Next Article in Journal
Production and Evaluation of Green Soybean (Glycine max L.) Powder Fortified with Encapsulated Crude Procyanidin Extract Powder
Previous Article in Journal
Optimal Placement and Sizing of Reactive Power Compensation Devices in Power Grids with High Penetration of Distributed Generation
Previous Article in Special Issue
Pyrolytic Valorization of Polygonum multiflorum Residues: Kinetic, Thermodynamic, and Product Distribution Analyses
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Processes
Volume 13
Issue 9
10.3390/pr13092954
processes-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Advancements in Functional Endophytic Bacterium-Assisted Phytoremediation of PHC-Contaminated Soils: A Review

by
Yuyan Qiao
1,
Jie Xu
2,
Yichun Wu
2,
Jianfeng Bao
1,
Haifeng Wang
3,
Longxiang Liu
1,
Jiqiang Zhang
1,
Jian Li
1 and
Tao Wu
1,*
1
Shandong Key Laboratory of Eco-Environmental Science for the Yellow River Delta, Shandong University of Aeronautics, Binzhou 256600, China
2
Department of Bioengineering, Binzhou Polytechnic, Binzhou 256603, China
3
Sinopec Petroleum Engineering Corporation, Dongying 257099, China
*
Author to whom correspondence should be addressed.
Processes 2025, 13(9), 2954; https://doi.org/10.3390/pr13092954
Submission received: 10 August 2025 / Revised: 10 September 2025 / Accepted: 13 September 2025 / Published: 16 September 2025
(This article belongs to the Special Issue Advances in Remediation of Contaminated Sites: 3rd Edition)
Browse Figures
Versions Notes

Abstract

Petroleum hydrocarbons (PHC) are organic pollutants that pose serious health risks to humans and the environment. Treating soils contaminated with these persistent pollutants is a global concern that is challenging to implement effectively. Synergistic remediation strategies, particularly those involving plants and functional endophytic bacteria, offer ecologically sustainable approaches for remediating PHC-contaminated soil and thus hold broad application prospects. This review collected the literature from databases including Elsevier, Web of Science, PubMed, and CNKI, using keywords such as endophytic bacteria, petroleum hydrocarbons, plants, microorganisms, polycyclic aromatic hydrocarbons, and alkanes. After screening the titles, abstracts, and secondary headings, 123 articles were selected for narrative synthesis. It systematically elaborates on the types, functions, sources, and distribution characteristics within plants of hydrocarbon-degrading endophytic bacteria. It comprehensively summarizes the key molecular pathways involved in the bacterial degradation of alkanes and polycyclic aromatic hydrocarbons (PAHs). Furthermore, from four dimensions—PHC metabolism modes, plant growth promotion (PGP), production of biosurfactants (PBS), and horizontal gene transfer—this article innovatively analyzes the mechanisms underlying the synergistic remediation of petroleum hydrocarbon-contaminated soil through functional bacterium–plant interactions. Finally, the review outlines future research directions in the field, providing a theoretical foundation and practical pathways for advancing green remediation strategies for PHC-polluted soil.

1. Introduction

Petroleum hydrocarbons (PHC) are prevalent organic pollutants in the environment. They not only impair soil structure and inhibit crop growth but also exhibit “carcinogenic, teratogenic, and mutagenic” effects, thereby posing severe human health risks and ecological implications [1,2,3,4]. Consequently, the remediation of PHC-contaminated soils represents a paramount and urgent global.
Primary methods for mitigating soil contamination include physical, chemical, and biological remediation. Among biological remediation techniques, phytoremediation, in particular, offers various advantages such as environmental friendliness, low-cost, capability of large-scale treatment, and sustainable utilization. Consequently, phytoremediation has emerged as one of the frontier fields in global environmental remediation technology and engineering science research [5,6,7]. However, factors such as low remediation efficiency, long remediation cycles, and potential for atmospheric pollution due to evapotranspiration of volatile contaminants from plants have constrained the broader application and further development of phytoremediation [8]. The discovery of endophytic bacteria capable of degrading organic pollutants within plants has, however, provided a promising new solution for the phytoremediation of PHC-contaminated soil.
Studies have found that endophytic bacteria in plants can grow using PHC pollutants as the sole carbon source under the catalytic action of enzymes [9], but also mimic plant metabolic mechanisms to produce bioactive metabolites for co-metabolic degradation [10]. This mechanism can reduce the volatilization of pollutants into the atmosphere and their direct toxic effects on plants. Studies suggest that some endophytic bacteria can improve plant nutrition and enhance stress resistance through biological nitrogen fixation [11], phosphorus dissolution, iron carriers productions [12], specific enzymes synthesis [13], photosynthesis, and plant hormones secretions [14], thereby indirectly improving phytoremediation efficiency. In addition, compared with other endophytic bacteria, root endophytic bacteria have a higher colonization rate in the rhizosphere and plant tissues providing greater advantages in practices [15]. The synergistic use of endophytic bacteria with plants to remediate petroleum-contaminated soils is emerging with promising outcomes [10]. Studies have shown that, during synergistic remediation with plants, the inoculation of endophytic bacteria typically leads to a more significant degradation effect on PHC compared to non-inoculated controls. In soil contaminated with total petroleum hydrocarbons (TPHC) (17,500 mg/kg d. w. of soil), following the inoculation of Enterobacter ludwigii ZCR5 (from Zea mays) into Lolium perenne L. cv. Pinia, a four-week treatment with living bacterial cells significantly enhanced the TPHC removal rate by 74% compared to that of the thermal-inactivated control [16]. Additionally, Yang et al. [17] isolated Mycolicibacterium sp. Pyr9 from the root surface of Eleusine indica L. Gaertn., which possesses the ability to degrade various polycyclic aromatic hydrocarbons (PAHs), such as acenaphthylene (ACY), acenaphthene (ACN), phenanthrene (PHE), anthracene (ANT), fluoranthene (FLA), pyrene (PYR), and Benzo[a]pyrene (BaP). In a pot experiment, they inoculated white clover with Pyr9 to remediate pyrene-contaminated soil (48.5 mg/kg). After 30 days, the residual pyrene content was significantly reduced compared to both the Pyr9-free soil and white clover control, with 42% and 30% reductions in the shoots and roots, respectively. This review summarizes the types, source distribution, and hydrocarbon decomposition mechanism of plant endophytic bacteria, with a focus on their synergistic role in the phytoremediation of PHC-contaminated soils. It also outlines future research directions, aiming to provide a comprehensive reference for this field.

2. Plant Functional Endophytic Bacteria

2.1. Types and Functions of Endophytic Bacteria

In 1866, Bari discovered the existence of microorganisms within normally growing plant tissues and described them as “microorganisms within plant tissues” [10]. In 1992, Kleopper first proposed the concept of “endophytic bacteria, which are microorganisms capable of colonizing plant tissues and establishing a harmonious symbiotic relationship with the host plant [18]. In 2001, Siciliano et al. [19] first reported plant endophytic bacteria capable of degrading PHC pollutants.
After more than 30 years, researchers have isolated a type of endophytic bacteria with hydrocarbon-degrading and growth-promoting functions from different plants. Those endophytic bacteria reported for the remediation of PHC-contaminated soil are shown in Table 1. Endophytic bacteria that degrade PHC are mainly isolated from herbaceous plants (such as ryegrass, barygrass, small grass, ground skin, water hygrophila, and sedum lineare), and a few are isolated from woody plants (such as poplar). These functional endophytic bacteria mainly belong to the genera Pseudomonas, Bacillus, Enterobacter, Burkholderia, Pantoea, Stenotrophomonas, Acinetobacter, Kocuria, Plantibacter, Serratia and Sphingobium. Endophytic bacteria that simultaneously decompose hydrocarbons, generate biosurfactants, and promote growth have more advantages than single-function endophytic bacteria in soil remediation. Such endophytic bacteria have been isolated from the roots, stems, and leaves of plants growing in PHC-contaminated soils [20]. These strains can degrade PHC substances, such as saturated hydrocarbons and aromatic hydrocarbons [14], and can also produce biosurfactants [21], indole-3-acetic acid (IAA) [12], iron carriers [22], and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase [23], and have nitrogen fixation effects [24]. These endogenous functional bacteria mainly belong to the genera Pseudomonas, Bacillus, Enterobacter and Stenotrophomonas [16,21,25,26].

2.2. Sources and Distribution of Functional Endogenous Bacteria

Functional endophytic bacteria are widely present in the interstitial spaces of plant tissues, such as roots, stems, leaves, flowers, fruits, and seeds, as well as inside the organs [50,51]. Seed carriers and external environmental microorganisms are the main sources of functional endophytic bacteria. Functional endophytic bacteria enter seeds through three primary pathways: via the maternal plant’s non-vascular or xylem tissues, through floral structures, or from the external environment. These bacteria are subsequently transmitted between parental and offspring plants through seeds [52,53]. Soil microorganisms serve as the primary external source of functional endophytic bacteria in plants [54], with roots constituting the main entry-point for these microbes [55]. Before invading the internal tissues of plant roots, bacteria initially colonize the rhizosphere, adhering to the root surfaces. Their ability to produce antioxidant enzymes, lipopolysaccharides, siderophores, and antimicrobial substances, as well as to utilize root-secreted organic acids, are key factors determining the successful colonization of the rhizosphere [56]. Root hair cells, tissue wounds, lateral root fissures, and germinating radicles are the primary entry-points for bacteria [57]. After passing through the epidermal cells of the roots, the endophytic bacteria infest the cortical cells or xylem vessels and migrate from the roots to the aboveground parts under the action of a transpiration pull [55]. In addition, endophytic bacteria have been reported to mobilize through the plant body from stomata on new stems and leaves [58].
The distribution and abundance of hydrocarbon-degrading endophytic bacteria within plants primarily depend on the plant species, tissue location, genotype, soil type, and contaminant level in the soil. Phillips et al. [59] demonstrated that different plants and tissues of the same plant growing in PHC-contaminated soil harbor distinct endophytic bacterial communities. Wu et al. [24] used high-throughput sequencing and microbial isolation/culture techniques to investigate the characteristics of endophytic bacterial communities in Phragmites australis and Chloris virgata from petroleum-contaminated sites in the Yellow River Delta. They found that the diversity of the endophytic bacterial communities in Chloris virgata was generally higher than that in Phragmites australis. Taghavi et al. [60] isolated endophytic bacteria capable of degrading aromatic hydrocarbons (e.g., toluene and xylene) from roots, stems, and leaves of different poplar varieties. These bacterial strains exhibit distinct spatial compartmentalization within host plants, demonstrating both host- and non-host-specific associations. The intercellular spaces in plant cells contain various nutrients, sugars, and amino acids that support the survival and proliferation of distinct types of hydrocarbon-degrading endophytic bacteria. Specific populations of these endophytic bacteria influence the efficiency of phytoremediation in hydrocarbon-contaminated soils [61]. Compared to stems and leaves, plant roots exhibit greater colonization efficiency and a higher abundance of hydrocarbon-degrading endophytic bacteria [62]. Duan et al. [63] inoculated phenanthrene-degrading endophytic bacterium Diaphorobacter sp. Phe15 in water spinach (Ipomoea aquatica). They observed that Phe15 most abundantly colonized the root surface, followed by the root interior, and then stems/leaves. Moreover, the inoculation of this strain significantly reduced phenanthrene concentrations in all plant parts and subcellular components, with the most pronounced reduction observed in the roots. Different soil types differentially influence the colonization levels of hydrocarbon-degrading endophytic bacteria in plants. Afzal et al. [64] inoculated the same functional endophytic bacterial strain into Lolium perenne grown in sandy, loamy sand, and loamy soils. They found that the abundance and expression of alkane-degrading genes in ryegrass grown in loamy sand were significantly higher than those grown in sandy or loamy sand. Furthermore, the concentration of PHC contaminants in the soil influences the colonization density of endophytic bacteria in plants. Andria et al. [65] discovered that at 2% diesel-contaminated soil, plants inoculated with the functional endophytic bacterium Rhodococcus sp. ITRH43 exhibited a significantly higher abundance of rhizospheric and root endophytic bacteria, along with elevated levels of contaminant-degrading gene than those grown in soils containing 0% or 1% diesel.
During phytoremediation of PHC-contaminated soil, the inoculation method affects the colonization activity and distribution of endophytic bacteria in plants. Afzal et al. [66] inoculated the endogenous bacterium Burkholderia phytofirmans PsJN into ryegrass grown in diesel-contaminated soil, and revealed that the colonization density of PsJN in ryegrass roots and shoots through seed inoculation was significantly higher than that achieved through foliar inoculation. Endophytic bacteria capable of degrading hydrocarbon pollutants preferentially colonized specific plant organs from which they were originally isolated. For instance, hydrocarbon-degrading endophytes isolated from roots demonstrated enhanced colonization of root tissues, whereas those isolated from shoots exhibited superior colonization of shoot tissues [15]. Moreover, functional endophytes derived from plants can successfully re-colonize other target host plants [39], offering a novel approach to address hydrocarbon residue contamination in crops and produce pollution-free agricultural products.

