Organic Phosphorus Cycling Research Articles

Soil Organic Phosphorus Cycling Around the Roots of a Native Grass in Two Contrasting Tropical Savannas

Soil Organic Phosphorus Cycling Around the Roots of a Native Grass in Two Contrasting Tropical Savannas

Organic phosphorus cycling may control grassland responses to nitrogen deposition: a long-term field manipulation and modelling study

Abstract. Ecosystems limited in phosphorous (P) are widespread, yet there is limited understanding of how these ecosystems may respond to anthropogenic deposition of nitrogen (N) and the interconnected effects on the biogeochemical cycling of carbon (C), N, and P. Here, we investigate the consequences of enhanced N addition for the C–N–P pools of two P-limited grasslands, one acidic and one limestone, occurring on contrasting soils, and we explore their responses to a long-term nutrient-manipulation experiment. We do this by combining data with an integrated C–N–P cycling model (N14CP). We explore the role of P-access mechanisms by allowing these to vary in the modelling framework and comparing model plant–soil C–N–P outputs to empirical data. Combinations of organic P access and inorganic P availability most closely representing empirical data were used to simulate the grasslands and quantify their temporal response to nutrient manipulation. The model suggested that access to organic P is a key determinant of grassland nutrient limitation and responses to experimental N and P manipulation. A high rate of organic P access allowed the acidic grassland to overcome N-induced P limitation, increasing biomass C input to soil and promoting soil organic carbon (SOC) sequestration in response to N addition. Conversely, poor accessibility of organic P for the limestone grassland meant N provision exacerbated P limitation and reduced biomass input to the soil, reducing soil carbon storage. Plant acquisition of organic P may therefore play an important role in reducing P limitation and determining responses to anthropogenic changes in nutrient availability. We conclude that grasslands differing in their access to organic P may respond to N deposition in contrasting ways, and where access is limited, soil organic carbon stocks could decline.

The wheat growth-promoting traits of Ochrobactrum and Pantoea species, responsible for solubilization of different P sources, are ensured by genes encoding enzymes of multiple P-releasing pathways

Production and release of organic acids and phosphatase enzymes by microbes are important for inorganic and organic phosphorus cycling in soil. The presence of microorganisms with corresponding traits in the plant rhizosphere lead to improved plant P uptake and ultimately growth promotion. We studied the potential of two rhizosphere-competent strains, Pantoea sp. MR1 and Ochrobactrum sp. SSR, for solubilization of different organic and inorganic P sources in vitro. In a pot experiment we further revealed the impact of the two strains on wheat seedling performance in soil amended with either phytate, rock phosphate or K2HPO4 as solely P source. To directly link P-solubilizing activity to the strain-specific genetic potential, we designed novel primers for glucose dehydrogenase (gcd), phosphatase (pho) and phytase (phy) genes, which are related to the organic and inorganic P solubilization potential. Quantitative tracing of these functional genes in the inoculated soils of the conducted pot experiment further allowed to compare strain abundances in the soil in dependency on the present P source. We observed strain- and P source-dependent patterns of the P solubilization in vitro as well as in the pot experiment, whereby P release, particularly from phytate, was linked to the strain abundance. We further revealed that the activity of microbial phosphatases is determined by the interplay between functional gene abundance, available soil P, and substrate availability. Moreover, positive impacts of microbial seed inoculation on wheat root architecture and aboveground growth parameters were observed. Our results suggest that screening for rhizosphere-competent strains with gcd, pho and phy genes may help to identify new microbial taxa that are able to solubilize and mineralize inorganic as well as organic bound P. Subsequently, the targeted use of corresponding strains may improve P availability in agricultural soils and consequently reduce fertilizer application.

Long-term farmyard manure application affects soil organic phosphorus cycling: A combined metagenomic and 33P/14C labelling study

Maintaining an adequate phosphorus (P) supply for plants and microorganisms is central to agricultural production; however, the long-term effects of organic manure and inorganic fertilizer application on soil P cycling remain unclear. Organic P cycling in a sandy loam soil receiving medium and high rates of farmyard manure (FYM) with and without mineral fertilisers was studied in a long-term field experiment with 14C/33P isotope labelling and metagenomic shotgun sequencing. FYM application alone negatively affected soil total P and organic P (Po) accumulation by enhancing crop offtake, enhancing Po mineralisation and stimulating P loss from the topsoil by reducing its P sorption potential. The P mineralisation/immobilisation rates detected by the 33P pool dilution method were significantly correlated with the abundance of microbial P cycling genes. Soil available C and N concentrations were related to gross P mineralisation/immobilisation rates and the abundance of P uptake/scavenging genes. Microbial genes related to P uptake and metabolism were more abundant than P scavenging genes, while P scavenging genes may work efficiently as both of them can sustain similar P mineralisation and immobilisation rates. The addition of FYM also promoted phosphatase activity reflecting the increased supply of Po in these soils. Our study demonstrates that long-term FYM application alters soil Po stocks and cycling, and that microbial functional gene abundance was coupled with P cycling rates.

