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Review

Research Progress and Hotspots in Microbial Remediation for Polluted Soils

by
Shuai Zhao
1,
Xue-Tao Yuan
1,2,3,*,
Xiao-Hong Wang
1,2,3,*,
Yan-Jun Ai
1,2,3 and
Fu-Ping Li
1,2,3
1
College of Mining Engineering, North China University of Science and Technology, Tangshan 063210, China
2
Hebei Key Laboratory of Mining Development and Security Technology, Tangshan 063210, China
3
Hebei Industrial Technology Institute of Mine Ecological Remediation, Tangshan 063210, China
*
Authors to whom correspondence should be addressed.
Sustainability 2024, 16(17), 7458; https://doi.org/10.3390/su16177458
Submission received: 19 July 2024 / Revised: 14 August 2024 / Accepted: 25 August 2024 / Published: 29 August 2024
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Abstract

:
Microbial remediation has become a prominent focus in soil pollution control due to its environmental friendliness, cost-effectiveness, and high efficiency. The effectiveness of microbial remediation is rooted in the interactions between microbial metabolic activities and the soil environment. Various microorganisms employ distinct mechanisms for pollutant treatment, including surface adsorption, intracellular accumulation, and biomineralization. Using the Web of Science Core Collection database, tools such as CiteSpace 6.1.R6, VOSviewer 1.6.20, and HistCite Pro were employed to conduct a quantitative analysis of several key aspects: the volume and thematic distribution of research papers on microbial remediation of soils, the cooperative networks between countries and institutions, the leading journals, major research hotspots, and emerging trends. The analysis reveals that utilizing microbial regulatory mechanisms and functions to remediate inorganic pollutants, such as heavy metals, and organic pollutants, such as PAHs, is becoming a significant frontier in future research. This study provides a valuable reference for scholars aiming to understand the current status of microbial research in soil remediation, both domestically and internationally. It also offers guidance for developing efficient, sustainable, and safe remediation strategies while identifying directions for future innovative research. The specific results are as follows: (1) China, the USA, India, and other countries have a high frequency of citations in this field, and the research is more in-depth. (2) More and more attention has been paid to the use of microbial remediation of contaminated soil in the world, mainly in Environmental Sciences. (3) Major publications include Chemosphere, Journal of Hazardous Materials, and Science of The Total Environment. In the key literature, the use of microorganisms to restore the soil environment and the combination of microorganisms and plants to repair soil contaminated by heavy metals occupy a high proportion. (4) The key areas of focus include the application of microorganisms in soil inorganic pollution remediation, the application of microorganisms in remediation of soil organic pollution (crude oil and polycyclic aromatic hydrocarbons (PAHs)), and the contribution of microorganisms to soil pollutant degradation and toxicity assessment systems. The research and development of combined microbial remediation technology is the current research hotspot in the field of soil remediation, focusing on the symbiosis between mycorrhizal fungi and plant roots, the enhancement in the ability of microorganisms to absorb and degrade pollutants and their tolerance, and the interaction mechanism between indigenous microorganisms and plants.

1. Introduction

With the rapid advancement of industrialization and urbanization, human activities have generated significant wastewater and waste from processes such as mining and smelting, pesticide and fertilizer use, electroplating, textile production, and sewage irrigation [1,2,3]. These activities have introduced large quantities of heavy metals and organic pollutants into the soil. The combined presence of heavy metals and organic pollutants intensifies the accumulation and toxicity of heavy metals, further degrading the ecological environment and severely impacting agricultural development and human health [4,5]. Consequently, researching remediation technologies for polluted soils, especially those addressing the combined pollution of heavy metals and organic pollutants, has become a critical issue in soil pollution prevention and control [6,7].
Current soil remediation technologies primarily include physical, chemical, and biological approaches [8,9,10]. Jianhua et al. successfully immobilized heavy metals, specifically cadmium (Cd), in soil by using a composite material combining shell powder, ball-milled phosphate rock (BSPR), and smooth porphyry (SV). Their findings indicated a 38.2% reduction in Cd content in crops [11]. Additionally, magnetic biochar coupled with Acinetobacter lwoffii DNS32 immobilized pellets (DMBC-P) were synthesized using sodium alginate embedding and fixation, effectively and rapidly removing atrazine from contaminated farmland soil [12]. Microbial remediation has garnered significant attention due to its advantages, such as thorough pollutant degradation, cost-effectiveness, and the absence of secondary pollution [13,14,15]. This method involves using microorganisms—including indigenous bacteria, foreign bacteria, and genetically engineered bacteria—to metabolize and degrade pollutants [16]. By altering environmental conditions such as nutrient availability [17], redox potential [18], and the presence of co-metabolic substrates [19], microbial degradation can be enhanced to achieve effective remediation [20,21]. Microbial remediation strategies primarily include biostimulation and bioaugmentation [22]. Biostimulation leverages the intrinsic restorative potential of indigenous bacteria; however, its effectiveness can vary significantly due to environmental factors, such as the duration of pollution and the composition of pollutants. Excessive fertilization, for example, can diminish the degradation capacity of microorganisms [23]. In contrast, bioaugmentation can enhance biostimulation, and these techniques are often employed in tandem to improve remediation outcomes [24].
Despite the significant potential of microbial remediation in environmental management, its application still faces several challenges, including the selection and optimization of microbial strains, the complexity of soil environments, and the practical feasibility of engineering operations [25,26]. Therefore, further in-depth research into the fundamental principles, influencing factors, and practical performance of microbial remediation is essential for advancing and refining this technology. This paper aims to systematically evaluate research outcomes on microbial soil remediation through bibliometric analysis, exploring its application prospects and development directions, thereby providing theoretical support and practical guidance for future research.