3. Molecular Mechanisms of PHC Degradation by Functional Endophytic Bacteria

Alkanes and polycyclic aromatic hydrocarbons (PAHs) represent the predominant hydrocarbon contaminants in petroleum-polluted soils. Advancing our understanding of the biodegradation pathways is crucial for the development of efficient bioremediation technologies. Substantial research has documented the molecular pathways of bacterial degradation for both alkanes and PAHs [67,68]. Due to their low molecular weight and reduced hydrophobicity, short-chain alkanes can be directly taken up and degraded by bacteria. Medium- to long-chain alkanes exhibit greater recalcitrance to degradation than their short-chain counterparts. Current research has confirmed multiple bacterial degradation pathways for these hydrocarbons, with aerobic degradation primarily occurring through four major routes: terminal oxidation, subterminal oxidation, ω-oxidation, and the Finnerty pathway [69]. Anaerobic degradation proceeds via two principal mechanisms: fumarate addition and carboxylation [70]. The oxidative pathways for bacterial alkane degradation are schematically summarized in Figure 1. The terminal oxidation pathway involves the oxidation of alkanes to fatty acids via alkane monooxygenase, alcohol dehydrogenase, and aldehyde dehydrogenase. The biterminal oxidation pathway involves the oxidation of the alkane terminus via ω-fatty acid monooxygenase, alcohol dehydrogenase, and aldehyde dehydrogenase based on terminal oxidation, converting it into dicarboxylic acids [71]. The subterminal oxidation pathway involves the oxidative dehydrogenation of alkanes at subterminal positions to generate alcohols or methyl ketones, which are subsequently converted to alcohols and fatty acids through catalytic hydrolysis by Baeyer–Villiger monooxygenase and esterases. The Finnerty oxidation pathway involves the formation of n-alkyl hydroperoxides through the action of dioxygenase, which subsequently converts them into fatty acids via catalysis by alcohol and aldehyde dehydrogenases. A study by Jiang et al. [72] found that the bacterial agent ECT degrades n-dodecane and n-hexadecane through both terminal and subterminal oxidation pathways. The fumarate addition pathway cleaves the carbon chain through carbon skeleton rearrangement and oxidation; the subterminal carboxylation pathway converts odd-numbered alkane substrates into even-chain fatty acids. Regardless of whether alkanes are derived from aerobic or anaerobic degradation by bacteria, the resulting acids enter β-oxidation, producing acetyl-CoA, which subsequently undergoes the tricarboxylic acid (TCA) cycle to achieve complete mineralization of the alkanes.
PAHs are typically classified into low-molecular-weight PAHs and high-molecular-weight PAHs based on their structures. Different PAHs undergo distinct biodegradation pathways, and a single PAH may be degraded via multiple pathways [73,74]. Low-molecular-weight PAHs, such as naphthalene and phenanthrene, and high-molecular-weight PAHs, such as pyrene, are commonly employed as model compounds for studying polycyclic aromatic hydrocarbon degradation characteristics. Table 1 reveals that functional endophytic bacteria capable of degrading naphthalene and phenanthrene are the most frequently documented, followed by those capable of degrading pyrene. The bacterial degradation pathways for naphthalene, phenanthrene, and pyrene are depicted in Figure 2 [75].
The bacterial degradation of naphthalene is initiated by the dioxygenase-catalyzed formation of naphthalene cis-1,2-dihydrodiol, which is subsequently dehydrogenated to 1,2-dihydroxynaphthalene by dehydrogenase and then metabolized through 2-hydroxy-2H-chromene-2-carboxylic acid, cis-o-hydroxybenzalpyruvate, and 2-hydroxybenzaldehyde to yield salicylate. The study by Li et al. [76] revealed that Pseudomonas putida ND6 degrades naphthalene precisely through this pathway. Additionally, 1,2-dihydroxynaphthalene can be spontaneously oxidized to 2-formylbenzoic acid via non-enzymatic processes [76].
The molecular mechanism of phenanthrene degradation is complex; it typically undergoes dioxygenation at the C-3,4 positions to form 3,4-dihydrophenanthrene-3,4-diol. This intermediate is then enzymatically converted to 1,2-dihydroxynaphthalene, which subsequently diverges into either the phthalate or salicylate pathways, ultimately achieving thorough mineralization via the TCA cycle [77]. However, some bacteria use both pathways simultaneously. As found in studies such as Sun et al. [78], the strain Mycobacterium sp. WY10 degrades phenanthrene. When the dioxygenation reaction occurs at the 3,4-position of the carbon atoms, one portion is converted to phthalate via 1-hydroxynaphthalene-2-carboxylic acid and then further metabolized to protocatechuate. The second involves the oxidation of 1-hydroxynaphthalene-2-carboxylic acid to 1,2-dihydroxynaphthalene, which is further metabolized into ring-cleavage products and converted to salicylate. Additionally, some bacteria initiate reactions at the 1,2- or 9,10-carbon positions of phenanthrene, and ultimately enter the TCA cycle for mineralization [79].
The degradation of pyrene occurs primarily at the C-1,2 and C-4,5 positions, where dioxygenase and dehydrogenase catalyze the formation of diol intermediates. These intermediates are subsequently metabolized through a series of enzymatic reactions. Among these, pyrene-1,2-diol is metabolized through a series of enzymatic reactions into 2-methoxy-1-hydropyrene and 4-hydroxyacenaphthenone. pyrene-4,5-diol diverges through three metabolic pathways: I, Formation of phenanthrene-4,5-dicarboxylic acid, followed by metabolism to 5-hydroxyphenanthrene-4-carboxylic acid, ultimately entering the TCA cycle via the phthalate pathway or mineralization through phenanthrene degradation after forming phenanthrene-4-carboxylic acid; II, Generation of pyrene-4,5-dione, subsequently metabolized identically to phenanthrene-4,5-dicarboxylic acid; III, Production of 2-hydroxy-2-(phenanthren-5-one-4-enyl)-acetic acid, which is then metabolized to 5-hydroxy-5H-4-oxapyrene-5-carboxylic acid. As observed in Klebsiella michiganensis EF4 and Klebsiella oxytoca ETN19, 4,5-Dihydropyrene-4,5-diol is first generated and then decomposed via the second pathway [80]. All these products are eventually channeled through either the phthalates or salicylates. Under the catalysis of de-esterase and dioxygenase, they are further converted into benzoate and protocatechuate, respectively, and finally completely mineralized via the TCA cycle. with the final mineralization of the resulting small carboxylic acids occurring through the TCA cycle [81,82].
Processes 13 02954 g002aProcesses 13 02954 g002b
Figure 2. Metabolic pathways of naphthalene (58 in figure), phenanthrene (43 in figure) and pyrene (1 in figure) by bacterial degradation (adapted from [73,75,81]).
Figure 2. Metabolic pathways of naphthalene (58 in figure), phenanthrene (43 in figure) and pyrene (1 in figure) by bacterial degradation (adapted from [73,75,81]).
Processes 13 02954 g002aProcesses 13 02954 g002b

4. Synergistic Mechanism of Functional Endophytic Bacteria

The ways in which endophytic bacteria synergistically degrade PHC with plants are diverse. They can degrade PHC in plants through direct or co-metabolism means, while also degrading them through pathways such as promoting plant growth, producing biosurfactants, and utilizing horizontal gene transfer (HGT) (as seen in Figure 3).

4.1. Direct Degradation or Co-Metabolism of PHC in Plants

Plants are autotrophic organisms that do not depend on pollutants as carbon or energy sources, yet can metabolize certain hydrocarbons within their tissues using oxidizing or reducing enzymes [83,84]. Colonizing functional endophytic bacteria can directly metabolize hydrocarbon pollutants. This capability is due to its suite of genes encoding various enzymes (e.g., alkane hydroxylase, esterase, dioxygenase, monooxygenase, alcohol dehydrogenase, aldehyde dehydrogenase, hydratase, aldolase, and isomerase) that are essential for the oxidation of alkanes and the cleavage of aromatic rings [85]. For example, Pseudomonas aeruginosa L10, isolated from reed roots by Wu et al. [14], effectively degrades C10–C26 n-alkanes and PAHs such as naphthalene, phenanthrene, and pyrene in pure culture systems. Genome annotation confirmed that it possesses genes regulating enzymes involved in the degradation pathways of alkanes and aromatic hydrocarbons. The endophytic bacterium Pseudomonas aeruginosa WS02, isolated from the stem of M. verticillatum, completely degrades short-chain PHC (C10–C14) after 14 days of cultivation, and achieves a degradation rate of over 90% for C15–C22. Additionally, genome annotation revealed multiple genes involved in the degradation of alkanes and phenolics, such as alkB, cytochrome P450, and polyphenol oxidase [21]. On the other hand, endophytic bacteria can mimic the metabolic mechanisms of plants by producing bioactive metabolites such as flavonoids, alkaloids, quinones, steroids, benzopyranones, terpenoids, and xanthones [10]. These metabolites contribute to the degradation of hydrocarbon pollutants in plants through co-metabolism. However, concrete examples of these functionsin hydrocarbon-degrading endophytic bacteria remain limited. Functional endophytic bacteria possess the ability to degrade complex organic compounds such as hydrocarbons, either directly or through co-metabolism, which confers greater competitiveness when colonizing different plants or plant tissues in polluted environments [86].

