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Bacteria isolated from the ectomycorrhizosphere ofCastanea henryi weather insoluble inorganic phosphates and simultaneously form carbonates
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Lu QIAN1, Zhenying HE3, Gang HE1, 2, Xiaohong JI1, 2, Jianping OUYANG1, Ye CHEN1, 2, Qibiao SUN1, 2, *
Acta Microbiologica Sinica | 2024, 64(6) : 2042 - 2056
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Acta Microbiologica Sinica | 2024, 64(6): 2042-2056
• Geomicrobiological Applications •
Bacteria isolated from the ectomycorrhizosphere ofCastanea henryi weather insoluble inorganic phosphates and simultaneously form carbonates
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Lu QIAN1, Zhenying HE3, Gang HE1, 2, Xiaohong JI1, 2, Jianping OUYANG1, Ye CHEN1, 2, Qibiao SUN1, 2, *
Affiliations
  • 1 Jiujiang Key Laboratory of Fungal Resources Conservation and Utilization, College of Pharmacy and Life Sciences, Jiujiang University, Jiujiang 332005, Jiangxi, China
  • 2 Jiangxi Province Key Laboratory of Watershed Ecological Process and Information, Jiujiang 332005, Jiangxi, China
  • 3 College of Resources & Environment, Jiujiang University, Jiujiang 332005, Jiangxi, China
Published: 2024-06-04 doi: 10.13343/j.cnki.wsxb.20240148
Outline
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[Objective] Ectomycorrhizal fungi can shape the bacterial community in the ectomycorrhizosphere, which represents an important way to mobilize and acquire insoluble mineral elements from the soil. This study aims to investigate the composition and phosphate-solubilizing characteristics of the dominant phosphate-solubilizing bacteria (PSB) in the ectomycorrhizosphere ofCastanea henryi. [Methods] The transparent halo method was employed to isolate PSB from the ectomycorrhizosphere ofC.henryi. The strains were identified by 16S rRNA gene sequencing. The degradation abilities of the strains for tricalcium phosphate (TCP) and apatite were studied by liquid fermentation. A scanning electron microscope and a X-ray diffractometer were used to observe the appearance and crystal structures of the degradation products. [Results] Five highly efficient strains of PSB were isolated from the ectomycorrhizosphere ofC.henryi. Strains LSCh1, LSCh2, and LSCh5 were identified asBurkholderia lata, and strains LSCh3 and LSCh4 were identified asParaburkholderia sp. The degradation abilities of the strains for TCP followed the trend of LSCh3 (556.94 mg/L) > LSCh2 (206.91 mg/L) > LSCh1 (170.83 mg/L) > LSCh5 (55.16 mg/L) > LSCh4 (14.21 mg/L). The degradation abilities of the strains for apatite were in a descending order of LSCh2 (51.33 mg/L) > LSCh1 (43.51 mg/L) > LSCh3 (40.99 mg/L) > LSCh5 (1.11 mg/L) > LSCh4 (1.00 mg/L). [Conclusion] Strain LSCh3 showed good performance in degrading both TCP and apatite and induced the formation of carbonates. It is a plant growth-promoting bacterium with potential application values in improving the phosphorus nutrients of plants and the quality of soil.

Castanea henryi  /  ectomycorrhiza  /  phosphate-solubilizing bacteria  /  apatite  /  carbonate
Lu QIAN, Zhenying HE, Gang HE, Xiaohong JI, Jianping OUYANG, Ye CHEN, Qibiao SUN. Bacteria isolated from the ectomycorrhizosphere ofCastanea henryi weather insoluble inorganic phosphates and simultaneously form carbonates[J]. Acta Microbiologica Sinica, 2024 , 64 (6) : 2042 -2056 . DOI: 10.13343/j.cnki.wsxb.20240148
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Phosphorus (P) is one of the essential macro-mineral elements necessary for the growth and development of plants. It is an important component of cell membranes and nucleic acids and is involved in almost all metabolic processes of plants, such as photosynthesis, cell division, signal transmission, respiration, energy production, and macromolecular biosynthesis[1-2]. Although the total amount of P in the soil is abundant, the content of bioavailable P is often in a deficiency state. Only about 0.1% of P (such as HPO42− and H2PO4−) can be absorbed and utilized directly by plants. Most P is easily passivated by Ca2+, Fe3+, Al3+, and soil aggregates or is in the form of organophosphorus and P-containing minerals[3-6].