2. Materials and Methods

2.1. Data Source

The data for this analysis were obtained from the Web of Science (WOS) Core Collection database, which is widely recognized as one of the most significant and frequently used databases in scientific research. The retrieval formula of this subject was TS = (Microorganism OR Microbial remediation OR Mechanism of action OR Influencing factor) AND (Soil remediation OR Contaminated soil remediation OR Soil environment OR Soil microorganism). The search period was set from 2000 to 2024, and all retrieved literature was dated up to 9 March 2024. The selected reference types were articles and reviews, resulting in a total of 2371 retrieved documents.

2.2. Research Methods

This study employs the built-in analytical tools of the WOS Core Collection database, as well as CiteSpace 6.1.R6, VOSviewer 1.6.20, and HistCite Pro software, to conduct a bibliometric analysis of 2371 publications from 2000 to 2024. The analysis covers regions and disciplines of publication, journals, key literature, research hotspots, and other relevant content. CiteSpace 6.1.R6 was used to analyze the source literature, obtain keyword burst information, and calculate the centrality of key literature. VOSviewer 1.6.20 was utilized to assess the cooperation intensity between countries and institutions and to perform a co-occurrence analysis of all keywords, reflecting research hotspots and future trends in the field. HistCite Pro was employed to calculate the total local citation score (TLCS) and the total global citation score (TGCS) of the literature to identify the primary academic journals in the research area of microbial soil remediation.

3. Results and Analysis

3.1. Number of Publications and Distribution across Disciplines

The search results indicate a consistent annual increase in the number of publications related to microorganisms in soil remediation research, reflecting the growing attention and advancement in this field. As illustrated in Figure 1, China leads in the number of published papers on soil remediation over the past 20 years, with a total of 1032 publications, followed by India (270), the USA (268), Australia (107), and Poland (105). The development of research in this area can be categorized into four distinct stages: the initial exploration stage, the fluctuating development stage, the stable growth stage, and the rapid development stage. The period from 2000 to 2006 represents the preliminary exploration stage, during which only 140 papers were published. From 2007 to 2010, the field entered a fluctuating development stage, showing an increasing trend with 200 papers published. Between 2011 and 2018, research maintained steady interest, with 723 papers published. In 2019, the field entered a rapid development stage, marked by the publication of 1307 papers, indicating a significant rise in research activity related to microbial remediation. During the stable growth and rapid development stages, there was a notable surge in the number of papers published in China, underscoring the increasing focus of Chinese researchers on this area of study.
As shown in Figure 2, microbial soil remediation research spans multiple disciplines and fields, with environmental sciences (1478 publications) representing the highest proportions, followed by environmental engineering (397 publications), biotechnology and applied microbiology (345 publications), microbiology (205 publications), soil science (182 publications), water resources (134 publications), chemical engineering (123 publications), multidisciplinary chemistry (118 publications), toxicology (90 publications), and plant sciences (74 publications) from 2000 to 2024. Among the various disciplines, environmental sciences, environmental engineering, and biotechnology/applied microbiology have published the most papers on soil remediation over the past 20 years, accounting for 58.44%, 15.70%, and 13.64% of the total, respectively. This distribution highlights that microbial remediation has consistently been a key focus within the fields of environmental science, engineering, and microbial applications.

