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The Green Revolution has led to a threefold growth in food production in the last 50 to 75 years, hut increases in crop production have required a concurrent increase in the use of inorganic phosphorus as fertilizer. A sustainable phosphorus supply is not assured, though, and food production depends on mineral phosphorus supplies that are nonrenewable and are being depleted. Phosphorus is effectively a nonsubstitutable necessity for all life. Because mineral phosphorus deposits are not distributed evenly, future phosphorus scarcity may have national security implications. Some projections show economically viable mineral reserves becoming depleted within a few decades. Phosphorus-induced food shortages are therefore a possibility, particularly in developing countries where farmers are more vulnerable to volatile fertilizer prices. Sustainable solutions to such future challenges exist, and involve closing the loop on the human phosphorus cycle. We review the current state of knowledge about human phosphorus use and dependence and present examples of these sustainable solutions.

Soil chemical fumigation is an effective and popular method to increase agricultural productivity. However, the broad-spectrum bioactivity of fumigants causes harm to soil beneficial microorganisms involved in the soil phosphorous cycle, such as soil phosphorus solubilizing microorganisms (PSMs). We review the effects of soil chemical fumigation on soil phosphorus cycling, and the potential underlying mechanisms that ultimately lead to altered phosphorus availability for crops. These complex processes involve the highly diverse PSM community and a plethora of soil phosphorus forms. We discuss phosphatizing amendments aimed at counteracting the possible negative effects of fumigation on phosphorus availability, phosphorus use efficiency, and crop yields. We also emphasize distinguishing between the effects on soil phosphorus cycling caused by the chemical fumigants, and those caused by the fumigation process (e.g. plastic mulching). These are typically conflated in the literature; distinguishing them is critical for identifying appropriate amendments to remediate possible post-fumigation soil phosphorus deficiencies.

Phosphorus (P) is a vital nutrient for all living organisms and may control the growth of bacteria in the ocean. Bacteria induce alkaline phosphatases when inorganic phosphate (P i ) is insufficient to meet their P-requirements, and therefore bulk alkaline phosphatase activity measurements have been used to assess the P-status of microbial assemblages. In this study, the molecular basis of marine bacterial phosphatases and their potential role in the environment were investigated. We found that only a limited number of homologs to the classical Escherichia coli alkaline phosphatase (PhoA) were present in marine isolates in the Bacteroidetes and γ- proteobacteria lineages. In contrast, PhoX, a recently described phosphatase, was widely distributed among diverse bacterial taxa, including Cyanobacteria , and frequently found in the marine metagenomic Global Ocean Survey database. These taxa included ecologically important groups such as Roseobacter and Trichodesmium . PhoX was induced solely upon P-starvation and accounted for approximately 90% of the phosphatase activity in the model marine bacterium Silicibacter pomeroyi . Analysis of the available transcriptomic datasets and their corresponding metagenomes indicated that PhoX is more abundant than PhoA in oligotrophic marine environments such as the North Pacific Subtropical Gyre. Those analyses also revealed that PhoA may be important when Bacteroidetes are abundant, such as in algal bloom episodes. However, PhoX appears to be much more widespread. Its identification as a gene that mediates organic P acquisition in ecologically important groups, and as a marker of P i -stress, constitutes an important step toward a better understanding of the marine P cycle.

Low phosphorus burial in shallow marine sedimentary rocks before about 750 million years ago implies a change in the global phosphorus cycle, coinciding with the end of what may have been a stable low-oxygen world. A history of phosphorus limitation It is thought that the nutrient phosphorus limits marine primary productivity on geological timescales, but it is not clear whether phosphorus limitation has persisted throughout Earth's history. On the basis of a compilation of phosphorus abundances in marine sedimentary rocks spanning the past 3.5 billion years, and a biogeochemical model, Christopher Reinhard, Noah Planavsky and colleagues suggest that a prolonged period of phosphorus biolimitation was followed by a fundamental shift in the phosphorus cycle during the late Proterozoic eon (between 800 million and 635 million years ago). This is coincident with a previously inferred shift in marine redox states, severe perturbations to Earth's climate system, and the emergence of animals. The macronutrient phosphorus is thought to limit primary productivity in the oceans on geological timescales 1 . Although there has been a sustained effort to reconstruct the dynamics of the phosphorus cycle over the past 3.5 billion years 2 , 3 , 4 , 5 , it remains uncertain whether phosphorus limitation persisted throughout Earth’s history and therefore whether the phosphorus cycle has consistently modulated biospheric productivity and ocean–atmosphere oxygen levels over time. Here we present a compilation of phosphorus abundances in marine sedimentary rocks spanning the past 3.5 billion years. We find evidence for relatively low authigenic phosphorus burial in shallow marine environments until about 800 to 700 million years ago. Our interpretation of the database leads us to propose that limited marginal phosphorus burial before that time was linked to phosphorus biolimitation, resulting in elemental stoichiometries in primary producers that diverged strongly from the Redfield ratio (the atomic ratio of carbon, nitrogen and phosphorus found in phytoplankton). We place our phosphorus record in a quantitative biogeochemical model framework and find that a combination of enhanced phosphorus scavenging in anoxic, iron-rich oceans 6 , 7 and a nutrient-based bistability in atmospheric oxygen levels could have resulted in a stable low-oxygen world. The combination of these factors may explain the protracted oxygenation of Earth’s surface over the last 3.5 billion years of Earth history 8 . However, our analysis also suggests that a fundamental shift in the phosphorus cycle may have occurred during the late Proterozoic eon (between 800 and 635 million years ago), coincident with a previously inferred shift in marine redox states 9 , severe perturbations to Earth’s climate system 10 , and the emergence of animals 11 , 12 .

