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Article

The Impacts of Phosphorus-Containing Compounds on Soil Microorganisms of Rice Rhizosphere Contaminated by Lead

by
Xingchen Pan
1,
Wenjun Shi
2,
Guiping Feng
2,
Xiaolong Li
1,
Qingwei Zhou
1,2,3,*,
Li Fu
1,
Meiqing Jin
1 and
Weihong Wu
1,*
1
College of Materials and Environmental Engineering, Hangzhou Dianzi University, Hangzhou 310018, China
2
Zhe Jiang Huachuan Industrial Group Co., Ltd., Yiwu 322003, China
3
School of Environment Science and Spatial Informatics, Xuzhou Campus, China University of Mining and Technology, Xuzhou 221008, China
*
Authors to whom correspondence should be addressed.
Diversity 2023, 15(1), 69; https://doi.org/10.3390/d15010069
Submission received: 15 November 2022 / Revised: 28 December 2022 / Accepted: 2 January 2023 / Published: 5 January 2023
(This article belongs to the Special Issue Emerging Pollutants in Aquatic Ecosystems: Effects on Biodiversity and Solutions)
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Abstract

:
The cost effectiveness of using exogenous phosphorus to remediate heavy metals in soil, which would alter the structure of the soil microbial community, had been widely acknowledged. In the present study, phospholipid fatty acid (PLFA) technology was taken as the breakthrough point, and rhizosphere soil microorganisms in different growth stages (jointing stage and maturity stage) of Minghui 86 (MH) and Yangdao No.6 (YD) rice were taken as the research objects. As revealed by the results, the rhizosphere soil microorganisms of MH and YD had distinct sensitivities to exogenous phosphorus and had a certain inhibitory effect on MH and YD enhancement. The sensitivity of rice root soil microorganisms to exogenous phosphorus also varied in different growth stages of rice. Bacteria were the dominant microorganism in the soil microbial community of rice roots, and the gain of exogenous phosphorus had a certain impact on the structure of the two soil microbial communities. Through analysis of the microbial community characteristics of MH rice and YD soil after adding exogenous phosphorus, further understanding was attained with respect to the effect of exogenous phosphorus on the microbial community characteristics of rice rhizosphere soil and the impact thereof on ecological functions.

1. Introduction

Soil is regarded as a complex mixture of various animals, plants, microorganisms, and inorganic substances [1]. In particular, as a significant factor in all aspects of soil, soil microorganisms are indispensable to the biosphere [2]. For example, microbial community biodiversity is the driving force of plant growth and soil health [3]. Monitoring and proper regulation of microbial communities are beneficial to plant growth and soil restoration. Research has shown that microbes can alter the nutrient supply, soil structure, and soil fertility for plant growth [4,5]. For instance, bacteria and fungi in soil are vital in different biogeochemical cycles and are responsible for the recycling of organic compounds [6]. As such, the research on soil microorganisms needs to be supplemented and strengthened.
Rice is a traditional food staple for most regions of China. Pollutants in soil can be cleansed by absorption, volatilization, root filtration, degradation, and stabilization during the soil remediation process, which is based on rice’s tolerance and superaccumulation tendencies to heavy metals such as lead and cadmium [7]. Lead, for example, may enter rice via a proton pump, a cotransporter, an antitransporter, and an ion channel [8]. Heavy metal contamination of paddy fields in lead–zinc mining areas has emerged as a serious concern that threatens China’s food security [9]. The area of arable land contaminated by heavy metals in China is vast, accounting for about 20% of the total arable land area [10]. Thus, further developments are needed in the treatment of paddy fields contaminated by heavy metals. Phosphorus-containing materials (exogenous phosphorus) have recently been identified as effective remediation materials for heavy metals [5,11]. Such materials can reduce the migration and bioavailability of heavy metals in soil ecosystems by fixing heavy metals, so as to reduce the accumulation of heavy metals in plants [12]. At the same time, phosphate fertilizers have also been extensively adopted in agricultural production [13].
The addition of exogenous phosphorus in the soil remediation of heavy metals will affect the structure of the soil microbial community, thereby having a promoting or inhibiting effect on the soil microbial community depending on the rice variety [14]. As a significant nutrient element for microbial growth, the addition of phosphorus can considerably impact the soil microbial population and community composition [15]. Therefore, more information about the relationship between community composition and the phosphorus processing of heavy metals is needed. In bacterial cells, lipids are the main components of biological cell membranes, and the content thereof is stable in cells, accounting for about 5% of the dry weight of cells [16]. The proportion of fatty acids in biological biomass is approximately constant, and the presence of indicative fatty acids can be used to differentiate dominant microbial populations from others [17]. Hence, changes in fatty acid fractions can represent changes in microbial populations. On the basis of different fatty acid groupings representing distinct microbial populations, phospholipid fatty acid (PLFA) analysis can provide information on microbial community structure and diversity [18]. Phospholipid fatty acid (PLFA) analysis may quantitatively characterize the microbial population by analyzing the fatty acid spectrum, which is convenient and rapid, avoids human error, and is more accurate. It can also give us information on how soil microbial populations vary under different situations, providing a better scientific foundation for us to examine the remediation impact of polluted soil [19]. Such an approach has been employed to investigate the changes in microbial community composition by [20,21].
The objective of the present study was to investigate the variations in soil microbial community structure by adding different concentrations of exogenous phosphorus to the rice soil contaminated with heavy metals, and to use the phospholipid fatty acid analysis method to explore the soil microbial community structure in different periods of rice growth.

