately basophilic endophytic bacterium, Bacillus ferribacterium (Kx898362), was isolated from Asiatica sinensis. After optimization, the biodegradation rate of this strain could reach 92.76% after 72 h under the conditions of a DB-14 dye concentration of 68.78 ppm and the addition of 1 g of sucrose and 2.5% (v/v) inoculants [95]. The halo-alkaliphilic Nesterenkonia lacusekhoensis EMLA3 strain, isolated from textile effluents, degraded 94% of the dye in just 1 h [96]. Pu et al. found that polysaccharide B2, produced by Bacillus gigantium strain PL8, can effectively remove Congo red dye (88.14%) and Pb(II) ions (82.64%) [50]. The MBF showed superior dye removal performance compared to conventional flocculants like polyaluminum chloride and polyacrylamide. The dye-containing MBF flocs could be easily separated by settling or filtration, thus facilitating the removal and recovery of dye pollutants [97].

4.4. Removal and Recovery of Sulfur Compounds

MBFs play a vital role in the treatment of sulfur-laden wastewater, facilitating the separation and recovery of sulfur compounds. While polyaluminum chloride (PAC) demonstrates higher efficiency, MBFs are still effective in flocculating biogenic elemental sulfur (S0), especially when combined with other flocculants like polymer iron sulfate, achieving high turbidity and color removal [98]. Sulfide-laden water can be treated microbially, with Thiobacillus denitrificans oxidizing sulfides to sulfate and a co-culture with floc-forming heterotrophs enabling stable flocculation over extended periods [99]. The sulfate removal efficiency of CYBF biological flocculant reached 54.4%, significantly surpassing that of FeCl3 and alum at the optimal dosage of 8 mg/L and pH 6 [100]. Microbial fuel cells (MFCs) utilizing sulfate-reducing bacteria (SRB) and sulfide-oxidizing bacteria (SOB) biofilms efficiently convert sulfate to sulfide and then to elemental sulfur, enhancing MFC performance [101]. The sulfur cycling mediated by microorganisms has significant environmental implications, particularly in wastewater treatment and pollution bioremediation [102]. Introducing elemental sulfur in denitrification systems can enhance nitrogen removal efficiency in organic-limited nitrate wastewater, with key microbial species contributing to sulfur and nitrogen metabolism [103]. Optimization techniques such as response surface methodology (RSM) can improve the efficiency of MBFa, and solid composite microbial inoculants (SCMIs) offer better storage stability and enhanced removal performance for volatile organic sulfide compounds (VOSCs) compared to microbial suspensions [98,104]. In conclusion, MBFs are effective and environmentally significant in treating sulfur-laden wastewater, with the potential for optimization and improved stability through solid composite inoculants.

4.5. Other Applications

As shown in Figure 3, apart from the above-mentioned contaminants, MBFs have also shown potential in the removal of other pollutants from wastewater, such as nutrients (e.g., nitrogen, phosphorus), oils, microplastics, and organic matter. For instance, the MBF was found to remove 99.2% of arsenite from an aqueous solution [105]. The marine B. cereus-derived MBF exhibited robust flocculation performance, effectively catalyzed the synthesis of antibacterial silver nanoparticles, and facilitated the removal of heavy metals [106]. The MBF from Klebsiella oxytoca GS-4-08 can degrade nitriles in a continuous flow reactor [107]. Microplastics have emerged as a significant environmental and health concern due to their widespread presence in water bodies, soil, and even air [108]. A Promising Approach Biological method for removing microplastics from water and soil offers a sustainable and eco-friendly solution, such as the MBF from Bacillus enclensis being able to biodegrade polyethylene, polypropylene, and polystyrene microplastics [109]. Bacillus gottheilii also appeared as a better potential microplastic degrader [110]. It was proposed that the removal mechanisms involve the complexation and charge neutralization between the pollutants and the functional groups on MBFs. MBFs are also used as eco-friendly flocculants for microalgae harvesting and sludge dewatering in wastewater treatment processes. The MBF can facilitate the flocculation and settling of microalgal cells, thus improving the harvesting efficiency while avoiding the use of harmful chemical flocculants [111]. Similarly, MBFs can enhance the dewaterability of waste sludge by promoting the formation of larger and stronger flocs, thus reducing the moisture content and volume of the sludge [112]. The application of MBFs in microalgae harvesting and sludge dewatering not only reduces the economic and environmental costs but also improves the quality and safety of the harvested biomass. Moreover, bioflocculants can function as an efficient eco-friendly corrosion inhibitor, significantly reducing negative environmental impacts and offering a sustainable alternative to synthetic polymers [113].
Meanwhile, concerning the safety evaluation of bioflocculants, some researchers have uncovered their notable bactericidal and antibacterial properties, for example, in a series of experiments using model water, different raw water sources, and mixed water containing a mixture of these two waters, M. oleifera was found to remove 88%, 82%, and 66% of E. coli [114]. Biological flocculants kill mosquito larvae. With the increase in the dosage of biological flocculant, the mortality rate of larvae increased in Ae. aegypti and C. quinquefasciatus mosquitoes [115]. Tsilo et al. found that bioflocculants showed significant antibacterial properties against both Gram-positive and Gram-negative bacteria [116]. These studies indicate their potential utility as antibacterial agents.