Phosphorus is an essential element for life, and phosphorus cycling is crucial to planetary habitability. In aquatic environments, microorganisms are a major component of phosphorus cycling and rapidly transform the diverse chemical forms of phosphorus through various uptake, assimilation and release pathways. Recent discoveries have revealed a more dynamic and complex aquatic microbial phosphorus cycle than previously understood. Some microorganisms have been shown to use and produce new phosphorus compounds, including those in reduced forms. New findings have also raised numerous unanswered questions that warrant further investigation. There is an expanding influence of human activity on aquatic ecosystems. Advancements in understanding the phosphorus biogeochemistry of evolving aquatic environments offer a unique opportunity to comprehend, anticipate and mitigate the effect of human activities. In this Review, I discuss the wealth of new aquatic phosphorus cycle research, spanning disciplines from omics and physiology to global biogeochemical modelling, with a focus on the current comprehension of how aquatic microorganisms sense, transport, assimilate, store, produce and release phosphorus. Of note, I delve into cellular phosphorus allocation, an underexplored topic with wide-ranging implications for energy and element flux in aquatic ecosystems. In this Review, Solange Duhamel explores the critical role of microorganisms in regulating the aquatic phosphorus cycle, emphasizes the effect of human activity on phosphorus cycling and suggests future research directions to better understand the microbial phosphorus cycle in a changing world.

Phosphorus is a limiting nutrient that is thought to control oceanic oxygen levels to a large extent 1 – 3 . A possible increase in marine phosphorus concentrations during the Ediacaran Period (about 635–539 million years ago) has been proposed as a driver for increasing oxygen levels 4 – 6 . However, little is known about the nature and evolution of phosphorus cycling during this time 4 . Here we use carbonate-associated phosphate (CAP) from six globally distributed sections to reconstruct oceanic phosphorus concentrations during a large negative carbon-isotope excursion—the Shuram excursion (SE)—which co-occurred with global oceanic oxygenation 7 – 9 . Our data suggest pulsed increases in oceanic phosphorus concentrations during the falling and rising limbs of the SE. Using a quantitative biogeochemical model, we propose that this observation could be explained by carbon dioxide and phosphorus release from marine organic-matter oxidation primarily by sulfate, with further phosphorus release from carbon-dioxide-driven weathering on land. Collectively, this may have resulted in elevated organic-pyrite burial and ocean oxygenation. Our CAP data also seem to suggest equivalent oceanic phosphorus concentrations under maximum and minimum extents of ocean anoxia across the SE. This observation may reflect decoupled phosphorus and ocean anoxia cycles, as opposed to their coupled nature in the modern ocean. Our findings point to external stimuli such as sulfate weathering rather than internal oceanic phosphorus–oxygen cycling alone as a possible control on oceanic oxygenation in the Ediacaran. In turn, this may help explain the prolonged rise of atmospheric oxygen levels. Reconstruction of oceanic phosphorus concentrations during a large negative carbon-isotope excursion co-occurring with global oceanic oxygenation and evolution of some of Earth’s earliest animals suggests that decoupled phosphorus and ocean anoxia cycles during the Ediacaran may have prolonged the rise of atmospheric oxygen.