2. Materials and Methods

2.1. Sampling Site and Experimental Set-Up

The soil for the present experiment was obtained from cultivated soil (0–20 cm) of a nearby paddy field, which was contaminated by a lead–zinc mine located in Shangyu County, Shaoxing, Zhejiang Province (120.87° E 30.03° N, Figure 1 ). According to a 2009 survey by Hangzhou Dianzi University, the total stock of lead and zinc tailings in Yinshan is about 103,100 tonnes. This was an important source of heavy metal pollution in this area. The obtained soil was flattened indoors and air-dried under natural conditions. After air-drying, the soil was crushed and ground, and then passed through a 2 mm sieve. Different concentrations of exogenous phosphorus (calcium dihydrogen phosphate) were mixed into the experiment soil, and after incubating for a period of time, the soil was used in the present root box experiment.

2.2. Basic Physical and Chemical Properties of Soil

The basic properties of the soil were determined according to conventional methods, as shown in Table 1. An observation could be made that the pH value of the soil samples was about 5.70. The soil samples were acidic, which was consistent with the soil characteristics in Zhejiang. The organic matter content was 21.8 g/kg-1. The heavy metal contents, such as lead, zinc, copper, cadmium, and arsenic, all exceeded the second level of China’s soil environmental quality standards (GB15618-1995).

2.3. Root Box Experiment

The soil and calcium dihydrogen phosphate were mixed with four concentration gradients of 0, 0.5, 1, and 2 in the molar ratio of P to Pb, respectively. Subsequently, the tested soil samples in the pots were flooded and aged for 7 weeks. The tested rice varieties were Minghui 86 (MH) and Yangdao 6 (YD), which were provided by the Zhejiang Academy of Agricultural Sciences. Strong tillering capacity, huge panicle and numerous grains, and strong pour resistance were the three characteristics of the two rice types offered by the Zhejiang Academy of Agricultural Sciences. Before transplantation, rice seeds were sown in quartz sand and then transplanted into the tested soil samples when the rice seedlings reached three leaves. The same plant growth seedlings (the length of the ground was about 5 cm) were chosen and transplanted into a PVC root box with 10 bundles of rice. The length, width, and height of each box were 100, 40, and 40 cm, respectively. The experiment was conducted at the Zhejiang Academy of Agricultural Sciences under the same natural conditions with 8 root boxes. Rhizosphere soil and non-rhizosphere soil of MH and YD were collected at the jointing and mature stages. Rice plant with roots and soil was dug up, and a large soil block was shaken off. The rhizosphere soil was collected by the shaking roots according to Barillot [22]. Briefly, 5 bundles of rice were pulled from the soil in each root box, gently shaken to remove any excess surface soil, and then brushed to gently remove the 1–2 mm thick soil adhering to the root surface. This was the rhizosphere soil sample, which was used for PLFA analysis.

2.4. Phospholipid Fatty Acid (PLFA) Analysis

Phospholipids were extracted from each subsample and analyzed using GC/MS. Briefly, 3 g of fresh substrate without any root, withered branches, or leaves was extracted with a chloroform: methanol: pH 7.4 phosphate buffer (1:2:0.8, v/v/v), and then the total lipids extracted were further fractionated into neutral lipids, glycol-lipids and phosphor-lipids on a silica-bonded phase column (SPE-Si, 500 mg/6 mL, Agilent). The polar lipids were transesterified with mild alkali to recover the PLFA as methyl esters in hexane. The PLFAs were separated, identified, and quantified by an Agilent 6890N with a nonpolar capillary column. Helium was used as the carrier gas. The temperature of the injector was set at 250 °C. Samples (1 μL) were injected via spitless injection. The initial column temperature was maintained at 80 °C for 2 min, increased to 150 °C at 50 °C/min, and then increased to 195 °C at 2.5 °C/min, which remained constant for 3 min, before being further increased to 240 °C. Mass spectra were determined by means of electron impact at 70 eV. The method described by Macnaughton was adopted to qualify and quantify the PLFAs [23]. The fatty acid nomenclature used in the present study complied with that described by Macnaughton [24].

2.5. Nomenclature of Phosphate Fatty Acids

The commonly used naming form of phosphate fatty acid was X:YwZ(c/t), where X represented the total number of carbon atoms, followed by a colon; Y represented the number of double bonds between atoms; w represented the methyl end; Z was the length from the methyl end; c indicated the molecule was in cis form; t indicated the molecule was in trans form; a indicated branched chain trans isomerism; i indicated branched chain isomerism; 10Me indicated that a methyl group counts the first carbon from the end of the molecule; and cy represented cyclopropane fatty acid. Through PLFA spectrum analysis, prior scholars counted the types and contents of diverse PLFA to evaluate the structure and biomass of the soil microbial community [25]. The specific analogous instructions are shown in Table 2.

2.6. Data Analysis

All experimental data were analyzed and graphed using Microsoft Office 2010 and Origin 2021.

