Short-Term Phosphorus Fertilization Alters Soil Fungal Community in Long-Term Phosphorus-Deprived Yellow Soil Paddy Fields
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Site
2.2. Experimental Design
2.3. Soil Sampling and Measurements
2.3.1. Soil Sample Collection
2.3.2. Determination of Soil Physical and Chemical Properties
2.3.3. DNA Extraction and Illumina Sequencing
2.4. Statistical Analysis
3. Results
3.1. Changes in Soil Physicochemical Properties After Phosphorus Fertilization
3.2. Effect of Phosphorus Fertilizer on Soil Fungal α-Diversity Indices
3.3. Effect of Phosphorus Fertilizer on Soil Fungal Community Composition
3.4. Response of Specific Fungal Groups to Different Phosphorus Fertilizers
3.5. Functional Prediction of Soil Fungal Community
3.6. Relationships Between Soil Fungal Community Composition and Soil Physicochemical Properties
4. Discussion
4.1. The Addition of Phosphorus Fertilizer Can Increase Soil Fungal Diversity
4.2. The Addition of Chemical Phosphorus Fertilizer Significantly Improved the Fungal Community Structure
4.3. Soil Total Nitrogen and Organic Matter Contents Are Key Factors Affecting the Composition of Fungal Communities
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Veneklaas, E.J.; Lambers, H.; Bragg, J.; Finnegan, P.M.; Lovelock, C.E.; Plaxton, W.C.; Price, C.A.; Scheible, W.; Shane, M.W.; White, P.J.; et al. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol. 2012, 195, 306–320. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, Y.; Katoh, M. Root Response and Phosphorus Acquisition under Partial Distribution of Phosphorus and Water-soluble Organic Matter. Soil Use Manag. 2024, 40, e13038. [Google Scholar] [CrossRef]
- Langhans, C.; Beusen, A.H.W.; Mogollón, J.M.; Bouwman, A.F. Phosphorus for sustainable development goal target of doubling smallholder productivity. Nat. Sustain. 2021, 5, 57–63. [Google Scholar] [CrossRef]
- Vitousek, P.M.; Porder, S.; Houlton, B.Z.; Chadwick, O.A. Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen–phosphorus interactions. Ecol. Appl. 2010, 20, 5–15. [Google Scholar] [CrossRef]
- Wang, J.; Yuan, J.; Wang, L.; Zhang, H.; Tang, Z.H.; Zhao, P.; Zhang, A.J.; Wang, J.D.; Zhang, Y.C. Effects of fertilizer application methods on fungal communities in sweet potato rhizosphere. J. Plant Nutr. Fertil. 2023, 29, 876–888. [Google Scholar]
- Zhong, J.P.; Zheng, Z.C.; Li, T.X.; He, X.L. Effect of phosphorus fertilizer application rates on the loss of colloidal phosphorus on purple soil slopes. Sci. Agric. Sin. 2024, 57, 1547–1559. [Google Scholar]
- Zou, T.; Zhang, X.; Davidson, E.A. Global trends of cropland phosphorus use and sustainability challenges. Nature 2022, 611, 81–87. [Google Scholar] [CrossRef]
- Ducousso-Détrez, A.; Fontaine, J.; Lounès-Hadj Sahraoui, A.; Hijri, M. Diversity of phosphate chemical forms in soils and their contributions on soil microbial community structure changes. Microorganisms 2022, 10, 609. [Google Scholar] [CrossRef]
