Microbe–plant–nanoparticle interactions: role in bioremediation of petroleum hydrocarbons

Man's quest to satisfy his needs coupled with an increase in urbanization, advancement, and civilization has resulted in the generation of waste with an eventual contamination of the environment (Kour et al. 2022). Owing to its limited degradability, high persistence in environmental matrices, and toxic nature, pollution by petroleum hydrocarbons (PHCs) has become a global concern and a subject of scientific interest (Unimke et al. 2020, 2021; De Almeida et al. 2021). The limitations of conventional physicochemical and biological remediation solutions could be solved by combining remediation techniques (Bensaidia et al. 2021). An effective, affordable, and environmentally benign method of reducing petroleum toxins is provided by the advanced idea of bioremediation, which has evolved into nanobioremediation (Cheng et al. 2019; Nandini et al. 2023). In the context of remediation, nanomaterials are defined as particles that, in their single-dimensional form, are at least 100 nm in size. As such, they differ from their bulk counterparts in important physical, chemical, and biological ways. Under various circumstances, the cleanup of PHC has been accomplished with the use of many nanomaterials (De Almeida et al. 2021). When nanoparticles (NPs) are used in conjunction with microorganisms and plants to remove PHCs, the interplay between these three elements determines how effective the remediation process is. This interaction can also affect the ability of the bacteria to remediate. Microbes that interact with one another may become more noxious, adaptable, or proliferate more rapidly (Barathi et al. 2023).

According to Barathi et al. (2023), abiotic and biotic processes are combined in the integrated concepts of NPs, bacteria, and plants known as nanobioremediation and nanorhizoremediation. The first stage involves the introduction of NPs into a contaminated system and is followed by adsorption, dissolution, photochemical reactions, and absorption. Microbial introduction mechanisms like bioaccumulation, biostimulation, and biotransformation are included in the second phase. In the beginning, the NPs increase the bioavailability for microbial assault by adsorbing hydrocarbons onto their surfaces. This provides an integrated method for treating PHC contamination that combines the advantages of bioremediation with nanotechnology. Many types of nanomaterials with the ability to remediate polycyclic aromatic hydrocarbons (PAHs) can be produced chemically or biologically (Bensaidia et al. 2021). Although they can be hazardous at greater quantities, they also aid in the growth and adaptability of bacteria that break down PHCs. Rhizoremediation has gained popularity among scientists as an attractive strategy because, in addition to providing a rich niche for bacteria to flourish at the expense of root exudates, bacteria also act as biocatalysts that remove contaminants (Ehmedan et al. 2021). The intricate beneficial relationships between microbes and plants are the subject of fascinating research. Rhizobacteria efficiently invade plant roots and degrade a wide range of pollutants. Plants influence the selection of their own rhizospheric bacteria, natural secondary plant compounds can promote catabolic pathways, and horizontal gene transfer is important for bioremediation (Ehmedan et al. 2021). Improved remediation results could be achieved by manipulating the interactions among microbes, plants, and NPs. The effective breakdown of total PHCs can be achieved by introducing oil-tolerant plants and bacteria into oil-contaminated environments through the use of microbe–plant–NP interactions, this approach presents a successful remediation technology (Cheng et al. 2019; Chaudhary et al. 2023; Nandini et al. 2023).

This article discusses the special qualities of microorganisms, plants, and NPs as well as their production processes and interactions during the remediation of PHC contaminants. Similarly, the role of microbe–plant–NP interactions in the bioremediation of PHCs will be detailed.

Microbe–plant–nanobioremediation offers several advantages over conventional remediation methods when it comes to addressing pollution, particularly in the context of petroleum hydrocarbon contamination. Here's why this interaction is considered better in many cases (Cheng et al. 2019; Chaudhary et al. 2023; Nandini et al. 2023; Rajput et al. 2023; Wang et al. 2023a, b):

• (a) Enhanced efficiency: microbe–plant–nanobioremediation possesses a large surface area-to-volume ratio, which increases their reactivity and ability to interact with contaminants, thereby speeding up the degradation process. They can improve the bioavailability of pollutants by breaking them down into smaller particles that microbes can more easily consume.

• (b) Targeted action: microbe–plant–nanobioremediation can be engineered to specifically target pollutants, making them highly effective in focusing on the contamination area. They can be functionalized with specific chemicals or enzymes that are capable of breaking down complex hydrocarbons, which makes them ideal for bioremediation tasks.

• (c) Enhanced microbial activity: in nanobioremediation, the interactions between microbe–plant–NPs can support the growth and activity of microbes by providing nutrients or improving environmental conditions (e.g., pH, oxygen levels). Some NPs act as electron donors or acceptors, boosting the metabolic processes of microbes involved in breaking down hydrocarbons.

• (d) Versatility in harsh conditions: NPs are more resilient in extreme environments (high salinity, temperature, or toxicity) where traditional bioremediation techniques might fail. They can be adapted for use in various soil types and water bodies.

• (e) Reduced secondary pollution: compared to chemical or physical methods (e.g., burning, solvent extraction), microbe–plant–nanobioremediation tends to produce fewer harmful byproducts or secondary pollutants. It is an eco-friendlier approach since the degradation byproducts are often less toxic than those resulting from chemical treatments.

• (f) Cost-effective: while the initial development and deployment of nanomaterials may be costly, the efficiency and reduced time needed for remediation can lower the overall cost in the long term. Microbe–plant–nanobioremediation can reduce the need for frequent treatments, minimizing labor and operational costs.

• (g) And finally microbe–plant–nanobioremediation offers enhanced soil and water quality.