3. Results and Discussion

3.1. PLFA Distribution of Rice in Different Rice Stages

As soil microbes were susceptible to conditions, such as pH, soil texture, temperature, moisture, and aeration, the input of exogenous phosphorus must have distinct impacts on microorganisms [26,27]. Such impacts not only altered the total amount of soil microorganisms, but also led to changes in the structure of the microbial community [28]. The molar fraction distributions of the microbial PLFAs of MH and YD at the jointing and mature stages are shown in Figure 2. The numbers of specific fatty acids in MH and YD were 16 and 17, respectively. The results revealed that the i15:0, 17:0, i16:0, and i17:0 fatty acid mole fractions in MH decreased with rice growth. At the same time, 15:0, a15:0, cy17:0, 10Me17:0, and 18:3w6c (6, 9, and 12) fatty acid mole fractions remained stable, while the 16:1w7c, 18:1w7c, cy19:0 w8c, 18:1 w9c, and 10Me16:0 fatty acid mole fractions increased with rice growth. Compared with YD, most fatty acids did not increase or decrease apparently at the joining and maturity stages. Only 18:1 w9c and 10Me16:0 decreased with rice growth, while 18:2 w6,9c disappeared at the maturity stage. Being a distinctive fatty acid of fungi, 18:2 w6,9c might have disappeared due to the death of the corresponding fungi [29]. An observation could be made that the variations in the root soil microbial community characteristics of MD and YD were disparate in different periods. The fatty acid of YD remained fundamentally steady, indicating that the growth of YD had minimal influence on the soil microbial community structure. The relative change of the fatty acid in MH was visible, demonstrating that the growth of MH had a certain influence on the soil microbial structure. Meanwhile, the results also showed that different rice varieties had diverse impacts on the microbial community structure of rice root soil [30].

3.2. PLFA Distribution of Different Concentrations of Exogenous Phosphorus

3.2.1. The PLFA Distribution of YD at Given Concentrations

The variations in the mole fraction distribution of each characteristic fatty acid in PLFA after adding given concentrations of exogenous phosphorus to YD are presented in Figure 3 (the numerical representations of the soil labels are detailed in Table 3). At the jointing stage of YD, there was no apparent variations in most PLFAs with the increase in exogenous phosphorus concentration, and the most stable acid was 10Me17:0. The most apparent variety was in the fatty acid 18:1 w9c, of which the molar concentration decreased from 10% to below 2%, when the exogenous phosphorus concentration reached 2. For the characteristic fatty acid 18:3 w6c (6, 9, and 12) represented by protozoa, the mole fraction increased from less than 1% to 5%. It might be that the added concentration of exogenous phosphorus promoted the soil pH decrease, which could affected protozoa [31]. In the characteristic fatty acids representing bacteria from 15:0 to cy19:0 w8c, except for 17:0 and cy19:0 w8c, the maximum molar content of characteristic fatty acids appeared when the exogenous phosphorus concentration was 0.5 or 1, indicating that the application of low concentrations of exogenous phosphorus was conducive to bacterial growth, as shown in previous research [32,33]. The characteristic fatty acids of fungi 18:2 w6,9c and 18:1 w9c exhibited the opposite trend. They decreased with the increase in exogenous phosphorus concentration, especially when the exogenous phosphorus concentration reached 2, which severely inhibited the growth of fungi [34]. The characteristic fatty acids 10Me16:0, 10Me17:0, and 10Me18:0 represented by actinomycetes exhibited minimal fluctuation, suggesting that the application of exogenous phosphorus in YD had only a slight effect on actinomycetes. According to the aforementioned analysis, strains had diverse degrees of adaptation to the applied concentration of exogenous phosphorus, and the individual characteristic fatty acids of the same strain also had distinct variations [35]. Compared with the PLFA characteristic fatty acid distribution of YD at the jointing stage, the PLFA characteristic fatty acid distribution at the mature stage had diverse characteristics. Overall, YD at the mature stage exhibited apparently large variation under the application of given concentrations of exogenous phosphorus, whereas the single fatty acid did not fluctuate as much as that at the jointing stage. The characteristic fatty acids of bacteria from 15:0 to cy19:0 w8c, aside from 15:0 and 17:0, had the highest molar content when the exogenous phosphorus content reached 2, being distinct from the jointing stage. In the absence of exogenous phosphorus application, the characteristic fatty acid 18:2 w6,9c of the fungus was found to be 0 and reappeared at other concentrations, possibly due to the application of exogenous phosphorus favoring the growth of such fatty acid. It could be deduced that the addition of exogenous phosphorus improved soil fertility, promoted the growth of plants, facilitated plant development, fostered the growth of fungus, increased the quantity of fungi, and finally raised the amount of fatty acids in the soil [36].

3.2.2. The PLFA Distribution of MH at Given Concentrations

Figure 4 shows the characteristic fatty acid distribution of exogenous phosphorus and PLFA at given concentrations at the jointing and mature stages of MH. During the jointing stage of MH, the fluctuation of each characteristic fatty acid at given concentrations was relatively light. In parallel, the changes in contents of bacterial characteristic fatty acids with the increase in exogenous phosphorus concentration did not exhibit a uniform trend, with most tending to remain steady. The molar fraction of w7c and 18:1 w7c also increased with the increase in exogenous phosphorus concentration, which could be attributed to the accumulation capacity of different rice cultivars changing soil properties and pH and further affecting the content of microbial characteristic fatty acids [37]. However, only one fungal characteristic fatty acid, 18:1 w9c, was detected in MH, and the molar content thereof was highest when the exogenous phosphorus concentration was 1. The characteristic fatty acid molar concentrations of both actinomycetes and protozoa almost leveled off. Compared with YD, the microbial community of MH at the jointing stage was not susceptible to exogenous phosphorus application, and each microbial community remained relatively stable.