3.2. Countries/Regions and Institutions of Publications

Using VOSviewer 1.6.20 visualization software, an integrated analysis of collaboration between countries/regions and institutions in microbial soil remediation research was conducted, as shown in Figure 3. The size of the circles represents the number of publications from each country/region or institution, while the distance between circles indicates the closeness of collaboration, with shorter distances signifying closer collaboration. Figure 3a shows that countries with close cooperation with China mainly include the USA, Germany, Australia, Canada, South Korea, etc. Although there are connections among countries, the density of the cooperation network is not large, indicating the lack of cooperation and exchange among countries, which should be paid attention to in future research work. In addition, it can be seen from the institutional cooperation analysis network that the institutions with more than 50 published papers and close cooperation relations include Chinese Acad Sci (the total connection strength is 168, and the number of published papers is 150), Univ Chinese Acad Sci (the total connection strength is 93, and the number of published papers is 53), and Zhejiang Univ (the total connection strength is 54, and the number of published papers is 60) (Figure 3b). As can be seen from the connection in Figure 3b, Chinese Acad Sci has close cooperation with Univ Chinese Acad Sci, Zhejiang Univ, South China Agr Univ, and other institutions and has a high influence. In addition, there is usually a cooperative relationship between different agencies in the same country, while there is less cooperation and exchange between different agencies internationally.
According to the total link strength (TLS) summarized in Table 1, countries with high publication volumes exceeding 150 and close collaboration include China (TLS of 364), the United States (TLS of 224), and India (TLS of 168). Globally, the total citation frequency for microbial soil remediation research is 98,590, with an average citation frequency per article of 27. China has the highest total citation frequency (27,299) and the second highest average citation frequency per article (26), followed by the United States (12,788 total citation frequency, average citation frequency per article of 48) and India (12,745 total citation frequency, average citation frequency per article of 47).

3.3. Major International Journals and Key Publications

Using HistCite Pro software, the top ten journals with the highest number of publications in the field of microorganisms in soil remediation are presented in Table 2. The leading journals in terms of publication volume include Chemosphere (146 articles), Journal of Hazardous Materials (141 articles), Science of The Total Environment (137 articles), Environmental Science and Pollution Research (111 articles), and Environmental Pollution (74 articles), among others. Notably, in 2024, the journals with an impact factor greater than 5 are Chemosphere (8.8), Journal of Hazardous Materials (13.6), Science of The Total Environment (9.8), Environmental Science and Pollution Research (5.8), Environmental Pollution (8.9), Ecotoxicology and Environmental Safety (6.8), Journal of Environmental Management (8.7), and Frontiers in Microbiology (5.2). The total local citation score (TLCS) from HistCite Pro measures the influence of journals within the field of microbial soil remediation research. Notably, Chemosphere (46 citations) and the Journal of Hazardous Materials (45 citations) have high TLCS values, indicating that articles published in these journals have a significant impact on the field of microbial remediation.
The top ten highly cited articles in microbial soil remediation research are detailed in Table 3. The most cited article is “Trace elements in agroecosystems and impacts on the environment” by U.S. scholar He, ZLL, published in Journal of Trace Elements in Medicine and Biology (total citations: 1048; average citations per article: 95). This is followed by “A New Strategy for Heavy Metal Polluted Environments: A Review of Microbial Biosorbents” by South African scholar Ayangbenro, AS, in International Journal of Environmental Research and Public Health (total citations: 811; average citations per article: 84), and “Chemical and microbial remediation of hexavalent chromium from contaminated soil and mining/metallurgical solid waste: A review” by Indian scholar Dhal, B, in Journal of Hazardous Materials (total citations: 788; average citations per article: 230). Other notable articles include “A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludge” by British scholar Smith, SR, in Environment International (total citations: 644; average citations per article: 144), and “Nitroaromatic Compounds, from Synthesis to Biodegradation” by U.S. scholar Ju, KS, in Microbiology and Molecular Biology Reviews (total citations: 635; average citations per article: 220). The findings from highly cited literature indicate that the research in microbial remediation has evolved from a macro to a micro scale, with research methods becoming increasingly advanced and reliable in both qualitative and quantitative approaches.
Based on the analysis of total citations in the field of microbial soil remediation research (Figure 4, Table 4), it is evident that publications holding the top ten positions in centrality values from 2000 to 2024 constitute nearly 70% of the total, indicating a sustained high interest in this area. Significant literature in this field includes N. Bolan’s “Remediation of heavy metal(loid)s contaminated soils—To mobilize or to immobilize?” published in the Journal of Hazardous Materials. This study primarily discusses the use of soil amendments to regulate the bioavailability of heavy metals in contaminated soils, noting the limitations of plant uptake capacities for heavy metals and their susceptibility to leaching, which is a major constraint in current soil metal activation technologies. The article also emphasizes the need for long-term stability monitoring of immobilized heavy metals in fixed technologies [27]. Another notable work is S.J. Varjani’s “Microbial degradation of petroleum hydrocarbons”, published in Bioresource Technology. This review covers bioremediation techniques for petroleum hydrocarbon pollutants and includes explanations of microbial hydrocarbon metabolism mechanisms [28]. In the Plant Science article “Phytoremediation and Rhizoremediation of Organic Soil Contaminants: Potential and Challenges”, Gerhardt KE explores the potential and challenges of using rhizobia for the remediation of organic soil pollutants [29]. The study highlights that plant stress factors, often absent in laboratory and greenhouse settings, may present significant challenges in field applications. This research places a strong emphasis on the microbial community structure in soil and its impact on the degradation processes of heavy metals and organic pollutants, as well as its role in metabolic activities. Other significant literature focuses on the remediation of polycyclic aromatic hydrocarbon (PAH)-contaminated soils, where PAHs undergo processes such as adsorption, volatilization, photolysis, and chemical oxidation, with microbial transformation being the primary ecologically acceptable neutralization process [30].