PHCs are complex mixtures made up of several components aggregated together, such as solids, slurry, emulsion, and crude oil. They consist mostly of hazardous and non-biodegradable materials (Wu et al. 2023). In addition to posing a direct and indirect risk to human, animal, and plant health, the extraction, processing, transportation, and leaking of petroleum and its products have severely contaminated soil and water (Ossai et al. 2019; Shahzad et al. 2020; Karam & Al-Wazzan 2021). All kinds of life are impacted, either directly or indirectly, by the inadvertent or intentional release of these substances into the environment, (Ahmed et al. 2020a, b). The intermittent release and disposal of petroleum and hydrocarbon wastes results in soil pollution. Thus, the petroleum wastes that affected the soil would not support the flora and the land remained barren for decades until remediated (Sattar et al. 2022). In a similar vein, excessive reliance on petroleum resources contaminates water resources, especially rivers, streams, and agricultural waterways near oil rigs and processing complexes (Balogh & Watson 2020). Because oily wastes are less dense than other wastes, they can float over the surface of water and settle in areas that support photosynthetic plants and creatures. Heavy petroleum waste, on the other hand, seeps below, reducing soil porosity and tainting groundwater (Sayed et al. 2021). According to Srivastava et al. (2019), hydrocarbons are known to contain a variety of hazardous chemicals, depending on the source, organic materials present, the geological setting, and the rate of decomposition. This is more probable due to the fact that petroleum is produced from biomass of biogenic origin, such as phytoplankton and marine algae and terrestrial plants. Additionally, marine algae have a high concentration of organic materials, particularly nitrogenous and fatty molecules, whereas terrestrial plants have significant concentrations of lignin, cellulose, and other carbon-containing components. Different hydrocarbons originating from terrestrial plants or algae have different structures and behaviors, which lead to different kinds of pollution during the exploration process (Sattar et al. 2022).

One of the most prevalent types of environmental contamination is PHC. When introduced into a habitat, it alters and becomes less functional for ecosystems (Truskewycz et al. 2019). The presence of PHCs in the environment can inhibit or hinder microbial species, altering the ecosystem and microbial community functionality. The direct toxicity of hydrocarbons also affects plants, and their productivity is much reduced since they are unable to receive light, nutrients, or water because the oil blocks their passage through the soil matrix. Both natural and man-made sources allow them to enter the environment, which causes weathering. Physical (dispersion), physiochemical (evaporation, dissolution, sorption), chemical (photo-oxidation, auto-oxidation), and biological (plant and microbial hydrocarbon catabolism) factors all play a role in the weathering of PHCs (Hoang et al. 2021a).

Despite the large number of hydrocarbons found in petroleum products and the widespread nature of petroleum use around the world and its attendant contamination, only a relatively small number of the compounds are well characterized for toxicity (Hegazy et al. 2023). The health effects of some fractions can be well characterized, based on their components or representative compounds (e.g., light aromatic fraction-BTEX-benzene, toluene, ethylbenzene, and xylenes). However, heavier TPH fractions have far fewer well-characterized compounds.

Polycyclic aromatic hydrocarbons (PAHs) are widespread persistent contaminants that enter the environment from both natural and anthropogenic sources (Panchenko et al. 2023). The principal role of PAHs in environmental degradation is played by biological systems. The most important among these are plants and microorganisms, which have a flexible metabolism and unique mechanisms of pollutant detoxification.

The rhizosphere is a microhabitat made up of roots and the 1–2 mm of soil that surrounds them. Plants and microorganisms engage in a vigorous chemical conversation in the rhizosphere (Sasse et al. 2018; Caracciolo & Terenzi 2021). It is the area around a plant's roots where microbial activity reaches its peak and is essential to the preservation of the plant's health (Wang et al. 2023a, b). Plant and microbial communication is particularly active in the soil microzone known as the root zone (Rzehak et al. 2022). This is because different microbially helpful vitamins, enzymes, plant growth regulators, and amino acids can be secreted by plant roots (Chamkhi et al. 2021a, b), and these substances can affect the species, quantity, and distribution of rhizosphere bacteria (Vives-Peris et al. 2020).

One of the planet's most complex and functionally active ecosystems, the rhizosphere improves plant health and lessens the effects of biotic and abiotic challenges (Afridi et al. 2022). This is because plants have the ability to draw in and support a variety of microbe populations that coexist as a single organism to form microbial communities (Krishna et al. 2019; Yuan et al. 2022). These communities can coexist and produce synergistic effects that can enhance plant productivity and functions as well as the plants' ability to adapt to stressful environments (Caracciolo & Terenzi 2021). Plants have unique rhizospheric bacteria ecological niches in their roots that allow them to invade the phylosphere. Numerous microbial communities related to plants, such as fungi, actinomycetes, nematodes, bacteria, protozoa, protists, and archaea, inhabit the rhizosphere, also known as the plant microbiome (Zhang et al. 2021). These microorganisms are essential for restoring the degraded environment and maintaining the productivity and characteristics of the soil. Research conducted by Adedeji et al. (2020) demonstrated that several low-weight organic compounds secreted by plants, which facilitate the cooperation between host plants and particular symbionts or microbes in the rhizosphere, enhance plant development, diminish systemic resistance, and augment agricultural productivity. According to Wahab et al. (2023), fungi, for example, improve a plant's ability to absorb water and nutrients, increase its resilience to disease, and release hormones that aid in the development of a large root system.

According to Kumawat et al. (2021), root exudates have the ability to alter the chemical and physical properties of soil and may operate as potential motors to draw microorganisms from the bulk soil into the targeted rhizosphere niche. Microbes that promote plant growth have been shown to have beneficial effects (Wang et al. 2023a, b) and have been employed to boost crop productivity. These microbes promote plant growth through a variety of mechanisms, such as nutrient activation and a reduction in reliance on synthetic fertilizers (Olenska et al. 2020), as well as the inhibition of soil-borne illnesses (Jiao et al. 2021). The rhizosphere is home to a variety of microorganisms, including bacteria and fungi, which support root zone plant rejuvenation (Yu et al. 2020). The most common bacterial species in the soil rhizosphere, according to studies by Zhao et al. (2021), are Blastoccocus, Nocardiodes, Sphingomonas, Bacillus, and Solirubrobacter. These bacteria have been found in crops including maize (Zhao et al. 2021) and cucumber (Li et al. 2021). According to Yu et al. (2020), rhizosphere soils are frequently a rich source of microorganisms with the metabolic capacity to break down organic pollutants like crude oil while also promoting plant growth. Similarly, Bhuyan et al. (2023) found that in crude oil-contaminated soil, a bacterial consortium-NPK-biostimulation changed the rhizosphere microbiome and increased the breakdown of PHCs.