3.3. Variation in Microbial Community Structure at Jointing Stage

Bacteria, fungi, and actinomycetes were the dominating components of microorganisms in soil ecosystems [38]. The proportion of biomass of each functional group to the total biomass of the soil food cycle affects the carbon and nitrogen mineralization rate characteristics thereof [39]. The characteristic fatty acids of the two types of rice are approximately identical, and Table 4 shows the relative contents of PLFAs in soil microorganisms at the jointing stage of rice. An observation could be made that bacteria, fungi, and actinomycetes occupied most of the total soil microbial PLFA. Among the two kinds of rice, MH 0 had the lowest content of total microbial PLFA with 47.91%, while YD 1 had the highest with 73.64%. Bacteria occupied the largest proportion of the three populations. The molar ratio of bacteria in MH was between 34% and 41%, and the molar ratio of bacteria in rice YD was between 44% and 57%. As such, the proportion of bacteria in YD was higher than that in MH.
After adding calcium dihydrogen phosphate, the proportion of bacteria, fungi, and actinomycetes in YD was apparently larger than that of the control. Despite such findings, the gain of calcium dihydrogen phosphate did not augment the proportion, which was maintained around 73%. The proportion of bacteria, fungi, and actinomycetes in MH was the largest in the control, and decreased after calcium dihydrogen phosphate was added, but did not change much and remained around 52%. The results showed that diverse varieties of rice root soil microorganisms had disparate responses to exogenous phosphorus, with both promoting and inhibiting effects. The total amount of PLFA in YD rice was augmented after adding exogenous phosphorus. The reason for such findings might be that the two kinds of rice root soil microorganisms had distinct sensitivities to exogenous phosphorus. Exogenous phosphorus had an inhibitory influence on the rice root soil microorganisms of MH, which indirectly affects the decomposition of soil organic matter and the synthesis of humus. In addition, the transformation of exogenous phosphorus affects soil fertility, carbon sequestration, and environmental detoxification [40]. For example, Syers suggested that adding phosphorus could effectively increase soil fertility [41].
Both bacteria and fungi were decomposers of soil ecosystems, promoting carbon and nitrogen cycling in the soil [42]. In soils dominated by bacterial decomposition, organic matter degraded rapidly and the nitrogen mineralization rate was high, which was favorable to nutrient supply [43]. Meanwhile, the transformation of nitrogen and energy was relatively slow in soils dominated by fungi, which was beneficial for organic matter storage and nitrogen retention [44]. The higher the F/B value in soil, the higher the sustainability of the ecosystem, which had positive significance for nutrient cycling and plant growth [45]. A line graph of the enhancement of bacteria/fungi with the concentration of exogenous phosphorus at the jointing stages of YD and MH is presented in Figure 5. An observation could be made that the broken line of MH attained the highest point at the concentration of 0.5, and YD reached the maximum at the concentration of 1. Both types of rice showed that with longer exposure to exogenous phosphorus, the soil microbial community of their own soil roots formed in a direction more conducive to rice growth; however, the most suitable exogenous phosphorus concentration ranges for the two types of rice were distinct. MH was around 0.5, and YD was around 1. The overall higher ratio of fungi to bacteria suggests fungi dominance, increasing interaction between other microorganisms and the plant, therefore assisting the plant in obtaining nutrients and reducing plant water stress [46].
Gram-positive bacteria (G+), such as denitrifying bacteria, were often destructive in soil; Gram-negative bacteria (G−), such as nitrogen-fixing bacteria, were often beneficial in soil. This ratio (G−/G+) had an impact on both plants and microbial populations [47]. Notably, it also had a certain impact on the growth of rice [48]. As shown in Figure 6, MH G−/G+ reduced with the increase in exogenous phosphorus, reaching a minimum value when the exogenous phosphorus concentration was 1 before increasing again. The ratio of YD increased with the increase in exogenous phosphorus concentration. Such findings implied that diverse varieties of rice rhizosphere soil microorganisms had different levels of sensitivity to exogenous phosphorus. The addition of exogenous phosphorus had minimal effect on the overall proportion of bacteria, fungi, and actinomycetes, but apparently altered the ratios of bacteria/fungi and G−/G+, indicating that exogenous phosphorus had a non-negligible effect on the community structure of soil microorganisms in rice roots.

3.4. The Molar Fraction Ratio at Mature Stage

At the maturity stage of rice, the change tendency of the molar fraction ratio of each flora with the gain of exogenous phosphorus concentration was basically the same as that at the jointing stage, as shown in Figure 7. The total amounts of bacteria, fungi, and actinomycetes in the soil of MH reduced with the increase in exogenous phosphorus, while the total amounts of bacteria, fungi, and actinomycetes in the soil of YD increased with the concentration of exogenous phosphorus, reaching a maximum value at an exogenous phosphorus concentration of 0.5.

3.5. The absolute contents of the two kinds of rice

At the same time, there were distinct variations in absolute content. The absolute contents of the two kinds of rice at the jointing stage and the mature stage are presented in Figure 8. At the mature stage, with the gain of exogenous phosphorus in the soil, the total amount of PLFA of bacteria, fungi, and actinomycetes also increased; the total PLFA amounts of bacteria, fungi, and actinomycetes in MH decreased first and then increased with the increase in exogenous phosphorus. Compared with the rice root soil microorganisms at the jointing stage, MH exhibited an apparent decrease, while Yangdao 6 exhibited a slight decrease, and even increased when the exogenous phosphorus concentration was 1. The change tendency of the total soil microbial PLFA amount in the jointing stage and maturity stage of the two kinds of rice was consistent with the addition of exogenous phosphorus. With the growth of rice, the PLFA content of rice soil microorganisms decreased, which could be attributed to the influence of nutrients, water, and climate during the growth process.