4.2. Growth Promotion and Enhanced Remediation Efficiency in Restored Plants

In addition to the direct degradation mechanisms mentioned above, endophytic bacteria can also enhance the phytoremediation of PHC through various indirect pathways. For example, they can promote plant growth by assisting in nutrient acquisition, producing plant growth hormones, and suppressing pathogen growth, thereby indirectly enhancing the bioremediation efficiency of contaminated soil [10]. In PHC-contaminated soil, the scarcity of plant-available nutrients such as nitrogen, phosphorus, and iron [55], leading to slow plant growth. Furthermore, an imbalanced C:N ratio inhibits soil microbial activity [87], thereby reducing the efficiency of PHC degradation by plants. Endophytic bacteria enhance hydrocarbon bioremediation through multifunctional plant growth promotion: (i) N2-fixation yielding NH3 [88,89], (ii) P-solubilization via phosphatase/mineralization or pH-modulated dissolution [90], and (iii) siderophore-mediated Fe3+ reduction to Fe2+ [91]. These mechanisms collectively overcome nutrient limitations in contaminated soils, thereby amplifying remediation efficiency. The soybean-derived Serratia sp. Wed4 (Lin et al. [82]) exhibits multipotent plant growth-promoting traits, including diazotrophy and dual-phase phosphorus solubilization. Endophytic colonization in barley upregulated PAH-catabolic gene expression and attenuated pyrene bioaccumulation.
Endophytic bacteria directly or indirectly influence plant growth, development, and nutrient uptake through phytohormone production. Certain hydrocarbon-degrading endophytic bacteria enhance root growth and development by producing IAA, thereby improving the uptake and degradation of hydrocarbon contaminants [92]. Stress caused by petroleum hydrocarbon contamination increases the levels of ACC synthase and ACC oxidase in plants, leading to ethylene accumulation, which inhibits plant growth. Many hydrocarbon-degrading endophytic bacteria possess ACC deaminase activity, which degrades ACC to produce α-ketobutyrate and ammonia [93,94], thereby indirectly mitigating ethylene production. Pacwa-Płociniczak et al. [16] isolated Enterobacter ludwigii ZCR5 from maize leaves in PHC-contaminated soil and found that it produces ammonia, IAA, and ACC deaminases. When inoculated into ryegrass grown in PHC-contaminated soil, ZCR5 efficiently colonizes the roots and shoots of the ryegrass and significantly reduces the PHC content in the soil.
Endophytic bacteria can mitigate or entirely prevent pathogen damage in plants through mechanisms such as competition for nutrients and space, production of antimicrobial compounds and hydrolytic enzymes, and induced systemic resistance (ISR) in plants. This enhances plant stress tolerance and improves remediation efficiency [95,96]. Different endophytic bacteria can produce antimicrobial compounds (e.g., antibiotics, toxins, siderophores, and volatile organic compounds) and hydrolytic enzymes (e.g., proteases, cellulases, and chitinases) tailored to specific stresses. These substances suppress pathogen growth and activity [96,97]. Some endophytic bacteria can form symbiotic interactions with host plants. They upregulate the expression of pathogen-related proteins by activating the salicylic acid pathway [98]. Alternatively, they sensitize plants to cellular mechanisms by activating the jasmonic acid and ethylene pathways [99]. Thus, they initiate induced systemic resistance mechanisms to protect host plants from pathogen attack. Endophytic bacteria from the genera Bacillus, Pseudomonas, and Serratia have been demonstrated to protect plant hosts by stimulating the defense system via ISR [100]. Bisht et al. [30] isolated the endophyte Bacillus sp. SBER3 from poplar trees, which is capable of degrading PAHs. Through in vitro experiments, it was found that this strain could produce toxic substances, such as hydrogen cyanide (HCN) and siderophores, thereby inhibiting the growth of the plant pathogens Rhizoctonia solani, Macrophomina phaseolina, Fusarium oxysporum, and Fusarium solani.

4.3. Generation of Biosurfactants to Enhance Bioavailability of PHC

Beyond these plant-associated benefits, a critical challenge in PHC bioremediation lies in the inherent physicochemical properties of the contaminants themselves. Specifically, PHC are highly hydrophobic and exhibit poor mobility in soil environments. This hydrophobicity leads to their low bioavailability, making it one of the main factors limiting the efficiency of bioremediation in contaminated soil [101]. However, hydrocarbon-degrading bacteria can enhance the bioavailability of pollutants by secreting biosurfactants that reduce the binding force between PHC pollutants and soil particles [102], increase the solubility and mobility of PHC [103,104], promote biofilm formation [105], and alter soil enzyme activity [106]. This accelerated the biodegradation of pollutants in the soil environment. Recently, a variety of endophytic bacteria capable of efficiently producing biosurfactants have been isolated from plants. For example, the endophytic bacterium Pseudomonas chlororaphis 23aP can utilize phenanthrene as its sole carbon and energy source to produce rhamnolipids, alter cell surface properties, and promote phenanthrene biodegradation [12]. The biosurfactant produced by the endophytic bacterium Bacillus amyloliquefaciens MEBAphL4 exhibited fairly high emulsifying and surface activities, enabling the effective remediation of PHC-contaminated soil [25]. Research on the function of endophytic bacteria in the production of biosurfactants has mostly been conducted in vitro. However, the potential of these bacteria to produce biosurfactants in situ remains poorly understood. Some studies have suggested that endophytic bacteria produce biosurfactants within plants, thereby facilitating the degradation of organic pollutants in plant tissues. Endophytic bacteria colonizing the plant rhizosphere or roots can directly act on the rhizosphere environment by secreting biosurfactants, facilitating the desorption of pollutants from soil particle surfaces [107]. Studies have also found that plant secondary metabolites may induce endophytic bacteria to synthesize biosurfactants, thereby forming a positive regulatory loop [108].

4.4. HGT Increases the Abundance and Activity of PHC-Degrading Bacteria

Building upon these direct and indirect mechanisms, hydrocarbon-degrading bacteria also employ sophisticated genetic strategies to amplify remediation potential. Studies have shown that hydrocarbon-degrading bacteria can also facilitate the transfer and integration of hydrocarbon-degrading genes through horizontal gene transfer (HGT), thereby enhances the host bacterial adaptability to PHC-contaminated environments and improves degradation efficiency of pollutants [109].This process is mediated by mobile genetic elements (MGEs), including plasmids, bacteriophages, transposons, genomic islands (GIs), and integrative and conjugative elements (ICEs) [110], and operates through mechanisms including transposition, conjugation, outer membrane vesicle transfer, transduction, and transformation. Hydrocarbon-degrading bacteria utilize HGT to disseminate hydrocarbon-catabolizing genes from one strain to another and between microbial communities [111]. French et al. [109] demonstrated that inoculated bacteria can transfer PHC degradation genes to indigenous bacterial communities via HGT mechanisms such as conjugation and nanotube-mediated cytoplasmic exchange. This process resulted in a 46% reduction in the total PHC content of contaminated soil. The alkB is a key gene involved in PHC degradation. It was first discovered in 1989 on the OCT plasmid of Pseudomonas putida GPo1. As of 2023, Fenibo et al. [112] retrieved 230 bacterial species harboring the alkB gene from the NCBI database and found that all of them had acquired this gene through HGT. Current research suggests that hydrocarbon-degrading genes are ubiquitous in plant endophytic bacteria. Through metagenomic analysis, Sessitsch et al. [113] found that endophytic bacteria in the roots of rice grown in uncontaminated soil harbored abundant hydrocarbon-degrading genes, indicating their potential to degrade both aliphatic and aromatic hydrocarbons.
Plasmids are non-chromosomal DNA elements found within bacterial genomes [111,114]. Several plasmids carrying hydrocarbon degradation genes have been reported [115]. For instance, naphthalene degradation genes are present on the mega-plasmids pND6-1, pDTG1, NAH7, and pDTG1 [116,117]; catechol degradation genes are found on plasmids pVI150 and pPGH1 [118,119]; and plasmid pBN2 harbors both naphthalene degradation genes and a benzene/toluene/xylene degradation gene cluster [120]. In petroleum-hydrocarbon-contaminated environments, plasmids harboring hydrocarbon degradation genes are directly involved in bioremediation by hydrocarbon-degrading bacteria. Transposons are self-transposable genetic elements capable of autonomously moving between bacterial chromosomes, plasmids, or bacteriophages. Based on their structural features, transposons can be classified into three types: composite, Tn3 family, and conjugative transposons. Transposon technology enables the creation of novel bacterial mutants with specific structural features and improved performance. Muneeswari et al. [121] used conjugation to transfer the plasmid pBAM1, carrying the Tn5-mariner minitransposon, from DE.coliλ pir strain to WTE. xiangfangensis. From a pool of 2500 mutants, they screened and isolated two high biosurfactant-producing strains M257E.xiangfangensis and M916E.xiangfangensis. Compared with the wild-type strain, both mutants exhibited significantly increased PHC degradation efficiency, achieving rates of 82% and 88%, respectively. GIs represent the family of MGEs (plasmids, bacteriophages, transposons, etc.), obtained through multiple pathways and possessing different functional lifestyles [122]. GIs facilitate the transfer of large gene cassettes and maintain genetic plasticity, thereby enhancing host bacterial adaptability and competitiveness under specific environmental stresses, such as exposure to antibiotics, heavy metals, or during pathogenesis [123]. However, the harnessing of GIs to improve the environmental adaptability of hydrocarbon-degrading bacteria remains largely unknown.
The efficiency and effectiveness of HGT are influenced by inoculum size, microbial stability, and selective pressure. Wang et al. [117] transferred the naphthalene-catabolizing megaplasmid pND6-1 and conjugation-associated megaplasmid pND6-2 from Pseudomonas sp. ND6 to P. putida KT2440. They observed that, under identical mating times but varying inoculum concentrations, the transfer rate of plasmid pND6-2 initially increased to a maximum and then decreased as the donor concentration increased. Additionally, in the absence of selective pressure, approximately 90% of the host KT2440 cells lost at least one plasmid after 20 generations of subculturing.

5. Prospects

Endophytic bacteria-assisted phytoremediation technology offers advantages such as environmental friendliness and high efficiency, providing an effective solution for the green remediation of PHC-contaminated soil. In recent years, significant progress has been made in research on functional strain screening, characterization, and mechanisms of synergistic phytoremediation, both domestically and internationally. However, challenges remain, including limited sources of strains, unclear mechanisms of bacterium-plant interactions, and unstable remediation efficiencies. Future research should focus on the following eight aspects:
  • Isolating endophytic bacterial resources from woody plants; evaluating the efficacy of endophytic bacterium-assisted phytoremediation of PHC-contaminated soil by woody plants; and exploring the remediation potential of deep-rooted woody plant systems for deep-layer PHC pollutants in soil.
  • Employing integrated multi-omics technologies to analyze the interaction network among endophytic bacteria, plants, and PHC pollutants; elucidating the molecular regulatory mechanisms underlying synergistic remediation by endophytic bacteria and host plants; constructing a metabolic network model for plant-endophytic bacterial interactions; and developing “Engineered Bacterial–Plant Remediation Systems”.
  • Exploring the efficiency and stability of horizontal gene transfer in enhancing microbial community function within PHC-contaminated environments; monitoring microbial community succession and soil microecological changes during remediation; and assessing the ecological risks of gene diffusion.
  • Constructing multifunctional microbial consortia that combine degradation, plant growth promotion, and production of surface-active agents; investigating microbial interaction networks and functional complementarity mechanisms; and developing efficient and stable functional endophytic bacterial agents. Optimizing agent delivery technologies (e.g., nanocarriers, biochar immobilization, and seed coating) to improve the colonization efficiency and environmental adaptability of endophytic bacteria.
  • Directionally developing efficient remediation technology systems utilizing endophytic bacteria in synergy with plants for PHC-contaminated sites under different soil types, pollutant concentrations, climatic conditions, and other factors; and enhancing the engineering application potential of remediation technologies.
  • Strengthening the development of a biosafety and ecological risk regulatory framework. Conducting systematic assessments of the survival, dispersal capacity, and potential ecological impacts of exogenous and engineered bacterial agents in the environment, and establishing an environmental behavior tracking system based on molecular monitoring technologies. Developing environmental safety standards and application guidelines for the use of endogenous bacterial agents to prevent ecological risks associated with horizontal gene transfer.
  • Conducting a full life-cycle cost–benefit analysis to optimize techno-economic feasibility. Overcoming bottlenecks such as high mass-production costs, stringent storage requirements, and unstable field colonization effects of bacterial agents, and develop low-cost, long-acting microbial remediation materials. Exploring integrated “remediation–energy–agriculture” models, such as the resource utilization of phytoremediation biomass, to enhance the techno-economic sustainability of the technology.
  • Promoting multi-stakeholder collaboration and policy support to facilitate technology integration and demonstration. Establishing a cooperative platform involving research institutions, enterprises, and regulatory agencies, and developing guidance documents and application standards for endophytic bacterial phytoremediation technology. Selecting typical petroleum-contaminated sites for long-term engineering demonstrations to validate their applicability and stability under real-world conditions, thereby supporting the standardization and large-scale application of the technology.