- Li, J.; Delgado-Baquerizo, M.; Wang, J.-T.; Hu, H.-W.; Cai, Z.-J.; Zhu, Y.-N.; Singh, B.K. Fungal richness contributes to multifunctionality in boreal forest soil. Soil Biol. Biochem. 2019, 136, 107526. [Google Scholar] [CrossRef]
- Tedersoo, L.; Bahram, M.; Põlme, S.; Kõljalg, U.; Yorou, N.S.; Wijesundera, R.; Ruiz, L.V.; Vasco-Palacios, A.M.; Thu, P.Q.; Suija, A.; et al. Global diversity and geography of soil fungi. Science 2014, 346, 1256688. [Google Scholar] [CrossRef]
- Delgado-Baquerizo, M.; Maestre, F.T.; Reich, P.B.; Jeffries, T.C.; Gaitan, J.J.; Encinar, D.; Berdugo, M.; Campbell, C.D.; Singh, B.K. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 2016, 7, 10541. [Google Scholar] [CrossRef] [PubMed]
- Nicolás, C.; Martin-Bertelsen, T.; Floudas, D.; Bentzer, J.; Smits, M.; Johansson, T.; Troein, C.; Persson, P.; Tunlid, A. The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen. ISME J. 2019, 13, 977–988. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.L.; Liu, K.L.; Zhao, X.Q.; Zhang, H.Q.; Li, D.; Li, J.J.; Shen, R.F. Balanced fertilization over four decades has sustained soil microbial communities and improved soil fertility and rice productivity in red paddy soil. Sci. Total Environ. 2021, 793, 148664. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Huang, X.; Li, Y.; Liu, Y.; Zhang, Y.; Zhu, H.; Xiong, H.; Zhang, S.; Jiang, T. Characteristics of the soil microbial community structure under long-term chemical fertilizer application in yellow soil paddy fields. Agronomy 2024, 14, 1186. [Google Scholar] [CrossRef]
- Semenov, M.V.; Krasnov, G.S.; Semenov, V.M.; Van Bruggen, A. Mineral and organic fertilizers distinctly affect fungal communities in the crop rhizosphere. J. Fungi 2022, 8, 251. [Google Scholar] [CrossRef]
- Pan, H.; Chen, M.; Feng, H.; Wei, M.; Song, F.; Lou, Y.; Cui, X.; Wang, H.; Zhuge, Y. Organic and inorganic fertilizers respectively drive bacterial and fungal community compositions in a fluvo-aquic soil in northern China. Soil Tillage Res. 2020, 198, 104540. [Google Scholar] [CrossRef]
- Wang, Y.; Xu, Y.; Jiang, L.; Yang, Y.; Shi, J.; Guan, X.; Sun, T.; Zhao, H.; Wang, Y.; Liu, Y. Effect of Mild Organic Substitution on Soil Quality and Microbial Community. Agronomy 2024, 14, 888. [Google Scholar] [CrossRef]
- Du, J.; Yu, Y.; Tang, C.; Zong, K.; Zhang, S.; Zhang, Q.; Fang, L.; Li, Y. Organic Fertilizers increase the proportion of saprotrophs favoring soil nitrification under medicinal plants Fritillaria thunbergii. Ind. Crops Prod. 2024, 219, 119129. [Google Scholar] [CrossRef]
- Yang, Y.H.; Huang, X.C.; Zhu, H.Q.; LI, Y.; Zhang, S.; Zhang, Y.R.; Liu, Y.L.; Jiang, T.M. Bacterial community structure and composition under long-term combined application of organic and inorganic fertilizers in a yellow paddy soil. J. Plant Nutr. Fert. 2022, 28, 984–992. [Google Scholar]
