Phosphorus Cycling as a Function of Soil Microbiome

IF 10.8 1区 环境科学与生态学 Q1 BIODIVERSITY CONSERVATION Global Change Biology Pub Date : 2024-12-10 DOI:10.1111/gcb.17611
Youzhi Feng, Ruirui Chen
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In addition to the shortage, the global distribution of soil P is highly uneven (Ringeval et al. <span>2017</span>; He et al. <span>2023</span>), which has far-reaching effects on productivity and ecosystem health worldwide. For example, P is especially depleted in tropical and subtropical regions of the planet, and in very cold soils, P often declines as ecosystem develops. In this respect, advancing our understanding of how to promote P use efficiency and reducing the dependency on P fertilizers is critical to support sustainable agriculture and promote food security for the next generations.</p><p>Given the vast importance of P for energy metabolism, growth, and productivity, plants and microbes have developed a large number of mechanisms to cope with P limitations and support P availability in terrestrial environments. Those include, for example, cluster roots, typically found in the Proteaceae family, arbuscular mycorrhizal fungi–plant associations, the release of phosphatase enzymes by roots and microbes to decompose organic matters, or the exudation of organic acids such as oxalate and malate aimed to digest carbonate rocks. Advancing our understanding on the mechanisms behind the contribution of plants and microbes in supporting P availability is critical for supporting phosphorus use efficiency. Microorganisms play a pivotal role in P cycling and enhance its bioavailability in soils by regulating the balance between “nutrient availability” and “nutrient immobilization.” Specifically, microbes can promote P availability via mineralizing, dissolving, and transforming difficult-to-access inorganic and organic P in soils, which is made available for microbial and plant uptake (Liang et al. <span>2020</span>). Microbes also contribute to P immobilization in soils via retaining P in living and dead cells (Chen et al. <span>2023</span>). The immobilized P then can be converted back to available P through the rapid cell turnover when facing low-P environments. In many farmlands with P imbalances, despite high total P content in soils, crops still exhibit P deficiency symptoms due to low levels of available P. The tradeoff between “nutrient availability” and “nutrient immobilization” is essential for soil microbial communities to regulate soil P cycling (Chen et al. <span>2023</span>).</p><p>Global changes, such as intensified anthropogenic activity and climate change, are driving unprecedented changes in biosphere processes. Microorganisms, due to their invisibility, are often overlooked and rarely characterized in the context of global changes, compared to plants and animals. However, changes in microbial biodiversity and activity can significantly impact the resilience of other organisms and their overall responses to environmental shifts. A recent study underscores the central role of microorganisms in global changes and calls for the recognition of how profoundly human activities influence these vital microbial communities (Cavicchioli et al. <span>2019</span>). Human activities, such as intensive fertilization, land-use change, deforestation, and urban expansion, significantly impact P-cycling microbes and concomitantly alter natural P cycling in soils (Demay et al. <span>2023</span>). For instance, excessive inputs in P-rich soils always weaken the functions of P solubilization and mineralization, while P deficiency can reshape soil microbial communities and their metabolic capabilities to scavenge phosphate (Oliverio et al. <span>2020</span>). Thus, understanding the multifaceted impacts of global changes, especially human activities on P-cycling microbes, is essential for maintaining the stability of ecological functions and promoting sustainable global P management.</p><p>The article published in Global Change Biology by Wang, Zhu, and Ge (<span>2024</span>) makes several key discoveries with substantial implications for understanding the global soil P cycling and ecological effects of human activities. With 3321 soil metagenomic samples distributed across the globe, this study maps the global distribution of total and five key P cycling processes: organic phosphoester hydrolysis, inorganic P solubilization, two-component system, phosphotransferase system, and transporters. Furthermore, the authors confirm that human-related factors, such as economic activities and population, are important drivers for the variation in P-cycling gene abundances. They provide several new insights for sustainable global P management, a pressing need in light of intensified anthropogenic disturbances, and global environmental changes.</p><p>Unlike many prior studies focused on local or regional scales, Wang, Zhu, and Ge (<span>2024</span>) provide a comprehensive analysis of P-cycling microbes at the global level. By exploring the abundances of P-cycling genes, this study highlights the global distribution and characteristics of soil P-cycling microbes as well as their responses to environmental changes across different regions. It offers a mechanistic understanding of P availability, transformation, and turnover, filling critical gaps in existing literature that often measure P fluxes, quantify P availability, and map soil P resources (Helfenstein et al. <span>2024</span>). This work represents the first comprehensive examination of soil P cycling on a global scale, specifically through the lens of microbial functional genes.</p><p>This study refines our understanding of how soil P-cycling microbes respond to varying levels of human disturbance (Wang, Zhu, and Ge <span>2024</span>). Results indicate that moderate human activities, such as limited agricultural intervention, generally increase microbial abundance, while intensive activities, like urbanization and intensive farming, exhibit a threshold effect where moderate disturbance can enhance microbial function, but excessive disturbance suppresses it. This insight is vital for guiding land management and fertilization strategies to balance productivity with the preservation of soil ecosystems. Additionally, the research identifies key microbial taxa sensitive to human-induced changes, including genera like <i>Pseudomonas</i> and <i>Lysobacter</i>. These microbes ensure P availability for plants and other organisms, particularly in moderately disturbed areas where their abundance and activity increased. This finding opens new avenues for optimizing soil P cycling through targeted management of these microbial communities.</p><p>Furthermore, Wang, Zhu, and Ge (<span>2024</span>) bring methodological innovations by integrating metagenomic sequencing, statistical modeling, and global mapping to examine key P-cycling genes. By employing structural equation modeling and random forest analysis, the study effectively decouples the impacts of human activities from natural climatic and edaphic factors. These multi-dimensional analyses effectively bridge previous gaps regarding the complex interactions between climate changes, human activities, and microbial communities, providing critical data and theoretical support for future strategies on sustainable soil and P resource management.</p><p>Soil P cycling is a key factor determining how terrestrial ecosystems respond to climate change and human activities. While conventional chemical indicators for soil P measurement, such as Olsen-P and the Hedley sequential extraction method, remain important, evaluating microbial functional genes can offer a new and more sensitive approach to study soil P cycling. Insights from soil P-cycling processes, like the five key processes in the study of Wang, Zhu, and Ge (<span>2024</span>), allow a deeper mechanistic understanding of P availability and transfer in soil ecosystems. In the context of global changes, the increased focus on soil P cycling is crucial for sustainable management, agricultural production, and environmental conservation strategies.</p><p><b>Youzhi Feng:</b> writing – review and editing. <b>Ruirui Chen:</b> writing – original draft.</p><p>The authors declare no conflicts of interest.</p>","PeriodicalId":175,"journal":{"name":"Global Change Biology","volume":"30 12","pages":""},"PeriodicalIF":10.8000,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/gcb.17611","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Global Change Biology","FirstCategoryId":"93","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/gcb.17611","RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIODIVERSITY CONSERVATION","Score":null,"Total":0}
引用次数: 0