6. Conclusions

This study reviews the species, source distribution, molecular pathways of hydrocarbon degradation, and mechanisms of synergistic plant remediation of PHC-contaminated soil by functional endophytic bacteria. Currently, hydrocarbon-degrading endophytic bacteria are primarily isolated from herbaceous plants, with most belonging to the phyla Proteobacteria, Firmicutes, and Actinobacteria. The distribution and abundance of hydrocarbon-degrading endophytes within plants are primarily determined by plant types, functions, tissue type, genotype, soil type, and soil contaminant concentration. Those endophytic bacteria can effectively remove alkane and PAH pollutants through various pathways such as direct degradation and co-metabolism. Simultaneously, they enhance plant stress resistance via mechanisms including nitrogen fixation, phosphorus solubilization, ACC deaminase production, and phytohormone secretion, thereby indirectly improving phytoremediation efficiency. Furthermore, these bacteria can secrete biosurfactants to increase the bioavailability of petroleum hydrocarbons and disseminate hydrocarbon degradation genes through horizontal gene transfer, further enhancing the overall degradative capacity of the microbial community. Despite considerable progress in this field, critical limitations in current research remain to be addressed. The functional stability and ecological adaptability of microbial communities under actual contamination scenarios have not been thoroughly evaluated, and there is a lack of targeted regulation strategies tailored to diverse environmental conditions. Addressing these key gaps will significantly facilitate the transition of this technology from mechanistic investigation to field application.

Author Contributions

Y.Q., J.X., J.B. and T.W. have conceptualized, interpreted, corrected, and compiled the literature and technically sound final versions of the manuscript; Y.Q., L.L., J.B., and J.L. have compiled the tables for manuscripts; Y.Q., Y.W., J.Z., H.W., and T.W. have read the manuscript and provided suggestions and corrections for the final submission. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Shandong Sci-Tech SME Innovation Capacity Improvement Project, grant number 2024TSGC0967; General Program of National Natural Science Foundation of China, grant number 41977124; Science and Technology Support Plan for Youth Innovation of Colleges and Universities in Shandong Province, grant number 2020KJD005; and Key R&D Program of Shandong Province, China, grant number 2019GSF109036; Natural Science Foundation of Shandong Province, grant number ZR2023YQ024 and ZR2022QC121.

Data Availability Statement

No data was used for the research described in the article.

Acknowledgments

During the preparation of this manuscript, the authors used chemdraw (21.0.0), and adobe illustrator (2025), for the purposes of Figure 1, Figure 2 and Figure 3. The authors have reviewed and edited the output and take full responsibility for the content of this publication.

Conflicts of Interest

Author Haifeng Wang was employed by Sinopec Petroleum Engineering Corporation. The remaining author declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Sinopec Petroleum Engineering Corporation had no role in the design of the study, the collection, analysis, or interpretation of data, the writing of the manuscript, or the decision to publish the results.

Abbreviations

The following abbreviations are used in this manuscript:
PHCPetroleum Hydrocarbon
ACC1-Aminocyclopropane-1-Carboxylic Acid
PGPPlant Growth Promotion
PBSProduction of Biosurfactant
PYRPyrene
BaPBenzo[a]pyrene
ACYAcenaphthylene
ACNAcenaphthene
PHEPhenanthrene
FLAFluoranthene
FLEFluorene
ANTAnthracene
NAPNaphthalene
TOLToluene
PAHsPolyaromatic Hydrocarbons
TCATricarboxylic Acid
HGTHorizontal Gene Transfer
IAAIndole-3-Acetic Acid
ISRInduced Systemic Resistance
HCNHydrogen Cyanide
MGEsMobile Genetic Elements
ICEsIntegrative and Conjugative Elements
GIsGenomic Islands