5. Challenges and Future Perspectives

As shown in Figure 4, a microbial flocculant (MBF) exhibits environmentally friendly characteristics, biodegradability, superior efficiency, and selectivity, and shows promise in various applications such as the removal of suspended solids (SSs) and the treatment of heavy metal wastewater, dye wastewater, and sulfur-containing wastewater. Additionally, it can be used for microalgae harvesting, microplastic removal, and bacteria inhibition, making it highly attractive.
However, despite these advantages, MBFs have not yet become a mainstream treatment process due to several challenges and limitations. The main obstacles to MBF production are high substrate cost, low yield, and a complex purification process, leading to increased production costs. Furthermore, the poor stability of biological flocculants, caused by the susceptibility of microorganisms to environmental influences, hinders the large-scale use of these flocculants. Nevertheless, significant progress has been made in screening strains with high yield, high flocculation rates, and improved stability, enhancing the stability of biological flocculants.
Although many hypotheses exist regarding the flocculation mechanism of biological flocculants, further in-depth studies are still required. The advancement of science and technology can aid in exploring the mechanism of flocculation. Before bioflocculants can be produced and used, safety assessments need to be conducted. While some scholars have researched this area, there is currently no unified industry standard in place.
To reduce the production cost, cheap and waste-derived substrates such as agricultural residues, industrial effluents, and wastewater can be used as low-cost carbon and nitrogen sources for MBF production [117]. Strain improvement by mutagenesis and genetic engineering is also a promising approach to enhance the MBF yield and reduce the substrate cost [118]. The variable composition and impurity of MBF products is another challenge that affects their flocculation performance and stability. The composition and properties of MBFs depend on the microbial species, cultivation conditions, and extraction methods, which may lead to batch-to-batch variation and inconsistent product quality [1,119]. Therefore, quality control and standardization of the MBF production process are crucial to ensure the reliability and reproducibility of MBF applications. An in-depth characterization of MBF composition and structure by advanced analytical techniques like FTIR, NMR, GC-MS, and MALDI-TOF is helpful for establishing the quality criteria and optimizing the production process [24,120,121]. The potential microbial contamination and health risks associated with MBF application should also be considered and evaluated. Although MBFs are generally regarded as safe and non-toxic, some MBF-producing strains are opportunistic pathogens that may cause infections in immunocompromised individuals. The presence of residual microbial cells, endotoxins, or pyrogens in MBF products may also pose health hazards [122]. Therefore, strict biosafety assessment and quality control are required to ensure the safety and hygiene of MBF products [123]. The use of non-pathogenic strains, screening biological flocculants with antibacterial activity, cell removal by ultrafiltration, and sterilization by UV or heat treatment can minimize the microbial contamination risks [115]. The potential of bioflocculants as bacteriostatic agents should also be considered in the safety assessment of bioflocculants. Bioflocculants with antibacterial activity serve as effective natural disinfectants for wastewater treatment. Screening biological flocculants with high bacteriostatic performance can make the MBF have both flocculating and disinfecting effects, offering a cost-effective solution for sewage treatment [124].
For future research, more efforts are needed to elucidate the flocculation mechanisms of MBFs and establish the structure–activity relationship [125]. Advanced characterization techniques like SEM, TEM, AFM, and QCM-D can be used to visualize the floc structure and probe the molecular interactions during the MBF flocculation process [126]. Molecular dynamics simulations and quantum chemical calculations are also powerful tools for studying the binding mechanism and energy involved in the MBF–contaminant interaction. A better mechanistic understanding will guide the rational screening and design of MBF for specific wastewater treatment. The combination of MBFs with other physical, chemical, or biological treatment methods is another research direction to enhance the overall treatment efficiency and economy. For example, the sequential use of MBFs and membrane filtration can improve the removal efficiency and flux of the membrane process while reducing the membrane fouling [127]. The modified bioflocculant carrier doped with polylactic acid (PLA) can obviously promote the colonization rate and number of microorganisms on the carrier, and improve the purification efficiency of COD and ammonia nitrogen in wastewater [128]. The development of multifunctional MBFs and their synergistic application with other technologies are expected to bring new opportunities for wastewater treatment and reuse.
Moreover, the emergence of novel nitrogen removal processes, such as partial nitrification, anaerobic ammonium oxidation (anammox), and sulfide-driven autotrophic denitrification, has opened up new avenues for the application of MBFs in wastewater treatment. These innovative biological nitrogen removal methods offer distinct advantages over conventional nitrification–denitrification processes, including reduced energy consumption, lower carbon source requirements, and decreased sludge production [129,130,131]. As these cutting-edge nitrogen removal technologies continue to advance and gain traction, the potential of MBFs in enhancing wastewater treatment efficiency and sustainability becomes increasingly apparent. MBFs can play a pivotal role in wastewater treatment through multiple mechanisms. Firstly, the synergistic use of MBFs with other flocculants can significantly improve pollutant removal efficiency, creating optimal conditions for subsequent nitrogen removal processes [132,133,134]. Secondly, MBFs can promote sulfide-driven autotrophic denitrification, enabling the use of sulfide as an electron donor and the coupling of this process with anammox to further optimize nitrogen removal performance [135,136]. The application of solid composite microbial inoculants in lieu of microbial suspensions can further enhance the storage stability and pollutant removal capabilities of MBFs, contributing to the development of more robust and efficient wastewater treatment systems. As research continues to delve into the integration of MBFs with novel nitrogen removal processes, the potential of MBFs in revolutionizing wastewater treatment and enabling resource recovery becomes increasingly evident. By leveraging the synergies between these technologies, it is possible to develop sustainable, efficient, and cost-effective solutions for wastewater treatment, fostering the protection of aquatic environments and the advancement of a circular economy.

