Bibliometric analysis of soil phosphate solubilizing microorganisms research using VOSviewer

Phosphorus-solubilizing microbes play key roles in improving phosphorus availability and in alleviating phosphorus nutrient limitation in soils. However, we did not have a comprehensive understanding of the overall research progress and development trend of phosphorus solubilizing microorganisms. In this study, we obtain documents from the Web of Science (WOS) core collection between 2002 and 2022, and a comprehensive review of the progress of global research on soil phosphate solubilizing microorganisms was conducted by using the VOSviewer bibliometric analysis tool. The results showed an increasing trend in the number of published articles from 2002 to 2022. India, accounting for 28% of the total number of published articles, became the most productive country. However, Canada was the country with the highest average citation frequency of articles.


Background
Phosphorus is involved in various physiological and biochemical processes in all living organisms and is one of the essential nutrients for maintaining the lives on the Earth [1][2].Soils are a significant source of phosphorus nutrients for plant growth.However, most of the phosphorus elements in the soils existed in the organic phosphorus pool, which cannot be directly assimilated and utilized by vegetations.The contents of organic phosphorus in the grassland ecosystem accounted for more than 80% of total phosphorus in soils [3].Furthermore, inorganic phosphorus at a low level in soils is often adsorbed or immobilized by metal elements, which further reduces the amount of available phosphorus [1,4].For example, inorganic phosphorus tends to react with iron and aluminum oxides in acidic soils [4][5], and tends to react with calcium and magnesium ions in neutral or alkaline soils [6].As a result of these above factors, the contents of available phosphorus in the soils were severely deficient.To date, about 5.7 billion hectares of arable land in the world have been exposed to the problem of phosphorus deficiency [7][8].
In agricultural management, exogenous phosphate fertilizer additions are often used to compensate for the shortage of available phosphorus in the soils [9][10].However, the minerals that are needed for the production of phosphate fertilizers are non-renewable resources.In addition, the substantial application of phosphorus fertilizers could cause a series of environmental problems [11].Phosphorus-solubilizing microbes are a group of widespread distributed microorganism taxa in soils that can convert organic phosphorus or insoluble phosphate immobilized by metal ions into active phosphorus that can be assimilated and utilized readily by plants [12][13][14][15].Therefore, phosphorus-solubilizing microbes play key roles in improving phosphorus availability and in alleviating phosphorus nutrient limitation in soils [15].Thus, the full utilization of phosphorus solubilizing microorganisms in native soils would be a natural solution to slow down the increasing depletion of phosphorus resources and maintain environmental health [14].
Microbial involved in the solubilization of insoluble phosphates was discovered in 1903 [16].Bacillus megatherium was the first strain of phosphorus solubilizing microorganisms isolated from soils in 1935 [17].To date, there were 36 genera and 89 species were found for phosphorus solubilizing microorganisms, which mainly included phosphate solubilizing bacteria (PSB), phosphate solubilizing fungi (PSF) and phosphate solubilizing actinomycetes (PSA) [14][15][16][17].The mechanisms for the solubilization of insoluble phosphorus by phosphate solubilizing microorganisms were described as Figure 1.
With the increasing research on phosphorus-solubilizing microbes, the number of review papers has increased rapidly [12][13][14][15][16][17][18].However, most of these papers were limited to summarizing the research advances in a certain field, which cannot provide a comprehensive understanding of the overall research progress and development trend of phosphorus solubilizing microorganisms.
In this study, we obtained documents from the Web of Science (WOS) core collection between 2002 and 2022, and a comprehensive review of the progress of global research on soil phosphate solubilizing microorganisms was conducted using the VOSviewer bibliometric analysis tool to fill in the gaps of the previous reviews.

Materials and methods
In this paper, data were obtained from the Web of Science (WOS) databases.The search formula was: TS = "soil" AND "phosphate solubilizing microorganism" OR "phosphate solubilizing microbes" OR "phosphate solubilizing bacteria" OR "phosphate solubilizing fungi".The time span was set from 2002 to 2022.The literature type was set to "Article" or "Review".A total of 2304 articles were obtained by eliminating irrelevant and repetitive articles.
The bibliometric analysis of soil phosphate solubilizing microbes based on the published documents was conducted using VOSviewer (V1.6.19).In this bibliometric analysis, annual publication number, citation frequency, journals, countries, institutions and keywords were examined.The research hotspots, frontiers and future development trends were clarified by the co-occurrence network visualization of the keywords based on a minimum frequency of 20 [19].

The volume of published articles
The volumes of published articles are important indicators for the interest of the specific field [17,20].The number of published articles about soil phosphate solubilizing microorganisms between 2002 and 2022 were shown in Figure 2. In general, the topic had shown a growing tendency over the years.However, compared to last year, the number of published documents in 2010 has decreased.The highest volume of publication was in 2022, with 303 documents, accounting for 13.2% of the total number of documents.In addition, more than 50% of the documents were published during the past five years, suggesting that the research on soil phosphorus solubilizing microorganisms had been highly investigated in recent years.