References

  1. Li, Y.Q.; Chen, H.M.; Li, W.; Xi, B.; Huang, C. A novel immobilized bacteria consortium enhanced remediation efficiency of PAHs in soil: Insights into key removal mechanism and main driving factor. J. Hazard. Mater. 2025, 486, 137144. [Google Scholar] [CrossRef]
  2. Karishma, S.; Saravanan, A.; Deivayanai, V.C.; Ajithkumar, U.; Yaashikaa, P.R.; Vickram, A.S. Emerging strategies for enhancing microbial degradation of petroleum hydrocarbons: Prospects and challenges. Bioresour. Technol. Rep. 2024, 26, 101866. [Google Scholar] [CrossRef]
  3. Zhang, X.L.; Li, R.X.; Song, J.T.; Ren, Y.; Luo, X.; Li, Y.; Li, X.; Li, T.; Wang, X.; Zhou, Q. Combined phyto-microbial-electrochemical system enhanced the removal of petroleum hydrocarbons from soil: A profundity remediation strategy. J. Hazard. Mater. 2021, 420, 126592. [Google Scholar] [CrossRef] [PubMed]
  4. Ullah, H.F.; Mukkaram, E.; Alam, C.S.; Khan, M.I.; Zhao, B.; Liqun, C.; Salim, M.A.; Naveed, M.; Khan, N.; Núñez-Delgado, A.; et al. Phytotoxicity of petroleum hydrocarbons: Sources, impacts and remediation strategies. Environ. Res. 2021, 197, 111031. [Google Scholar] [CrossRef]
  5. Cary, T.J.; Rylott, E.L.; Zhang, L.; Routsong, R.M.; Palazzo, A.J.; Strand, S.E.; Bruce, N.C. Field trial demonstrating phytoremediation of the military explosive RDX by XplA/XplB-expressing switchgrass. Nat. Biotechnol. 2021, 39, 1216–1219. [Google Scholar] [CrossRef]
  6. Liu, C.J.; Deng, S.G.; Hu, C.Y.; Gao, P.; Khan, E.; Yu, C.P.; Ma, L.Q. Applications of bioremediation and phytoremediation in contaminated soils and waters: CREST publications during 2018–2022. Crit. Rev. Environ. Sci. Technol. 2023, 53, 723–732. [Google Scholar] [CrossRef]
  7. Wang, J.Y.; Aghajani Delavar, M. Techno-economic analysis of phytoremediation: A strategic rethinking. Sci. Total Environ. 2023, 902, 165949. [Google Scholar] [CrossRef] [PubMed]
  8. Devendrapandi, G.; Liu, X.H.; Balu, R.; Ayyamperumal, R.; Valan Arasu, M.; Lavanya, M.; Minnam Reddy, V.R.; Kim, W.K.; Karthika, P.C. Innovative remediation strategies for persistent organic pollutants in soil and water: A comprehensive review. Environ. Res. 2024, 249, 118404. [Google Scholar] [CrossRef]
  9. Oso, S.; Fuchs, F.; Übermuth, C.; Zander, L.; Daunaraviciute, S.; Remus, D.M.; Stötzel, I.; Wüst, M.; Schreiber, L.; Remus-Emsermann, M.N.P. Biosurfactants Produced by Phyllosphere-Colonizing Pseudomonads Impact Diesel Degradation but Not Colonization of Leaves of Gnotobiotic Arabidopsis thaliana. Appl. Environ. Microbiol. 2021, 87, e00091-21. [Google Scholar] [CrossRef]
  10. Tiwari, P.; Kang, S.; Bae, H. Plant-endophyte associations: Rich yet under-explored sources of novel bioactive molecules and applications. Microbiol. Res. 2023, 266, 127241. [Google Scholar] [CrossRef] [PubMed]
  11. Faoro, H.; Rene Menegazzo, R.; Battistoni, F.; Gyaneshwar, P.; do Amaral, F.P.; Taulé, C.; Rausch, S.; Gonçalves Galvão, P.; de los Santos, C.; Mitra, S.; et al. The oil-contaminated soil diazotroph Azoarcus olearius DQS-4T is genetically and phenotypically similar to the model grass endophyte Azoarcus sp. BH72. Environ. Microbiol. Rep. 2017, 9, 223–238. [Google Scholar] [CrossRef] [PubMed]
  12. Karaś, M.A.; Wdowiak-Wróbel, S.; Marek-Kozaczuk, M.; Sokolowski, W.; Melianchuk, K.; Komaniecka, I. Assessment of phenanthrene degradation potential by plant-growth-promoting endophytic strain Pseudomonas chlororaphis 23aP isolated from Chamaecytisus albus (Hacq.) Rothm. Molecules 2023, 28, 7851. [Google Scholar] [CrossRef]
  13. Kukla, M.; Płociniczak, T.; Piotrowska-Seget, Z. Diversity of endophytic bacteria in Lolium perenne and their potential to degrade petroleum hydrocarbons and promote plant growth. Chemosphere 2014, 117, 40–46. [Google Scholar] [CrossRef]
  14. Wu, T.; Xu, J.; Xie, W.J.; Yao, Z.G.; Yang, H.J.; Sun, C.L.; Li, X.B. Pseudomonas aeruginosa L10: A Hydrocarbon-Degrading, Biosurfactant-Producing, and Plant-Growth-Promoting Endophytic Bacterium Isolated From a Reed (Phragmites australis). Front. Microbiol. 2018, 9, 01087. [Google Scholar] [CrossRef]
  15. Yousaf, S.; Afzal, M.; Reichenauer, T.G.; Brady, C.L.; Sessitsch, A. Hydrocarbon degradation, plant colonization and gene expression of alkane degradation genes by endophytic Enterobacter ludwigii strains. Environ. Pollut. 2011, 159, 2675–2683. [Google Scholar] [CrossRef]
  16. Pacwa-Płociniczak, M.; Byrski, A.; Chlebek, D.; Prach, M.; Płociniczak, T. A deeper insight into the phytoremediation of soil polluted with petroleum hydrocarbons supported by the Enterobacter ludwigii ZCR5 strain. Appl. Soil Ecol. 2023, 181, 104651. [Google Scholar] [CrossRef]
  17. Yang, J.; Gu, Y.J.; Chen, Z.G.; Song, Y.; Sun, F.F.; Liu, J.; Waigi, M.G. Colonization and performance of a pyrene-degrading bacterium Mycolicibacterium sp. Pyr9 on root surfaces of white clover. Chemosphere 2021, 263, 127918. [Google Scholar] [CrossRef]
  18. Kloepper, J.W.; Schippers, B.; Bakker, P.A.H.M. Proposed elimination of the term Endorhizosphere. Phytopathology 1992, 82, 726–727. [Google Scholar] [CrossRef]
  19. Siciliano, S.D.; Fortin, N.; Mihoc, A.; Wisse, G.; Labelle, S.; Beaumier, D.; Ouellette, D.; Roy, R.; Whyte, L.G.; Banks, M.K.; et al. Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl. Environ. Microbiol. 2001, 67, 2469–2475. [Google Scholar] [CrossRef] [PubMed]
  20. Fatima, K.; Afzal, M.; Imran, A.; Khan, Q.M. Bacterial rhizosphere and endosphere populations associated with grasses and trees to be used for phytoremediation of crude oil contaminated soil. Bull. Environ. Contam. Toxicol. 2015, 94, 314–320. [Google Scholar] [CrossRef]
  21. Luo, P.H.; Tang, Y.K.; Lu, J.H.; Jiang, L.; Huang, Y.T.; Jiang, Q.M.; Chen, X.M.; Qin, T.F.; Shiels, H.A. Diesel degradation capability and environmental robustness of strain Pseudomonas aeruginosa WS02. J. Environ. Manag. 2024, 351, 119937. [Google Scholar] [CrossRef]
  22. Zhao, H.; Gu, Y.J.; Liu, X.Y.; Liu, J.; Waigi, M.G. Reducing phenanthrene contamination in Trifolium repens L. with root-associated phenanthrene-degrading bacterium Diaphorobacter sp. Phe15. Front. Microbiol. 2021, 12, 792698. [Google Scholar] [CrossRef]
  23. Guan, C.F.; Fu, W.T.; Zhang, X.G.; Li, Z.M.; Zhu, Y.L.; Chen, F.Y.; Ji, J.; Wang, G.; Gao, X.P. Enhanced phytoremediation efficiency of PHE-contaminated soil by rape (Brassica napus L.) assisted with PHE-degradable PGPR through modulating rhizobacterial communities. Ind. Crops Prod. 2023, 202, 117057. [Google Scholar] [CrossRef]
  24. Wu, T.; Li, X.b.; Xu, J.; Liu, L.X.; Ren, L.-l.; Dong, B.; Li, W.; Xie, W.-j.; Yao, Z.-g.; Chen, Q.-f.; et al. Diversity and functional characteristics of endophytic bacteria from two grass species growing on an oil-contaminated site in the Yellow River Delta, China. Sci. Total Environ. 2021, 767, 144340. [Google Scholar] [CrossRef]
  25. Biswas, S.; Jayaram, S.; Philip, I.; Balasubramanian, B.; Pappuswamy, M.; Barceló, D.; Chelliapan, S.; Kamyab, H.; Sarojini, S.; Vasseghian, Y. Appraisal of the potential of endophytic bacterium Bacillus amyloliquefaciens from Alternanthera philoxeroides: A triple approach to heavy metal bioremediation, diesel biodegradation, and biosurfactant production. J. Environ. Chem. Eng. 2024, 12, 113454. [Google Scholar] [CrossRef]
  26. Wang, X.; Lin, C.B.; Wang, D.Q.; Zhu, X.Z.; Zhao, H.Y.; Lyu, B.T. Colonization performance and pyrene degradation characteristics of Stenotrophomonas maltophilis PX1. Chin. J. Appl. Ecol. 2022, 33, 2547–2556. (In Chinese) [Google Scholar] [CrossRef]
  27. Sun, K.; Liu, J.; Li, X.; Ling, W. Isolation, identification, and performance of two pyrene-degrading endophytic bacteria. Acta Ecol. Sin. 2014, 34, 853–861. (In Chinese) [Google Scholar] [CrossRef]
  28. Marchut-Mikolajczyk, O.; Drożdżyński, P.; Struszczyk-Świta, K. Biodegradation of slop oil by endophytic Bacillus cereus EN18 coupled with lipase from Rhizomucor miehei (Palatase®). Chemosphere 2020, 250, 126203. [Google Scholar] [CrossRef]
  29. Marchut-Mikolajczyk, O.; Drożdżyński, P.; Pietrzyk, D.; Antczak, T. Biosurfactant production and hydrocarbon degradation activity of endophytic bacteria isolated from Chelidonium majus L. Microb. Cell Fact. 2018, 17, 171–179. [Google Scholar] [CrossRef]
  30. Bisht, S.; Pandey, P.; Kaur, G.; Aggarwal, H.; Sood, A.; Sharma, S.; Kumar, V.; Bisht, N.S. Utilization of endophytic strain Bacillus sp. SBER3 for biodegradation of polyaromatic hydrocarbons (PAH) in soil model system. Eur. J. Soil Biol. 2014, 60, 67–76. [Google Scholar] [CrossRef]
  31. Lumactud, R.; Shen, S.Y.; Lau, M.; Fulthorpe, R. Bacterial endophytes isolated from plants in natural oil seep soils with chronic hydrocarbon contamination. Front. Microbiol. 2016, 7, 755. [Google Scholar] [CrossRef]
  32. Sheng, X.F.; Chen, X.B.; He, L.Y. Characteristics of an endophytic pyrene-degrading bacterium of Enterobacter sp. 12J1 from Allium macrostemon Bunge. Int. Biodeterior. Biodegrad. 2008, 62, 88–95. [Google Scholar] [CrossRef]
  33. Tao, J.Y.; Hong, Y.J.; Chen, X.M.; Liu, W.T.; Zhu, X.Z.; Miao, Y.H. Isolation, identification and PAH-degrading performance of an endophytic bacterium Enterobacter sp. PRd5. J. Ecol. Rural Environ. 2019, 35, 83–90. (In Chinese) [Google Scholar] [CrossRef]
  34. Mitter, E.K.; Kataoka, R.; de Freitas, J.R.; Germida, J.J. Potential use of endophytic root bacteria and host plants to degrade hydrocarbons. Int. J. Phytoremediation 2019, 21, 928–938. [Google Scholar] [CrossRef]
  35. Liu, J.; Liu, S.; Sun, K.; Sheng, Y.; Gu, Y.; Gao, Y. Colonization on root surface by a phenanthrene-degrading endophytic bacterium and its application for reducing plant phenanthrene contamination. PLoS ONE 2014, 9, e108249. [Google Scholar] [CrossRef]
  36. Lu, L.; Chai, Q.W.; He, S.Y.; Yang, C.P.; Zhang, D. Effects and mechanisms of phytoalexins on the removal of polycyclic aromatic hydrocarbons (PAHs) by an endophytic bacterium isolated from ryegrass. Environ. Pollut. 2019, 253, 872–881. [Google Scholar] [CrossRef] [PubMed]