3.4. Keyword Clustering Analysis

Keyword visualization quickly provides insight into the primary content and research goals of the literature. The frequency of keyword occurrence indicates the level of interest in relevant topics. This study employed VOSviewer 1.6.20 software to construct a co-occurrence network of high-frequency keywords (Figure 5). The most frequently occurring keywords were “remediation”, “heavy metal”, and “bioremediation”, with occurrences of 563, 491, and 486, respectively, suggesting that heavy metal pollution remediation is a current research hotspot (Table 5). Following this, organic soil remediation is also a significant focus, with bioremediation emphasized as a sustainable and promising treatment method. In the co-occurrence network, terms closely related to bioremediation include “bioaugmentation”, “biodegradation”, “soil”, “fungi”, “bioavailability”, and “crude oil” (Figure 5). Recent research has mainly concentrated on three areas: microbial remediation of heavy metal pollution in soil, microbial remediation of organic soil pollution, and the assessment of ecological risks linked to soil contamination (Figure 5). Additionally, Table 5 compiles the top 20 high-frequency keywords in this field from 2000 to 2024, discussing these research hotspots based on the appearance of high-frequency keywords within each cluster.
Cluster 1 focuses on soil pollution control and remediation technologies, incorporating keywords such as “phytoremediation”, “soil remediation”, “heavy metal”, “immobilization”, “rhizosphere”, and “soil microbial community” [31,32]. This research area includes studies on the solidification of soil heavy metals and soil microbial remediation agents, with particular attention to soil microbial communities, plant remediation technologies, and pollutants like arsenic in soil [33]. These research hotspots are expected to drive further development and application of technologies for controlling and remediating soil heavy metal pollution.
Cluster 2 primarily addresses the use of bioremediation to tackle petroleum pollutants, including crude oil and polycyclic aromatic hydrocarbons (PAHs). Keywords such as “bioremediation”, “biodegradation”, “bioaugmentation”, “bioavailability”, “contaminated soil”, “crude oil”, and “PAHs” are central to this cluster [34]. This research area focuses on bioaugmentation, biodegradation, and bioavailability of petroleum pollutants in contaminated soil, offering promising advancements in organic soil pollution remediation [35].
Cluster 3 covers topics related to the degradation and toxicity assessment of soil pollutants. Key terms include “soil”, “degradation”, “toxicity”, “groundwater”, “contamination”, “petroleum”, and “phenanthrene” [36]. This domain investigates natural soil degradation processes, the degradation and toxicity of diesel, the effects of petroleum pollutants on groundwater, and the assessment and remediation of soil pollution [37]. These research hotspots are vital for understanding the behavior and impact of petroleum pollutants in soil and for developing effective soil remediation technologies.

3.5. Research Focus and Development Trends

By integrating key literature on microbial soil remediation (Table 4), hot cluster analysis (Figure 5, Table 5), and keyword burst analysis (Table 6), this study synthesizes and summarizes the research focus and trends in microbial soil remediation. Table 5 presents the top 20 keywords in global and Chinese publications from 2000 to 2024 in this research field. The data reveal a strong alignment between global and Chinese research priorities regarding the response of soil microorganisms to heavy metals, organic pollutants, and inorganic pollutants. Globally, researchers are particularly focused on soil environmental management and pollution remediation, with a notable emphasis on strategies to combat heavy metal pollution. Globally, researchers have shown significant interest in environmental governance and pollution remediation, particularly in addressing heavy metal pollution. Key terms such as “remediation”, “bioremediation”, and “biodegradation” reflect sustained attention to environmental remediation technologies and strategies. Furthermore, the important role of microbes in environmental remediation is highlighted by terms like “microbial community” and “microorganism.” Compared to global trends, Chinese research places greater emphasis on practical applications and operational aspects of environmental governance. Chinese scholars show significant interest in keywords such as “heavy metal”, which appears 247 times (Table 5), indicating a strong focus on heavy metals as key pollutants in microbial soil remediation research [38,39]. Other high-frequency keywords suggest significant research directions in the microbial degradation of petroleum pollutants, aligning with China’s emphasis on developing green and sustainable agricultural practices [40,41]. Recent studies have highlighted a synergistic interaction between the diverse microbiota naturally present in soil and the functional bacteria responsible for degradation in oil-contaminated soils. This interaction not only modifies the composition of native microbial communities but also fosters an environment conducive to the biodegradation of petroleum pollutants. Furthermore, the introduction of live bacterial preparations into oil-polluted soils enhances the interaction between microbes and hydrocarbons, thereby improving the efficiency of petroleum hydrocarbon degradation [42,43].
Based on CiteSpace 6.1.R6 analysis of keyword burst indicators in the field of microbial soil remediation, along with hotspot analysis (Figure 5) and keyword burst analysis (Table 6), this study synthesizes the primary research trends in bioremediation and immobilization mechanisms. Keywords with high burst strengths include “phenanthrene” (11.14, 2000–2019), “microorganism” (10.14, 2005–2014), “mechanism” (13.62, 2020–2024), “immobilization” (11.46, 2020–2024), and “biochar” (10.08, 2020–2024). Long-standing burst indicators include “microbial activity” (7.75, 2001–2014), “diesel oil” (9.59, 2005–2014), and “biostimulation” (9.42, 2005–2019), indicating early 21st-century research focuses on microbial mechanisms related to pollutants like phenanthrene and diesel oil. As research progressed, keywords such as “biostimulation” and “sludge” suggest ongoing investigations into microbial actions on pollutants. Bursting keywords from 2019 onwards include “agricultural soil”, “biosorption”, “polluted soil”, and “amendment”, reflecting growing attention to health risks posed by soil heavy metal pollution and related risk assessments in agricultural soils. Recent burst keywords include “mechanism”, “biochar”, and “arbuscular mycorrhizal fungi”, highlighting emerging research on novel materials and biotechnologies [44,45]. For instance, composite materials like zero-valent iron-modified biochar (CF-nZVI) are identified as potential soil remediation materials due to their low cost, excellent adsorption properties, and ease of separation, which help reduce the bioavailability of heavy metals in contaminated soils [46,47]. Jianhua et al. developed a mixture containing FeS and FePO4 by using sulfurized and phosphorus-doped biochar. Their results demonstrated that this mixture effectively degraded trichloroethylene (TCE) [48].