Country analysis
Analyzing the differences in the number of publications across countries can provide a quick insight into the influence and contribution of each country to the research on soil phosphorus solubilizing microorganisms [20][21].A total of 67 countries were involved in the publication of the topic on soil phosphorus solubilizing microorganisms.The 15 countries with the highest number of publications were shown in Table 1.The most productive country was the India (673), accounting for 28% of the total number of articles published, followed by China (585), Pakistan (165), Brazil (153), the USA (141), and Iran (114).The above six countries accounted for about 76% of all publications, which indicated that they were more concerned about soil phosphorus solubilizing microorganisms and may be in the leading position in this issue.Notably, India and China contributed approximately 52% of the global number of papers.Therefore, we also observed that the citations of India and China far exceeds that of other countries, which may be due to their relatively high number of published articles.
Interestingly, Canada was the country with the highest average citation frequency of articles (58).The top 5 countries with the highest average citation frequency of articles also included Spain (55), France (52), Australia (51) and the United States (48).However, China ranked 11th, with a low average citation frequency (20), which was only higher than Egypt and Iran.This finding indicated that China and other developing countries with similar problems should improve their international influence.

Institution analysis
Variations in the number of publications from different institutions can be used to represent the extent of academic support for research on soil phosphate solubilizing microorganisms [21].A total of 225 institutions were involved in research on soil phosphorus solubilizing microorganisms, and the top 20 institutions in terms of the number of publications were shown in Table 2.Among the institutions, the Chinese Academy of Sciences (CAS) ranked first with 127 publications, and became the greatest contributor.We also observed that more than half of the top 20 institutions with the largest publications were agricultural or forestry research communities or universities.There are three institutions with a total citation frequency over 1000, which are the Chinese Academy of Sciences (2477), the Ministry of Agriculture, India (1516) and China Agricultural University (1175).Among the 20 institutions, Zhejiang University in China has only 25 publications, but the average citation frequency of articles had exceeded 40, which made it an influential research center in the field of soil phosphorus solubilizing microorganisms in China with strong academic power.Therefore, these institutions would be a good choice for those who are interested in collaborating on research on soil phosphorus solubilizing microorganisms.

Journal analysis
The analysis of published journals is helpful for researchers to quickly

Keyword analysis
Keywords represent the core content of the study, which can summarize the main topics of an article in a precise and clear overview [21].High-frequency keywords mean research hotspots of this research direction in phosphorus solubilizing microorganisms [22][23][24].In this study, we adopted keyword analysis based on the co-occurrence network method to identify current hot themes and directions for observing and following up on the progress in the international academic community.The co-occurrence mapping of high-frequency keywords for soil phosphorus solubilizing microorganism was shown in Figure 3.The larger nodes in the network meant the more frequencies of keywords that appeared in the publications, which indicates that the topic is highly concerned [25].The thick line between two keywords provides an estimate of how closely the keywords are related to each other.In addition, the node in different colors indicates the time in which the keyword appeared, which is used to reflect the development trend of this direction [26].Therefore, we observed the top 5 keywords with , and plant-growth (461).It is well known that a considerable number of microorganisms were associated with the plant rhizosphere due to its carbon concentration.Soil phosphorus solubilizing microorganisms as heterotrophic organisms need carbon sources and energy for the synthesis of new cell material.Therefore, the population of phosphorus solubilizing microorganisms in the rhizosphere soil was higher than those in non-rhizosphere soil.A high proportion of phosphorus solubilizing microorganisms found in the plant rhizosphere, are metabolically more active than other sources [17].
Other important keywords were yield, rock phosphate, inoculation, nitrogen, wheat, diversity and maize.Most of these keywords were related to agricultural management, which may be attributed to the important role of phosphorus solubilizing microorganisms in promoting the growth and yields of crops [27][28][29].A number of phosphorus solubilizing strains with various plant growth-promoting rhizobacteria (PGPR) properties can colonize crop roots and increase crop yields.The properties of these phosphorus solubilizing strains are usually associated with plant growth promoting properties including: nitrogen fixation, auxin production, phytopathogen antagonism, and phosphate solubilization [16,30].Therefore, the use of phosphorus solubilizing microbial inoculants as biofertilizers represents a promising alternative to chemical fertilizers.
The most recent topics were related to carbon, organic-matter, biochar, manure, diversity, microbial community, mechanism and biofertilizer.Microorganisms affect soil characteristics through the excretion of polysaccharides.The production of polysaccharides by phosphorus solubilizing microorganisms is responsible for soil structure improvement [17].Studies have shown that phosphorus solubilizing microorganisms are capable of increasing soil aggregate stability, water-soluble carbon and carbohydrate carbon [16][17].In addition, culture-independent methods developed in the recent past pave the way for the study of community characteristics for phosphorus solubilizing microorganisms.Development of PCR and high throughput sequencing techniques recently were used for detecting diversity and quantifying expression of target genes in soil [31][32].It has been reported that phosphorus solubilizing microorganisms played a decisive role in improving microbial community structure and soil properties [17].Although phosphorus solubilizing microorganisms are abundant across varieties of soils, isolation, identification and selection of phosphorus solubilizing strains have not as yet been successfully commercialized, thus application is still found to be limited.Investigations on the subject are often designed to confirm a specific response of phosphorus solubilizing microorganisms to a particular environment, thus large scale application at field level is still limited.Therefore, it is necessary to use advanced technology to strengthen the deep excavation of phosphorus solubilizing strains to provide more strain resources.In addition, in-depth research on the interaction mechanism among phosphorus solubilizing strains, and systematic analysis of the effects of multi-factor interactions on phosphorus solubilizing strains, which can provide valuable information for improving their use.
In conclusion, there had been an overall increase in the number of international publications in the field of soil phosphorus solubilizing microorganisms from 2002 to 2022.India and China with the highest publication outputs, ranked 1st and 2nd in the world, respectively.The top 5 countries in terms of average citation frequency of articles included Canada, Spain, France, Australia and the USA.Biology and Fertility of Soils and Plant and Soil with the 5374 and 4026 citation frequency became the top two main journals due to the highest publications.Bioresource Technology had the highest impact factor in this field among the top 15 journals in the publications.In respect of the institutions, the Chinese Academy of Sciences ranked first in the world for the largest number of articles published and total citation frequency.Based on the keyword analysis, the topics of plant growth and agricultural production became the most frequent content.A more in-depth assessment was investigated in the following years involving the mechanisms between phosphorus-solubilizing microbes and the soil carbon cycles with the different management practices.