More than 80% of terrestrial plants can form mycorrhizal associations with soil fungi, and the fungal symbionts play an extremely important role in promoting plan uptake of mineral nutrients, particularly P, nitrogen, and potassium[7]. As one of the most important types of mycorrhizal fungi, ectomycorrhizal (ECM) fungi play a crucial role in the growth of forest trees. The reciprocal symbiosis between forest trees and ECM fungi is one of the most widespread and successful interactions in terrestrial ecosystems. The fundamental groups and dominant tree species (accounting for about 2% of plant species) in forest ecosystems, includingPinaceae,Fagaceae,Betulaceae,Salicyaceae, andDipteraceae, can form ectomycorrhizas[8]. ECM fungi obtain mineral nutrients through mycelial absorption, enzymatic hydrolysis, and bioweathering and then transport them to symbiotic plants. For example, more than 15% of P required for plant growth is provided by ECM fungi[9-10]. Bioweathering is one of the important ways for ECM fungi to obtain soil P, mainly through the secretion of protons and low molecular weight organic acids to trigger acidification or complexation to weather soil minerals[11-13]. Smits et al.[14] studied the weathering efficiency ofPaxillus involutus on apatite under P deficiency using the microcosmic method. The result showed that the colonization ofP.involutus increased the release of P from apatite by three times compared to the control. Wallander[15] studied the weathering effect of three ECM fungi on apatite and the growth-promoting effect onPinus sylvestris through pot experiments. It showed that the weathering rate of apatite by fungi was 0.3%–0.9% after 6 months of cultivation. However, many studies have found significant differences in the mineral weathering capacity among different ECM fungi[16-20]. Under the background of increasing atmospheric CO2 concentration, nutrient deficiency stress caused by the intensification of plant photosynthesis has increased[21], resulting in increased demand for ECM fungi. Furthermore, in the process of long-term symbiotic evolution, the ability of ECM fungi to use complex organic matter in the soil is constantly weakened due to the loss of genes related to the degradation of complex organic substances[22-23]. Due to these factors, it is essential for ECM fungi to improve the nutrient supply to plants in exchange for the carbon source they themselves require. Therefore, it is particularly important to explore the way ECM fungi acquire soil mineral elements (e.g. P).
The interaction between ECM fungi and bacteria is a common phenomenon in natural forest ecosystems, and its important role in promoting soil mineral weathering and plant nutrition is receiving increasing attention[24-26]. Nicolitch et al.[27] compared and analyzed the mineral weathering capacity of bacteria isolated from the ectomycorrhizosphere ofFagus sylvatica and the adjacent bulk soil. The results showed that the ectomycorrhizosphere has a significant enrichment effect on bacteria (mainlyBurkholderia andCollimonas) with high mineral weathering ability. This shows that the lower the soil bioavailable P content, the more specific bacterial taxa related to inorganic nutrient mobilization are largely and exclusively enriched in the ectomycorrhizosphere[27]. Fontaine et al.[28] obtained similar results that there are large number of phosphate-solubilizing bacteria (PSB) in the ectomycorrhizosphere ofPicea glauca, andBurkholderia showed a particularly prominent ability to weather fluorapatite. Sun et al.[29] also concluded that ECM fungi can enrich bacteria with high mineral weathering potential and promote apatite weathering through the mesh bagin situ culture method. These suggest that the formation of specific PSB could be one of the essential ways for ECM fungi to promote P nutrition of plants under P-deficient conditions.