The escalating concern surrounding PHCs, a critical byproduct of industrial development, is garnering significant attention globally. These contaminants, originating primarily from crude oil and its derivatives, have become pervasive across various environments such as soil, water, and air, as highlighted by studies from Mohammadi et al. (2020). Nigeria's intensive processing and exploitation of crude oil has resulted in significant environmental deterioration, making the country a prime example of the environmental impact of these pollutants (Adeola et al. 2022). PHCs consist of a number of compounds, such as PAHs and BTEX (benzene, toluene, ethylbenzene, and xylene). PAHs are notorious for their toxicity, propensity to bioaccumulate, and, most importantly, their carcinogenic, tumorigenic, and mutagenic qualities, which provide serious health dangers. In the environment, these hydrocarbons often bind to organic matter, which hinders microbial degradation (Zhang et al. 2020).

The infiltration of PHCs into ecosystems has far-reaching and detrimental consequences. Soil contamination affects microbial and chemical dynamics, leading to reduced fertility and altered nutrient cycles (Russo et al. 2023). Water bodies contaminated with these hydrocarbons experience decreased oxygen levels and disrupted aquatic ecosystems, while air quality deterioration leads to various health issues in humans and animals (Russo et al. 2023). The carcinogenic and mutagenic nature of many hydrocarbon compounds underscores the urgent need for effective management and remediation strategies. Exploration and extraction of crude oil, particularly in the Niger Delta, is the main cause of environmental degradation in Nigeria that is associated with oil pollution. This region has suffered from numerous pollution hazards, including accidental oil spillage and pipeline vandalism (Akpoghelie et al. 2021). The Nigerian National Petroleum Corporation estimates an annual spillage of approximately 2,300 m³ of oil across over 3,000 incidents (Ejeromedoghene et al. 2020). Such spillages pose a significant threat to farmlands, crops, and forest species, altering soil properties and impacting both terrestrial and aquatic ecosystems. One indirect effect includes oxygen deprivation in plant roots due to soil oxygen consumption by oil-degrading microorganisms, leading to anaerobic conditions and potential hydrogen sulfide formation (Ukhurebor et al. 2021).

Microorganisms are essential to the process of bioremediation, with bacteria, fungi, and algae effectively breaking down complex hydrocarbon structures (Bala et al. 2022; Haripriyan et al. 2022). These organisms utilize mechanisms like mineralization, where pollutants serve as a carbon and energy source, and co-metabolism, where pollutant degradation occurs alongside other metabolic processes. Bacteria are particularly crucial in degrading aromatic compounds, although limitations exist, such as the specificity of degrading enzymes and the need for direct contact with pollutants to initiate enzyme synthesis (Bala et al. 2022). Fungi, another key group in bioremediation, efficiently degrade a wide variety of compounds, including aromatic ones, through various enzymatic systems (Singh et al. 2019). Their ability to secrete extracellular enzymes with low substrate specificity enhances their effectiveness in complex pollutant degradation. Specific microorganisms, such as Pseudomonas and Mycobacterium species in bacteria, and Phanerochaete chrysosporium in fungi, have shown significant potential in degrading various PHCs. However, challenges persist, including the adaptation of these organisms to polluted environments and the degradation of more complex compounds (Victor et al. 2020; Premnath et al. 2021).

The most rapid and complete degradation of the majority of petroleum pollutants is brought about under aerobic conditions (Sayed et al. 2021). The initial intracellular attack of the pollutants is an oxidative process and the activation as well as incorporation of oxygen is the enzymatic key reaction catalyzed by oxygenases and peroxidases. Biosynthesis of cell biomass occurs from the central precursor metabolites, for example, acetyl-CoA, succinate, and pyruvate. Sugars required for various biosynthesis and growth are synthesized by gluconeogenesis. The degradation of PHCs can be mediated by specific enzyme systems. Other mechanisms involved are the attachment of microbial cells to the substrates and the production of biosurfactants. The uptake mechanism linked to the attachment of cells to oil droplets is still unknown but the production of biosurfactants has been well studied (De Almeida et al. 2021).

The extent of the harm caused by crude oil pollution depends on a number of variables, including the amount and kind of oil, the presence of vegetation in the affected area, the current weather, the degree of oil degradation, and the soil's structure. These hydrocarbons are made up of complex chemical compounds that are widely distributed and have different molecular weights, including non-hydrocarbon constituents.

The development of nanobioremediation in recent years has shown promise in the cleanup of PHC-contaminated soil and water (Rajput et al. 2022). This is due to the effectiveness of combining bioremediation with the supremacy of nanotechnology to address the challenges. Nanobioremediation is a component of bioremediation, that utilizes the special properties of nanomaterials, such as high reactivity, high surface area, low percolation threshold, catalytic properties, etc., to boost microbial activity and enhance microbial processes in the remediation of environmental contaminants. This synergy between bioremediation and nanotechnology offers several advantages in various ways, i.e., by creating a protective shield, nanomaterials can shield microorganisms from unfavorable environmental factors (such as fluctuating temperatures, high pH, and salinity) in contaminated settings (Balla et al. 2022). Second, nanomaterials have the ability to encapsulate hydrophobic hydrocarbons, thereby enhancing their bioavailability for microbial degradation and hence, accelerating the remediation activities (Zhu et al. 2022). Additionally, engineered nanomaterials, such as iron NPs have demonstrated the potential of converting harmful PHCs into less toxic compounds, thereby removing these contaminants from the environment (Chauhan et al. 2023). Furthermore, it was also proven that nanomaterials serve as carriers for hydrocarbon-degrading microorganisms (Kundu et al. 2024), transporting them to the contaminated sites, thereby facilitating the degradation of the contaminants, and hence ameliorating the hazardous impact of the contaminants.