- Bo, H.; Li, Z.; Jin, D.; Xu, M.; Zhang, Q. Fertilizer Management Methods Affect Bacterial Community Structure and Diversity in the Maize Rhizosphere Soil of a Coal Mine Reclamation Area. Ann. Microbiol. 2023, 73, 24. [Google Scholar] [CrossRef]
- Zhang, L.F.; Ma, L.; Li, Y.D.; Zheng, F.L.; Wei, J.L.; Tan, D.S.; Cui, X.M.; Li, Y. Effects of long-term synergistic application of organic materials and chemical fertilizers on bacterial community and enzyme activity in wheat-maize rotation fluvo-aquic soil. Scient. Agric. Sin. 2023, 56, 3843–3855. [Google Scholar]
- Schlatter, D.C.; Gamble, J.D.; Castle, S.; Rogers, J.; Wilson, M. Abiotic and biotic drivers of soil fungal communities in response to dairy manure amendment. Appl. Environ. Microbiol. 2023, 89, e01931-22. [Google Scholar] [CrossRef] [PubMed]
- Hu, X.; Liu, J.; Wei, D.; Zhu, P.; Cui, X.; Zhou, B.; Chen, X.; Jin, J.; Liu, X.; Wang, G. Effects of over 30-year of different fertilization regimes on fungal community compositions in the black soils of northeast China. Agric. Ecosyst. Environ. 2017, 248, 113–122. [Google Scholar] [CrossRef]
- Paungfoo-Lonhienne, C.; Yeoh, Y.K.; Kasinadhuni, N.R.P.; Lonhienne, T.G.A.; Robinson, N.; Hugenholtz, P.; Ragan, M.A.; Schmidt, S. Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere. Sci. Rep. 2015, 5, 8678. [Google Scholar] [CrossRef]
- Huang, R.; McGrath, S.P.; Hirsch, P.R.; Clark, I.M.; Storkey, J.; Wu, L.; Zhou, J.; Liang, Y. Plant-microbe networks in soil are weakened by century-long use of inorganic fertilizers. Microb. Biotechnol. 2019, 12, 1464–1475. [Google Scholar] [CrossRef]
- He, D.; Xiang, X.; He, J.-S.; Wang, C.; Cao, G.; Adams, J.; Chu, H. Composition of the soil fungal community is more sensitive to phosphorus than nitrogen addition in the alpine meadow on the Qinghai-Tibetan Plateau. Biol. Fertil. Soils 2016, 52, 1059–1072. [Google Scholar] [CrossRef]
- Jirout, J.; Šimek, M.; Elhottová, D. Inputs of nitrogen and organic matter govern the composition of fungal communities in soil disturbed by overwintering cattle. Soil Biol. Biochem. 2011, 43, 647–656. [Google Scholar] [CrossRef]
- Lu, R.K. Methods of Soil Agricultural Chemistry Analysis; China Agriculture Press: Beijing, China, 1999; pp. 296–338. [Google Scholar]
- Segata, N.; Izard, J.; Waldron, L.; Gevers, D.; Miropolsky, L.; Garrett, W.S.; Huttenhower, C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 12, R60. [Google Scholar] [CrossRef]
- Nguyen, N.H.; Song, Z.; Bates, S.T.; Branco, S.; Tedersoo, L.; Menke, J.; Schilling, J.S.; Kennedy, P.G. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 2016, 20, 241–248. [Google Scholar] [CrossRef]
- Banerjee, S.; Van Der Heijden, M.G.A. Soil microbiomes and one health. Nat. Rev. Microbiol. 2023, 21, 6–20. [Google Scholar] [CrossRef]
- 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]
- Zhou, W.J.; Chen, J.G.; Tan, Z.J.; Zhang, Y.Z.; Ceng, X.B. Response of paddy soil health to continuous amendments of organic fertilizer and lime separately under double-cropping rice fields. Scient. Agric. Sin. 2010, 29, 29–35. [Google Scholar]