4. Discussion

4.1. Research Trends and Hotspots of Microbial Remediation of Contaminated Soil

In the realm of contaminated soil remediation, interest in microbial remediation has demonstrated a consistently upward trend. Research indicates that since 2010, the number of publications on microbial remediation has significantly increased, with an average of at least 18 papers published per year (Figure 1). This rise reflects the growing recognition of the crucial role microorganisms play in soil pollutant remediation, soil environment enhancement, and vegetation restoration [10,49,50]. Between 2017 and 2023, developing countries, particularly China and India, accounted for 67% of global publications in this field. This underscores the significant demand for microbial remediation in developing countries. Moreover, developing nations like China and India maintain close collaborative relationships with developed countries such as the United States, Australia, and Poland (Figure 3). China, in particular, is central to the international cooperation network, highlighting the urgent need for both developing and developed countries to achieve breakthroughs in microbial soil remediation [51].
The clustering results from highly cited literature and co-citation analysis (Table 3 and Figure 4) reveal that research on microbial remediation of contaminated soil has progressed from initial investigations into the community composition and structural characteristics of soil microorganisms to more advanced studies on the diversity, structure, function, and regulatory mechanisms of microbial remediation under various environmental conditions [52,53]. This shift indicates a transition from a macro to a micro focus, with increased attention now directed towards understanding the mechanisms of microbial remediation, providing a theoretical foundation for this field [54]. Keyword clustering, ranking, and burst keyword analyses highlight that current research hotspots in microbial remediation focus on inorganic pollutants such as heavy metals and organic pollutants such as PAHs (Figure 5, Table 5). This emphasis suggests that global soil pollution issues are predominantly centered around these two types of contaminants. Possible causes include the release of heavy metals and PAHs into the soil due to mineral resource extraction, pesticide and fertilizer application, industrial spills, and waste accumulation [55]. Additionally, recent research has also concentrated on the combined use of microorganisms and new materials for soil pollution treatment (Table 6). This indicates that single remediation technologies often face limitations regarding effectiveness, cost, and efficiency, necessitating solutions through interdisciplinary approaches or technological integration [56,57].