The techniques of nanobioremediation continue to evolve rapidly due to the synergistic nature of the nanomaterials with the microorganisms (Table 2). Some of the recently recognized developments include but are not limited to the following. Metal nanomaterials such as iron nanomaterials were recognized for their ability to stimulate anaerobic hydrocarbon degradation and reductive dichlorination (Chen et al. 2020). Also, silver nanomaterials were recognized to curb the risk of secondary pollution in contaminated sites, through inhibition of microbial growth, due to their antibacterial properties (Padhye et al. 2023). Because of their strong adsorption capacities, nanostructured materials such as zeolites and dendritic polymers are receiving more attention in the degradation of hydrocarbon pollutants (Arkas et al. 2022). Additionally, functionalized carbon nanotubes are being used to strengthen microorganisms in the degradation of PHC through the promotion of biofilm formation (Li et al. 2022). Additionally, in an effort to improve the remediation of PHC pollution, researchers are assembling microbial consortia made up of bacteria that degrade hydrocarbons and microorganisms that reduce metals (Irfan et al. 2020; Mahmud et al. 2022; Lashani et al. 2023; Zhou et al. 2023).

The region surrounding plant roots that is nutrient-aggregated is known as the rhizosphere. It is made up of a population of microbes that stimulate or improve plant development (Pantigoso et al. 2022). These microbes interact with plants on a large scale and help reduce harmful soil pollutants like polychlorinated biphenyls, halogenated chemicals, pesticides that contain atrazine, heavy metals like mercury and cadmium, and PHCs (Riseh et al. 2023). The cleansing process of hazardous pollutants facilitated by the rhizospheric microorganisms is referred to as rhizoremediation, signifying a critical role in soil remediation by promoting plant growth and simultaneously acting as a remedial force against various hazardous substances present in the soil environment. Rhizoremediation harnesses the collaborative action of plant roots and their associated microorganisms to break down, confine, or immobilize contaminants within soil matrices. The rhizospheric environment provides an ideal habitat for the growth of microbes that specialize in the breakdown of PHCs (Hoang et al. 2021a). The combined action of root exudate effusions (which include sugars, organic, and amino acids) and the presence of microbes that break down PHCs makes this process extremely effective. This synergy accelerates the degradation rate, rendering rhizoremediation a highly efficient approach for the treatment of contaminated environments (Alotaibi et al. 2021). An environmentally beneficial method for cleaning up PHC contamination is rhizoremediation. The results are remarkable, either totally eliminating contaminants or changing them into innocuous forms, despite the time commitment. Both large and small pollution sites with low to moderate pollutant levels can use this technique (Hoang et al. 2021a).

Rhizoremediation is a non-invasive technique that reduces the bulk movement of pollutants while protecting soil from structural and functional damage. The diverse nature of root exudates produced by plants can potentially stimulate the initial establishment of a microbial community driven by available substrates, leading to subsequent alterations in rhizosphere dynamics (Chojnacka et al. 2023). Consequently, even among closely related plant genotypes, considerable diversity may exist in the microbial populations within the rhizosphere, showcasing distinct abilities to degrade contaminants at varying rates. Plant species, including closely related genotypes, display differences in their capacity for the remediation of PHCs (Dagher et al. 2019). According to Kiamarsi et al. (2020) and Steliga & Kluk (2020), grasses are good candidates for TPH removal in soil, suggesting their potential importance in rhizoremediation. The intricate relationship between plant roots and microbes establishes a fertile environment for microbial growth, sustained by root effusions (Hatami et al. 2019). These microbes, functioning as biocatalysts, undertake the critical task of pollutant removal. Certain contaminants, such as aliphatic hydrocarbons (n-alkane, for example), are easily broken down by aerobic microbes, which are first activated by using molecular oxygen. This degradation pathway's mechanism is represented by terminal oxidation. The first stage is the oxidation of the substrate molecule, which results in the addition of an oxygen atom to the terminal methyl group and the creation of an alcohol group (Laczi et al. 2020).

The industries that have demonstrated a great deal of interest in nanotechnology—a field of study that deals with the creation, modification, and application of NPs (sizes between 1 and 100 nm)—include agriculture, medical sciences, pharmaceuticals, electronics, textiles, and biochemical sensors. When NPs are applied to soils, the region where plant roots and soil come in contact with NPs is referred to as the rhizosphere, which is a microecological niche that is considered as a site for elevated biochemical activities. The rhizosphere acts as the plant's first line of defense against contaminants, such as NPs, and also acts as a point of entry for bacteria and nutrients that operate on plant roots by going through the root system and taking part in the movement of materials. Plant growth and development are dependent on a healthy rhizosphere environment.

The presence of NPs in the soil can result in a significant impact on the microbial numbers and type as well as stimulate or inhibit microbial growth and abundance further selecting their diversity.

Application of nanoagrochemicals, NP-containing supplements (such as biosolids, sludge, and manure), contamination by industrial wastes, irrigation water, plant litter, animal feces, carcasses, exuviae, and atmospheric deposition are some of the ways that NPs can enter soil (Tian et al. 2019). According to Wang et al. (2023a, b), the buildup of metal NPs in the soil–plant system may unavoidably have a direct or indirect impact on the rhizosphere microecology by changing the pH of the soil, changing the activity of enzymes, creating resistant bacteria, and harming plant roots. Additionally, Zhou et al. reported in 2020 that metal NPs' high adsorption properties may change the bioavailability and adsorption–desorption behavior of ionic nutrients and pollutants, thereby affecting the concentration of available nutrients and the environmental toxicity of other pollutants.

