Biogeography of Soil Phosphorus-Cycling Microbes in a Changing World

Abstract

Phosphorus is an essential macronutrient for all life forms on Earth, playing a vital role in various metabolic processes. While living organisms store some phosphorus, soil serves as the primary reservoir for this nutrient. However, the biological availability of phosphorus in soil is often limited, leading to widespread phosphorus deficiency across terrestrial ecosystems worldwide (Hou et al. 2018). This limitation can impede essential ecological functions, such as net primary productivity, nitrogen fixation, and carbon storage. As a pivotal element in the nutrient cycle, soil phosphorus exerts significant regulatory influence over ecosystem structure, functions, and processes (Hou et al. 2018). Over geological time, the primary source of phosphorus for living organisms has been the weathering of phosphorus-rich rocks, but soil microorganisms are also integral to the phosphorus cycle. Soil microorganisms involved in phosphorus cycling facilitate the fixation and mineralization of phosphorus through various biological processes. For instance, phosphorus-solubilizing microbes play a crucial role by mobilizing organic phosphorus, dissolving inorganic phosphorus minerals, and retaining phosphorus in biomass (Li et al. 2021). These activities significantly contribute to maintaining effective phosphorus levels in the soil. Despite the importance of microbial processes in phosphorus cycling, the underlying genetic mechanisms and the multitude of factors influencing these interactions remain complex and not fully understood. Currently, research exploring the roles of phosphorus-cycling microbes in the global soil environment is still limited, highlighting the need for further study in this essential area.

Soil microbial biogeography focuses on examining the ecological distribution of soil microbial diversity, community composition, and functional traits across various temporal and spatial scales, ranging from regional to global levels. Understanding these distribution patterns is vital for uncovering the mechanisms that drive microbial diversity and influence ecosystem processes (Chu et al. 2020). In the context of soil ecosystems, Bahram et al. (2018) confirmed that fungi and bacteria displayed a global niche differentiation pattern in the global topsoil, mainly due to their differential responses to precipitation and soil pH. Additionally, they discovered spatial variations in the relative contributions of these soil microbes to global nutrient cycling. Recent research has further demonstrated that soil biodiversity and its associated functions exhibited widespread nonlinear patterns worldwide, with moisture availability—determined by precipitation and potential evapotranspiration—being a primary factor influencing these patterns (Zhang et al. 2023).

Research has shown a significant positive correlation between the density of phosphorus-solubilizing microbial populations in environmental samples and total phosphorus at both continental and global scales. Notably, the study found no relationship between these populations and soil pH, suggesting that phosphorus-solubilizing microbes can thrive across a broad range of pH conditions (Li et al. 2021). Additionally, metabolic activity among phosphorus-cycling microbes appears to be higher in warmer and wetter regions compared to cold and arid areas. There may also be functional interactions between these microbes and those responsible for soil nitrification and organic matter degradation (Li et al. 2021). A deeper understanding of the global distribution of phosphorus-cycling microbes is therefore crucial for fully appreciating their ecological roles and leveraging their functions. In a recent research article published in Global Change Biology, Wang, Zhu, and Ge (2024) presented findings on the global distribution patterns of phosphorus-cycling microbial communities. By analyzing 3321 soil metagenomic samples worldwide, they quantified the abundance of genes associated with key phosphorus-cycling processes. This enabled the creation of global distribution maps for five essential processes: organic phosphate ester hydrolysis, inorganic phosphorus solubilization, two-component systems, phosphotransferase systems, and transporters. This study marks the first comprehensive assessment of soil phosphorus-cycling microbial genes and their associated processes on a global scale, providing critical insights into the geographical patterns of the phosphorus cycle.

In the biogeography of soil microorganisms, large-scale environmental factors are often the primary determinants of soil microbial community distribution. This is largely due to the fact that, while the Earth's environmental conditions have evolved over a long time span, the duration of human activities has been relatively brief. However, it is crucial to recognize that in the mere two centuries since the onset of industrialization, human impacts on climate change, soil health, and global ecosystems have already surpassed the natural changes that have unfolded over thousands of years. Thus, contemporary environmental factors influencing soil microbial community distribution are often closely intertwined with human activities. Various human activities—such as agricultural practices, land use changes, pollution, urbanization, and deforestation—continuously reshape the global environment. These activities exacerbate climate change, contribute to environmental degradation, and lead to the disruption of biological communities. For instance, a global synthesis showed that soil biodiversity and functions were most negatively affected when native forests were converted to cropland and in warmer and wetter ecosystems. Changes in soil pH and total phosphorus primarily regulated the responses of the microbial community to deforestation (Qu et al. 2024). Anthropogenic nitrogen emissions have altered global nitrogen deposition patterns, causing shifts from nitrogen limitation to phosphorus limitation in certain regions. Moreover, phosphorus limitation may hinder the ability of current and future ecosystems to respond effectively to rising carbon dioxide levels and the impacts of climate change (Du et al. 2020).

Human activities, particularly population growth and fertilizer management, are major contributors to phosphorus inputs in soils. These actions have significantly disrupted the phosphorus cycling process in surface soils (Demay et al. 2023), adversely affecting the microbial communities involved in this cycle. Research conducted by Wang, Zhu, and Ge (2024) revealed that, at low to moderate levels of human activity, the abundance of genes associated with phosphorus cycling increases in response to higher levels of human disturbance. This finding suggests a close link between the extent of human impact and the response of phosphorus-cycling microorganisms. The consequences of human activities on climate change are becoming increasingly severe, contributing not only to a gradual rise in global average temperatures but also to escalating the frequency and intensity of extreme weather events, including heatwaves, droughts, and soil freezing. Therefore, it is essential to fully consider the influence of human activities, not only in studies of phosphorus-cycling microorganisms but also in future research on the biogeography of soil microorganisms. Such considerations are vital for effectively addressing the challenges posed by climate change.

Furthermore, agricultural management stands out as the human activity most significantly impacting soil phosphorus levels, often leading to fertilizer application rates in farmland that exceed recommended planetary boundaries. In contrast, some countries continue to face phosphorus shortages. Therefore, the primary global challenge of phosphorus management remains to boost crop yields while minimizing human disruptions to the phosphorus balance in farmlands (Zou, Zhang, and Davidson 2022). Addressing both phosphorus pollution and scarcity is crucial for fostering sustainable agriculture in future. One promising approach involves the management and application of microorganisms that play a role in soil phosphorus cycling. These microorganisms can significantly improve plant phosphorus uptake efficiency, thus meeting agricultural productivity goals while maintaining ecological balance. Research by Wang, Zhu, and Ge (2024) highlights several key genera involved in phosphorus cycling, such as Pseudomonas and Lysobacter, which are particularly sensitive to variations in human activity. Their findings provide valuable insights for further exploring the functions and potential applications of phosphorus-cycling microorganisms in the face of intensifying human influences. Overall, it is imperative to underscore the profound impact of human activities on the microbial communities that govern phosphorus cycling in soils amidst ongoing global climate change. This will significantly contribute to refining soil management practices and fostering sustainable human interactions essential for safeguarding soil ecosystems in our ever-changing world.

Haiyan Chu: conceptualization, funding acquisition, supervision, writing – original draft, writing – review and editing. Yuying Ma: validation, writing – original draft, writing – review and editing.

The authors declare no conflicts of interest.

This article is a Invited Commentary on Wang et al., https://doi.org/10.1111/gcb.17477.