Biosurfactants as Key Agents in Microbial Remediation of Polycyclic Aromatic Hydrocarbons: A Review

Introduction

The persistent release of harmful organic contaminants, stemming from natural and anthropogenic activities such as industrial expansion, vehicular exhaust, cigarette smoke, municipal waste drain-offs, forest fires, and volcanic eruptions underscores the urgent need for effective pollution mitigation strategies (Liu et al., 2019).  These organic pollutants cover a wide array of xenobiotic chemicals including polychlorinated biphenyls, polycyclic aromatic hydrocarbons, gasoline, paints, plastics, adhesives, pesticides, and toluene (Sánchez, 2022). The frequent usage of petroleum and its derivatives has released a major portion of polycyclic aromatic hydrocarbons into the environment (Silva et al., 2014). Polycyclic aromatic hydrocarbons, a major constituent of petroleum, pose a severe threat to human health and ecosystem (Souza et al., 2014). Polycyclic aromatic hydrocarbons stand out due to their carcinogenic and mutagenic properties, necessitating the development of innovative remediation approaches (Nanca et al., 2018; Mobeen & Dawood, 2022). Polycyclic aromatic hydrocarbons contain two or more fused benzene rings arranged in various positions. PAH properties vary significantly with molecular weight, affecting their behavior and fate in the environment. The hydrophobic nature of PAHs facilitates their cellular uptake, where they induce cytochrome P450 enzyme expression, catalysing their biotransformation into reactive intermediates capable of forming DNA adducts, thereby contributing to carcinogenicity (Honda & Suzuki, 2020). Therefore, it is crucial to eliminate or detoxify PAHs from the environment to alleviate toxic effects on humans, plants, and animals.  

Conventional methods for PAHs removal, including soil washing and thermal treatments, often prove costly, ineffective, and environmentally disruptive, creating a demand for eco-friendly alternatives (Patel et al., 2020). This has led to increased interest in bioremediation techniques, which control the natural abilities of microorganisms to degrade pollutants (Koshlaf & Ball, 2017). Bioremediation, which harnesses the metabolic abilities of microorganisms to degrade or transform contaminants, has emerged as a promising strategy (Lipińska et al., 2014). The major challenge for biodegradation of PAHs is their low water solubility.  However, certain microbes can produce surface-active compounds known as biosurfactants. Biosurfactants are amphipathic and can be synthesized by bacterial, fungal, and yeast strains (Nie et al., 2010) and offer various advantages such as enhanced microbial activity, bioavailability, and solubility. Microbial strategies involve robust enzymatic systems comprising stable enzymes produced under extreme conditions, along with the ability to synthesize natural surfactants that enhance the bioavailability of hydrophobic organic pollutants (Kaczorek et al., 2018). Biosurfactants enhance the hydrophobicity of the microbial cell surface, thereby facilitating the access to and utilization of hydrophobic substrates by the producing microorganisms (Perfumo et al., 2010; Vischer & Burkard, 2023). For instance, rhamnolipids produced by Bacillus Lz-2 were used to increase the solubilization of PAHs, facilitating enhanced biodegradation (Shudong et al., 2015). Hence, the application of biosurfactants in bioremediation has been recognized as a promising approach to mitigating PAH's environmental pollution. 

Polycyclic Aromatic Hydrocarbons Properties, Sources and Bioavailability

Polycyclic Aromatic Hydrocarbons (PAHs) are a group of organic compounds/pollutants comprised of multiple fused benzene rings, produced due to incomplete combustion of coal, oil and petroleum, automobile exhaust, forest fires, and cigarette smoke. The increasing demand for processed petroleum and agricultural products has contributed to the contamination of the environment with PAHs (Satyaprakash et al., 2017). Due to low water solubility and lipophilic nature, PAHs tend to persist in the environment, accumulating in soils and sediments, and posing long-term risks to the environment and health of humans. PAHs can contaminate various environmental compartments, including soil, water, and air, posing risks to ecosystems and human health. The environmental impact of PAHs is further exacerbated by their ability to undergo long-range transport, facilitating their dispersal across geographical boundaries. PAHs are classified based on chemical structure and molecular weight including low and high molecular weight PAHs. The no. of aromatic rings in low molecular weight is ≤3, whereas in high molecular weight is >3. For example, low molecular weight PAHs include naphthalene, fluorene, acenaphthene, anthracene, and phenanthrene; whereas high molecular weight PAHs comprise chrysene, benz(a)anthracene, pyrene, benzo(a)pyrene, benzo(b)fluoranthene, and indeno(c,d)pyrene.  PAHs are neutral and non-polar molecules, their hydrophobicity, vapor pressure, and solubility in water vary with molecular weight as shown in Table 1. As molecular weight increases, the melting and boiling points increase, and the vapor pressure and solubility in water decreases. The US Environmental Protection Agency (EPA) recognized that 16 PAHs are highly concerned pollutants. The International Agency for Research on Cancer (IARC) categorized three specific PAHs as probable carcinogens (Group 2A) namely benzo(a)anthracene, dibenz(a,h)anthracene, and benzo(a)pyrene (Nagar et al., 2023).  Considering PAH's status as carcinogenic, widespread, and persistent chemicals in the environment, raises significant concern on PAHs pollution. PAH toxicity has adverse health effects on humans, animals, aquatic life, and plants. For instance, in humans PAH exposure via inhalation and dermal contact cause cancer, respiratory, neurological, and cardiovascular problems (Barathi et al., 2023). Hence, it is critical to plan effective, sustainable, and eco-friendly remediation strategies to eliminate carcinogenic PAHs from water and soil sediments. Among various available bioremediation methods, microbial bioremediation with biosurfactant production is a promising and sustainable approach for the effective handling of PAH environmental pollution. 