Plant–microbe interactions must be robust and long-lasting for microbial homeostasis in the rhizosphere to be maintained. By encouraging nutrient cycling, inhibiting pathogenic bacteria, and enhancing tolerance to heavy metal pollution, rhizosphere microorganisms can have a significant impact on how well plants develop (Wang et al. 2023a, b). Research has demonstrated that NPs affect rhizosphere soil microorganisms by altering the microbial community's structure and function in addition to affecting microbial diversity, abundance, and composition (Macurkava et al. 2021; Zarco-González et al. 2023).

The microbial community is impacted by NPs when they come into direct contact with microorganisms, release toxic metal ions, or change the availability of nutrients. These effects include altered microbial growth behavior, biofilm destruction, protein inactivation, altered gene expression, and oxidative damage (Ahmed et al. 2020a, b). Plant development, nutrient uptake, and disease resistance will all be seriously threatened by significant changes in the microbial communities brought about by exposure to these NPs. The degree to which this effect varies primarily depends on the type of soil and the kind and concentration of NPs (Macurkava et al. 2021). In a different case, metal oxide nanoparticles (NPs) have a harder time colonizing the associative nitrogen-fixing bacteria Pseudomonas stutzeri A1501 due to the production of reactive oxygen species.

Soil enzyme activity, as a measure of microbial activity, is essential for the breakdown of organic matter, the cycling of nutrients, and the preservation of soil quality. However, it also makes the soil environment more vulnerable to external contaminants, such as NPs. According to studies, these NPs prevented the synthesis of phosphatase and urease, two enzymes involved in the cycling of phosphorus and nitrogen (Ajiboye et al. 2023; Wang et al. 2023a, b).

Another way that metal NPs can enter a plant is by entering through the cell wall, accumulating in the root tissue via the apoplast, symbiont, endocytosis, and other pathways, and then being transferred to the aerial regions of the plant by the xylem. The capacity of the plant to absorb nutrients and water may be connected to the uptake and transport mechanism of these metal NPs and metal derivatives by the plant. Strong transpiration in plants may promote metal NPs and metal derivative absorption and transport (Wang et al. 2023a, b).

Environmental contamination by different xenobiotics and other toxic compounds such as PHCs has been an issue of global concern which poses major risks to living and non-living components of the environment, including humans (Rajput et al. 2023). Bioremediation has been considered an effective technique for the removal and mitigation of PHCs in the environment due to its environmentally friendly, cost-effective, efficient, and community-acceptance nature (Sattar et al. 2022). However, the oily components of crude petroleum are not very readily available for the bioremediation process due to their hydrophobic and resistant nature (Patowary et al. 2023). Additional restrictions that impact the bioremediation rate of hydrocarbons include their low solubility and high molecular weight (Khan et al. 2022); soil toxicity to the degrading microbes and plants; and high site specificity, treatment time (Vasilyeva et al. 2022). Thus, improved techniques that may involve the combined use of bioremediation and nanotechnology such as the addition of biosurfactants, microbe–NP and microbe–plant–NP methods are being employed recently (Cheng et al. 2019; Vázquez-Núñez et al. 2020). Nanobioremediation is the method of eliminating toxins by utilizing live organisms such as microorganisms and/or plants in combination with NPs.

Different hydrocarbons that are present in petroleum differ in their chemical and other properties which render some to be easily and readily degraded, some to be resistant and others non-degradable at all (Khan et al. 2022). Also, certain nanomaterials are stimulants for microorganisms, while others are toxic, making it of paramount importance to carry out proper selection (Vázquez-Núñez et al. 2020). Increased bioavailability, enhanced sorption, small size, high reactivity, catalytic activities, and facilitated degradation are some unique properties of nanomaterials that improve their potentiality and effectiveness in the bioremediation process (Chaudhary et al. 2023; Nandini et al. 2023). Microbial species present or added to the soil can become attached to the hydrocarbons where they utilize them as their source of carbon and energy (Khan et al. 2022). Certain enzymes produced by other bacteria are utilized in the bioremediation of PHCs. Different organisms and strategies are employed for the bioremediation of petroleum based on the hydrocarbon present in the contaminants (Khan et al. 2022). Some of the roles and mechanisms played by the plant–microbe–NP interactions in the process of PHC bioremediation are explained.

Nanomaterials can accelerate the degradation, transformation, and conversion of contaminants in the environment into less toxic or non-toxic forms by acting as catalysts or co-catalysts (Vasilyeva et al. 2022). They participate in redox reactions, where they can serve as intermediaries between pollutants and microbes, facilitating the transfer of electrons and stimulating the activity of enzymes during the degradation process (Nandini et al. 2023). Vasilyeva et al. (2022) stated that the introduction of biopreparation in conjunction with natural sorbents led to an efficient bioremediation of gray forest soil contaminated with crude oil (40.1 g TPH kg⁻¹). The study found that the total PHC content in the best samples was lowered to ≤5 g kg⁻¹, which is the allowed concentration in the area for soils. The result, according to the authors was related to the beneficial effects of the sorbent amendments in reducing the soil toxicity because of reversible sorption of hydrocarbons and their toxic metabolites.

Microbes utilize several processes, such as immobilization and mobilization to eliminate contaminants. According to Ayilara & Babalola (2023), immobilization entails biosorption, bioaccumulation, complexation, and precipitation, whereas mobilization entails biostimulation, bioaugmentation, enzymatic oxidation, bioleaching, and enzymatic reduction. Solubility and mobility of PHCs and other soil organic contaminants are decreased through sorption, hence reducing their environmental impact (Bala et al. 2022). It is claimed that phenanthrene and phenanthrene emitted from contaminated aquifer material are more soluble when polymeric nanonetwork particles are present (Bala et al. 2022).