  37. Afzal, M.; Yousaf, S.; Reichenauer, T.G.; Sessitsch, A. The inoculation method affects colonization and performance of bacterial inoculant strains in the phytoremediation of soil contaminated with diesel oil. Int. J. Phytoremediation 2012, 14, 35–47. [Google Scholar] [CrossRef] [PubMed]
  38. Yousaf, S.; Ripka, K.; Reichenauer, T.G.; Andria, V.; Afzal, M.; Sessitsch, A. Hydrocarbon degradation and plant colonization by selected bacterial strains isolated from Italian ryegrass and birdsfoot trefoil. J. Appl. Microbiol. 2010, 109, 1389–1401. [Google Scholar] [CrossRef]
  39. Sun, K.; Liu, J.; Gao, Y.Z.; Jin, L.; Gu, Y.; Wang, W.Q. Isolation, plant colonization potential, and phenanthrene degradation performance of the endophytic bacterium Pseudomonas sp. Ph6-gfp. Sci. Rep. 2014, 4, 5462. [Google Scholar] [CrossRef]
  40. Germaine, K.J.; Keogh, E.; Ryan, D.; Dowling, D.N. Bacterial endophyte-mediated naphthalene phytoprotection and phytoremediation. FEMS Microbiol. Lett. 2009, 296, 226–234. [Google Scholar] [CrossRef]
  41. Khan, Z.; Roman, D.; Kintz, T.; delas Alas, M.; Yap, R.; Doty, S. Degradation, phytoprotection and phytoremediation of phenanthrene by endophyte Pseudomonas putida, PD1. Environ. Sci. Technol. 2014, 48, 12221–12228. [Google Scholar] [CrossRef]
  42. Iqbal, A.; Arshad, M.; Karthikeyan, R.; Gentry, T.J.; Rashid, J.; Ahmed, I.; Schwab, A.P. Diesel degrading bacterial endophytes with plant growth promoting potential isolated from a petroleum storage facility. 3 Biotech 2019, 9, 35. [Google Scholar] [CrossRef]
  43. Wu, T.; Xu, J.; Guo, W.H.; Xia, J.B.; Li, X.B.; Wang, R.Q. Isolation and characterization of a halotolerant, hydrocarbon-degrading endophytic bacterium from halobiotic reeds (Phragmites australis) growing in petroleum-contaminated soils. Sci. Adv. Mater. 2019, 11, 189–195. [Google Scholar] [CrossRef]
  44. Zhu, X.Z.; Ni, X.; Waigi, M.; Liu, J.; Sun, K.; Gao, Y.Z. Biodegradation of mixed PAHs by PAH-degrading endophytic bacteria. Int. J. Environ. Res. Public Health 2016, 13, 805–817. [Google Scholar] [CrossRef] [PubMed]
  45. Zhang, X.Y.; Liu, X.Y.; Wang, Q.; Chen, X.P.; Li, H.B.; Wei, J.; Xu, G. Diesel degradation potential of endophytic bacteria isolated from Scirpus triqueter. Int. Biodeterior. Biodegrad. 2014, 87, 99–105. [Google Scholar] [CrossRef]
  46. Zhu, X.Z.; Wang, W.Q.; Crowley, D.E.; Sun, K.; Hao, S.P.; Waigi, M.G.; Gao, Y.Z. The endophytic bacterium Serratia sp. PW7 degrades pyrene in wheat. Environ. Sci. Pollut. Res. 2017, 24, 6648–6656. [Google Scholar] [CrossRef] [PubMed]
  47. Chen, S.; Ma, Z.; Li, S.Y.; Waigi, M.G.; Jiang, J.D.; Liu, J.; Ling, W.T. Colonization of polycyclic aromatic hydrocarbon-degrading bacteria on roots reduces the risk of PAH contamination in vegetables. Environ. Int. 2019, 132, 105081. [Google Scholar] [CrossRef] [PubMed]
  48. Zhang, Z.M. A Preliminary Study on the Mechanismsinvolved in Reducing Plant Phenanthrenepollution Level by Phenanthrenedegrading Bacterium RS2 on Root Surfaces. Master’s Thesis, The College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, China, 2019. (In Chinese). [Google Scholar]
  49. Baoune, H.; Aparicio, J.D.; Pucci, G.; Ould El Hadj-Khelil, A.; Polti, M.A. Bioremediation of petroleum-contaminated soils using Streptomyces sp. Hlh1. J. Soils Sediments 2019, 19, 2222–2230. [Google Scholar] [CrossRef]
  50. Hardoim, P.R.; van Overbeek, L.S.; Berg, G.; Pirttilä, A.M.; Compant, S.; Campisano, A.; Döring, M.; Sessitsch, A. The hidden world within plants: Ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 2015, 79, 293–320. [Google Scholar] [CrossRef]
  51. Hnamte, L.; Vanlallawmzuali; Kumar, A.; Yadav, M.K.; Zothanpuia; Singh, P.K. An updated view of bacterial endophytes as antimicrobial agents against plant and human pathogens. Curr. Res. Microb. Sci. 2024, 7, 100241. [Google Scholar] [CrossRef]
  52. Shahzad, R.; Khan, A.L.; Bilal, S.; Asaf, S.; Lee, I.-J. What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Front. Plant Sci. 2018, 9, 00024. [Google Scholar] [CrossRef]
  53. Pal, G.; Saxena, S.; Kumar, K.; Verma, A.; Kumar, D.; Shukla, P.; Pandey, A.; Verma, S.K. Seed endophytic bacterium Bacillus velezensis and its lipopeptides acts as elicitors of defense responses against Fusarium verticillioides in maize seedlings. Plant Soil 2023, 492, 109–124. [Google Scholar] [CrossRef]
  54. Banerjee, S.; van der Heijden, M.G.A. Soil microbiomes and one health. Nat. Rev. Microbiol. 2022, 21, 6–20. [Google Scholar] [CrossRef]
  55. Afzal, I.; Shinwari, Z.K.; Sikandar, S.; Shahzad, S. Plant beneficial endophytic bacteria: Mechanisms, diversity, host range and genetic determinants. Microbiol. Res. 2019, 221, 36–49. [Google Scholar] [CrossRef] [PubMed]
  56. Santoyo, G. How plants recruit their microbiome? New insights into beneficial interactions. J. Adv. Res. 2022, 40, 45–58. [Google Scholar] [CrossRef] [PubMed]
  57. Aswani, R.; Jishma, P.; Radhakrishnan, E.K. Endophytic bacteria from the medicinal plants and their potential applications. In Microbial Endophytes, 2nd ed.; Kumar, A., Singh, V.K., Eds.; Woodhead Publishing: Cambridge, UK, 2020; pp. 15–36. [Google Scholar] [CrossRef]
  58. Santoyo, G.; Moreno-Hagelsieb, G.; Orozco-Mosqueda Mdel, C.; Glick, B.R. Plant growth-promoting bacterial endophytes. Microbiol. Res. 2016, 183, 92–99. [Google Scholar] [CrossRef]
  59. Phillips, L.; Germida, J.; Farrell, R.; Greer, C. Hydrocarbon degradation potential and activity of endophytic bacteria associated with prairie plants. Soil Biol. Biochem. 2008, 40, 3054–3064. [Google Scholar] [CrossRef]
  60. Taghavi, S.; Weyens, N.; Vangronsveld, J.; van der Lelie, D. Improved phytoremediation of organic contaminants through engineering of bacterial endophytes of trees. In Endophytes of Forest Trees: Biology and Applications; Pirttilä, A.M., Frank, A.C., Eds.; Springer: Dordrecht, The Netherlands, 2011; Volume 80, pp. 205–216. [Google Scholar] [CrossRef]
  61. Bacon, C.W.; Hinton, D.M. Bacterial endophytes: The endophytic niche, its occupants, and its utility. In Plant-Associated Bacteria; Gnanamanickam, S.S., Ed.; Springer: Dordrecht, The Netherlands, 2007; pp. 155–194. [Google Scholar] [CrossRef]
  62. Yousaf, S.; Andria, V.; Reichenauer, T.G.; Smalla, K.; Sessitsch, A. Phylogenetic and functional diversity of alkane degrading bacteria associated with Italian ryegrass (Lolium multiflorum) and Birdsfoot trefoil (Lotus corniculatus) in a petroleum oil-contaminated environment. J. Hazard. Mater. 2010, 184, 523–532. [Google Scholar] [CrossRef]
  63. Duan, Z.Y.; Gao, N.Z.; Zhang, G.C.; Wang, J.; Ling, W.T. Inoculation of endophytic bacteria for the abatement of the phenanthreneaccumulation in vegetable subcellular fraction:Efficiency and mechanism. Acta Sci. Circumstantiae 2021, 41, 1529–1537. (In Chinese) [Google Scholar] [CrossRef]
  64. Afzal, M.; Yousaf, S.; Reichenauer, T.G.; Kuffner, M.; Sessitsch, A. Soil type affects plant colonization, activity and catabolic gene expression of inoculated bacterial strains during phytoremediation of diesel. J. Hazard. Mater. 2011, 186, 1568–1575. [Google Scholar] [CrossRef] [PubMed]
  65. Andria, V.; Reichenauer, T.G.; Sessitsch, A. Expression of alkane monooxygenase (alkB) genes by plant-associated bacteria in the rhizosphere and endosphere of Italian ryegrass (Lolium multiflorum L.) grown in diesel contaminated soil. Environ. Pollut. 2009, 157, 3347–3350. [Google Scholar] [CrossRef]
  66. Afzal, M.; Khan, S.; Iqbal, S.; Mirza, M.S.; Khan, Q.M. Inoculation method affects colonization and activity of Burkholderia phytofirmans PsJN during phytoremediation of diesel-contaminated soil. Int. Biodeterior. Biodegrad. 2013, 85, 331–336. [Google Scholar] [CrossRef]
  67. Zhou, N.; Guo, H.J.; Liu, Q.X.; Zhang, Z.T.; Sun, J.; Wang, H. Bioaugmentation of polycyclic aromatic hydrocarbon (PAH)-contaminated soil with the nitrate-reducing bacterium PheN7 under anaerobic condition. J. Hazard. Mater. 2022, 439, 129643. [Google Scholar] [CrossRef] [PubMed]
  68. Rao, Q.Y.; Lu, J.C.; Liu, S.C.; Chen, M.Y.; Ma, Y.L. Biodegradation of C18 n-alkane by biosurfactant-producing Pseudomonas aeruginosa TJM4 and its genomic analysis. J. Environ. Chem. Eng. 2025, 13, 115590. [Google Scholar] [CrossRef]
  69. Liu, X.L.; Cui, Q.F.; Yang, Z.M.; Wei, S.P.; Zhang, Q. Microbial degradation and molecular mechanism of medium and long-chain alkanes in petroleum: A review. Microbiol. China 2023, 50, 1559–1575. (In Chinese) [Google Scholar] [CrossRef]
  70. Ji, Y.; Mao, G.; Wang, Y.; Bartlam, M. Structural insights into diversity and n-alkane biodegradation mechanisms of alkane hydroxylases. Front. Microbiol. 2013, 4, 58. [Google Scholar] [CrossRef] [PubMed]
  71. Xu, C.Y.; Qaria, M.A.; Xu, Q.; Chen, Z.D. The role of microorganisms in petroleum degradation: Current development and prospects. Sci. Total Environ. 2023, 865, 161112. [Google Scholar] [CrossRef]
  72. Jing, J.W.; Wang, T.T.; Guo, X.Y.; Huang, P.F.; Li, C.; Qu, Y.Y. Construction and application of petroleum-degrading bacterial agents: Community composition, lyophilization technology, and degradation mechanism. J. Environ. Chem. Eng. 2024, 12, 114904. [Google Scholar] [CrossRef]
  73. Haritash, A.K.; Kaushik, C.P. Biodegradation aspects of Polycyclic Aromatic Hydrocarbons (PAHs): A review. J. Hazard. Mater. 2009, 169, 1–15. [Google Scholar] [CrossRef]
  74. Fuchs, G.; Boll, M.; Heider, J. Microbial degradation of aromatic compounds—From one strategy to four. Nat. Rev. Microbiol. 2011, 9, 803–816. [Google Scholar] [CrossRef]
  75. Seo, J.-S.; Keum, Y.-S.; Li, Q.X. Bacterial degradation of aromatic compounds. Int. J. Environ. Res. Public Health 2009, 6, 278–309. [Google Scholar] [CrossRef] [PubMed]