6. Conclusions

This review summarizes the research progress and application potential of MBFs in wastewater treatment and resource recovery. As eco-friendly and sustainable alternatives to synthetic chemical flocculants, MBFs have demonstrated excellent flocculation performance and versatile functions in removing various contaminants (e.g., suspended solids, dyes, heavy metals) from wastewater. The biodegradability, low toxicity, and high selectivity of MBFs make them promising tools for wastewater purification and sludge dewatering processes.
To address the challenges related to high production costs and quality inconsistencies, certain strategies can be adopted, such as waste valorization, strain improvement, and process optimization. Additionally, the biosafety evaluation and standardization of MBF production are essential to ensure reliability and safety in practical applications. Future research should focus on elucidating the flocculation mechanisms, designing novel composite MBF flocculants, and integrating MBFs with other technologies to achieve synergistic wastewater treatment.
This paper reviews the research progress and application potential of MBFs in wastewater treatment and resource recovery from different sources, main categories, production processes, flocculation properties, and mechanisms, and combines new scientific research technologies. Advanced analytical techniques were used to characterize the composition and structure of MBFs to study the mechanism of flocculation, to develop the collaborative application of MBFs with other technologies, to evaluate the safety of biological flocculants, to study MBFs with both flocculation and bactericidal functions, and to develop the application potential in novel nitrogen removal processes.
As the demand for sustainable and cost-effective water treatment solutions continues to grow, the development and application of MBFs in wastewater purification and resource recovery are expected to receive increased attention and momentum in the future.

Author Contributions

Conceptualization, Y.Y. and C.J.; resources, X.W., Y.X., D.W., L.F., J.P., X.Z. (Xinyuan Zhang) and T.Y.; writing—original draft preparation, Y.Y.; writing—review and editing, C.J. and X.Z. (Xuliang Zhuang); supervision, X.Z. (Xuliang Zhuang); funding acquisition, X.Z. (Xuliang Zhuang). All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (nos. 42177099 and 42230411), the Provincial Science and Technology Innovative Program for Carbon Peak and Carbon Neutrality of Jiangsu of China, the “Leading Goose” R&D Program of Zhejiang (no. 2023C03131 and no. 2023C03132), and the Key Technology and Equipment System for Intelligent Control of the Water Supply Network (no. 2022YFC3203800).