4. Conclusions

In this study, the fatty acid distribution of YD remained basically steady, while the relative changes of MH were more distinct. During the jointing stage of YD rice, with the increase in exogenous phosphorus concentration, the relative content of bacterial characteristic fatty acids increased, and reached the highest when the exogenous phosphorus content was 1. The content of bacteria in YD rice at the mature stage was the highest when the exogenous phosphorus concentration was 2, while the content of actinomycetes and fungi remained stable. In contrast, the relative contents of bacteria, fungi, and actinomycetes in MH at the maturity and jointing stages were not apparently altered compared with YD. The gain of exogenous phosphorus had a considerable impact on the structure of both soil microbial communities, especially the ratios of G−/G+. The change tendency of the total amount of soil microbial PLFA at the jointing stage and the maturity stage of the two kinds of rice was consistent with the addition of exogenous phosphorus. In general, a phosphorus-to-lead molar ratio of 1 was the most beneficial to rice growth and microbial diversity. The PLFA content was generally high at this time, indicating that the microbial community could apparently promote, meanwhile, the F/B concentration was also high, indicating that the soil was conducive to nitrogen retention and increasing the connection between plants and microorganisms.

Author Contributions

Conceptualization, W.W.; methodology, Q.Z. formal analysis, X.P. and X.L.; investigation, M.J.; writing—original draft preparation, X.P.; writing—review and editing, Q.Z.; L.F.; M.J. and W.W.; supervision, W.S.; project administration, G.F.; All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Science Foundation of China, grant number [42173073; 42277017] and Pioneer” and “Leading Goose” R&D Programs of Zhejiang, grant number [2022C02022].