  76. Li, S.S.; Xu, J.G.; Hua, T.Y.; Liu, M.M.; Yan, W. Combined transcriptome and metabolome analysis reveal the dual catabolic pathways of naphthalene in Pseudomonas putida ND6. J. Environ. Chem. Eng. 2025, 13, 115632. [Google Scholar] [CrossRef]
  77. Li, J.L.; Peng, W.L.; Yin, X.Q.; Wang, X.Z.; Liu, Z.X.; Liu, Q.C.; Deng, Z.X.; Lin, S.J.; Liang, R.B. Identification of an efficient phenanthrene-degrading Pseudarthrobacter sp. L1SW and characterization of its metabolites and catabolic pathway. J. Hazard. Mater. 2024, 465, 133138. [Google Scholar] [CrossRef]
  78. Sun, S.S.; Wang, H.Z.; Chen, Y.Z.; Lou, J.; Wu, L.S.; Xu, J.M. Salicylate and phthalate pathways contributed differently on phenanthrene and pyrene degradations in Mycobacterium sp. WY10. J. Hazard. Mater. 2019, 364, 509–518. [Google Scholar] [CrossRef]
  79. Seo, J.S.; Keum, Y.S.; Hu, Y.T.; Lee, S.E.; Li, Q.X. Phenanthrene degradation in Arthrobacter sp. P1-1: Initial 1,2-, 3,4- and 9,10-dioxygenation, and meta- and ortho-cleavages of naphthalene-1,2-diol after its formation from naphthalene-1,2-dicarboxylic acid and hydroxyl naphthoic acids. Chemosphere 2006, 65, 2388–2394. [Google Scholar] [CrossRef] [PubMed]
  80. Lou, F.Y.; Okoye, C.O.; Lu, G.; Jiang, H.; Wu, Y.; Wang, Y.; Li, X.; Jiang, J. Whole-genome sequence analysis reveals phenanthrene and pyrene degradation pathways in newly isolated bacteria Klebsiella michiganensis EF4 and Klebsiella oxytoca ETN19. Microbiol. Res. 2023, 273, 127410. [Google Scholar] [CrossRef]
  81. Kweon, O.; Kim, S.-J.; Holland, R.D.; Chen, H.; Kim, D.-W.; Gao, Y.; Yu, L.-R.; Baek, S.; Baek, D.-H.; Ahn, H.; et al. Polycyclic aromatic hydrocarbon metabolic network in Mycobacterium vanbaalenii PYR-1. J. Bacteriol. 2011, 193, 4326–4337. [Google Scholar] [CrossRef]
  82. Lin, C.B.; Zhang, F.Y.; Chen, R.; Lin, S.P.; Jiao, P.Y.; Ma, Y.J.; Zhu, X.Z.; Lv, B.T. Potential of a novel endophytic diazotrophic Serratia sp. Wed4 for pyrene biodegradation. Int. Biodeterior. Biodegrad. 2024, 186, 105705. [Google Scholar] [CrossRef]
  83. Calderón-Preciado, D.; Renault, Q.; Matamoros, V.; Cañameras, N.; Bayona, J.M. Uptake of organic emergent contaminants in spath and lettuce: An in vitro experiment. J. Agric. Food Chem. 2012, 60, 2000–2007. [Google Scholar] [CrossRef]
  84. Bittsánszky, A.; Gullner, G.; Gyulai, G.; Komives, T. A case study: Uptake and accumulation of persistent organic pollutants in Cucurbitaceae species. In Organic Xenobiotics and Plants: From Mode of Action to Ecophysiology, 4th ed.; Schröder, P., Collins, C.D., Eds.; Springer: Dordrecht, The Netherlands, 2011; pp. 77–85. [Google Scholar] [CrossRef]
  85. Wu, H.J.; Song, Q.W.; Zheng, J.; Yu, W.H.; Zhang, K.F.; Lin, S.J.; Liang, R.B. Function genes in microorganisms capable of degrading petroleum hydrocarbon. Microbiol. China 2020, 47, 3355–3368. (In Chinese) [Google Scholar] [CrossRef]
  86. Mitter, B.; Petric, A.; Shin, M.W.; Chain, P.S.G.; Hauberg-Lotte, L.; Reinhold-Hurek, B.; Nowak, J.; Sessitsch, A. Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front. Plant Sci. 2013, 4, 120. [Google Scholar] [CrossRef]
  87. Gao, Y.C.; Du, J.H.; Bahar, M.M.; Wang, H.; Subashchandrabose, S.; Duan, L.; Yang, X.; Megharaj, M.; Zhao, Q.Q.; Zhang, W.; et al. Metagenomics analysis identifies nitrogen metabolic pathway in bioremediation of diesel contaminated soil. Chemosphere 2021, 271, 129566. [Google Scholar] [CrossRef]
  88. Wu, M.L.; Ma, C.; Wang, D.; Liu, H.; Zhu, C.C.; Xu, H.N. Nutrient drip irrigation for refractory hydrocarbon removal and microbial community shift in a historically petroleum-contaminated soil. Sci. Total Environ. 2020, 713, 136331. [Google Scholar] [CrossRef] [PubMed]
  89. Yang, H.Q.; Zhang, X.L.; Yan, C.H.; Zhou, R.; Li, J.H.; Liu, S.Q.; Wang, Z.; Zhou, J.; Zhu, L.; Jia, H. Novel Insights into the Promoted Accumulation of Nitro-Polycyclic Aromatic Hydrocarbons in the Roots of Legume Plants. Environ. Sci. Technol. 2024, 58, 2058–2068. [Google Scholar] [CrossRef] [PubMed]
  90. Kour, D.; Rana, K.L.; Kaur, T.; Yadav, N.; Yadav, A.N.; Kumar, M.; Kumar, V.; Dhaliwal, H.S.; Saxena, A.K. Biodiversity, current developments and potential biotechnological applications of phosphorus-solubilizing and -mobilizing microbes: A review. Pedosphere 2021, 31, 43–75. [Google Scholar] [CrossRef]
  91. Khan, S.; Afzal, M.; Iqbal, S.; Khan, Q.M. Plant–bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere 2013, 90, 1317–1332. [Google Scholar] [CrossRef]
  92. Glick, B.R. Plant growth-promoting bacteria: Mechanisms and applications. Scientifica 2012, 2012, 963401. [Google Scholar] [CrossRef]
  93. Orozco-Mosqueda, M.d.C.; Glick, B.R.; Santoyo, G. ACC deaminase in plant growth-promoting bacteria (PGPB): An efficient mechanism to counter salt stress in crops. Microbiol. Res. 2020, 235, 126439. [Google Scholar] [CrossRef]
  94. Li, X.Z.; Peng, D.L.; Zhang, Y.; Ju, D.; Guan, C.F. Klebsiella sp. PD3, a phenanthrene (PHE)-degrading strain with plant growth promoting properties enhances the PHE degradation and stress tolerance in rice plants. Ecotoxicol. Environ. Saf. 2020, 201, 110804. [Google Scholar] [CrossRef]
  95. Oukala, N.; Aissat, K.; Pastor, V. Bacterial endophytes: The hidden actor in plant immune responses against biotic stress. Plants 2021, 10, 1012. [Google Scholar] [CrossRef]
  96. Muhammad, M.; Wahab, A.; Waheed, A.; Mohamed, H.I.; Hakeem, K.R.; Li, L.; Li, W.-J. Harnessing bacterial endophytes for environmental resilience and agricultural sustainability. J. Environ. Manag. 2024, 368, 122201. [Google Scholar] [CrossRef]
  97. Eid, A.M.; Fouda, A.; Abdel-Rahman, M.A.; Salem, S.S.; Elsaied, A.; Oelmüller, R.; Hijri, M.; Bhowmik, A.; Elkelish, A.; Hassan, S.E.-D. Harnessing bacterial endophytes for promotion of plant growth and biotechnological applications: An overview. Plants 2021, 10, 935. [Google Scholar] [CrossRef]
  98. Boraschi, D.; Alijagic, A.; Auguste, M.; Barbero, F.; Ferrari, E.; Hernadi, S.; Mayall, C.; Michelini, S.; Navarro Pacheco, N.I.; Prinelli, A.; et al. Addressing nanomaterial immunosafety by evaluating innate immunity across living species. Small 2020, 16, 2000598. [Google Scholar] [CrossRef]
  99. Naskar, S.; Roy, C.; Ghosh, S.; Mukhopadhyay, A.; Hazarika, L.K.; Chaudhuri, R.K.; Roy, S.; Chakraborti, D. Elicitation of biomolecules as host defense arsenals during insect attacks on tea plants (Camellia sinensis (L.) Kuntze) Appl. Microbiol. Biotechnol. 2021, 105, 7187–7199. [Google Scholar] [CrossRef] [PubMed]
  100. Pieterse, C.M.J.; Van der Does, D.; Zamioudis, C.; Leon-Reyes, A.; Van Wees, S.C.M. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 2012, 28, 489–521. [Google Scholar] [CrossRef]
  101. Feng, L.Y.; Jiang, X.P.; Huang, Y.N.; Wen, D.D.; Fu, T.Y.; Fu, R.B. Petroleum hydrocarbon-contaminated soil bioremediation assisted by isolated bacterial consortium and sophorolipid. Environ. Pollut. 2021, 273, 116476. [Google Scholar] [CrossRef]
  102. Ahmad, Z.; Zhang, X.; Imran, M.; Zhong, H.; Andleeb, S.; Zulekha, R.; Liu, G.; Ahmad, I.; Coulon, F. Production, functional stability, and effect of rhamnolipid biosurfactant from Klebsiella sp. on phenanthrene degradation in various medium systems. Ecotoxicol. Environ. Saf. 2021, 207, 111514. [Google Scholar] [CrossRef]
  103. Sharuddin, S.S.N.; Abdullah, S.R.S.; Hasan, H.A.; Othman, A.R.; Ismail, N.I. Potential bifunctional rhizobacteria from crude oil sludge for hydrocarbon degradation and biosurfactant production. Process Saf. Environ. Prot. 2021, 155, 108–121. [Google Scholar] [CrossRef]
  104. Zhang, K.C.; Tao, W.Y.; Lin, J.Z.; Wang, W.D.; Li, S. Production of the biosurfactant serrawettin W1 by Serratia marcescens S-1 improves hydrocarbon degradation. Bioprocess Biosyst. Eng. 2021, 44, 2541–2552. [Google Scholar] [CrossRef]
  105. Vijayakumar, S.; Saravanan, V. Biosurfactants-types, sources and applications. Res. J. Microbiol. 2015, 10, 181–192. [Google Scholar] [CrossRef]
  106. Li, X.J.; Zhao, Q.; Wang, X.; Li, Y.T.; Zhou, Q.X. Surfactants selectively reallocated the bacterial distribution in soil bioelectrochemical remediation of petroleum hydrocarbons. J. Hazard. Mater. 2018, 344, 23–32. [Google Scholar] [CrossRef] [PubMed]
  107. Sarfaraz, A.; Sumbal, S.; Qin, Y.; Faqir, Y.; Zveushe, O.K.; Zhou, L.; Zhang, W.; Li, J.; Lv, Z.; Han, Y.; et al. Bioaugmentation-assisted phytoremediation of petroleum hydrocarbon-contaminated soils. J. Environ. Chem. Eng. 2025, 13, 115895. [Google Scholar] [CrossRef]
  108. Jha, P.; Panwar, J.; Jha, P.N. Secondary plant metabolites and root exudates: Guiding tools for polychlorinated biphenyl biodegradation. Int. J. Environ. Sci. Technol. 2014, 12, 789–802. [Google Scholar] [CrossRef]
  109. French, K.E.; Zhou, Z.R.; Terry, N. Horizontal ‘gene drives’ harness indigenous bacteria for bioremediation. Sci. Rep. 2020, 10, 15091. [Google Scholar] [CrossRef]
  110. Mohapatra, B.; Phale, P.S. Microbial degradation of naphthalene and substituted naphthalenes: Metabolic diversity and genomic insight for bioremediation. Front Bioeng. Biotech 2021, 9, 602445. [Google Scholar] [CrossRef]
  111. Bhatt, P.; Bhandari, G.; Bhatt, K.; Maithani, D.; Mishra, S.; Gangola, S.; Bhatt, R.; Huang, Y.; Chen, S. Plasmid-mediated catabolism for the removal of xenobiotics from the environment. J. Hazard. Mater. 2021, 420, 126618. [Google Scholar] [CrossRef]
  112. Fenibo, E.O.; Selvarajan, R.; Abia, A.L.K.; Matambo, T. Medium-chain alkane biodegradation and its link to some unifying attributes of alkB genes diversity. Sci. Total Environ. 2023, 877, 162951. [Google Scholar] [CrossRef] [PubMed]
  113. Sessitsch, A.; Hardoim, P.; Döring, J.; Weilharter, A.; Krause, A.; Woyke, T.; Mitter, B.; Hauberg-Lotte, L.; Friedrich, F.; Rahalkar, M.; et al. Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol. Plant. Microbe Interact. 2012, 25, 28–36. [Google Scholar] [CrossRef]