4.2. Mechanism and Influencing Factors of Microbial Remediation of Contaminated Soil

The characteristics of pollutants significantly influence the effectiveness of microbial remediation [58]. Both excessive and insufficient pollutant concentrations within a certain range can impact remediation outcomes. For example, the optimal concentration for removing chromium (Cr) from soil using Streptomyces or chromium-specific soil is around 1800 mg/L, where the removal efficiency is highest [59,60]. The physicochemical properties and bioavailability of pollutants are critical factors affecting microbial degradation efficiency [61]. Bioavailability refers to the extent of substances that are physically and chemically accessible to microorganisms [62,63]. Generally, complex organic pollutants tend to be more hydrophobic, less water-soluble, and less bioavailable, making them more challenging to degrade compared to simpler organic pollutants (e.g., long-chain alkanes versus short-chain alkanes). While simpler structures are more bioavailable and easier to degrade, they often exhibit higher biological toxicity [64,65,66]. Cerqueira et al. demonstrated that both the characteristics and bioavailability of pollutants directly influence the degradation efficiency of petroleum hydrocarbons, with simpler structures leading to higher microbial degradation efficiency [67]. Additionally, variations in soil environment conditions can impact the efficacy of microbial remediation [59,68]. Suboptimal temperatures can hinder microbial growth, impairing adsorption, degradation, and other functions, disrupting the exchange of substances and energy within and outside the cells, and thereby affecting soil remediation results [69]. Microorganisms are also highly sensitive to oxygen levels [70]. Oxygen concentration can regulate the entire nitrogen fixation process in bacteria, including the expression of the nifA protein associated with nitrogen fixation [71,72,73]. Furthermore, appropriate salt concentrations can help maintain osmotic pressure inside and outside cells during the remediation of heavily contaminated soil [74]. For instance, when Serratia marcescens was used to adsorb cadmium (Cd), it was observed that at zero sodium chloride concentration, the microbial removal rate of Cd was high. However, as the concentration of sodium chloride increased, the removal efficiency of heavy metals decreased [75].
Currently, microbial remediation of contaminated soil primarily involves biological adsorption and biological REDOX processes [76,77]. Biological adsorption relies on the ability of microorganisms to trap heavy metals through functional groups present on their surfaces. For instance, Deepika et al. isolated Rhizobium radiobacter from mung bean root nodules. In arsenate tolerance experiments, arsenic stress on the extracellular polysaccharides of Rhizobium enhanced its arsenate adsorption capacity [78]. Biological REDOX processes can convert heavy metals into less toxic forms. For example, Bacillus amylolyticus can reduce Cr(VI) to Cr(III) and bind it to the bacterial cell surface [79]. Similarly, Pseudomonas B50A can reduce Hg(II) to Hg(0) via Hg reductase [80]. Microorganisms can also facilitate the deposition of heavy metals through biomineralization, forming insoluble oxides, sulfides, phosphates, or carbonate coprecipitates. This process reduces the bioavailability of heavy metals and aids in their recovery [81]. Xu et al. examined the effects of microbial-induced carbonate precipitation (MICP) on soil near a contaminator and used urease-producing microorganisms to convert heavy metal ions into stable carbonates, significantly lowering the levels of exchangeable heavy metals in the soil [82]. Li et al. demonstrated that using corn cobs loaded with urease bacteria for carbonate precipitation reduced the exchangeable cadmium (Cd) in soil by 68.54% [83]. For the remediation of organic contaminants, microbial degradation and transformation are key. For example, bacteria can catalyze the oxygenation of polycyclic aromatic hydrocarbons (PAHs) by producing dioxygenases, while fungi can oxidize PAHs by secreting lignin-degrading enzymes or monooxygenases. These processes reduce the stability of PAHs, making them easier to degrade [84,85,86].

5. Future Research Directions

(1) Research on bioremediation technologies for PAHs and heavy metal co-contaminated soils. Effective bioremediation materials for soils co-contaminated with PAHs and heavy metals are still limited. There is a need to increase the screening and development of remediation materials that efficiently remove both PAHs and heavy metals from soil. This involves utilizing plants and microorganisms capable of secreting extracellular polymeric substances (EPSs), organic acids, surfactants, and other metabolites under co-contaminant stress conditions.
(2) Development of integrated remediation technologies. Single remediation techniques often fail to achieve desired results, particularly for large areas or soils with moderate to low pollution levels. Integrated remediation technologies show promising potential for the remediation of heavy-metal-contaminated soils, especially when combined with agronomic control measures. These methods can reduce remediation costs while ensuring effectiveness, potentially becoming the preferred choice for future soil remediation.
(3) Promoting adaptation between fungi and indigenous bacteria. While microbial remediation technology is a growing trend for the future, it faces limitations. For example, fungi selected through cultivation may compete unfavorably with indigenous microorganisms, potentially leading to their elimination, particularly in the case of heavy-metal-tolerant fungi.
(4) Combining microorganisms with modified biochar and similar materials. Modified biochar provides colonization sites for microorganisms, increasing their activity and competitive advantage against indigenous bacteria. However, the long-term efficacy and stability of modified biochar in remediating heavy-metal-contaminated soils lack comprehensive experimental research. Further investigation is needed into the aging effects of modified biochar on soil remediation.
(5) Studies of the remediation effectiveness and mechanisms of modified mineral materials combined with arbuscular mycorrhizal fungi for soil immobilization of heavy metals. Mineral materials have abundant resources and low costs, promising broad application prospects. Current research predominantly focuses on clay mineral modification and its adsorption and immobilization effects. However, there is a lack of studies on the interaction mechanisms between modified clay mineral materials and other organic compounds, inorganic substances, and microorganisms once they enter contaminated soils.