Figure 3
Figure 3 Visualization of keywords co-occurrence network in soil phosphate solubilizing microorganismsthe highest frequency during the period from 2002 to 2022 were phosphorus (704), rhizosphere (626), bacteria (502), microorganism (496), and plant-growth (461).It is well known that a considerable number of microorganisms were associated with the plant rhizosphere due to its carbon concentration.Soil phosphorus solubilizing microorganisms as heterotrophic organisms need carbon sources and energy for the synthesis of new cell material.Therefore, the population of phosphorus solubilizing microorganisms in the rhizosphere soil was higher than those in non-rhizosphere soil.A high proportion of phosphorus solubilizing microorganisms found in the plant rhizosphere, are metabolically more active than other sources[17].Other important keywords were yield, rock phosphate, inoculation, nitrogen, wheat, diversity and maize.Most of these keywords were related to agricultural management, which may be attributed to the important role of phosphorus solubilizing microorganisms in promoting the growth and yields of crops[27][28][29].A number of phosphorus solubilizing strains with various plant growth-promoting rhizobacteria (PGPR) properties can colonize crop roots and increase crop yields.The properties of these phosphorus solubilizing strains are usually associated with plant growth promoting properties including: nitrogen fixation, auxin production, phytopathogen antagonism, and phosphate solubilization[16,30].Therefore, the use of phosphorus solubilizing microbial inoculants as biofertilizers represents a promising alternative to chemical fertilizers.The most recent topics were related to carbon, organic-matter, biochar, manure, diversity, microbial community, mechanism and biofertilizer.Microorganisms affect soil characteristics through the excretion of polysaccharides.The production of polysaccharides by phosphorus solubilizing microorganisms is responsible for soil structure improvement[17].Studies have shown that phosphorus solubilizing microorganisms are capable of increasing soil aggregate stability, water-soluble carbon and carbohydrate carbon[16][17].In addition, culture-independent methods developed in the recent past pave the way for the study of community characteristics for phosphorus solubilizing microorganisms.Development of PCR and high throughput sequencing techniques recently were used for detecting diversity and quantifying expression of target genes in soil[31][32].It has been reported that phosphorus solubilizing microorganisms played a decisive role in improving microbial community structure and soil properties[17].Although phosphorus solubilizing microorganisms are abundant across varieties of soils,

Table 1 The top 15 countries with the most publication for soil phosphate solubilizing microorganisms
[20][21]rnals in the field of phosphate solubilizing microbes, which not only offered the information on collecting the relevant papers more comprehensively, but also provided an important reference value for the selection of journals when submitting the paper[20][21].The 15 journals with the highest number of publications were shown in Table3.Among these journals, Frontiers in Microbiology (63), Applied Soil Ecology (57), Plant and Soil (57) were the top three core journals in this field.The above 3 journals together accounted for about 26% of the total number of articles published.It is worth noting that the top two core journals in this field were Biology and Fertility of Soils and Plant and Soil with the 5374 and 4026 citation frequency.The journal with the highest average citation frequency was Biology and Fertility of Soils (103), followed by Plant and Soil (94), a manuscript: https://www.tmrjournals.com/lrget the

Table 3 The top 15 journals with the most publications for soil phosphate solubilizing microorganisms
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