The taxa of rhizospheric PSB formed by different plant ectomycorrhiza are diverse. Furthermore, it remains unclear which specific group of species is enriched with highly effective mineral weathering bacteria by ECM fungi. Therefore, studying the composition and ability of PSB in the ectomycorrhizosphere is helpful to understand the interaction between ECM fungi and bacteria and the use of functional bacterial resources to promote plant growth. In this study,Castanea henryi (Fagaceae) in Lushan National Nature Reserve was selected as the research object. The main soil type in this reserve is acidic red soil with a very low content of bioavailable P. The PSB of the ectomycorrhizosphere ofC.henryi were isolated and their phosphate- solubilization ability was analyzed. This will provide a theoretical basis for solving the problem of low P and soil fertility in acidic-red soils.
1 Materials and Methods
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1.1 Isolation and identification of PSB
The ectomycorrhizospheric soil ofC.henryi was collected from Lushan National Nature Reserve, and PSB were isolated by the phosphate-solubilizing halo method. After repeated rescreening, five strains with high phosphate-solubilizing ability were finally obtained and used for this study. The obtained PSB strains were inoculated in Luria-Bertani (LB) liquid medium, and cultured at 30 ℃ and 180 r/min for 2 days. Then the fermentation broth was centrifuged at 12 000 r/min for 2 min to collect bacteria. DNA (deoxyribonucleic acid) was extracted using the Bacterial Genomic DNA Rapid Extraction Kit (Sangon Biotech Co., Ltd., Shanghai, Chian), and 16S rRNA gene was amplified using primers 27F (5′-AGAGTTTGA TCMTGTGGCTCAG-3′) and 1492R (5′-CGGTT ACCTTGTTACGACTT-3′)[30]. The PCR reaction system (25 μL): 2×Phanta Max Master Mix (Vazyme Biotech Co., Ltd., Nanjing, China) 12.5 μL, primer 27F (10 μmol/L) 1 μL, primer 1492R (10 μmol/L) 1 μL, DNA template 0.1 μL, ddH2O 10.4 μL. Reaction procedure: predenaturation at 95 ℃ for 3 min, denaturation at 95 ℃ for 15 s, annealing at 56 ℃ for 15 s, extension at 72 ℃ for 90 s, 30 cycles; at 72 ℃ for 5 min. The PCR products were detected by 1% agarose gel electrophoresis and sent to Sangon Biotech Co., Ltd. for sequencing. DNA base quality obtained by sequencing was assessed using SnapGene Viewer 6.2.1 software, pairwise sequencing results were spliced using the SeqMan tool in Lasergene 7.1 software to obtain a complete 16S rRNA gene sequence, and BLAST (Basic Local Alignment Search Tool) program was performed in GenBank, and finally MEGA 11.0 software was used for sequence alignment and phylogenetic tree construction.
The NBRIP medium was use as the isolation medium (g/L): glucose 10.00, (NH4)2SO4 0.50, MgSO4·7H2O 0.30, MnSO4 0.03, KCl 0.30, FeSO4 0.03, NaCl 0.30, Ca3(PO4)2 (tricalcium phosphate, TCP) 5.00, agar 20.00, pH 7.0–7.2[31].
1.2 Assay of the capacity of bacteria to degrade TCP and apatite
Five bacterial strains were each inoculated onto solid LB medium and cultured at 37 ℃ for 48 h. Subsequently, a ring of bacterial thalli was picked and inoculated in NBRIP and modified NBRIP (TCP was replaced with the equivalent apatite powder) liquid media (without soluble phosphate) and cultured at 30 ℃, 150 r/min for 10 days. Each treatment was carried out in triplicate. The pH and soluble P content of the culture solution were measured every 2 days using the molybdenum-antimony resistance colorimetry method[32].
Analytical pure TCP was purchased from Sinopharm Chemical Reagent Co., Ltd. Apatite powder (75–150 μm) consists mainly of fluoropapatite, hydroxyapatite and a small amount of phlogopite. X-ray fluorescence analysis showed that the main elements were O 77.35%, Ca 11.10%, P 6.09%, F 1.58%, Mg 1.36%, Si 1.33%, Al 0.35%, Fe 0.29%, Sr 0.23%, K 0.19%, S 0.06%, I 0.06% and Y 0.01%.