Absorption and adsorption are the two components of sorption. Absorption involves the penetration of pollutants into deeper layers of the sorbent, while adsorption has to do with the interaction of pollutants and sorbent at the surface (Vázquez-Núñez et al. 2020). Unique physicochemical properties and high surface area of NPs help in their sorption and sequestration of pollutants (Nandini et al. 2023) leading to the removal of the contaminants even at lower concentrations. The sequestration of contaminants by NPs makes them form complexes which make them immobile with reduced bioavailability thereby reducing their potential of causing harm and improving the effectiveness of the bioremediation process. A conducive environmental network was established in the rhizosphere of Iris tectorum using magnetite and external electrodes to improve rhizobacterial interactions and PHCs degradation, and their findings indicated a huge increase in the biodegradation process. This provides insight into overcoming the problem of inefficient electron transfer that hinders PHC decomposition and absorption by plant roots.

The performance of microbes which are the key players in biodegradation and transformation of environmental contaminants is significantly enhanced by NPs. The high reactivity and broad surface area of the nanomaterials create a suitable and favorable environment for the colonization of microbes (Bala et al. 2022). This, however, also enhances the microorganisms' development, spread, biomass, and bioremediation process. Nanomaterials can act as carriers of essential nutrients, vitamins, and compounds that are needed for microbial growth and biomass production. The availability of nutrients promotes plant and microbial growth, which improves the bioremediation process. The ability of various fungi to degrade PAHs was examined by Arifeen et al. (2022). Schizophyllium commune 20R-7-F01 was shown to have the maximum activity, degrading phenanthrene, pyrene, and benzo[a]pyrene by 25, 18, and 13%, respectively. The ability of fungus to degrade PAHs and anaerobic growth are positively correlated, suggesting that fungi may use PAHs as their only carbon source in anoxic environments.

Plants and associated microbes secrete a number of beneficial substances including plant root exudates, enzymes, vitamins, and the like during the rhizoremediation process (Ite & Ibok 2019), which stimulate the survival and activities of both the microbes and plants involved in PHC degradation and removal. Different microbes produce different enzymes which are involved in the bioremediation of petroleum via different pathways (Khan et al. 2022). As earlier stated, the hydrophobic nature of PHCs makes them complex and inaccessible to certain microbes and plants. When pollutants are made more bioavailable and soluble by nanomaterials and other advantageous microbiological compounds, microbes, plants, and other bioremediation processes can more easily access the contaminants. This makes it easier for toxins to build up inside organisms and for the environment to remove them. According to Parthipan et al. (2022), mixed bacterial strains of Pseudomonas stutzeri NA3 and Acinetobacter baumannii MN3 were able to biodegrade PHCs by 85% when iron NPs and biosurfactant generated by Bacillus subtilis A1 were combined. The addition of the NPs and biosurfactant also improved the bacterial biomass in addition to the biodegradation rate, and according to the study, the optimum level of the NP for the enhanced growth was 10 mg/L concentration. Some studies that have explored the use of microbe–plant–NP interactions in bioremediation of PHCs in the last 5 years are provided in Table 3.

While bioremediation is regarded as a safe, affordable, and ecologically beneficial way to remove PHC waste, it has been noted that the process takes a long time to finish and that its effectiveness decreases when microbes or plants are unable to survive in the unfavorable conditions of a polluted medium or environment (Vázquez-Núñez et al. 2020, Gao & Gu 2021 and Patowary et al. 2023). Furthermore, the oily components of the PHCs are typically not fully available to the plants or microbes for the remediation process because of their resistant and hydrophobic qualities (Patowary et al. 2023). Therefore, there is a need to improve the working principles of bioremediation for optimum remediation. Studies on the improvement of remediation processes through the integration or hybridization of various remediation systems or processes for better and more effective PHC remediation have been conducted in light of these and other shortcomings of the traditional bioremediation processes. To improve the effectiveness of the individual radiation processes, a remediation method called nanobioremediation, which combines bioremediation and NPs for the cleanup of PHCs or other contaminated sites, was introduced (Kumari et al., 2023; Chauhan et al. 2023; Patowary et al. 2023). According to Rajput et al. (2022), nanobioremediation is a procedure that combines NPs with dangerous pollutants using bacteria or plants in order to remove them from media like soil, water, or oil.

The basic technological limitations of traditional bioremediation methods are visibly addressed by nanobioremediation, which is an effective and environmentally friendly way to remove PHCs from the environment by using biogenic nanomaterials and microbes to increase remediation efficiency (Chauhan et al. 2023; Patowary et al. 2023; Satta et al. 2022). Increasing the surface area available for microbial activity and giving the microorganisms a food source (nutrients) improves the bioremediation process (Chauhan et al. 2023). By offering a sizable surface area for microbial adhesion and nutrient delivery, NPs are used in the process of PHC removal by nanobioremediation to accelerate the biodegradation of PHCs (Chauhan et al. 2023). The type of organism utilized for pollution remediation (nanophytoremediation and microbial nanoremediation) defines specific nanobioremediation processes (Burachevskaya et al. 2020; Rajput et al. 2023). A study by Younis et al. (2020) state that nanobioremediation uses a range of NPs, such as metal oxide, carbon nanotubes, biopolymers, and nanoscale zeolites. The growing expenses of chemical and physical processes have led to a greater interest in nanobioremediation technologies mediated by microbes and plants (Rajput et al. 2022). The efficiency of the remediation process when using microorganisms and NPs to remove PHCs is solely dependent on how the two interact, which can also have an impact on how efficiently the bacteria are able to remove the hydrocarbon. Interacting microorganisms can grow more virulent, versatile, or multiply more quickly. Systems contaminated by petroleum have been bioremediated using a range of nanomaterials. With amazing success, metallic NPs, carbon-based NPs, nanocomposites, and nanozeolites were employed (Chauhan et al. 2023).

Nowadays, molecular methods have produced green NPs with controlled dimensions and resolved the issue of NPs' lack of structural stability, claimed Rajput et al. (2023). One important reducing agent and stabilizer for green synthesis is known to be nitrate reductase. Green synthesis uses different plant extracts or phytochemicals (terpenoids, flavonoids, etc.) and microorganisms (fungi, bacteria, etc.) to create metallic NPs in an environmentally benign manner. The primary benefits of this approach are its minimal waste product generation, low cost, low energy consumption, and appropriateness for large-scale production.

