3.2. Publication Distribution of Countries/Territories
The 7575 records in the WOS database indicate that 90 countries/territories contributed to the bioremediation of PCS publication records.
Table 2 shows the top ten countries and territories ranked by the number of total publications produced in each, and also contains other indices, such as total cited frequency and average cited frequency per paper, as well as the country’s
h-index. The
h-index was designed as a score to quantify the impact of scientific research. It is defined by the h of total
Np papers having at least h citations each while other (
Np-h) papers have no more than h citations [
34,
35]. The
h-index reflects both the quantity (number of publications) and quality (number of citations) of the publications and is therefore widely used to evaluate the scientific research impact of scholars, journals, and countries [
36,
37]. The top 10 countries were responsible for 68.9% of the total number of publications. The number of publications, citation frequency, and
h-index of the United States were in the top places, indicating that the United States had a relatively high level of influence in the field. China was the most productive country with 1476 articles, accounting for 19.5% of the total, but the average cited frequency per paper was only 23, which was much lower than that of developed countries, such as Spain, France, Germany, etc. Combined with the annual trend in the number of publications from each top 10 productive country (
Figure 2), it was speculated that this might be caused by China’s relatively late start in the field of PCS bioremediation.
Figure 2 shows the top 10 most productive countries with respect to the time-trend analysis during 2000–2019. The research on PCS bioremediation in the United States started early, while the number of articles published from 2000 to 2009 showed a stable state, and the number of articles published increased year by year since 2010. Although China started a little bit late in the field of PCS bioremediation, the number of articles published increased rapidly. In 2009, China surpassed the United States as the country with the largest number of publications. This shows that in recent years, with the rapid development of China’s economy and the acceleration of industrialization, the problem of PCS in China had become increasingly prominent and had gradually received extensive attention. Simultaneously, the remediation technology had also gradually developed from high-cost and irreversible physical and chemical technology to low-cost, no secondary pollution biotechnology and biological combined remediation technology. In addition to China and the United States, the annual number of publications issued by the other eight major countries showed an increasing trend year by year.
For further study, VOSviewer software was used to visualize the cooperative relationships among the top 30 productive countries and regions during 2000–2019, and the results are shown in
Figure 3. Each country or region is represented by a circle, and its size depends on the number of publications produced by that particular country. The curve connecting the two circles represents a cooperative relationship between the two linked countries. The thicker the curve, the stronger the collaborations between the two countries. The color of the circle in the visualization networks is determined by the cluster to which the country belongs. The distance between circles implies the degree of cooperation between countries or regions. As can be seen from
Figure 3, there were close cooperative relations among all countries. The United States had the most cooperative relations, cooperating with 28 countries or regions, with a total cooperation intensity of 438. China cooperated with 27 countries or regions, mainly the United States, Canada, and England, with a total cooperation intensity of 365. Of all the countries and regions that collaborated, China and the United States had the largest strength of cooperation, which illustrates that the two countries had the closest cooperation.
3.3. Publication Distribution of Institutions
A total of 4070 institutions were involved in the 7575 publications related to PCS bioremediation during 2000–2019. The top 10 most productive institutions in terms of total publication numbers are shown in
Table 3. The top 10 institutions originated from six countries—namely, China (4), France (2), India (1), Russia (1), Spain (1), Germany (1)—and accounted for 1329 total publications (17.5%). The United States, Canada, England, Italy, and Brazil belonged to the 10 most productive countries and regions. However, none of these countries’ institutions appeared in the list of the top 10 most productive institutes. The Chinese Academy of Sciences reported the highest number of publications, with 347 articles, which accounted for 4.6% of the total number of citations. The total frequency of citations was also the highest, which was 8994. From the total number of publications, citation frequency, and
h-index, it can be seen that the Chinese Academy of Sciences has made outstanding contributions in the field of PCS bioremediation. The average citations of articles published by two French institutions, Center National De La Recherche Scientifique and Universite De Lorraine, reached 39.2 and 39.6, respectively, indicating that they made a significant contribution to the field of PCS bioremediation. VOSviewer software was used to visualize the cooperative relationships among the research institutions with more than 15 articles published in the field of PCS bioremediation. The results are shown in
Figure 4. There were close and complex cooperative relationships among almost all institutions, and the cooperation network can be divided into three clusters: red, green, and blue. The red cluster is represented by the Chinese Academy of Sciences, primarily consisting of research institutions form China, South Korea, and the United States; the green cluster is chiefly composed of institutions from European countries, such as Spain and Russia; the blue cluster mainly is comprised institutions from Australia, and also includes some institutions from Middle East countries, such as Iran, and Asian countries, such as India. As shown in
Figure 4, the Chinese Academy of Sciences was not only the institution with the largest number of papers but also the institution with the largest partnership and cooperation intensity. It cooperated with 52 institutions, with a total cooperation intensity of 220. This shows that the Chinese Academy of Science made an outstanding contribution and had great influence in PCS bioremediation. All research institutions were inclined to cooperate with other domestic institutions. Therefore, strengthening cooperation with overseas institutions is suggested.