6. Conclusions

This study offers a visual analysis of the plant-growth-promoting rhizobacteria (PGPR) research field based on 2371 publications from the Web of Science Core Collection database from 2000 to 2024. The analysis emphasizes the main contributing countries, disciplines, journals, research hotspots, and development trends. The findings show collaborative research efforts among multiple countries and institutions in microbial soil remediation, with China leading in publication volume. Major collaborations in microbial soil remediation research include the Chinese Academy of Sciences, University of Chinese Academy of Sciences, Zhejiang University, and South China Agricultural University. Key journals, such as Chemosphere (146 publications), are identified as significant contributors to the literature on microbial soil remediation, focusing on topics like microbial restoration of soil environments and combined microbial–plant remediation of heavy-metal-contaminated soils. Additionally, keyword co-occurrence networks in this field primarily cluster around soil pollution control and remediation, bioremediation for handling petroleum pollutants, including polycyclic aromatic hydrocarbons (PAHs), and degradation of contaminants in soil, along with toxicity assessment. The development of integrated remediation technologies remains a current research hotspot. Future research in this field is expected to focus on symbiotic relationships between arbuscular mycorrhizal fungi and plant root systems to improve plant absorption and tolerance of pollutants such as heavy metals, as well as interactions between indigenous microbial communities and plants.

Author Contributions

S.Z. contributed to the validation, original draft, and literature collection. F.-P.L. contributed to the validation, framework, and supervision. X.-H.W. contributed to the software, validation, and framework. Y.-J.A. contributed to the literature collection. X.-T.Y. contributed to the validation, framework, and correction process. All authors have read and agreed to the published version of the manuscript.