According to Patowary et al. (2023), research has shown that nanomaterials such as carbon nanostructures, nanodispersions, magnetic nanocomposites, membranes, foams and meshes, filters and pads, and TiO₂ have the potential to be used in nanobioremediation of PHCs. Selectivity of the nanomaterial is one of the main parameters controlling how oil is sequestered from the oil–water phase, according to Vázquez-Núñez et al. (2020). Certain nanomaterials, such as Recam, CNTs, and nanowire membranes, can selectively adsorb oil from an oil–water mixture; on the other hand, other nanomaterials, such as polypropylene, raw cotton, and glass fibers coated with silicon, tend to adsorb both organic solvents and water.

Plants are unable to withstand adverse ecological conditions, predator attacks, parasitic infections, and other threats because of their immovable nature. To combat these adverse effects, plants have developed a multitude of mechanisms that are impacted by various forms of plant–microbe interactions (Singh et al. 2019). Such interactions may result in the stimulation of plant growth and tolerance mechanisms (Chen et al. 2023). It could also lead to negative effects, leading to the development of disease (Nadarajah & Abdul Rahman 2021). A range of signal molecules released by root and shoot exudates as byproducts of secondary metabolites to strengthen plant defense mechanisms improve interactions between microbes and plants. Plant exudates from roots provide nutrients and energy to soil microbes, with which they form complex systems of communication. Therefore, it is crucial to comprehend the communication pathways between plants and microbes in order to lessen the detrimental impacts that biotic and abiotic challenges have on plants (Chamkhi et al. 2021a, b; Rane et al. 2022). Certain useful bacteria and fungi have the ability to reduce toxic effects caused by pollutants and promote plant growth in two ways: First, by inducing defense mechanisms against phytopathogens; secondly, directly by solubilizing mineral nutrients like phosphorous, nitrogen, iron, potassium, and others; thirdly, by producing substances that promote plant growth, like phytohormones; and lastly, by secreting particular enzymes, like 1-aminocyclopropane-1-carboxylate deaminase (ACCd) (Jain et al. 2020). These bacteria can also alter the bioavailability of hydrocarbons in soil through several processes, including redox processes, acidification, precipitation, chelation, and the complexation process (Nishad et al. 2020).

Reactive oxygen species generation is another mechanism of plant response against microbe invasion (Castro et al. 2021; Dora et al. 2022). According to Janků et al. (2019), it comprises extremely reactive compounds such as superoxide ⁠, hydrogen peroxide (H₂O₂), and singlet oxygen (O₂). Through the stimulation of cellulose production genes, reactive oxygen species strengthen cell walls and contribute to physically obstructing the invader's passage (Wang et al. 2023a, 2023b). Plants respond to microbial invasion by producing lignin, which initiates the synthesis of phenylpropanoid compounds (Lee et al. 2019). The typical phenylpropanoid biosynthesis route in the cytosol produces lignin, which is released to the apoplast after three primary monolignols undergo oxidative polymerization (Mnich et al. 2020). Plants use microbe-associated molecular patterns to recognize microbes inside the apoplast. The primary groups of microbe-associated molecular patterns are proteins, lipids, carbohydrates, nucleic acids, and lipids (Buscaill & van der Hoorn 2021).

Nanomaterials must be ingested by the plant cell and pass through a number of routes, including pore formation, carrier proteins, endocytosis, plasmodesmata, and ion channels, to cross the plasma membrane and reach the symplastic pathway (Singh et al. 2022). When applied topically, NPs have to get past the cuticle's barrier via either the hydrophilic or lipophilic route. The lipophilic path exploits polar aqueous pores found in the cuticle and stomata, while the hydrophilic route diffuses through the waxes on the coticules (Mohamed & Nafady 2020).

Interactions between microbes, plants, and NPs are essential to the bioremediation of PHCs. Microorganisms like yeast, fungi, algae, and bacteria aid in the breakdown of hydrocarbons. The breakdown process is aided by the surface-active biopolymers and biosurfactants produced by these bacteria. It has been observed that bacterial consortia effectively detoxify PHCs in contaminated soil (Sarma et al. 2022). Additionally, they promote plant growth by minimizing phytotoxic effects and enhancing nutrient uptake and antioxidant mechanisms. Understanding the processes underlying hydrocarbon degradation is essential to the development of efficient bioremediation systems. This is because the physical and chemical characteristics of hydrocarbons make them resistant to degradation. White-rot fungi have shown promise in the bioremediation of soil-based total PHCs. Moreover, combining fungus and surfactants can improve bioremediation's effectiveness. Bioelectrochemical systems are another potential method for cleaning up soil contaminated with PHCs. The utilization of biosurfactants and biochar in bioelectrochemical systems enhances degradation through extracellular electron transfer and biofilm formation (Vu & Mulligan 2023).

The remediation of PHCs through the interaction of microorganisms, plants, and NPs offers a potentially effective solution for mitigating the environmental consequences of petroleum contamination. A successful and economical method of decomposing hydrocarbons is to use a variety of microorganisms, such as bacteria, fungi, yeast, and algae, in the bioremediation process (Ali et al. 2023). By cultivating and evaluating microbial consortia, researchers have been able to ascertain their capacity to detoxify PHCs in soil that has been compromised, resulting in enhanced plant development and diminished phytotoxicity (Adedeji et al. 2022). The process of biodegradation, which is carried out by microorganisms and plays a crucial role in the remediation process, is primarily responsible for the degradation of petroleum-contaminated ecosystems; additionally, the use of biological agents can convert complex organic and inorganic pollutants into simpler compounds (Yuan et al. 2023). Phytoremediation – the combination of plant activity and rhizosphere microbe support – has also demonstrated promise in the breakdown and absorption of petroleum pollutants in soil (Meki 2022). Furthermore, a sustainable and successful method for treating high salinity and PHCs in polluted soils has been suggested: a blend of microorganisms, plants, and biochar (Meki 2022 & Yuan et al. 2023).