- Liu, H.; Xu, W.; Li, J.; Yu, Z.; Zeng, Q.; Tan, W.; Mi, W. Short-term effect of manure and straw application on bacterial and fungal community compositions and abundances in an acidic paddy soil. J. Soils Sediments 2021, 21, 3057–3071. [Google Scholar] [CrossRef]
- Blagodatskaya, E.; Kuzyakov, Y. Active microorganisms in soil: Critical review of estimation criteria and approaches. Soil Biol. Biochem. 2013, 67, 192–211. [Google Scholar] [CrossRef]
- He, M.; Tian, G.; Semenov, A.M.; Van Bruggen, A.H.C. Short-term fluctuations of sugar beet damping-off by pythium ultimum in relation to changes in bacterial communities after organic amendments to two soils. Phytopathology 2012, 102, 413–420. [Google Scholar] [CrossRef] [PubMed]
- Semenov, M.V.; Krasnov, G.S.; Semenov, V.M.; Ksenofontova, N.; Zinyakova, N.B.; Van Bruggen, A.H.C. Does fresh farmyard manure introduce surviving microbes into soil or activate soil-borne microbiota? J. Environ. Manage. 2021, 294, 113018. [Google Scholar] [CrossRef]
- Ye, G.; Lin, Y.; Luo, J.; Di, H.J.; Lindsey, S.; Liu, D.; Fan, J.; Ding, W. Responses of soil fungal diversity and community composition to long-term fertilization: Field experiment in an acidic Ultisol and literature synthesis. Appl. Soil Ecol. 2020, 145, 103305. [Google Scholar] [CrossRef]
- Ma, L.; Zhang, J.; Li, Z.; Xin, X.; Guo, Z.; Wang, D.; Li, D.; Zhao, B. Long-term phosphorus deficiency decreased bacterial-fungal network complexity and efficiency across three soil types in China as revealed by network analysis. Appl. Soil Ecol. 2020, 148, 103506. [Google Scholar] [CrossRef]
- Ma, S.; Chen, X.; Su, H.; Xing, A.; Chen, G.; Zhu, J.; Zhu, B.; Fang, J. Phosphorus addition decreases soil fungal richness and alters fungal guilds in two tropical forests. Soil Biol. Biochem. 2022, 175, 108836. [Google Scholar] [CrossRef]
- Yao, X.; Guo, H.; Zhang, K.; Zhao, M.; Ruan, J.; Chen, J. Trichoderma and its role in biological control of plant fungal and nematode disease. Front. Microbiol. 2023, 14, 1160551. [Google Scholar] [CrossRef]
- Tayyab, M.; Islam, W.; Lee, C.G.; Pang, Z.; Khalil, F.; Lin, S.; Lin, W.; Zhang, H. Short-term effects of different organic amendments on soil fungal composition. Sustainability 2019, 11, 198. [Google Scholar] [CrossRef]
- Zhang, F.; Yang, Y.-Q.; Zhou, F.-P.; Xiao, W.; Boonmee, S.; Yang, X.-Y. Multilocus Phylogeny and characterization of five undescribed aquatic carnivorous fungi (Orbiliomycetes). J. Fungi 2024, 10, 81. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Hyde, K.D.; McKenzie, E.H.C.; Jiang, Y.-L.; Li, D.-W.; Zhao, D.-G. Overview of Stachybotrys (Memnoniella) and current species status. Fungal Divers. 2015, 71, 17–83. [Google Scholar] [CrossRef]
- Pinto, M.R.; Mulloy, B.; Haido, R.M.T.; Travassos, L.R.; Barreto Bergter, E. A Peptidorhamnomannan from the mycelium of Pseudallescheria boydii is a potential diagnostic antigen of this emerging human pathogen. Microbiology 2001, 147, 1499–1506. [Google Scholar] [CrossRef]
