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Restoration boosts soil P-cycle multifunctionality in karst ecosystems by modulating soil properties and rare bacterial taxa

Fujing Pan15, Xuan Yu1, 5, Yueming Liang2#, Peilei Hu3, 4, Kelin Wang3, 4, Wei Zhang3, 4#, Qian Yang1, 5

Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology/College of Environmental and Engineering, Guilin University of Technology, Guilin 541006, China

Karst Dynamics Laboratory of Ministry of Natural Resources, Institute of Karst Geology, Chinese Academy of Geological Sciences, Guilin 541004, China

Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, China

Huanjiang Agriculture Ecosystem Observation and Research Station of Guangxi/Guangxi Key Laboratory of Karst Ecological Processes and Services/Huanjiang Observation and Research Station for Karst Ecosystems, Chinese Academy of Sciences, Huanjiang 547100, China

5 University Engineering Research Center of Watershed Protection and Green Development, Guangxi, Guilin University of Technology, Guilin 541006, China

 Highlights 

Natural restoration improves karst soil P-cycle multifunctionality compared to artificial restoration and cropland

Natural restoration boostSOC and bacterial complexity and network tightness

Rare phoD-harboring bacterial taxa play a more critical role in driving soil P-cycle than dominant taxa

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摘要  

磷是一种重要的营养元素,对植物生长和生态系统功能至关重要。土壤磷循环具有维持植物生长和生产力、调节生态系统养分平衡、增强生态系统适应性和恢复力等多种作用。这一循环受恢复方式和微生物群落动态等因素的影响。然而,在喀斯特生态系统,恢复方式改变磷循环的程度和潜在的微生物机制仍然知之甚少。磷循环多功能指数是评价土壤磷循环功能的综合指标,为了解不同修复方式间磷循环的变化提供依据。为了研究不同修复方式下土壤磷循环多功能指数的变化及其微生物机制,我们分析了土壤有效磷、总磷、微生物生物量磷含量以及酸性磷酸酶和碱性磷酸酶的活性。利用这些数据,对中国亚热带喀斯特生态系统6个样点的两种恢复方式(人工恢复森林(AF)和自然恢复森林(NF))和对照(农田,CP)的z得分进行平均,计算磷循环多功能指数。同时,测定了土壤有机碳、交换性钙和交换性镁、pH、容重、微生物生物量碳和微生物生物量氮,以及携带phoD基因细菌的群落结构、相对丰度、多样性指数和共生网络。结果表明,携带phoD基因细菌的群落结构在AFNFCP之间以及在不同温度梯度之间都存在显著差异。这些细菌的共现网络的复杂性和紧密性从CPAF再到NF增加,酸性磷酸酶和碱性磷酸酶活性也增加,但总磷和有效磷含量则相反。土壤磷循环多功能性指数在NF显著高于AFCP,指数的变化受恢复、温度、微生物生物量碳、微生物生物量氮、有机碳、可交换性钙、容重、携带phoD基因细菌群落结构和可交换性镁的显著影响。此外,自然恢复对磷循环多功能性指数的影响比温度更显著,其提高了土壤有机碳、微生物生物量、携带phoD基因细菌群落结构的复杂性和共生网络紧密度以及酸性磷酸酶和碱性磷酸酶活性,但降低了土壤容重。与优势菌属相比,稀有菌属对土壤磷循环多功能性指数的影响更显著。本研究强调了喀斯特生态系统中携带phoD基因细菌的稀有属在驱动土壤磷循环多功能性方面的重要性,另外,自然修复在提高土壤有机质和微生物群落复杂性方面比人工方法更有效。



Abstract  

Phosphorus (P) is an essential nutrient element that is critical for plant growth and ecosystem functionality. The soil P cycle plays multiple roles, such as sustaining plant growth and productivity, regulating nutrient balance within ecosystems, and enhancing ecosystem adaptability and resilience. This cycle is influenced by factors such as the restoration approach and microbial community dynamics. However, the extent to which the restoration approach alters the P cycle in karst ecosystems and the underlying microbial mechanisms remain poorly understood. The P-cycle multifunctionality index (P-cycle MFI) serves as a comprehensive indicator for evaluating soil P cycle function, and it provides insights into changes in the P cycle between different restoration approaches. To investigate the shifts in soil P-cycle MFI and microbial mechanisms between different restoration approaches, we analyzed soil available P (AP), total P (TP), microbial biomass P (MBP), and the activities of acid phosphatase (ACP) and alkaline phosphatase (ALP). These data were used to calculate the P-cycle MFI by averaging the Z-scores between two restoration approaches (artificial restoration of forest (AF) and natural restoration of forest (NF)) and a control (cropland, CP) at six subtropical karst ecosystem sites in China. We also determined the soil organic carbon (SOC), exchangeable calcium (Ca) and magnesium (Mg), pH, bulk density (BD), microbial biomass C (MBC), and microbial biomass nitrogen (MBN), as well as the community structure, relative abundance, diversity indices, and co-occurrence networks of phoD-harboring bacteria. The results showed that the community structure of phoD-harboring bacteria varied significantly among AF, NF, and CP and across different temperature gradients. These bacteria exhibited increasing complexity and tightness in co-occurrence networks from CP to AF and then to NF, along with the ACP and ALP activities, but not the TP and AP contents. The P-cycle MFI values were significantly higher in NF compared to AF and CP, and the variation was significantly explained by restoration approach, temperature, MBC, MBN, SOC, exchangeable Ca, BD, community structure of phoD-harboring bacteria, and exchangeable Mg. Furthermore, natural restoration had a more substantial impact on the P-cycle MFI than temperature by enhancing SOC, microbial biomass, the complexity and co-occurrence network tightness of the phoD-harboring bacterial community structure, and ACP and ALP activities, but it reduced soil BD. The rare genera of phoD-harboring bacteria significantly influenced the variation of soil P-cycle MFI compared to the dominant genera. This study highlights the importance of rare genera of phoD-harboring bacteria in driving soil P-cycle multifunctionality in karst ecosystems, with natural restoration being more effective than artificial methods for enhancing soil organic matter and microbial community complexity.

Keywords:  Karst ecosystem       restoration       community       phoD-harboring bacteria       P-cycle multifunctionality       rare taxa  
Online: 01 May 2025  
Fund: 

The study was supported by the National Key Research and Development Program of China (2022YFF1300705), the Key Research and Development Project of Guangxi, China (Guike AB24010051), the National Natural Science Foundation of China (42261011, 32271730 and U20A2011), and the Central Public Welfare Research Institutes, Chinese Academy of Geological Sciences (2023020)

About author:  Fujing Pan, E-mail: panfujing@glut.edu.cn; #Correspondence Wei Zhang, E-mail: zhangw@isa.ac.cn; Yueming Liang, E-mail: yueming0919@163.com

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Fujing Pan, Xuan Yu, Yueming Liang, Peilei Hu, Kelin Wang, Wei Zhang, Qian Yang. 2025. Restoration boosts soil P-cycle multifunctionality in karst ecosystems by modulating soil properties and rare bacterial taxa. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.05.001

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