1.3 Detection of mineral components in precipitates
After cultivation, the precipitates were collected and purified three times each with deionized water and anhydrous ethanol. Finally, the precipitates were dried in an oven at 60 ℃. A scanning electron microscope (SEM) VEGA Ⅱ LSU (TESCAN, Czech Republic) equipped with an energy dispersive X-ray spectrometer (EDS) Inca X-act (Oxford, UK) was used to observe and analyze the micromorphology and elemental composition of the precipitates. The structure and composition of the precipitates were determined with an X-ray diffractometer (XRD) D8 ADVANCE (Bruker, Germany) using Cu-Kα radiation with a voltage of 35 kV.
1.4 Data processing
The data are expressed in the form: mean ± standard deviation (bars) using the three replicates. Pearson correlation analysis between pH and P concentration was performed in R version 4.1.3 using the ggplot2 package.
2 Results and Discussion
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2.1 Molecular identification of PSB
Secretion of gluconic acid is one of the essential ways for bacteria to dissolve insoluble phosphates. Therefore, it is an effective mean to identify PSB by identifying the key genes of its synthesis. For example, pyrroloquinoline quinine is an important cofactor of glucose dehydrogenase in the production of gluconic acid, and its synthetic genes (pqqA,pqqB,pqqC,pqqD, andpqqE) are widely used for PSB detection[33]. However, determining the formation of phosphate-solubilizing halo is still the most direct and effective way for screening PSB. PSB tend to weaken or even lose phosphate solubilization ability during the cultivation process[34]. Therefore, in this study, five PSB strains (LSCh1, LSCh2, LSCh3, LSCh4, and LSCh5) with strong and stable phosphate solubilization ability were isolated from the ectomycorrhizosphere ofC.henryi by multiple rescreening. Subsequently, their 16S rRNA gene sequences were obtained by sequencing and submitted to GenBank (accession numbers: OQ519686, OQ519687, OQ519694, OQ519695, and OQ519688, respectively). Phylogenetic analysis showed that strains LSCh1, LSCh2 and LSCh5 belonged toBurkholderia lata, while LSCh3 and LSCh4 belonged toParaburkholderia sp. (Figure 1). To date,Burkholderia which belongs toPseudomonadaceae are considered to be the most efficient mineral weathering bacteria in the ectomycorrhizosphere[27-28,35-37]. In this study, the high-efficiency phosphate-solubilizing strains isolated from the ectomycorrhizosphere ofC.henryi belonged toBurkholderia andParaburkholderia. It further indicated that bacteria in these taxonomic groups play an important role in mobilizing insoluble phosphates in the ectomycorrhizosphere.Paraburkholderia was newly separated from the genusBurkholderia based on molecular signatures and phylogenomic analysis by Sawana et al.[38], and is primarily an environmental species with plant growth promotion effects. Therefore, a large proportion of previously reportedBurkholderia strains with high weathering potential actually belong toParaberkholderia, indicating that as bacterial taxonomy continues to evolves, the understanding of highly efficient mineral weathering bacteria in the ectomycorrhizosphere will also bring new changes.
2.2 Changes in pH during phosphate solubilization
Acidification is one of the most important ways for PSB to promote the dissolution of insoluble inorganic phosphates, such as secreted gluconic acid, acetic acid, lactic acid, oxalic acid, malic acid, and other low molecular weight organic acids, which not only acts directly to dissolve the fixed phosphates, but can also hinder the reimmobilization of P by Fe3+, Al3+ and other ions[39-41].Figure 2 shows the change in pH of liquid media during different strains degrading phosphates. In the initial degradation phase of TCP, the pH of the medium decreased significantly. The pH of the medium fluctuated between 4.27 and 7.96 during cultivation, with the pH trending to initially decrease and then increase again. During apatite degradation, the pH of the medium was between 3.31 and 6.92. These further indicate that acidification is an important way for PSB to mobilize insoluble phosphorus sources.