Environments contaminated with PHCs have been restored through microbe–plant–NP-mediated remediation. However, several factors such as temperature, moisture, availability of nutrients, and salinity affect the degradability of hydrocarbons (Amber et al. 2021). There are lots of physiochemical techniques involved in the traditional remediation of contaminated environments such as immobilization, electro-remediation, chemical reduction, and stabilization all of which have been found not only to be costly and are not environment friendly due to the requirement for trained manpower, high energy and use of hazardous chemicals, but also cause secondary pollution (Pooja et al. 2023). As a result, it has been shown that using plant-based, microbe-based, microbe–plant-based, and microbe–plant–NP-based techniques to remediate contaminated soils or water bodies can be both economical and environmentally beneficial. Above all, microorganisms have been reported as the treasure houses for the cleaning and recovery of hydrocarbon-contaminated environments, and the development of technologies for bioremediation requires an understanding of hydrocarbon degradation mechanisms. The method employed during the remediation of a petroleum-contaminated environment should be considered suitable after complexity, efficiency, cost-effectiveness, hazards, availability of resources, and duration are being evaluated and analyzed. It has been reported that it is inappropriate to apply a single method during remediation. Hence, the need to adopt integrated application methods comprising multiple technologies (biotic and abiotic processes) to overcome issues associated with single method application (Pooja et al. 2023). Moreover, the use of nanomaterials in remediation enhances the breakdown of the contaminants to a favorable biodegradable level which results in the biodegradation of the pollutant. Nanotechnology proffers a solution for the enhancement of responses to post-oil spills since NPs could be functionalized into pickering emulsions or responsive magnetic sorbents. The nanobioremediation of land and water bodies involves the use of NPs that are synthesized biologically using microorganisms, phytoextracts, or both. Iron NPs and iron-lead NPs which are biologically synthesized have proven useful not only in hydrocarbon treatment but also in the treatment of dyes, pesticides, lindane, and other chemical substances basically due to bacterial metabolism.

Rajput et al. (2022) reported that the first nanobioremediation phase involves the introduction of NPs into a contaminated environment through the process of adsorption, absorption, dissolution, and photochemical reaction while microbial introduction through bioaccumulation, biostimulation, and biotransformation processes occurs at the second phase. The combination of nanomaterials through the use of microbe–plant–NPs in the remediation of PHCs is an emerging area in the bioremediation of oil spills which has been reported to cause (i) an increase in the growth rate of oil degraders and an improvement in oil recovery for post-oil response advancement, (ii) effective extraction of oil, and (iii) tailored nutrient release that restricts growth.

The combination of multiple disciplines creates new possibilities and unique features, like the availability of ecofriendly and sustainable materials that can replace conventional methods for responding to oil spills; enhanced microbial growth on oil droplets instead of hazardous chemical dispersants; and effective oil removal using magnets instead of easily clogged skimmers and sorbents that frequently sink. The combined use of biological materials at nano-levels has opened a new area of interest in oil remediation which offers great opportunity and novel functionalities such as (i) environmentally friendly and sustainable materials which can be used as traditional post-oil spill response alternatives, (ii) increase in proliferation of microbes in oil droplets when compared with toxic chemical dispersants, and (iii) efficient magnetic removal of oil other than the use of easily clogged skimmers and sorbents which always sink (Amber et al. 2021). However, future prospects in microbe–plant–NP should be directed toward scale-up, problems associated with scale-up, cost-effectiveness compared to traditional technologies of remediation, verification that nano-enhanced remediation of PHCs are ecofriendly and evaluation of the biological impacts of NPs to the environment (ecosystem) since environmental persistence of NPs and its accumulation in organisms have been reported by Pooja et al. (2023).

PHCs are complicated combinations made largely of non-biodegradable and toxic substances. Extraction, processing, transportation, and leaking of petroleum and its products have severely polluted land and water. Plant, animal, and human health are all at risk from the improper disposal of petroleum and hydrocarbon wastes, which also cause pollution. Conventional approaches for cleaning up petroleum-contaminated soil and water involve the use of physical and chemical techniques; however, these approaches require a large investment of time and money, disturb the natural properties of the soil, and may result in secondary environmental contamination. This method is seen to be a viable and useful strategy to use environmentally friendly technologies like nanobioremediation for effective cleanup and ecosystem restoration.

Through the use of rhizospheric microorganisms, plant roots, and the microorganisms are linked to working together to break down, confine, or immobilize harmful pollutants within soil matrices. The combination of root exudate effusions and the presence of bacteria that break down PHCs makes rhizoremediation far more effective. For the cleanup of PHC pollution, this technology offers an ecologically benign solution. The results are astounding – pollutants are either entirely destroyed or converted into harmless forms. Numerous studies have looked into the application of microbe–plant NP interactions in the bioremediation of PHCs. Through a variety of functions and processes, interactions between microorganisms, plants, and NPs contribute to the bioremediation of PHCs.

Some of the roles and mechanisms played by the plant–microbe–NP interactions in the process of PHC bioremediation include degradation and transformation, immobilization and mobilization, sorption and sequestration, biomass growth, and microbial activity, as well as the production of exudates, enzymes, and other organic compounds. It is believed that PHC bioremediation is a cost-effective and ecologically benign method. The remediation procedure is time-consuming and less efficient when microorganisms or plants cannot thrive in the unfavorable circumstances of a contaminated medium. Furthermore, throughout the remediation process, the oily components of PHCs are frequently not entirely accessible to the bacteria or plants. As a result, the guidelines for bioremediation have been improved for the greatest feasible cleanup. The interaction of bacteria, plants, and NPs in the cleanup of PHCs is one potentially efficient strategy to lessen the environmental consequences of petroleum pollution. The bioremediation of PHCs requires the interplay of microorganisms, plants, and NPs; nonetheless, comprehensive treatment strategies are required.

All relevant data are included in the paper or its Supplementary Information.

The authors declare there is no conflict.