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We thank Hu ciming and Jiang tao for help with soil collection.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bonkowski, M.; Villenave, C.; Griffiths, B. Rhizosphere fauna: The functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant Soil 2009, 321, 213–233. [Google Scholar] [CrossRef]
  2. Lennon, J.T.; Aanderud, Z.T.; Lehmkuhl, B.K.; Schoolmaster, D.R., Jr. Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 2012, 93, 1867–1879. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Saleem, M.; Hu, J.; Jousset, A. More than the sum of its parts: Microbiome biodiversity as a driver of plant growth and soil health. Annu. Rev. Ecol. Evol. Syst. 2019, 50, 145–168. [Google Scholar] [CrossRef]
  4. Hemkemeyer, M.; Schwalb, S.A.; Heinze, S.; Joergensen, R.G.; Wichern, F. Functions of elements in soil microorganisms. Microbiol. Res. 2021, 252, 126832. [Google Scholar] [CrossRef] [PubMed]
  5. Yuan, Y.; Lu, M.; Tu, N.; Li, Y. Phosphate-modified ferric-based material remediates lead and arsenic co-contaminated soil and enhances maize seedling growth. Environ. Sci. Pollut. Res. 2019, 27, 7234–7243. [Google Scholar] [CrossRef] [PubMed]
  6. Bonkowski, M. Protozoa and plant growth: The microbial loop in soil revisited. New Phytol. 2004, 162, 617–631. [Google Scholar] [CrossRef]
  7. Pilon-Smits, E.A.H.; Freeman, J.L. Environmental cleanup using plants: Biotechnological advances and ecological considerations. Front. Ecol. Environ. 2006, 4, 203–210. [Google Scholar] [CrossRef] [Green Version]
  8. Hedrich, R. Ion Channels in Plants. Physiol. Rev. 2012, 92, 1777–1811. [Google Scholar] [CrossRef]
  9. Yang, Q.W.; Shu, W.S.; Qiu, J.W.; Wang, H.B.; Lan, C.Y. Lead in paddy soils and rice plants Lechang and its potential health risk around lead/zinc Mine, Guangdong, China. Environ. Int. 2004, 30, 883–889. [Google Scholar] [CrossRef]
  10. Huang, Y.; Wang, L.; Wang, W.; Li, T.; He, Z.; Yang, X. Current status of agricultural soil pollution by heavy metals in China: A meta-analysis. Sci. Total Environ. 2019, 651, 3034–3042. [Google Scholar] [CrossRef]
  11. Tan, Y.; Zhou, X.; Peng, Y.; Zheng, Z.; Gao, X.; Ma, Y.; Chen, S.; Cui, S.; Fan, B.; Chen, Q. Effects of phosphorus-containing material application on soil cadmium bioavailability: A meta-analysis. Environ. Sci. Pollut. Res. 2022, 29, 42372–42383. [Google Scholar] [CrossRef] [PubMed]
  12. Maenpaa, K.A.; Kukkonen, J.V.K.; Lydy, M.J. Remediation of heavy metal-contaminated soils using phosphorus: Evaluation of bioavailability using an earthworm bioassay. Arch. Environ. Contam. Toxicol. 2002, 43, 389–398. [Google Scholar] [CrossRef] [PubMed]
  13. Kataki, S.; West, H.; Clarke, M.; Baruah, D.C. Phosphorus recovery as struvite: Recent concerns for use of seed, alternative Mg source, nitrogen conservation and fertilizer potential. Resour. Conserv. Recycl. 2016, 107, 142–156. [Google Scholar] [CrossRef]
  14. Li, J.; Li, Z.; Wang, F.; Zou, B.; Chen, Y.; Zhao, J.; Mo, Q.; Li, Y.; Li, X.; Xia, H. Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol. Fertil. Soils 2015, 51, 207–215. [Google Scholar] [CrossRef]
  15. Widdig, M.; Heintz-Buschart, A.; Schleuss, P.-M.; Guhr, A.; Borer, E.T.; Seabloom, E.W.; Spohn, M. Effects of nitrogen and phosphorus addition on microbial community composition and element cycling in a grassland soil. Soil Biol. Biochem. 2020, 151. [Google Scholar] [CrossRef]
  16. Lechevalier, M.P. Lipids in bacterial taxonomy—A taxonomist’s view. CRC Crit. Rev. Microbiol. 1977, 5, 109–210. [Google Scholar] [CrossRef]
  17. Petersen, S.O.; Klug, M.J. Effects of sieving, storage, and incubation temperature on the phospholipid Fatty Acid profile of a soil microbial community. Appl. Environ. Microbiol. 1994, 60, 2421–2430. [Google Scholar] [CrossRef] [Green Version]
  18. Green, C.T.; Scow, K.M. Analysis of phospholipid fatty acids (PLFA) to characterize microbial communities in aquifers. Hydrogeol. J. 2000, 8, 126–141. [Google Scholar] [CrossRef]
  19. Roslev, P.; Iversen, N.; Henriksen, K. Direct fingerprinting of metabolically active bacteria in environmental samples by substrate specific radiolabelling and lipid analysis. J. Microbiol. Methods 1998, 31, 99–111. [Google Scholar] [CrossRef]
  20. Siciliano, S.D.; Germida, J.J. Biolog analysis and fatty acid methyl ester profiles indicate that pseudomonad inoculants that promote phytoremediation alter the root-associated microbial community of Bromus biebersteinii. Soil Biol. Biochem. 1998, 30, 1717–1723. [Google Scholar] [CrossRef]
  21. Zelles, L. Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: A review. Biol. Fertil. Soils 1999, 29, 111–129. [Google Scholar] [CrossRef]
  22. Barillot, C.D.C.; Sarde, C.-O.; Bert, V.; Tarnaud, E.; Cochet, N. A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system. Ann. Microbiol. 2013, 63, 471–476. [Google Scholar] [CrossRef]
  23. Macnaughton, S.J.; Stephen, J.R.; Venosa, A.D.; Davis, G.A.; Chang, Y.J.; White, D.C. Microbial population changes during bioremediation of an experimental oil spill. Appl. Environ. Microbiol. 1999, 65, 3566–3574. [Google Scholar] [CrossRef] [Green Version]
  24. Macnaughton, S.; Stephen, J.R.; Chang, Y.J.; Peacock, A.; Flemming, C.A.; Leung, K.T.; White, D.C. Characterization of metal-resistant soil eubacteria by polymerase chain reaction--denaturing gradient gel electrophoresis with isolation of resistant strains. Can. J. Microbiol. 1999, 45, 116–124. [Google Scholar] [CrossRef] [PubMed]