- Rougeron, A.; Schuliar, G.; Leto, J.; Sitterlé, E.; Landry, D.; Bougnoux, M.; Kobi, A.; Bouchara, J.; Giraud, S. Human-impacted areas of f rance are environmental reservoirs of the Pseudallescheria Boydii/Scedosporium apiospermum species complex. Environ. Microbiol. 2015, 17, 1039–1048. [Google Scholar] [CrossRef]
- Eichlerová, I.; Baldrian, P. Ligninolytic enzyme production and decolorization capacity of synthetic dyes by saprotrophic white rot, brown rot, and litter decomposing basidiomycetes. J. Fungi 2020, 6, 301. [Google Scholar] [CrossRef]
- Anthony, M.A.; Frey, S.D.; Stinson, K.A. Fungal community homogenization, shift in dominant trophic guild, and appearance of novel taxa with biotic invasion. Ecosphere 2017, 8, e01951. [Google Scholar] [CrossRef]
- Xie, F.; Ma, A.; Zhou, H.; Liang, Y.; Yin, J.; Ma, K.; Zhuang, X.; Zhuang, G. Revealing fungal communities in alpine wetlands through species diversity, functional diversity and ecological network diversity. Microorganisms 2020, 8, 632. [Google Scholar] [CrossRef]
- Yang, H.; Cheng, L.; Che, L.; Su, Y.; Li, Y. Nutrients addition decreases soil fungal diversity and alters fungal guilds and co-occurrence networks in a semi-arid grassland in northern China. Sci. Total Environ. 2024, 926, 172100. [Google Scholar] [CrossRef]
- Xiong, W.; Li, R.; Ren, Y.; Liu, C.; Zhao, Q.; Wu, H.; Jousset, A.; Shen, Q. Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol. Biochem. 2017, 107, 198–207. [Google Scholar] [CrossRef]
- Zhu, R.; Jin, L.; Sang, Y.; Hu, S.; Wang, B.-T.; Jin, F.-J. Characterization of potassium-solubilizing fungi, Mortierella spp., isolated from a poplar plantation rhizosphere soil. Arch. Microbiol. 2024, 206, 157. [Google Scholar] [CrossRef] [PubMed]
- Yan, Z.; Yang, S.; Chen, L.; Zou, Y.; Zhao, Y.; Yan, G.; Wang, H.; Wu, Y. Responses of soil fungal community composition and function to wetland degradation in the songnen plain, northeastern China. Front. Plant Sci. 2024, 15, 1441613. [Google Scholar] [CrossRef]
- Zhang, H.; Chen, W.; Dong, L.; Wang, W. Grassland degradation amplifies the negative effect of nitrogen enrichment on soil microbial community stability. Glob. Change Biol. 2024, 30, e17217. [Google Scholar] [CrossRef]
- Guo, W.; Wang, C.; Brunner, I.; Zhou, Y.; Tang, Q.; Wang, J.; Li, M.-H. Responses of soil fungi to long-term nitrogen-water interactions depend on fungal guilds in a mixed pinus Koraiensis forest. JGR Biogeosciences 2024, 129, e2023JG007826. [Google Scholar] [CrossRef]
- Chen, Y.; Xu, T.; Fu, W.; Hu, Y.; Hu, H.; You, L.; Chen, B. Soil organic carbon and total nitrogen predict large-scale distribution of soil fungal communities in temperate and alpine shrub ecosystems. Eur. J. Soil Biol. 2021, 102, 103270. [Google Scholar] [CrossRef]
- Lekberg, Y.; Arnillas, C.A.; Borer, E.T.; Bullington, L.S.; Fierer, N.; Kennedy, P.G.; Leff, J.W.; Luis, A.D.; Seabloom, E.W.; Henning, J.A. Nitrogen and phosphorus fertilization consistently favor pathogenic over mutualistic fungi in grassland soils. Nat. Commun. 2021, 12, 3484. [Google Scholar] [CrossRef]
- Rousk, J.; Bååth, E.; Brookes, P.C.; Lauber, C.L.; Lozupone, C.; Caporaso, J.G.; Knight, R.; Fierer, N. Soil bacterial and fungal communities across a ph gradient in an arable soil. ISME J. 2010, 4, 1340–1351. [Google Scholar] [CrossRef]
- Pang, F.; Li, Q.; Solanki, M.K.; Wang, Z.; Xing, Y.-X.; Dong, D.-F. Soil phosphorus transformation and plant uptake driven by phosphate-solubilizing microorganisms. Front. Microbiol. 2024, 15, 1383813. [Google Scholar] [CrossRef]
Treatment | Manure (g·pot−1) | Total Nutrient Content (g·pot−1) | ||
---|---|---|---|---|
N | P2O5 | K2O | ||
NK | 0.00 | 1.60 | 0.00 | 0.80 |
NPK | 0.00 | 1.60 | 0.80 | 0.80 |
MNP | 296.30 | 1.60 | 0.79 | 1.78 |
M | 592.59 | 1.60 | 0.77 | 3.56 |
Treatment | pH | OM (g·kg−1) | TN (g·kg−1) | AP (mg·kg−1) | AK (mg·kg−1) |
---|---|---|---|---|---|
NK | 6.56 ± 0.02 b | 36.70 ± 1.38 b | 1.91 ± 0.02 b | 8.13 ± 0.31 c | 361.00 ± 8.58 a |
NPK | 6.57 ± 0.01 b | 37.13 ± 2.57 b | 1.96 ± 0.05 ab | 9.15 ± 0.37 b | 351.50 ± 12.46 a |
MNP | 6.69± 0.01 a | 38.90 ± 1.74 b | 2.00 ± 0.01 ab | 10.47 ± 0.32 a | 282.50 ± 12.08 b |
M | 6.68 ± 0.02 a | 46.63 ± 1.15 a | 2.01 ± 0.04 a | 9.34 ± 0.16 b | 237.50 ± 11.59 c |
Treatment | Chao1 Index | Shannon Index | Simpson Index | Pielou e Index |
---|---|---|---|---|
NK | 300.36 ± 15.46 b | 2.61 ± 0.41 b | 0.19 ± 0.06 a | 0.47 ± 0.07 b |
NPK | 318.42 ± 8.92 ab | 4.15 ± 0.02 a | 0.04 ± 0.00 b | 0.72 ± 0.01 a |
MNP | 356.88 ± 7.56 a | 3.60 ± 0.22 a | 0.09 ± 0.02 ab | 0.62 ± 0.04 a |
M | 357.99 ± 20.50 a | 3.51 ± 0.21 a | 0.09 ± 0.02 ab | 0.61 ± 0.04 a |
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Yang, H.; Yang, Y.; Zhu, H.; Xiong, H.; Zhang, Y.; Liu, Y.; Huang, X.; Li, Y.; Jiang, T. Short-Term Phosphorus Fertilization Alters Soil Fungal Community in Long-Term Phosphorus-Deprived Yellow Soil Paddy Fields. Agriculture 2025, 15, 280. https://doi.org/10.3390/agriculture15030280
Yang H, Yang Y, Zhu H, Xiong H, Zhang Y, Liu Y, Huang X, Li Y, Jiang T. Short-Term Phosphorus Fertilization Alters Soil Fungal Community in Long-Term Phosphorus-Deprived Yellow Soil Paddy Fields. Agriculture. 2025; 15(3):280. https://doi.org/10.3390/agriculture15030280
Chicago/Turabian StyleYang, Huan, Yehua Yang, Huaqing Zhu, Han Xiong, Yarong Zhang, Yanling Liu, Xingcheng Huang, Yu Li, and Taiming Jiang. 2025. "Short-Term Phosphorus Fertilization Alters Soil Fungal Community in Long-Term Phosphorus-Deprived Yellow Soil Paddy Fields" Agriculture 15, no. 3: 280. https://doi.org/10.3390/agriculture15030280
APA StyleYang, H., Yang, Y., Zhu, H., Xiong, H., Zhang, Y., Liu, Y., Huang, X., Li, Y., & Jiang, T. (2025). Short-Term Phosphorus Fertilization Alters Soil Fungal Community in Long-Term Phosphorus-Deprived Yellow Soil Paddy Fields. Agriculture, 15(3), 280. https://doi.org/10.3390/agriculture15030280