3.6. Keyword Analysis
Keywords are highly concise terms that are related to the research content of an article. Consideration of keyword statistics and analyses of the keywords are helpful in identifying research hotspots and research directions in a field, and they are essential in monitoring the development of science and programs [
20,
30]. Articles with records of author keywords in the field of PCS bioremediation were analyzed. A total of 11,515 keywords were recorded by authors, among which 8592 (74.6%) keywords were used only once, 1324 (11.5%) keywords were used twice, 500 (4.3%) keywords were used three times, and 348 (3%) keywords were used more than 10 times. The large number of once-only author keywords probably indicates a lack of continuity in research and a wide disparity in research focuses [
40]. Only small numbers of keywords were used more than three times. This might be because the research in PCS bioremediation was mainly concentrated in a small field. For further study, keywords that were the same or close to the search terms, such as “soil”, “oil”, “petroleum”, “bioremediation”, were removed. Keywords that were meaningless and searched, such as “study” and “its”, were ignored. Keywords that were close to each other, such as “composing” and “compost”, were unified. The top 30 author-generated keywords for the study period are listed in
Table 6. Available for high-frequency keyword analysis, crude oil and diesel oil have been the main pollutant sources for the last two decades, with polycyclic aromatic hydrocarbons (PAHs), total petroleum hydrocarbons (TPHs), as well as heavy metals being the main pollutants. It should be noted that the frequency of PAHs is much higher than that of TPHs, which means that more attention has been paid to the bioremediation of PAHs pollution. The main bioremediation techniques were phytoremediation, bioaugmentation, biostimulation, and composting [
17]. The main auxiliary means was the addition of biosurfactants (BS), such as rhamnolipids [
41]. In addition, the related research on microorganisms, such as the screening of efficient petroleum hydrocarbon-degrading bacteria and the analysis of soil microbial community diversity, is also an important research direction [
42,
43].
VOSViewer was used to generate a keywords co-occurrence network that shows the connection and weightage of the top 100 most high frequency author keywords, and the results are displayed in
Figure 5. A complex and close relationship was formed between the keywords. Each circle represents a keyword. The size of the circle reflects the number of occurrences of a keyword. The connection means a co-occurrence relationship between two keywords, and the color represents the cluster of the keyword—that is, the research topic. As can be seen from
Figure 5, keywords were divided into four clusters, cluster 1, cluster 2, cluster 3, and cluster 4 are represented by blue, green, red, and yellow, respectively. The keywords “bacteria”, “fungi”, and “DGGE” indicate that cluster 1 focused on the analysis of microorganisms and the change of microbial diversity, which is more than important for improving the efficiency of bioremediation [
44]. From the keywords “phenanthrene”, “pyrene”, and “fluoranthene”, it can be seen that cluster 2 mainly involves the study of the degradation of single pollutants, which is helpful for understanding the degradation characteristics of certain pollutants [
45]. Cluster 3 contains keywords related to microbial remediation, such as “biostimulation” and “bioaugmentation”, which are important technologies of microbial remediation [
46,
47]. In addition, BS strengthening bioremediation of PCS is also an important theme. Cluster 4 focuses on phytoremediation, which can be seen from the keywords such as “phytoremediation”, “plants”, and “rhizosphere”. Cluster 4 also includes the keyword “bioavailability”. Bioavailability is one of the basic principles for judging whether microorganisms are suitable for remediation of contaminants [
48]. The study of bioavailability can better evaluate the degradation efficiency of petroleum hydrocarbons by microorganisms and should be the priority research goal in bioremediation [
49]. These four clusters reflect the main research content of the current publications on bioremediation of PCS.