  25. Grayston, S.J.; Campbell, C.D.; Bardgett, R.D.; Mawdsley, J.L.; Clegg, C.D.; Ritz, K.; Griffiths, B.S.; Rodwell, J.S.; Edwards, S.J.; Davies, W.J.; et al. Assessing shifts in microbial community structure across a range of grasslands of differing management intensity using CLPP, PLFA and community DNA techniques. Appl. Soil Ecol. 2004, 25, 63–84. [Google Scholar] [CrossRef]
  26. Qi, G.F.; Ma, G.Q.; Chen, S.; Lin, C.C.; Zhao, X.Y. Microbial Network and Soil Properties Are Changed in Bacterial Wilt-Susceptible Soil. Appl. Environ. Microbiol. 2019, 85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Germida, J.J.; Janzen, H.H. Factors affecting the oxidation of elemental sulfur in soils. Fertil. Res. 1993, 35, 101–114. [Google Scholar] [CrossRef]
  28. Dong, W.Y.; Zhang, X.Y.; Liu, X.Y.; Fu, X.L.; Chen, F.S.; Wang, H.M.; Sun, X.M.; Wen, X.F. Responses of soil microbial communities and enzyme activities to nitrogen and phosphorus additions in Chinese fir plantations of subtropical China. Biogeosciences 2015, 12, 5537–5546. [Google Scholar] [CrossRef] [Green Version]
  29. Jensen, H.L. THE FUNGUS FLORA OF THE SOIL. Soil Sci. 1931, 31, 123. [Google Scholar] [CrossRef]
  30. Santos-Medellín, C.; Edwards, J.; Liechty, Z.; Nguyen, B.; Sundaresan, V. Drought Stress Results in a Compartment-Specific Restructuring of the Rice Root-Associated Microbiomes. MBio 2017, 8, e00764-17. [Google Scholar] [CrossRef]
  31. Xu, R.; Zhang, M.; Lin, H.; Gao, P.; Yang, Z.; Wang, D.; Sun, X.; Li, B.; Wang, Q.; Sun, W. Response of soil protozoa to acid mine drainage in a contaminated terrace. J. Hazard. Mater. 2022, 421, 126790. [Google Scholar] [CrossRef] [PubMed]
  32. Shen, J.-P.; Zhang, L.-M.; Guo, J.-F.; Ray, J.L.; He, J.-Z. Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in Northeast China. Appl. Soil Ecol. 2010, 46, 119–124. [Google Scholar] [CrossRef]
  33. Wang, L.; Liang, T. Effects of exogenous rare earth elements on phosphorus adsorption and desorption in different types of soils. Chemosphere 2014, 103, 148–155. [Google Scholar] [CrossRef]
  34. Mexal, J.; Reid, C.P.P. The growth of selected mycorrhizal fungi in response to induced water stress. Can. J. Bot. 1973, 51, 1579–1588. [Google Scholar] [CrossRef]
  35. Ventosa, A.; Nieto, J.J.; Oren, A. Biology of Moderately Halophilic Aerobic Bacteria. Microbiol. Mol. Biol. Rev. 1998, 62, 504–544. [Google Scholar] [CrossRef] [Green Version]
  36. Hayat, R.; Ali, S.; Amara, U.; Khalid, R.; Ahmed, I. Soil beneficial bacteria and their role in plant growth promotion: A review. Ann. Microbiol. 2010, 60, 579–598. [Google Scholar] [CrossRef]
  37. Pennanen, T. Microbial communities in boreal coniferous forest humus exposed to heavy metals and changes in soil pH—A summary of the use of phospholipid fatty acids, Biolog® and 3H-thymidine incorporation methods in field studies. Geoderma 2001, 100, 91–126. [Google Scholar] [CrossRef]
  38. Polyanskaya, L.P.; Zvyagintsev, D.G. The content and composition of microbial biomass as an index of the ecological status of soil. Eurasian Soil Sci. 2005, 38, 625–633. [Google Scholar]
  39. Moore, J.C. Impact of agricultural practices on soil food web structure: Theory and application. Agric. Ecosyst. Environ. 1994, 51, 239–247. [Google Scholar] [CrossRef]
  40. Wu, J.; Li, R.; Lu, Y.; Bai, Z. Sustainable management of cadmium-contaminated soils as affected by exogenous application of nutrients: A review. J. Environ. Manag. 2021, 295, 113081. [Google Scholar] [CrossRef]
  41. Syers, K.; Bekunda, M.; Cordell, D.; Corman, J.; Johnston, J.; Rosemarin, A.; Salcedo, I.; Lougheed, T.J.U.y.b. Phosphorus and food production. In UNEP Year Book; UNEP: Nairobi, Kenya, 2011; pp. 34–45. [Google Scholar]
  42. Waring, B.G.; Averill, C.; Hawkes, C.V. Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: Insights from meta-analysis and theoretical models. Ecol. Lett. 2013, 16, 887–894. [Google Scholar] [CrossRef] [PubMed]
  43. Biswas, T.; Kole, S.C. Soil Organic Matter and Microbial Role in Plant Productivity and Soil Fertility. In Advances in Soil Microbiology: Recent Trends and Future Prospects: Volume 2: Soil-Microbe-Plant Interaction; Adhya, T.K., Mishra, B.B., Annapurna, K., Verma, D.K., Kumar, U., Eds.; Springer: Singapore, 2017; pp. 219–238. [Google Scholar]
  44. Doran, J.W.; Smith, M.S. Organic Matter Management and Utilization Of Soil and Fertilizer Nutrients. In Soil Fertility and Organic Matter as Critical Components of Production Systems; Wiley: Hoboken, NJ, USA, 1987; pp. 53–72. [Google Scholar]
  45. Heijboer, A.; ten Berge, H.F.M.; de Ruiter, P.C.; Jørgensen, H.B.; Kowalchuk, G.A.; Bloem, J. Plant biomass, soil microbial community structure and nitrogen cycling under different organic amendment regimes; a 15N tracer-based approach. Appl. Soil Ecol. 2016, 107, 251–260. [Google Scholar] [CrossRef]
  46. Requena, N.; Jimenez, I.; Toro, M.; Barea, J.M. Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol. 1997, 136, 667–677. [Google Scholar] [CrossRef] [PubMed]
  47. Hartmann, A.; Schmid, M.; Tuinen, D.v.; Berg, G. Plant-driven selection of microbes. Plant Soil 2009, 321, 235–257. [Google Scholar] [CrossRef]
  48. Eskin, N.; Vessey, K.; Tian, L. Research Progress and Perspectives of Nitrogen Fixing Bacterium, Gluconacetobacter diazotrophicus, in Monocot Plants. Int. J. Agron. 2014, 2014, 208383. [Google Scholar] [CrossRef]
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Figure 1. Soil sampling point map.
Figure 1. Soil sampling point map.
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Figure 2. PLFA distribution of soil microorganisms in the tested soil; mol% represents the change in the mole fraction distribution of each characteristic fatty acid.