Myriad field, laboratory, and modeling studies show that nutrient availability plays a fundamental role in regulating CO2 exchange between the Earth's biosphere and atmosphere, and in determining how carbon pools and fluxes respond to climatic change. Accordingly, global models that incorporate coupled climate–carbon cycle feedbacks made a significant advance with the introduction of a prognostic nitrogen cycle. Here we propose that incorporating phosphorus cycling represents an important next step in coupled climate–carbon cycling model development, particularly for lowland tropical forests where phosphorus availability is often presumed to limit primary production. We highlight challenges to including phosphorus in modeling efforts and provide suggestions for how to move forward.

Phosphorus (P) is essential for life, but most of the global surface ocean is P depleted, which can limit marine productivity and affect ecosystem structure. Over recent decades, a wealth of new knowledge has revolutionized our understanding of the marine P cycle. With a revised residence time (~10–20 kyr) that is similar to nitrate and a growing awareness that P transformations are under tight and elaborate microbial control, the classic textbook version of a tectonically slow and biogeochemically simple marine P cycle has become outdated. P moves throughout the world’s oceans with a higher level of complexity than has ever been appreciated before, including a vast, yet poorly understood, P redox cycle. Here, we illustrate an oceanographically integral view of marine P by reviewing recent advances in the coupled cycles of P with carbon, nitrogen and metals in marine systems. Through this lens, P takes on a more dynamic and connected role in marine biogeochemistry than previously acknowledged, which points to unclear yet profound potential consequences for marine ecosystems, particularly under anthropogenic influence. Phosphorus plays a dynamic and complex role in marine biogeochemistry, which is closely connected to carbon, nitrogen and metal cycling, according to a literature synthesis on recent advances in understandings of the marine phosphorus cycle.

The regeneration of bioavailable phosphate from immobilized organophosphorus represents a key process in the global phosphorus cycle and is facilitated by enzymes known as phosphatases. Most bacteria possess at least one of three phosphatases with broad substrate specificity, known as PhoA, PhoX, and PhoD, whose activity is optimal under alkaline conditions. The production and activity of these phosphatases is repressed by phosphate availability. Therefore, they are only fully functional when bacteria experience phosphorus-limiting growth conditions. Here, we reveal a previously overlooked phosphate-insensitive phosphatase, PafA, prevalent in Bacteroidetes, which is highly abundant in nature and represents a major route for the regeneration of environmental phosphate. Using the enzyme from Flavobacterium johnsoniae, we show that PafA is highly active toward phosphomonoesters, is fully functional in the presence of excess phosphate, and is essential for growth on phosphorylated carbohydrates as a sole carbon source. These distinct properties of PafA may expand the metabolic niche of Bacteroidetes by enabling the utilization of abundant organophosphorus substrates as C and P sources, providing a competitive advantage when inhabiting zones of high microbial activity and nutrient demand. PafA, which is constitutively synthesized by soil and marine flavobacteria, rapidly remineralizes phosphomonoesters releasing bioavailable phosphate that can be acquired by neighboring cells. The pafA gene is highly diverse in plant rhizospheres and is abundant in the global ocean, where it is expressed independently of phosphate availability. PafA therefore represents an important enzyme in the context of global biogeochemical cycling and has potential applications in sustainable agriculture.

Although nanomaterials have shown promising biomedical application potential, incomplete understanding of their molecular interactions with biological systems prevents their inclusion into mainstream clinical applications. Here we show that black phosphorus (BP) nanomaterials directly affect the cell cycle’s centrosome machinery. BP destabilizes mitotic centrosomes by attenuating the cohesion of pericentriolar material and consequently leads to centrosome fragmentation within mitosis. As a result, BP-treated cells exhibit multipolar spindles and mitotic delay, and ultimately undergo apoptosis. Mechanistically, BP compromises centrosome integrity by deactivating the centrosome kinase polo-like kinase 1 (PLK1). BP directly binds to PLK1, inducing its aggregation, decreasing its cytosolic mobility and eventually restricting its recruitment to centrosomes for activation. With this mechanism, BP nanomaterials show great anticancer potential in tumour xenografted mice. Together, our study reveals a molecular mechanism for the tumoricidal properties of BP and proposes a direction for biomedical application of nanomaterials by exploring their intrinsic bioactivities. Understanding the fundamental nano–bio interactions of nanomaterials intended for biomedical use might unlock potential alternative applications. Here the authors reveal a tumoricidal mechanism of black phosphorus nanomaterials where these nanomaterials directly affect the mitotic centrosome machinery by suppressing polo-like kinase 1, suggesting that nanomaterials can be applied in targeted cancer therapy with their intrinsic nano–bio properties.