3.7. Hot Issues
The overlay visualization networks reflect the evolution of research content in a certain field and help to understand the research hotspots and development prospects in this field [
29]. The same data filtering method was used to generate an overlay visualization network of high-frequency keywords in VOSviewer, as shown in
Figure 6. Different colors in the figure represent the average publication year of the literature to which the keyword belongs. The closer the color is to purple, the earlier the keyword appears on average. The closer the color is to yellow, the later the keyword appears on average and the more times it shows in the latest research. As displayed in
Figure 6, the average occurrence years of 100 high-frequency keywords were mainly concentrated between 2010 and 2013, and some emerging keywords were scattered among them. Keywords such as “phytoremediation”, “phenanthrene”, and “anthracene” appeared earlier, and keywords such as “microbial community”, “biochar”, “chemical oxidation”, and “heavy metals” appeared later. By analyzing the average time of these high-frequency keywords, combined with the previous highly cited literature analysis and keyword co-occurrence network, this study systematically reflected the evolution of the research topic of PCS bioremediation, and more comprehensively understood the research hotspots and further research directions in this field.
In the early study of petroleum pollution, due to the complex composition of petroleum pollutants, scholars tended to study naphthalene, phenanthrene, anthracene, and other single pollutants at the laboratory level in order to understand the degradation characteristics of certain pollutants. Cerniglia and Yang [
50] proved that fungi could oxidize anthracene and phenanthrene to form trans-dihydrodiols. Davies and Evans [
51] demonstrated that under aerobic conditions, naphthalene is oxidatively metabolized by soil pseudomonads, undergoing epoxidation and eventual decomposition to carbon dioxide. Kastner and Mahro [
52] studied the degradation of naphthalene, phenanthrene, anthracene, fluoranthene, and pyrene in soils and soil/compost mixtures. The results showed that the addition of compost promoted the degradation of other PAHs, such as naphthalene, in soil with low water content.
Phytoremediation has attracted the extensive attention of scholars at home and abroad in the early stage of bioremediation research because of its advantages of safe operation, low cost, sustainability, and environmental friendliness [
53,
54,
55]. Phytoremediation technology refers to the collective term of environmental technology that uses the plant root system (or stem and leaf) to absorb, adsorb, transfer, enrich, degrade, or immobilize contaminants in contaminated soil, water, and the atmosphere [
56,
57]. It can be divided into phytostabilization, phytostimulation, phytotransformation, phytofiltration, and phytoextraction [
58]. The mechanisms of phytoremediation mainly include the plant’s own absorption and metabolism mechanisms of pollutants and the plant’s rhizosphere remediation mechanisms of these two types [
59]. Rhizosphere remediation is the primary phytoremediation mechanism for organic pollutants [
60]. Siciliano et al. [
61] explored the mechanisms by which phytoremediation systems promoted hydrocarbon degradation in soil. The results suggested that phytoremediation systems enhanced the catabolic potential of rhizosphere soils by altering the functional composition of rhizosphere microbial communities. In phytoremediation, screening natural oil-tolerant plants as well as strengthening their growth ability in PCS are critical factors in the success of phytoremediation [
62]. Merkl et al. [
63] investigated the effects of three legumes (Calopogonium mucunoides, Centrosema brasilianum, Stylosanthes capitata) and three kinds of grass (Brachiaria brizantha, Cyperus aggregatus, Eleusine indica) on the remediation of heavy crude oil contaminated soil. The oil content of soil seeded with grasses was significantly lower compared with the control group. Although phytoremediation is in line with the concept of sustainable development, due to the long growth cycle of plants, slow repair speed, and limited by environmental conditions, it cannot be the most ideal restoration scheme.