Figure 2. PLFA distribution of soil microorganisms in the tested soil; mol% represents the change in the mole fraction distribution of each characteristic fatty acid.
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Figure 3. Distribution of PLFA with different concentrations of exogenous phosphorus added to YD: YD represents the YD; the numbers after YD represent the molar ratio of exogenous phosphorus to lead.
Figure 3. Distribution of PLFA with different concentrations of exogenous phosphorus added to YD: YD represents the YD; the numbers after YD represent the molar ratio of exogenous phosphorus to lead.
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Figure 4. Distribution of PLFA with different concentrations of exogenous phosphorus added to MH: MH represents the MH; the numbers after MH represent the molar ratio of exogenous phosphorus to lead.
Figure 4. Distribution of PLFA with different concentrations of exogenous phosphorus added to MH: MH represents the MH; the numbers after MH represent the molar ratio of exogenous phosphorus to lead.
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Figure 5. The ratio of fungi to bacteria at the jointing stage of rice (F/B): YD represents the YD; MH represents the MH.
Figure 5. The ratio of fungi to bacteria at the jointing stage of rice (F/B): YD represents the YD; MH represents the MH.
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Figure 6. The ratio of Gram-negative to Gram-positive bacteria at jointing stage of rice.
Figure 6. The ratio of Gram-negative to Gram-positive bacteria at jointing stage of rice.
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Figure 7. Relative content of rice strains.
Figure 7. Relative content of rice strains.
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Figure 8. Absolute content of PLFA at jointing stage and mature stage of two kinds of rice.
Figure 8. Absolute content of PLFA at jointing stage and mature stage of two kinds of rice.
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Table
Table 1. Physical and chemical properties of the tested soil samples.
Table 1. Physical and chemical properties of the tested soil samples.
ItemsContentsChinese Soil Environmental Quality Standard ii (GB15618-1995)
pH5.70 (water)/
Soil organic (g/kg)21.8/
Cation exchange capacity (cmol/kg)9.30/
CharacterSand (%)65.0/
Silt (%)15.5/
Clay (%)19.5/
Elemental analysisCa (mg/kg)1968/
Fe (mg/kg)8618/
Al (mg/kg)31,650/
Mn (mg/kg)1341/
P (mg/kg)3.23/
Total lead (mg/kg)15,258≤250
Total zinc (mg/kg)527.5≤200
Total copper (mg/kg)185.7≤50.0
Total cadmium (mg/kg)3.90≤0.30
Total arsenic (mg/kg)2790≤40
Table
Table 2. Indicative fatty acids for soil microbial biomass estimation.
Table 2. Indicative fatty acids for soil microbial biomass estimation.
MicroorganismCorresponding Fatty Acids
Bacteria15:0, 17:0, i15:0, i16:0, i17:0, al5:0, a17:0, 16:lω7, 18:lω5, 18:lω7, cyl7:0, cy19:0
Fungi18:lω9, 18:2ω6, 18:3ω6, 18:3ω3
Actinomycetes10Me16:0, 10Me17:0, 10Me18:0, 10Me19:0
Gram-positive bacteria (G+)i14:0, i15:0, a15:0, i16:0, i17:0, al7:0, 10Me16:0, 10Me17:0, 10Me18:0, 18:1ω9
Gram-negative bacteria (G−)16:1ω5, 16:lω7t, 16:1ω9, 18:1ω5, 18:1ω7, cy17:0, cyl9:0, 17:1w8c, 19:1w11c
The numbers represent the total number of carbon atoms; ω represents the position of the double bond from the methyl end of the molecule. The prefixes “a” and “i” indicate anteiso- and iso-branching, respectively, “10Me” describes a methyl group on the tenth carbon atom from the carboxyl end of the molecule, and “cy” represents a cyclopropane fatty acid.
Table
Table 3. The definition of each soil sample.
Table 3. The definition of each soil sample.
Soil SamplesDefinition (Concentration of Calcium Dihydrogen Phosphate Added to the Test Soil)
0The molar ratio of P to Pb was 0 (control)
0.5The molar ratio of P to Pb was 0.5
1The molar ratio of P to Pb was 1
2The molar ratio of P to Pb was 2
Table
Table 4. Relative contents of soil microbial PLFAs at the jointing stage of rice (MH indicates Hui 86 rice; YD indicates YD.).
Table 4. Relative contents of soil microbial PLFAs at the jointing stage of rice (MH indicates Hui 86 rice; YD indicates YD.).
Exogenous Phosphorus Addition Status0 (control)0.512
PLFA (mol%)MHYDMHYDMHYDMHYD
Bacteria40.8744.1236.8855.1734.8955.8038.8356.61
Fungi6.105.906.838.866.2110.726.449.04
Actinobacteria8.346.958.769.026.817.126.317.19
Total microbial PLFA55.3156.9752.4773.0547.9173.6451.5872.84
Fungi/Bacteria0.150.130.190.160.180.190.170.16
Gram-negative bacteria (G−)/Gram-positive bacteria (G+)0.880.550.740.730.600.770.690.83
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Pan, X.; Shi, W.; Feng, G.; Li, X.; Zhou, Q.; Fu, L.; Jin, M.; Wu, W. The Impacts of Phosphorus-Containing Compounds on Soil Microorganisms of Rice Rhizosphere Contaminated by Lead. Diversity 2023, 15, 69. https://doi.org/10.3390/d15010069

AMA Style

Pan X, Shi W, Feng G, Li X, Zhou Q, Fu L, Jin M, Wu W. The Impacts of Phosphorus-Containing Compounds on Soil Microorganisms of Rice Rhizosphere Contaminated by Lead. Diversity. 2023; 15(1):69. https://doi.org/10.3390/d15010069

Chicago/Turabian Style

Pan, Xingchen, Wenjun Shi, Guiping Feng, Xiaolong Li, Qingwei Zhou, Li Fu, Meiqing Jin, and Weihong Wu. 2023. "The Impacts of Phosphorus-Containing Compounds on Soil Microorganisms of Rice Rhizosphere Contaminated by Lead" Diversity 15, no. 1: 69. https://doi.org/10.3390/d15010069

APA Style

Pan, X., Shi, W., Feng, G., Li, X., Zhou, Q., Fu, L., Jin, M., & Wu, W. (2023). The Impacts of Phosphorus-Containing Compounds on Soil Microorganisms of Rice Rhizosphere Contaminated by Lead. Diversity, 15(1), 69. https://doi.org/10.3390/d15010069

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