  114. Billane, K.; Harrison, E.; Cameron, D.; Brockhurst, M.A. Why do plasmids manipulate the expression of bacterial phenotypes? Philos. Trans. R. Soc. B 2021, 377, 20200461. [Google Scholar] [CrossRef] [PubMed]
  115. Kim, J.; Park, W. Genome analysis of naphthalene-degrading Pseudomonas sp. AS1 harboring the megaplasmid pAS1. J. Microbiol. Biotechnol. 2018, 28, 330–337. [Google Scholar] [CrossRef]
  116. Boronin, A.M.; Kosheleva, I.A. The role of catabolic plasmids in biodegradation of petroleum hydrocarbons. In Current Environmental Issues and Challenges, 9th ed.; Cao, G., Orrù, R., Eds.; Springer: Dordrecht, The Netherlands, 2014; pp. 159–168. [Google Scholar] [CrossRef]
  117. Wang, S.; Li, S.S.; Du, D.; Wang, D.; Yan, W. Conjugative transfer of megaplasmids pND6–1 and pND6–2 enhancing naphthalene degradation in aqueous environment: Characterization and bioaugmentation prospects. Appl. Microbiol. Biotechnol. 2020, 104, 861–871. [Google Scholar] [CrossRef]
  118. Martínez-Lavanchy, P.M.; Müller, C.; Nijenhuis, I.; Kappelmeyer, U.; Buffing, M.; McPherson, K.; Heipieper, H.J. High stability and fast recovery of expression of the TOL plasmid-carried toluene catabolism genes of Pseudomonas putida mt-2 under conditions of oxygen limitation and oscillation. Appl. Environ. Microbiol. 2010, 76, 6715–6723. [Google Scholar] [CrossRef]
  119. Kasak, L.; Horak, R.; Nurk, A.; Talvik, K.; Kivisaar, M. Regulation of the catechol 1,2-dioxygenase- and phenol monooxygenase-encoding pheBA operon in Pseudomonas putida PaW85. J. Bacteriol. 1993, 175, 8038–8042. [Google Scholar] [CrossRef] [PubMed]
  120. Lee, Y.; Lee, Y.; Jeon, C.O. Biodegradation of naphthalene, BTEX, and aliphatic hydrocarbons by Paraburkholderia aromaticivorans BN5 isolated from petroleum-contaminated soil. Sci. Rep. 2019, 9, 860. [Google Scholar] [CrossRef] [PubMed]
  121. Muneeswari, R.; Iyappan, S.; Swathi, K.V.; Vinu, R.; Ramani, K.; Sekaran, G. Biocatalytic lipoprotein bioamphiphile induced treatment of recalcitrant hydrocarbons in petroleum refinery oil sludge through transposon technology. J. Hazard. Mater. 2022, 431, 128520. [Google Scholar] [CrossRef] [PubMed]
  122. Bellanger, X.; Payot, S.; Leblond-Bourget, N.; Guédon, G. Conjugative and mobilizable genomic islands in bacteria: Evolution and diversity. FEMS Microbiol. Rev. 2014, 38, 720–760. [Google Scholar] [CrossRef]
  123. Dobrindt, U.; Hochhut, B.; Hentschel, U.; Hacker, J. Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2004, 2, 414–424. [Google Scholar] [CrossRef]
Processes 13 02954 g001
Figure 1. Metabolic pathways of alkanes by bacterial degradation.
Figure 1. Metabolic pathways of alkanes by bacterial degradation.
Processes 13 02954 g001
Processes 13 02954 g003
Figure 3. Mechanism by which endophytic bacteria cooperate with plants to degrade PHC.
Figure 3. Mechanism by which endophytic bacteria cooperate with plants to degrade PHC.
Processes 13 02954 g003
Table 1. Degradation performance of functional endophytic bacteria in the microbial–plant combined remediation system for PHC contaminations.
Table 1. Degradation performance of functional endophytic bacteria in the microbial–plant combined remediation system for PHC contaminations.
Bacterial StrainsHost PlantsCharacterizationCultivation EnvironmentPollutants and Initial ConcentrationDegradation
Efficiency		References
Acinetobacter sp. BRSI56Brachiaria muticaplant growth promotion (PGP), production of biosurfactant (PBS)liquidCrude, 2% (w/v)78% (7 d)[20]
Acinetobacter sp. BJ03Conyza canadensis-liquidPYR, 50 mg/L65.0% (15 d)[27]
Bacillus amyloliquefaciens
MEBAphL4		Alternanthera philoxeroidesPBSliquidDiesel, 2% (v/v)56.46% (42 d)[25]
Bacillus cereus EN18Chelidonium majus-liquidDiesel, 5% (v/v)45.5% (14 d)[28]
Bacillus pumilus 2AChelidonium majus L.PGP, PBSliquidDiesel, 5% (v/v)98% (10 d)[29]
Bacillus sp. SBER3Populus deltoidesPGPliquidANT, 466 mg/L; naphthalene (NAP), 332 mg/LANT, 83.4% (6 d); NAP, 75.1% (6 d)[30]
Brevundimonas nasdae 210Solidago canadensis-liquidTOL, 1 mM; NAP, 1 mMTOL, 53%; NAP, 39% (7 d)[31]
Chryseobacterium sp. 127Dactylis glomerata-liquidTOL, 1 mM; NAP, 1 mMTOL, 53%; NAP, 41% (7 d)[31]
Curtobacterium flaccumflaciens 153Dactylis glomerata-liquidTOL, 1 mM; NAP, 1 mMTOL, 21%; NAP, 13% (7 d)[31]
Diaphorobacter sp. Phe15Eleusine indica L. Gaertn.PGPsoilPHE, 100 mg/kg39% (40 d)[22]
Enterobacter ludwigii ZCR5Zea maysPGP, PBSsoilCrude, 17,500 mg/kg30.62% (28 d)[16]
Enterobacter sp. 12J1Allium macrostemon BungePGP, PBSliquidPYR, 5 mg/L83.8% (7 d)[32]
Enterobacter sp. PRd5Ophiopogon japonicus-liquidPYR, 50 mg/L; NAP, 500 mg/L; fluorene (FLE), 100 mg/L; PHE, 50 mg/L; FLA, 50 mg/L; BaP, 10 mg/LPYR, 41.4~50.6% (10 d); NAP, FLE, PHE mixed hydrocarbons, 95.0% (7 d); FLA, 35.9% (10 d); BaP, 17.4% (10 d)[33]
Enterobacter cloacae LCRI86Lecucaena leucocephalaPGP, PBSliquidCrude, 2% (w/v)72% (7 d)[20]
Flavobacterium sp. EA2-30-PGPsoilDiesel, 10,000 mg/kg63.4% (65 d)[34]
Kocuria sp. BJ05Trifolium pratense L.-liquidPYR, 50 mg/L53.3% (15 d)[27]
Massilia sp. Pn2Alopecurus aequalis Sobol.-liquidNAP, 100 mg/L; ACN, 100 mg/L; ANT, 50 mg/L; PHE, 50 mg/L; PYR, 20 mg/L; BaP, 10 mg/LNAP, 95.8% (48 h); ACN, 97.3% (48 h); ANT, 27.8% (72 h); PHE, 99.6% (72 h); PYR, 67.6% (14 d); BaP, 2.5% (14 d)[35]
Methylobacterium extorquens C1Lolium perenne-liquidACY, 3.5 mg/L; PHE, 1.0 mg/LACY, 52.5% (3 d); PHE, 43.8% (3 d)[36]
Microbacterium foliorum 117Dactylis glomerata-liquidTOL, 1 mM; NAP, 1 mMTOL, 53%; NAP, 41% (7 d)[31]
Mycolicibacterium sp. Pyr9Eleusine indica L. Gaertn.PGPliquidPYR, 50 mg/L; ACY, 100 mg/L; ACN, 100 mg/L; PHE, 100 mg/L; ANT, 100 mg/L; FLA, 50 mg/L; BaP, 10 mg/LPYR, 98% (8 d); ACY, 93% (4 d); ACN, 88% (4 d); PHE, 100% (4 d); ANT, 31.5% (4 d); FLA, 9.9% (14 d); BaP, 23.2% (14 d)[17]
Pantoea sp. ITSI10Lolium multiflorum var. Taurus-soilDiesel, 7.5 g/kg69.2% (93 d)[37]
Diesel, 10 g/kg48.5% (155 d)[38]
Pantoea sp. EA4-40-PGPsoilDiesel, 10,000 mg/kg60.1% (65 d)[34]
Plantibacter flavus 259Achillea millefolium-liquidTOL, 1 mM; NAP, 1 mMTOL, 53%; NAP, 39% (7 d)[31]
Plantibacter flavus 279Achillea millefolium-liquidTOL, 1 mM; NAP, 1 mMTOL, 53%; NAP, 37% (7 d)[31]
Pseudomonas chlororaphis 23aPChamaecytisus albusPGP, PBSliquidPHE, 50, 100, 200, 500 ppm-[12]
Pseudomonas aeruginosa L10Phragmites australisPGP, PBSliquidDiesel, 5 g/L; NAP, 200 mg/L; PHE, 200 mg/L; PYR, 200 mg/LDiesel, 79.3% (7 d); NAP, 79.7% (10 d); PHE, 71.6% (10 d); PYR, 34.7% (10 d)[14]
Pseudomonas aeruginosa WS02Myriophyllum verticillatumPBSliquidDiesel, 8400 mg/LC10–C14, 100% (14 d); C15–C22, 90% (14 d)[21]
Pseudomonas sp. Ph6-gfpTrifolium pratense L-liquidPHE, 50 mg/L85% (15 d)[39]
Pseudomonas sp. MixRI75Lolium multiflorum var. Taurus-soilDiesel, 7.5 g/kg53% (93 d)[37]
Pseudomonas putida VM1441--soilNAP, 220~280 mg/kg68% (14 d)[40]
Pseudomonas putida PD1PopulusPGPsoilPHE, 100 mg/kg65% (30 d)[41]
Pseudomonas sp. J10Echinochloa crus-galliPGPliquidDiesel, 1.0% (v/v)69% (4 d)[42]
Pseudomonas stutzeri Z11Phragmites australis-liquidDiesel, 3000 mg/L72.1% (7 d)[43]
Pseudomonas sp. P3Trifolium pretense-liquidNAP, 100 mg/L; FLE, 100 mg/L; PHE, 100 mg/L; PYR, 100 mg/LNAP, 95.3%; FLE, 87.9%; PHE, 90.4%; PYR, 6.9% (7 d)[44]
Pseudomonas
aeruginosa BRRI54		Brachiaria muticaPGP, PBSliquidCrude, 2% (w/v)71% (7 d)[20]
Pseudomonas sp. J4AJScirpus triqueter-liquidDiesel, 6000 mg/L42.55% (7 d)[45]
Pseudomonas sp. ITRI15Lolium multiflorum var. Taurus-soilDiesel, 10 g/kg38.6% (90 d)[38]
Serratia sp. DLN5Festuca arundinacea Schreb.PGPsoilPHE, 100 mg/kg82.5% (40 d)[23]
Serratia sp. PW7Plantago asiatica-liquidPYR, 40 mg/L51.2% (14 d)[46]
Sphingobium sp. RS1-gfpPlantago depressa Willd-liquidPHE, 100 mg/L97% (48 h)[47]
Sphingobium sp. RS2Conyza Canadensis L.Cronq.PGPliquidPHE, 100 mg/L99% (72 h)[48]
Stenotrophomonas maltophilia PX1Eleusine indicaPGPliquidNAP, 100 mg/L; PHE, 50 mg/L; PYR, 20 mg/L; FLA, 20 mg/L; BaP, 10 mg/LNAP, 100% (7 d); PHE, 72.6% (10 d); PYR, 50.7% (10 d); FLA, 31.9% (10 d); BaP, 12.9% (10 d)[26]
Stenotrophomonas sp. EA1-17-PGPsoilDiesel, 10,000 mg/kg63.6% (65 d)[34]
Stenotrophomonas sp. P1Conyza canadensis-liquidNAP, 100 mg/L; FLE, 100 mg/L; PHE, 100 mg/L; PYR, 100 mg/L; BaP, 10 mg/LNAP, 98%; FLE, 83.1%; PHE, 87.8%; PYR, 14.4%; BaP, 1.6% (7 d)[44]
Streptomyces sp. Hlh1Zea maysPGP, PBSsoilPetroleum, 5% (w/w)51% (28 d)[49]
Xanthomonas gardneri 209Solidago canadensis-liquidTOL, 1 mM; NAP, 1 mMTOL, 49%; NAP, 40% (7 d)[31]
PGP: indicates plant growth promotion; PBS: indicates production of biosurfactant; -: indicates that the information is not listed in the text; d: indicates days; h: indicates hours; PYR: pyrene; BaP: benzo[a]pyrene; ACY: acenaphthylene; ACN: acenaphthene; PHE: phenanthrene; FLA: fluoranthene; FLE: fluorene; ANT: anthracene; NAP: naphthalene; TOL: toluene.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Qiao, Y.; Xu, J.; Wu, Y.; Bao, J.; Wang, H.; Liu, L.; Zhang, J.; Li, J.; Wu, T. Advancements in Functional Endophytic Bacterium-Assisted Phytoremediation of PHC-Contaminated Soils: A Review. Processes 2025, 13, 2954. https://doi.org/10.3390/pr13092954

AMA Style

Qiao Y, Xu J, Wu Y, Bao J, Wang H, Liu L, Zhang J, Li J, Wu T. Advancements in Functional Endophytic Bacterium-Assisted Phytoremediation of PHC-Contaminated Soils: A Review. Processes. 2025; 13(9):2954. https://doi.org/10.3390/pr13092954

Chicago/Turabian Style

Qiao, Yuyan, Jie Xu, Yichun Wu, Jianfeng Bao, Haifeng Wang, Longxiang Liu, Jiqiang Zhang, Jian Li, and Tao Wu. 2025. "Advancements in Functional Endophytic Bacterium-Assisted Phytoremediation of PHC-Contaminated Soils: A Review" Processes 13, no. 9: 2954. https://doi.org/10.3390/pr13092954

APA Style

Qiao, Y., Xu, J., Wu, Y., Bao, J., Wang, H., Liu, L., Zhang, J., Li, J., & Wu, T. (2025). Advancements in Functional Endophytic Bacterium-Assisted Phytoremediation of PHC-Contaminated Soils: A Review. Processes, 13(9), 2954. https://doi.org/10.3390/pr13092954

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop