Phosphorus Cycling Dominates Microbial Regulation of Synergistic Carbon, Nitrogen, and Phosphorus Gene Dynamics During <i>Robinia pseudoacacia</i> Restoration on the Loess Plateau

Carbon (C), nitrogen (N), and phosphorus (P) are key soil nutrients whose synergistic interactions regulate ecosystem nutrient cycling, yet the functional gene-level coordination and driving factors of these cycles remain poorly understood. This study addresses this gap by investigating the dynamic...

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Main Authors: Ning Peng, Yan Wang, Huifeng Wu, Hongjian Hao, Ahejiang Sailike, Zhouchang Yu, Shicai Li, Runhao Shi, Wenfang Hao, Wei Zhang
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Agronomy
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Online Access:https://www.mdpi.com/2073-4395/15/4/797
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author Ning Peng
Yan Wang
Huifeng Wu
Hongjian Hao
Ahejiang Sailike
Zhouchang Yu
Shicai Li
Runhao Shi
Wenfang Hao
Wei Zhang
author_facet Ning Peng
Yan Wang
Huifeng Wu
Hongjian Hao
Ahejiang Sailike
Zhouchang Yu
Shicai Li
Runhao Shi
Wenfang Hao
Wei Zhang
author_sort Ning Peng
collection DOAJ
description Carbon (C), nitrogen (N), and phosphorus (P) are key soil nutrients whose synergistic interactions regulate ecosystem nutrient cycling, yet the functional gene-level coordination and driving factors of these cycles remain poorly understood. This study addresses this gap by investigating the dynamic changes in C, N, and P cycling functional genes and their microbial and environmental drivers across <i>Robinia pseudoacacia</i> plantations of different restoration stages (10, 20, 30, and 40 years) on the Loess Plateau. We analyzed soil physicochemical properties and conducted metagenomic sequencing, redundancy analysis (RDA), and Partial Least Squares Structural Equation Modeling (PLS-SEM). Results showed that P-cycling functional genes, particularly <i>pqqC</i> and <i>spoT</i>, exhibited the highest network centrality, indicating their dominant role in regulating nutrient dynamics. Compared with farmland, STC, SOC, SAP, pH, and SWC significantly changed (<i>p</i> < 0.05) with restoration age, directly shaping key microbial groups such as <i>Proteobacteria</i>, <i>Acidobacteria</i>, <i>Actinobacteria</i>, and <i>Chloroflexi</i>. These microbial shifts were strongly correlated with the synergistic changes in C, N, and P functional gene abundance (<i>p</i> < 0.01). The findings highlight the central role of phosphorus-solubilizing genes in linking C, N, and P cycles and emphasize the microbial community responses to soil environmental changes as a key driver of nutrient cycling during ecological restoration. This study provides novel insights into microbial functional gene interactions and their ecological significance in soil nutrient dynamics, offering theoretical support for improving restoration strategies on the Loess Plateau.
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spelling doaj-art-01e6f03c1a4743c8bb23c248dc115d532025-08-20T03:14:17ZengMDPI AGAgronomy2073-43952025-03-0115479710.3390/agronomy15040797Phosphorus Cycling Dominates Microbial Regulation of Synergistic Carbon, Nitrogen, and Phosphorus Gene Dynamics During <i>Robinia pseudoacacia</i> Restoration on the Loess PlateauNing Peng0Yan Wang1Huifeng Wu2Hongjian Hao3Ahejiang Sailike4Zhouchang Yu5Shicai Li6Runhao Shi7Wenfang Hao8Wei Zhang9College of Life Sciences, Northwest Agriculture and Forestry University, Yangling 712100, ChinaCollege of Life Sciences, Northwest Agriculture and Forestry University, Yangling 712100, ChinaState Key Laboratory of Loess Science, Institute of Earth Environment, Chinese Academy of Sciences, Xi’an 710061, ChinaCollege of Grassland and Grassland, Northwest Agriculture and Forestry University, Yangling 712100, ChinaCollege of Grassland and Grassland, Northwest Agriculture and Forestry University, Yangling 712100, ChinaCollege of Grassland and Grassland, Northwest Agriculture and Forestry University, Yangling 712100, ChinaCollege of Grassland and Grassland, Northwest Agriculture and Forestry University, Yangling 712100, ChinaCollege of Grassland and Grassland, Northwest Agriculture and Forestry University, Yangling 712100, ChinaCollege of Life Sciences, Northwest Agriculture and Forestry University, Yangling 712100, ChinaCollege of Grassland and Grassland, Northwest Agriculture and Forestry University, Yangling 712100, ChinaCarbon (C), nitrogen (N), and phosphorus (P) are key soil nutrients whose synergistic interactions regulate ecosystem nutrient cycling, yet the functional gene-level coordination and driving factors of these cycles remain poorly understood. This study addresses this gap by investigating the dynamic changes in C, N, and P cycling functional genes and their microbial and environmental drivers across <i>Robinia pseudoacacia</i> plantations of different restoration stages (10, 20, 30, and 40 years) on the Loess Plateau. We analyzed soil physicochemical properties and conducted metagenomic sequencing, redundancy analysis (RDA), and Partial Least Squares Structural Equation Modeling (PLS-SEM). Results showed that P-cycling functional genes, particularly <i>pqqC</i> and <i>spoT</i>, exhibited the highest network centrality, indicating their dominant role in regulating nutrient dynamics. Compared with farmland, STC, SOC, SAP, pH, and SWC significantly changed (<i>p</i> < 0.05) with restoration age, directly shaping key microbial groups such as <i>Proteobacteria</i>, <i>Acidobacteria</i>, <i>Actinobacteria</i>, and <i>Chloroflexi</i>. These microbial shifts were strongly correlated with the synergistic changes in C, N, and P functional gene abundance (<i>p</i> < 0.01). The findings highlight the central role of phosphorus-solubilizing genes in linking C, N, and P cycles and emphasize the microbial community responses to soil environmental changes as a key driver of nutrient cycling during ecological restoration. This study provides novel insights into microbial functional gene interactions and their ecological significance in soil nutrient dynamics, offering theoretical support for improving restoration strategies on the Loess Plateau.https://www.mdpi.com/2073-4395/15/4/797synergistic change mechanismssoil biogeochemical cyclingfunctional genesmetagenomic sequencing<i>Robinia pseudoacacia</i> forest
spellingShingle Ning Peng
Yan Wang
Huifeng Wu
Hongjian Hao
Ahejiang Sailike
Zhouchang Yu
Shicai Li
Runhao Shi
Wenfang Hao
Wei Zhang
Phosphorus Cycling Dominates Microbial Regulation of Synergistic Carbon, Nitrogen, and Phosphorus Gene Dynamics During <i>Robinia pseudoacacia</i> Restoration on the Loess Plateau
Agronomy
synergistic change mechanisms
soil biogeochemical cycling
functional genes
metagenomic sequencing
<i>Robinia pseudoacacia</i> forest
title Phosphorus Cycling Dominates Microbial Regulation of Synergistic Carbon, Nitrogen, and Phosphorus Gene Dynamics During <i>Robinia pseudoacacia</i> Restoration on the Loess Plateau
title_full Phosphorus Cycling Dominates Microbial Regulation of Synergistic Carbon, Nitrogen, and Phosphorus Gene Dynamics During <i>Robinia pseudoacacia</i> Restoration on the Loess Plateau
title_fullStr Phosphorus Cycling Dominates Microbial Regulation of Synergistic Carbon, Nitrogen, and Phosphorus Gene Dynamics During <i>Robinia pseudoacacia</i> Restoration on the Loess Plateau
title_full_unstemmed Phosphorus Cycling Dominates Microbial Regulation of Synergistic Carbon, Nitrogen, and Phosphorus Gene Dynamics During <i>Robinia pseudoacacia</i> Restoration on the Loess Plateau
title_short Phosphorus Cycling Dominates Microbial Regulation of Synergistic Carbon, Nitrogen, and Phosphorus Gene Dynamics During <i>Robinia pseudoacacia</i> Restoration on the Loess Plateau
title_sort phosphorus cycling dominates microbial regulation of synergistic carbon nitrogen and phosphorus gene dynamics during i robinia pseudoacacia i restoration on the loess plateau
topic synergistic change mechanisms
soil biogeochemical cycling
functional genes
metagenomic sequencing
<i>Robinia pseudoacacia</i> forest
url https://www.mdpi.com/2073-4395/15/4/797
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