Abstract

Phosphorus (P) is one of the main elements limiting the productivity of terrestrial ecosystems (He et al. 2023). P availability is also critical for multiple ecosystem services such as food production, waste decomposition, and carbon sequestration (Helfenstein et al. 2024). Unfortunately, P is a nonrenewable resource linked to bedrock availability. Soil P primarily exists in insoluble mineral or organic forms, with only a limited fraction (usually less than 1%) available for plant uptake. Currently, 90% of global P demand is associated with food production, which is predicted to increase by 50%–100% by 2050 due to rising food demand and changing diets (Cordell, Drangert, and White 2009). In this regard, P faces potential shortages, threatening future global food supply. In addition to the shortage, the global distribution of soil P is highly uneven (Ringeval et al. 2017; He et al. 2023), which has far-reaching effects on productivity and ecosystem health worldwide. For example, P is especially depleted in tropical and subtropical regions of the planet, and in very cold soils, P often declines as ecosystem develops. In this respect, advancing our understanding of how to promote P use efficiency and reducing the dependency on P fertilizers is critical to support sustainable agriculture and promote food security for the next generations.

Given the vast importance of P for energy metabolism, growth, and productivity, plants and microbes have developed a large number of mechanisms to cope with P limitations and support P availability in terrestrial environments. Those include, for example, cluster roots, typically found in the Proteaceae family, arbuscular mycorrhizal fungi–plant associations, the release of phosphatase enzymes by roots and microbes to decompose organic matters, or the exudation of organic acids such as oxalate and malate aimed to digest carbonate rocks. Advancing our understanding on the mechanisms behind the contribution of plants and microbes in supporting P availability is critical for supporting phosphorus use efficiency. Microorganisms play a pivotal role in P cycling and enhance its bioavailability in soils by regulating the balance between “nutrient availability” and “nutrient immobilization.” Specifically, microbes can promote P availability via mineralizing, dissolving, and transforming difficult-to-access inorganic and organic P in soils, which is made available for microbial and plant uptake (Liang et al. 2020). Microbes also contribute to P immobilization in soils via retaining P in living and dead cells (Chen et al. 2023). The immobilized P then can be converted back to available P through the rapid cell turnover when facing low-P environments. In many farmlands with P imbalances, despite high total P content in soils, crops still exhibit P deficiency symptoms due to low levels of available P. The tradeoff between “nutrient availability” and “nutrient immobilization” is essential for soil microbial communities to regulate soil P cycling (Chen et al. 2023).