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Acknowledgments

We are grateful for the meticulous guidance provided by the teachers, and we extend our thanks to all the students who contributed to this article.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Water 16 01995 g001
Figure 1. Chemical structures of different categories of MBFs.
Figure 1. Chemical structures of different categories of MBFs.
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Figure 2. Proposed flocculation mechanisms of MBFs. (At present, there are three main hypotheses about the mechanism of bioflocculants: charge neutralization, adsorption bridging, and precipitation net trapping. In addition, there are other hypotheses about the mechanism, such as the formation of hydrogen bonds between bioflocculants and hydroxyl groups on MBFs and water molecules or particles.)
Figure 2. Proposed flocculation mechanisms of MBFs. (At present, there are three main hypotheses about the mechanism of bioflocculants: charge neutralization, adsorption bridging, and precipitation net trapping. In addition, there are other hypotheses about the mechanism, such as the formation of hydrogen bonds between bioflocculants and hydroxyl groups on MBFs and water molecules or particles.)
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Figure 3. Applications in wastewater treatment. (Biological flocculants hold significant promise for sewage treatment, as they can efficiently eliminate suspended solids, heavy metals, dyes, and sulfur compounds from water. They also have numerous other applications, such as microalgae harvesting and enhancing sludge dewatering capacity.)
Figure 3. Applications in wastewater treatment. (Biological flocculants hold significant promise for sewage treatment, as they can efficiently eliminate suspended solids, heavy metals, dyes, and sulfur compounds from water. They also have numerous other applications, such as microalgae harvesting and enhancing sludge dewatering capacity.)
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Figure 4. Challenges and future perspectives.
Figure 4. Challenges and future perspectives.
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Table 1. Typical MBF-producing microorganisms.
Table 1. Typical MBF-producing microorganisms.
MicroorganismSourceMBF YieldReference
Bacillus mucilaginosusFarmland soil1.58–2.19 g/L[26]
Bacillus licheniformisSoil2.84 g/L[27]
Bacillus velezensisActivated sludge7.6 g/L[28]
Bacillus mojavensisAgricultural soil1.33 g/L[29]
Aspergillus parasiticusActivated sludge0.54 g/L[30]
Enterobacter cloacaeRecycled sludge2.27 g/L[31]
Klebsiella variicolaSoil6.96 g/L[32]
Serratia ficariaSoil2.41 g/L[33]
Aspergillus flavus—0.4 g/L[34]
Penicillium purpurogenumLaboratory6.4 g/L[35]
Phanerochaete chrysosporiumWastewater sludge2.2 g/L[36]
Paenibacillus mucilaginosusSoil7.8 g/L[37]
Lipomyces starkeyiMangrove ecosystem62.1 ± 1.2 g/L[38]
Alcaligenes faecalisSediment sample4 g/L[39]
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Yang, Y.; Jiang, C.; Wang, X.; Fan, L.; Xie, Y.; Wang, D.; Yang, T.; Peng, J.; Zhang, X.; Zhuang, X. Unraveling the Potential of Microbial Flocculants: Preparation, Performance, and Applications in Wastewater Treatment. Water 2024, 16, 1995. https://doi.org/10.3390/w16141995

AMA Style

Yang Y, Jiang C, Wang X, Fan L, Xie Y, Wang D, Yang T, Peng J, Zhang X, Zhuang X. Unraveling the Potential of Microbial Flocculants: Preparation, Performance, and Applications in Wastewater Treatment. Water. 2024; 16(14):1995. https://doi.org/10.3390/w16141995

Chicago/Turabian Style

Yang, Yang, Cancan Jiang, Xu Wang, Lijing Fan, Yawen Xie, Danhua Wang, Tiancheng Yang, Jiang Peng, Xinyuan Zhang, and Xuliang Zhuang. 2024. "Unraveling the Potential of Microbial Flocculants: Preparation, Performance, and Applications in Wastewater Treatment" Water 16, no. 14: 1995. https://doi.org/10.3390/w16141995

APA Style

Yang, Y., Jiang, C., Wang, X., Fan, L., Xie, Y., Wang, D., Yang, T., Peng, J., Zhang, X., & Zhuang, X. (2024). Unraveling the Potential of Microbial Flocculants: Preparation, Performance, and Applications in Wastewater Treatment. Water, 16(14), 1995. https://doi.org/10.3390/w16141995

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