2.3 Different ability of strains to degrade different insoluble phosphates
Bashan et al.[42] suggested that TCP as a single insoluble phosphate is not suitable for screening PSB and that the determination should be combined with the characteristics of the isolation environment and other corresponding insoluble P sources. In this study, TCP was used as the insoluble phosphate for the first screening and apatite as the second phosphate for the re-screening and conformation. However, five PSB strains isolated by double screening showed different solubilization abilities toward different phosphates (Figure 3). The total P released from TCP peaked after 2 days of culture with strain LSCh1 ((170.83±37.40) mg/L), while the released P peaked on the 4th day ((206.91±1.91) mg/L) and 10th day ((55.16±9.33) mg/L) when cultivated with the strains LSCh2 or LSCh5, respectively.B.lata PN1 isolated from the rhizosphere of bamboo by Yang et al.[43] showed a peak of P dissolution (117.50 mg/L) on the 6th day of cultivation, which was lower than that of strains LSCh1 and LSCh2 in this study. Different strains have different phosphate solubilization abilities and the time at which the highest P-release level is reached also varies. For example, the highest P-releasing content (315.72 mg/L) was found inB.cepacia 71-2 isolated from tobacco rhizosphere by Liu et al.[44], while that ofB.cepacia P6 isolated from the rhizosphere ofCastanea mollissima by Chen et al.[45] was only 78.84 mg/L. In this study,Paraburkholderia sp. LSCh3 had the strongest phosphate-solubilization ability among the isolated five strains and the highest P-release capacity can reach (556.94±13.83) mg/L, whileParaburkholderia sp. LSCh4 had the weakest phosphate solubilization ability, with the maximum dissolved P content being only (14.21±1.63) mg/L.
Weathering of apatite, which accounts for more than 95% of the total P in the Earth's crust, is the main source of P in natural ecosystems[46-47]. However, so far there are only a few studies on the quantitative analysis ofBurkholderia andParaburkholderia for weathering apatite[48-49]. In this study, the apatite solubilization ability of five strains isolated from the ectomycorrhizosphere ofC.henryi was compared and analyzed. Compared to TCP, the apatite solubilization ability of this PSB was significantly lower, and the P-releasing amount was between 0.49 mg/L and 51.33 mg/L (Figure 3B). Among them, strains LSCh1, LSCh2, and LSCh3 had strong ability to dissolve apatite, and the highest P-releasing content was ((51.33±1.85) mg/L) (LSCh2). Sun et al.[49] isolated a strain ofB.gladioli MEL01 from the soil of a rice-wheat rotation field and found that it could dissolve TCP and apatite well. The liquid fermentation results showed that the release of P from apatite reached the peak value (107.69 mg/L) after 2 days of culture. Silva et al.[48] isolated a phosphate-solubilizing strain ofParburkholderia 149H from the root of the medicinal plantAloe vera, which can release 45.70 mg/L P from the apatite culture after 3 days.
These studies showed that there were significant differences in phosphate-solubility among different strains, even which the same species. Furthermore, the time required for different strains to show the highest P-releasing content was also inconsistent, which may be related to the growth characteristics and adaptability of PSB to P stress. Species ofBurkholderia andParaburkholderia typically have a variety of plant growth-promoting effects, such as nitrogen fixation, production of IAA and iron carriers as well as antibacterial effects[45,48,50-51]. It may have some influence on the strains' ability to solubilize phosphate. In addition, by comparing the correlation between the amount of released P and the pH of the fermentation solution, it was found that the phosphate dissolving ability of PSB had a significant negative correlation with the pH of the medium in the dissolution process of dissolving TCP and apatite (Figure 4). This further suggested that acidification is an important mechanism for PSB to solubilize insoluble inorganic phosphate.