With the passage of time, there was more and more research on the application of bioremediation technology to the actual soil pollution [
64]. Therefore, the research on petroleum pollutants has changed from a single pollutant to comprehensive research on total petroleum hydrocarbons (TPHs) and polycyclic aromatic hydrocarbons (PAHs). PAHs, which are classified as priority environmental pollutants by the US Environmental Protection Agency, are important components of petroleum hydrocarbons and present carcinogenic, teratogenic, and mutagenic hazards to humans and other organisms [
65,
66]. Because PAHs are stable in nature, difficult to degrade, and easy to accumulate in soils, PAHs remaining in soils not only seriously contaminate the soil environment but also have potential impact on human health. Therefore, it is necessary to study the remediation of PAHs in soil [
67]. Guerin [
68] used an ex-situ land treatment process with soil mixing, aeration, and slow-release fertilizer addition for remediation of soils from polycyclic aromatic hydrocarbon pollutants. The result showed that bioremediation significantly degraded low-molecular-weight PAHs by 97% and high-molecular-weight PAHs by 35%.
At the same time, with people’s deeper research on soil microorganisms, microbial remediation technology has gradually become a research hotspot at home and abroad. It refers to the use of the catabolic effect of microorganisms to degrade oil hydrocarbon pollutants in soils as a carbon source, eventually eliminating the pollutants [
17]. The essence of microbial remediation is biodegradation and biotransformation. Microbial remediation can be divided into two categories: biostimulation and bioaugmentation [
69]. Biostimulation refers to identifying and adjusting certain physical and chemical factors (such as temperature, pH, nutrients, etc.) based on the optimal conditions for indigenous degradation bacteria to improve the abundance and reactivity of indigenous microorganisms, so as to enhance the degradation effect of pollutants [
70,
71]. Bioaugmentation refers to inoculating exogenous bacteria with degradation function into soil to achieve rapid and efficient removal of pollutants [
72,
73]. Abdulsalam et al. [
74] conducted a study and comparison on biostimulation and bioaugmentation for remediation of soil contaminated with spent motor oil using aerobic fixed bed bioreactors. The results showed that the removal rates of oil by bioaugmentation and biostimulation were 66% and 75%, respectively. Kauppi et al. [
75] studied the effects of biostimulation and bioaugmentation on diesel oil contaminated soil in cold regions. The results showed that bioaugmentation is an effective way to improve the efficiency of bioremediation. Suja et al. [
71] used a combination of biostimulation and bioaugmentation to remediate crude oil contaminated soil. The results showed that the combination of bioaugmentation with microbial consortium and biostimulation with nutrients was the best treatment method for a contaminated site. Microbial remediation is a widely used remediation method because of its short cycle, easy operation, low cost, and no secondary pollution [
76,
77]. However, its response to environmental changes is relatively strong, and the degradation efficiency of natural microorganisms is low [
78], while inoculated microorganisms have the problem of competition with indigenous microorganisms [
79]. Therefore, single microbial remediation is not the best model.
With the development of this field, the trend in research on bioremediation of PCS is expected to continue to mature, especially in the following four main aspects.
3.7.1. Research on the Composite Pollution System of Oil and Heavy Metals
Since petroleum contains heavy metals such as cadmium, lead, and mercury, petroleum hydrocarbon pollution is often accompanied by heavy metal contamination [
80,
81]. A huge number of studies have pointed out that heavy metal pollution exists in oil fields or industrial soils [
82,
83]. Vanadium (V) and nickel (Ni) are found in large concentrations in crude oil [
84,
85], and drilling muds contain large amounts of heavy metals such as lead (Pb), chromium (Cr), zinc (Zn), cadmium (Cd), and copper (Cu) [
86]. The composite pollution of petroleum hydrocarbons and heavy metals in soil not only alters soil biosystem structure and adversely affects the stability of biodiversity and soil ecological function, but also accumulates along the food chain in plants, animals, and humans, causing serious threats to human health [
13,
87]. The interaction between petroleum hydrocarbons and heavy metals will change the form and bioavailability of pollutants, inhibit the activity of degrading bacteria, and make the remediation process more complex [
88,
89]. At present, there are few studies on the bioremediation of multiple-contaminations of heavy metals and petroleum hydrocarbon. The interaction mechanism of petroleum hydrocarbons and heavy metals in soil and the biodegradation mechanism of petroleum hydrocarbons under heavy metal stress need further study.