Global changes, such as intensified anthropogenic activity and climate change, are driving unprecedented changes in biosphere processes. Microorganisms, due to their invisibility, are often overlooked and rarely characterized in the context of global changes, compared to plants and animals. However, changes in microbial biodiversity and activity can significantly impact the resilience of other organisms and their overall responses to environmental shifts. A recent study underscores the central role of microorganisms in global changes and calls for the recognition of how profoundly human activities influence these vital microbial communities (Cavicchioli et al. 2019). Human activities, such as intensive fertilization, land-use change, deforestation, and urban expansion, significantly impact P-cycling microbes and concomitantly alter natural P cycling in soils (Demay et al. 2023). For instance, excessive inputs in P-rich soils always weaken the functions of P solubilization and mineralization, while P deficiency can reshape soil microbial communities and their metabolic capabilities to scavenge phosphate (Oliverio et al. 2020). Thus, understanding the multifaceted impacts of global changes, especially human activities on P-cycling microbes, is essential for maintaining the stability of ecological functions and promoting sustainable global P management.

The article published in Global Change Biology by Wang, Zhu, and Ge (2024) makes several key discoveries with substantial implications for understanding the global soil P cycling and ecological effects of human activities. With 3321 soil metagenomic samples distributed across the globe, this study maps the global distribution of total and five key P cycling processes: organic phosphoester hydrolysis, inorganic P solubilization, two-component system, phosphotransferase system, and transporters. Furthermore, the authors confirm that human-related factors, such as economic activities and population, are important drivers for the variation in P-cycling gene abundances. They provide several new insights for sustainable global P management, a pressing need in light of intensified anthropogenic disturbances, and global environmental changes.

Unlike many prior studies focused on local or regional scales, Wang, Zhu, and Ge (2024) provide a comprehensive analysis of P-cycling microbes at the global level. By exploring the abundances of P-cycling genes, this study highlights the global distribution and characteristics of soil P-cycling microbes as well as their responses to environmental changes across different regions. It offers a mechanistic understanding of P availability, transformation, and turnover, filling critical gaps in existing literature that often measure P fluxes, quantify P availability, and map soil P resources (Helfenstein et al. 2024). This work represents the first comprehensive examination of soil P cycling on a global scale, specifically through the lens of microbial functional genes.

This study refines our understanding of how soil P-cycling microbes respond to varying levels of human disturbance (Wang, Zhu, and Ge 2024). Results indicate that moderate human activities, such as limited agricultural intervention, generally increase microbial abundance, while intensive activities, like urbanization and intensive farming, exhibit a threshold effect where moderate disturbance can enhance microbial function, but excessive disturbance suppresses it. This insight is vital for guiding land management and fertilization strategies to balance productivity with the preservation of soil ecosystems. Additionally, the research identifies key microbial taxa sensitive to human-induced changes, including genera like Pseudomonas and Lysobacter. These microbes ensure P availability for plants and other organisms, particularly in moderately disturbed areas where their abundance and activity increased. This finding opens new avenues for optimizing soil P cycling through targeted management of these microbial communities.

Furthermore, Wang, Zhu, and Ge (2024) bring methodological innovations by integrating metagenomic sequencing, statistical modeling, and global mapping to examine key P-cycling genes. By employing structural equation modeling and random forest analysis, the study effectively decouples the impacts of human activities from natural climatic and edaphic factors. These multi-dimensional analyses effectively bridge previous gaps regarding the complex interactions between climate changes, human activities, and microbial communities, providing critical data and theoretical support for future strategies on sustainable soil and P resource management.

Soil P cycling is a key factor determining how terrestrial ecosystems respond to climate change and human activities. While conventional chemical indicators for soil P measurement, such as Olsen-P and the Hedley sequential extraction method, remain important, evaluating microbial functional genes can offer a new and more sensitive approach to study soil P cycling. Insights from soil P-cycling processes, like the five key processes in the study of Wang, Zhu, and Ge (2024), allow a deeper mechanistic understanding of P availability and transfer in soil ecosystems. In the context of global changes, the increased focus on soil P cycling is crucial for sustainable management, agricultural production, and environmental conservation strategies.

Youzhi Feng: writing – review and editing. Ruirui Chen: writing – original draft.

The authors declare no conflicts of interest.

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磷循环在土壤微生物群中的作用
磷(P),特别是其有效性,在陆地生态系统的生产力中起着关键作用。最近的文章提出了几个关键的发现,对理解全球土壤磷循环作为微生物组的功能和人类活动的生态效应具有重大意义。
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来源期刊
Global Change Biology
Global Change Biology 环境科学-环境科学
CiteScore
21.50
自引率
5.20%
发文量
497
审稿时长
3.3 months
期刊介绍: Global Change Biology is an environmental change journal committed to shaping the future and addressing the world's most pressing challenges, including sustainability, climate change, environmental protection, food and water safety, and global health. Dedicated to fostering a profound understanding of the impacts of global change on biological systems and offering innovative solutions, the journal publishes a diverse range of content, including primary research articles, technical advances, research reviews, reports, opinions, perspectives, commentaries, and letters. Starting with the 2024 volume, Global Change Biology will transition to an online-only format, enhancing accessibility and contributing to the evolution of scholarly communication.
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