2.4 Changes in crystal structure and secondary product formation during phosphate solubilization
Little attention is currently paid to the changes in crystal structure and morphology of phosphate minerals and the formation of secondary precipitates during phosphate solubilization by PSB. The study by Sun and Lian[52] showed thatAspergillus nidus can weather wollastonite (Ca-bearing mineral) with the formation of carbonate minerals. TCP and apatite are calcium-rich minerals. After treatment with PSB, the crystal morphology and structure may change and even form secondary minerals such as carbonate minerals. By analyzing the microscopic morphology and mineral composition of the precipitates after 10 days of cultivation, the results showed that precipitates of different sizes were formed in the TCP medium after bacterial exposure, and EDS analysis showed that these precipitates had high carbon content (Figure 5). In addition, the XRD results showed that the crystal planes (1 0 4) and (0 0 6) of the carbonate mineral calcite were detected in the precipitates after cultivation with the five strains (Figure 5), suggesting that these bacteria were able to induce the formation of carbonate in the process of mobilization of insoluble phosphate. The secondary precipitates produced by strain LSCh3, a strain with strong TCP dissolution ability, contained higher carbon content (45.01%,Figure 5D). At the same time, the crystal planes (0 2 0), (0 4 0), and (1 1 2) of the secondary mineral brushite were also detected in the precipitates after cultivation with LSCh3. Sun et al.[53] also found that bacteria have the ability to simultaneously induce the formation of bruschite and calcite. All strains also had an obvious weathering effect on apatite. The SEM results showed that the surface of apatite had obvious corrosion, and the XRD results also showed that the crystal structure of apatite also changed to different extents, such as that the crystal plane (1 2 1) of fluorapatite/hydroxyapatite disappeared after exposure to LSCh1 and LSCh5, and the strength of the crystal plane (1 1 3) of phlogopite was weakened or even disappeared (Figure 6). In addition, EDS analysis showed that high C content was detected on the surface of precipitates after bacterial exposure. For example, the secondary precipitates produced by strains LSCh4 and LSCh5 contained C element, but no carbonate minerals were detected by XRD. There may be amorphous carbonates or the content of carbonate minerals caused by bacteria is too low to be detected. The results of this study showed that bacteria can still induce carbonate precipitation even under weakly acidic conditions. The studies of Liu and Lian[54-55] showed that the microbially induced carbonate has robust stability under acidic conditions and has a good heavy metal adsorption effect. This indicates that the carbonate induced by PSB in the process of phosphate dissolution has a certain potential to buffer soil acidity and passivate heavy metals in acidic-red soil environment, thereby improving plant growth.
3 Conclusion
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In this study, a total of five PSB strains were isolated from the ectomycorrhizosphere ofC.henryi, belonging toBurkholderia andParaburkholderia sp., suggesting that they are widespread phosphate-solubilizing microorganisms in soil. By analyzing the solubility of these strains toward TCP and apatite, it was found that strain LSCh3 (Paraburkholderia sp.) had the strongest degradation ability for TCP, with the highest P-releasing amount of 556.94 mg/L, while strain LSCh2 (B.lata) had the strongest weathering ability for apatite, with the highest P-releasing amount of 51.33 mg/L. In general, strain LSCh3 had a good solubilization effect on both TCP and apatite and can induce the formation of carbonate, suggesting that it is a plant growth-promoting bacterium with potential application value for future use to improve P nutrition of plants and soil quality.
Funding
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  • National Natural Science Foundation of China(32260031)
  • National Natural Science Foundation of China(31900018)
  • Natural Science Foundation of Jiangxi Province(20202BAB213025)
  • Jiujiang High-level Scientific and Technological Innovation Talent Project(S2022QNZZ059)
  • Undergraduate Innovation and Entrepreneurship Training Program of Jiangxi Province(S202311843003)
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doi: 10.13343/j.cnki.wsxb.20240148
  • Receive Date：2024-03-08
  • Online Date：2026-03-19
  • Published：2024-06-04
Article Data
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History
  • Received：2024-03-08
  • Accepted：2024-05-07
Funding
National Natural Science Foundation of China(32260031)
National Natural Science Foundation of China(31900018)
Natural Science Foundation of Jiangxi Province(20202BAB213025)
Jiujiang High-level Scientific and Technological Innovation Talent Project(S2022QNZZ059)
Undergraduate Innovation and Entrepreneurship Training Program of Jiangxi Province(S202311843003)
Affiliations
    1 Jiujiang Key Laboratory of Fungal Resources Conservation and Utilization, College of Pharmacy and Life Sciences, Jiujiang University, Jiujiang 332005, Jiangxi, China
    2 Jiangxi Province Key Laboratory of Watershed Ecological Process and Information, Jiujiang 332005, Jiangxi, China
    3 College of Resources & Environment, Jiujiang University, Jiujiang 332005, Jiangxi, China

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SUN Qibiao, E-mail:
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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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