Table 1. Properties of some polycyclic aromatic hydrocarbons (NCBI, 2025)

Biosurfactants in PAHs Bioremediation

Biosurfactants are surface-active compounds produced by microorganisms, possessing both hydrophobic and hydrophilic regions that interact with different polarity molecules allowing them to reduce surface and interfacial tension between liquids, solids, and gases (Sharma et al., 2022). Their amphiphilic nature is crucial for enhancing the bioavailability and decreasing surface tension of hydrophobic pollutants like PAHs, thereby facilitating bacterial access.  Biosurfactants are highly beneficial compared to synthetic surfactants due to being non-toxic, biodegradable, higher specificity, and effective in extreme environments (Pi et al., 2017; Sanchali et al., 2024). These substances consist of a hydrophilic region composed of amino acids, mono- or polysaccharides, or peptides, and a hydrophobic region made up of saturated or unsaturated fatty acids (Ludovichetti et al., 2024; Sanchali et al., 2024). Biosurfactants are classified as glycolipids, phospholipids, polymeric macromolecules, lipopeptides/lipoproteins, and fatty acids (Nie et al., 2010).  Further biosurfactants sub classified based on chemical structure and molecular weight as low and molecular weight biosurfactants. High molecular-weight surfactants bind strongly to the surface, whereas low molecular-weight surfactants decrease surface and interfacial tension (Vogel et al., 2023; Banerjee et al., 2024). Among these, glycolipids and lipopeptides are promising biosurfactants in solubilizing PAHs, and facilitate access to microbial enzymes that break them down. Biosurfactants can increase the solubility of PAHs through micelle formation, wherein the hydrophobic tails of the bio-surfactant molecules aggregate to form a core that solubilizes the PAH molecules, while the hydrophilic heads interact with the surrounding water, facilitating their transport and uptake by microorganisms (Lamichhane et al., 2017; Mahmood et al., 2022). Eventually, results in the degradation of PAHs into less hazardous compounds as shown in Figure 1. Furthermore, biosurfactants can also promote the detachment of PAHs from soil particles, facilitating their mobilization and transport to microbial cells. Beyond their solubilization capabilities, biosurfactants can also alter the cell surface hydrophobicity of microorganisms, promoting their adhesion to hydrophobic pollutants and enhancing direct contact between the cells and PAHs.

Mechanisms of Biosurfactant Assisted PAHs Bioremediation

Biosurfactants enhance the bioremediation of PAHs through several mechanisms, including increasing the solubility and bioavailability of PAHs, enhancing microbial access to PAHs, and thus promoting the biodegradation of PAHs. By reducing surface tension and interfacial tension, biosurfactants facilitate the emulsification of PAHs and the formation of micelle, increasing the surface area available for microbial attack. Biosurfactants can interact with the cell membranes of microorganisms, increasing their hydrophobicity and promoting their adhesion to PAHs. Biosurfactants can directly interact with PAH molecules, altering their chemical structure and making them more susceptible to enzymatic degradation.

To mitigate oil spill pollution in the marine environment, synthetic surfactants are generally considered in the ocean, however, these are associated with certain drawbacks including toxicity, degradability, and secondary pollution (Liu et al., 2022; Sharma et al., 2022). Biosurfactants are a major alternative to synthetic surfactants, which have high emulsifying action and surface activity. When biosurfactants are released by microbes into aqueous PAHs suspension, their monomers form sphere-shaping micelles, as a result hydrophobic end of the surfactant turns towards the center, composing the nucleus, whereas the hydrophilic end is turned to the surface and interact with water. Thus, biosurfactants increase the solubility of PAHs, reduce surface tension at the interface, enhance the bioavailability of PAHs to microbes, and facilitate higher degradation rates (Soberon-Chavez & Maier, 2010). Some of the biosurfactants reported in the literature for improving the degradation of PAHs are presented in Table 2.

Table 2. Biosurfactants produced by different bacteria enhance the biodegradability of PAHs