3.7.2. Research on the Succession of Soil Microbial Community in the Process of Bioremediation
The degradation of petroleum hydrocarbons is often the result of a community-interacting microbial population [
90]. Understanding the changes of soil microbial diversity and activity in the bioremediation process is essential for understanding the behavior and function of the population and ensuring the effectiveness of bioremediation [
91]. A large number of studies have used biotechnology to analyze the changes of microbial community in the process of bioremediation. Ros et al. [
92] used aeration and organic amendment to remediate semi-arid soil contaminated by oily sludge. The changes of microbial community function and structure after bioremediation were studied by real-time PCR, BIOLOG, and DGGE. It was shown that bioremediation processes led to an increase in soil bacterial abundance, a decrease in microbial diversity, and changes in bacterial community structure and function. Sun et al. [
93] used 16S rRNA high-throughput sequencing technology to analyze the microbial community of nine kinds of PCS in Daqing and Changqing oil fields of China. The results showed that many dominant genera in PCS have phylogenetic relationships with known oil degrading species. With the development of molecular biology technology, more and more technologies for monitoring the dynamics of microbial communities will be applied in bioremediation, such as degradative enzyme assays, metagenomic/nucleic acid-based techniques, and phospholipid fatty acid analysis.
3.7.3. Application of BS in Bioremediation
BS is a surface active compound synthesized as metabolic products of different microorganisms [
94] that are able to reduce the interfacial tension, surface tension, and the critical micelle concentration and that are able to increase the surface area of hydrophobic pollutants, such as hydrocarbons, and improve their solubility and bioavailability [
95], thereby promoting the growth of microorganisms and the degradation of pollutants [
96,
97]. BS have the characteristics of low toxicity, biodegradability, and specific activity in extreme conditions [
98,
99]. They have broad application prospects in the bioremediation of PCS. Bezza and Chirwa [
3] showed that the degradation rate of PAHs in waste engine oil with BS was as high as 82%, which was more than twice as high as that without BS. Although many studies have proved that BS positively affected the removal of petroleum hydrocarbons at the laboratory level, some field studies have observed that BS have had no significant positive effect and may even have a negative impact on the pollutant treatment process [
100,
101]. This may be due to the BS deposition on the oil–water interface, which limits the contact between microorganism and substrate, thus inhibiting the biodegradation rate [
100]. In the future, more attention should be paid to elucidating the complex relationship between BS, microorganisms, and pollutants.
3.7.4. Application of Biological Combined Remediation Technology
Combined remediation technology organically integrates two or more repair methods, which can fully play to the advantages of each technology and improve remediation efficiency. At present, the biological combined remediation technology mainly includes bio-chemical remediation [
102] and inter-organismal (including plants, animals, microorganisms) remediation [
103,
104]. Among them, phyto–microbial remediation and chemical oxidation–microbial remediation are currently widely used biological combined remediation technologies to restore PCS [
105]. Phyto–microbial remediation technology utilizes the synergy between plants and microorganisms to immobilize, absorb and degrade pollutants [
103]. On the one hand, plant roots provide a living place for microorganisms [
44], and the chemical substances secreted by them improve the bioavailability of petroleum pollutants, which is conducive to microbial metabolism and decomposition [
106,
107]. On the other hand, microorganisms increase the biomass of plant roots, and their co-metabolism also improves the utilization efficiency of petroleum pollutants [
102,
108]. Xun et al. [
109] studied the effects of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) on the remediation of petroleum-contaminated saline alkali soil by oat plants. The results showed that the combination of PGPR and AMF made the plants more tolerant to petroleum hydrocarbons pollutants. Chemical oxidation combined with microbial remediation technology takes chemical oxidation as the pretreatment of bioremediation, which can improve the water solubility of petroleum hydrocarbons and transform the refractory macromolecular organic pollutants into small molecular substances [
110]. Gong [
111] used biostimulation and improved Fenton oxidation to decontaminate crude-oil-polluted soil. The results showed that the TPH content of the combined treatment decreased by 88.9%, while that of the biological treatment alone reduced by 55.1%. Biological combined remediation is the research hotspot in the field of PCS remediation. However, due to the differences between laboratory and remediation site environments, the specific effect of biological combined remediation on degradation of petroleum pollutants still needs to be verified by field research.
In general, based on keyword visualization analysis in the field of bioremediation of PCS, new research focuses on the compound pollution system of oil and heavy metals and how to improve the efficiency of bioremediation. As time goes on, the related research may be more abundant and in-depth.