Funding

This project was supported by the National Natural Science Foundation of China (No. 52274166), the Hebei Industrial Technology Institute of Mine Ecological Remediation, and the Central Guided Local Science and Technology Development Fund Project of Hebei Province (Grant No. 246Z4201G).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Sustainability 16 07458 g001
Figure 1. Statistics on the trend in the number of published documents from ten countries over the past 20 years.
Figure 1. Statistics on the trend in the number of published documents from ten countries over the past 20 years.
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Figure 2. Publication trend chart.
Figure 2. Publication trend chart.
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Figure 3. Analysis of the cooperation network between the producing country (a) and the institution (b).
Figure 3. Analysis of the cooperation network between the producing country (a) and the institution (b).
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Figure 4. Clustered co-citation network of literature. Note: The years in the figure represent the publication dates of the literature.
Figure 4. Clustered co-citation network of literature. Note: The years in the figure represent the publication dates of the literature.
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Figure 5. Co-occurrence network of keywords.
Figure 5. Co-occurrence network of keywords.
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Table 1. Top 10 total link strengths between countries and institutions.
Table 1. Top 10 total link strengths between countries and institutions.
RankCountryTotal Link StrengthTotal CitationAverage Citation
1China36427,29926
2America22412,78848
3India16812,74547
4Germany160408343
5Australia147439441
6Canada84328642
7Spain64306835
8Italy60336337
9Poland49280027
10Russia24113813
Table 2. Top 10 journals ranked by number of publications in the relevant field from 2000 to 2024.
Table 2. Top 10 journals ranked by number of publications in the relevant field from 2000 to 2024.
RankJournalNumber of PapersImpact FactorTotal Local Citation Score (TLCS)Total Global Citation Score (TGCS)
1Chemosphere1468.8466065
2Journal of Hazardous Materials14113.6456568
3Science of The Total Environment1379.8314927
4Environmental Science and Pollution Research1115.8212902
5Environmental Pollution748.9143351
6Ecotoxicology and Environmental Safety566.881381
7Journal of Environmental Management538.742597
8Frontiers in Microbiology525.2231874
9International Biodeterioration & Biodegradation454.8172036
10International Journal of Phytoremediation423.79828
Table 3. Basic information of the top 10 highly cited papers.
Table 3. Basic information of the top 10 highly cited papers.
TopicFirst AuthorCountryJournalTotal CitationAverage Citation per Year
Trace elements in agroecosystems and impacts on the environmentHe, ZLLUSAJournal of Trace Elements In Medicine and Biology104895
A New Strategy for Heavy Metal Polluted Environments: A Review of Microbial BiosorbentsAyangbenro, ASSouth AfricaInternational Journal of Environmental Research and Public Health81184
Chemical and microbial remediation of hexavalent chromium from contaminated soil and mining/metallurgical solid waste: A reviewDhal, BIndiaJournal of Hazardous Materials788230
A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludgeSmith, SRBritainEnvironment International644144
Nitroaromatic Compounds, from Synthesis to BiodegradationJu, KSUSAMicrobiology and Molecular Biology Reviews635220
Extracellular polymeric substances of bacteria and their potential environmental applicationsMore, TTCanadaJournal of Environmental Management627209
The relative impact of toxic heavy metals (THMs) (arsenic (As), cadmium (Cd), chromium (Cr)(VI), mercury (Hg), and lead (Pb)) on the total environment: an overviewRahman, ZIndiaEnvironmental Monitoring and Assessment576187
Phytoremediation of contaminated soils and groundwater: lessons from the fieldVangronsveld, JBelgiumEnvironmental Science and Pollution Research572205
Biogeochemical processes and geotechnical applications: progress, opportunities and challengesDejong, JTUSAGeotechnique571142
Effects and mechanisms of biochar-microbe interactions in soil improvement and pollution remediation: A reviewZhu, XMChinaEnvironmental Pollution568165
Table 4. Basic information on the top 10 key documents.
Table 4. Basic information on the top 10 key documents.
TopicFirst AuthorJournalCentralityLiteratures Type
Remediation of heavy metal(loid)s contaminated soils—To mobilize or to immobilize?Bolan NJournal of Hazardous Materials0.24Review paper
Microbial degradation of petroleum hydrocarbonsVarjani SJBioresource Technology0.13Review paper
Phytoremediation and rhizoremediation of organic soil contaminants: Potential and challengesGerhardt KEPlant Science0.12Review paper
R: A Language and Environment for Statistical ComputingR Core Team RR Foundation for Statistical Computing, Vienna0.07Book
DADA2: High-resolution sample inference from Illumina amplicon dataCallahan BJNature Methods0.04Article
Remediation approaches for polycyclic aromatic hydrocarbons (PAHs) contaminated soils: Technological constraints, emerging trends and future directionsKuppusamy SChemosphere0.03Review paper
Current State of Knowledge in Microbial Degradation of Polycyclic Aromatic Hydrocarbons (PAHs): A ReviewGhosal DFrontiers in Microbiology0.02Review paper
Remediation techniques for heavy metal-contaminated soils: Principles and applicabilityLiu LWScience of The Total Environment0.02Review paper
Phytoremediation of heavy metals—Concepts and applicationsAli HChemosphere0Review paper
Bioremediation of soils contaminated with polycyclic aromatic hydrocarbons, petroleum, pesticides, chlorophenols and heavy metals by composting: Applications, microbes and future research needsChen MBiotechnology Advances0Review paper
Table 5. Top 20 keywords in research publications on global and Chinese research areas from 2000 to 2024.
Table 5. Top 20 keywords in research publications on global and Chinese research areas from 2000 to 2024.
RegionRankKeywordsFrequencyRankKeywordsFrequency
Global1remediation56311microbial community233
2heavy metal49112phytoremediation221
3bioremediation48613bacteria197
4biodegradation47814diversity159
5degradation45515crude oil156
6soil38316growth135
7contaminated soil35517water121
8polycyclic aromatic hydrocarbon31518bacterial community116
9microorganism29419petroleum hydrocarbon116
10removal25120hydrocarbon115
China1heavy metal24711microorganism107
2remediation22412diversity99
3bioremediation19813phytoremediation85
4degradation18814bacteria84
5biodegradation17615bacterial community69
6soil16516cadmium67
7microbial community15817growth65
8contaminated soil14318community60
9polycyclic aromatic hydrocarbon12919water58
10removal11420accumulation58
Table 6. Key keyword emergence information.
Table 6. Key keyword emergence information.
KeywordsStrengthBeginEndTime Scale
Phenanthrene11.1420002019Sustainability 16 07458 i001
microbial activity7.7520012014Sustainability 16 07458 i002
microorganism10.1420052014Sustainability 16 07458 i003
diesel oil9.5920052014Sustainability 16 07458 i004
biostimulation9.4220052019Sustainability 16 07458 i005
sludge7.720072014Sustainability 16 07458 i006
agricultural soil8.2520162019Sustainability 16 07458 i007
biosorption8.1920152019Sustainability 16 07458 i008
polluted soil7.7720162019Sustainability 16 07458 i009
amendment7.1920152019Sustainability 16 07458 i010
copper7.1420152019Sustainability 16 07458 i011
mechanism13.6220202024Sustainability 16 07458 i012
immobilization11.4620202024Sustainability 16 07458 i012
biochar10.0820202024Sustainability 16 07458 i012
arbuscular mycorrhizal fungi8.220202024Sustainability 16 07458 i012
Note: The red portion of the time interval indicates the onset and end time of emergence.
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Zhao, S.; Yuan, X.-T.; Wang, X.-H.; Ai, Y.-J.; Li, F.-P. Research Progress and Hotspots in Microbial Remediation for Polluted Soils. Sustainability 2024, 16, 7458. https://doi.org/10.3390/su16177458

AMA Style

Zhao S, Yuan X-T, Wang X-H, Ai Y-J, Li F-P. Research Progress and Hotspots in Microbial Remediation for Polluted Soils. Sustainability. 2024; 16(17):7458. https://doi.org/10.3390/su16177458

Chicago/Turabian Style

Zhao, Shuai, Xue-Tao Yuan, Xiao-Hong Wang, Yan-Jun Ai, and Fu-Ping Li. 2024. "Research Progress and Hotspots in Microbial Remediation for Polluted Soils" Sustainability 16, no. 17: 7458. https://doi.org/10.3390/su16177458

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