Responses of alkaline phosphatase activity to wind-driven waves in a large, shallow lake: Implications for phosphorus availability and algal blooms

Phosphorus is a vital nutrient for algal growth, thus, a better understanding of phosphorus availability is essential to mitigate harmful algal blooms in lakes. Wind waves are a ubiquitous characteristic of lake ecosystems. However, its effects on the cycling of organic phosphorus and its usage by phytoplankton remain poorly elucidated in shallow eutrophic lakes. A mesocosm experiment was carried out to investigate the responses of alkaline phosphatase activity fractions to wind waves in large, shallow, eutrophic Lake Taihu. Results showed that wind-driven waves induced the release of alkaline phosphatase and phosphorus from the sediment, and dramatically enhanced phytoplanktonic alkaline phosphatase activity. However, compared to the calm conditions, bacterial and dissolved alkaline phosphatase activity decreased in wind-wave conditions. Consistently, the gene copies of Microcystis phoX increased but bacterial phoX decreased under wind-wave conditions. The ecological effects of these waves on phosphorus and phytoplankton likely accelerated the biogeochemical cycling of phosphorus and promoted phytoplankton production in Lake Taihu. This study provides an improved current understanding of phosphorus availability and the phosphorus strategies of plankton in shallow, eutrophic lakes.

Articles of Significant Interest in This Issue

Hyphae of phosphorus-solubilizing Penicillium strains are colonized by bacteria, which might affect their potential as biofertilizers to improve plant growth. Zhang et al. (e02969-19) investigated how different long-term soil fertilization regimes affected bacterial communities associating with P. canescens in soil. The hyphosphere community compositions varied with soil fertilization regime, and they had higher potential for nitrogen and organic phosphorus cycling than soil communities, in particular under low-P fertilization regimes. The high potentials might complement fungal phosphorus solubilization and improve fungal nitrogen nutrition, respectively. This work has relevance for the development of fungal-bacterial biofertilizer consortia for specific soil conditions.

Mobility and Bioavailability of Sediment Phosphorus in Urban Stormwater Ponds

AbstractStormwater ponds can serve as retention hotspots for phosphorus (P) moving out of the urban environment. This retention may be reduced by P speciation that reduces the bioavailability of P to primary producers and alters its mobility in sediments. Here we examined the mobility and fate of dissolved P in urban stormwater ponds with a set of complementary field measurements and short‐term laboratory and field experiments. We measured the types and amount of P in water column and sediments of urban stormwater ponds. We further assessed the mobility of different P types in pond sediments in the field and rates of P release from sediment cores maintained under laboratory conditions. Finally, we assessed P uptake rates by pond algal communities using short‐term bioassay experiments. We found that dissolved organic P was highly prevalent in urban pond water and sediments and that this type of P was mobile within sediments and could be released under high or low O2 conditions. We also found highly variable P demand by algae among stormwater ponds and that algal growth responses to P was correlated to water column N:P ratios. Altogether, our results indicate an important role for organic phosphorus cycling in urban stormwater ponds, which likely constrains the overall retention efficiency in these aquatic ecosystems.

On the history and future of soil organic phosphorus research: a critique across three generations

SummarySoil organic phosphorus has broad agronomic and ecological significance, but remains a neglected topic of research. This opinion paper reflects a collaborative discussion between three generations of scientists who have collectively studied soil organic phosphorus for almost 50 years. We discuss personal reflections on our involvement in the field, opinions about progress and promising opportunities for future research. We debate an apparent overemphasis on analytical methodology at the expense of broader questions, and whether this has stifled progress in recent decades. We reiterate the urgent need to understand organic phosphorus cycling in the environment to address fundamental questions about phosphate supply, crop nutrition, water quality and ecosystem ecology. We also contend that we must encourage and integrate the study of organic phosphorus across all scales, from molecular chemistry to global cycling. Our discussion among three generations of researchers shows the value of a long‐term perspective, emphasizes the changing nature of this field of research, and reinforces the importance of continuing to be curious about the dynamics of organic phosphorus in the environment.Highlights Critical evaluation of the current state of soil organic phosphorus research Collective views of three researchers whose careers span 50 years Research is driven by analytical development, but will benefit from broader conceptual approaches We emphasize the value of long‐term and broad‐scale perspectives on this important research topic

Screening and Characterization of Phytases from Bacteria Isolated from Chilean Hydrothermal Environments.

Phytases are enzymes involved in organic phosphorus cycling in nature and widely used as feed additives in animal diets. Thermal tolerance is a desired property of phytases. The objectives of this study were to screen and characterize bacterial phytases from Chilean hydrothermal environments. In this study, 60% (30 of 63) of screened thermophilic (60°C) isolates showed phytase activity in crude protein extracts. The characterization of phytase from two selected isolates (9B and 15C) revealed that both isolates produce phytases with a pH optimum at 5.0. The temperature optimum for phytate dephosphorylation was determined to be 60 and 50°C for the phytases from the isolates 9B and 15C, respectively. Interestingly, the phytase from the isolate 15C showed a residual activity of 46% after incubation at 90°C for 20min. The stepwise dephosphorylation of phytate by protein extracts of the isolates 9B and 15C was verified by HLPC analysis. Finally, the isolates 9B and 15C were identified by partial sequencing of the 16S rRNA gene as members of the genera Bacillus and Geobacillus, respectively.

Phylogenetic distribution, biogeography and the effects of land management upon bacterial non-specific Acid phosphatase Gene diversity and abundance

Background and aimsBacterial Non-Specific Acid Phosphatase (NSAP) enzymes are capable of dephosphorylating diverse organic phosphoesters but are rarely studied: their distribution in natural and managed environments is poorly understood. The aim of this study was to generate new insight into the environmental distribution of NSAPs and establish their potential global relevance to cycling of organic phosphorus.MethodsWe employed bioinformatic tools to determine NSAP diversity and subcellular localization in microbial genomes; used the corresponding NSAP gene sequences to census metagenomes from diverse ecosystems; studied the effect of long-term land management upon NSAP diversity and abundance.ResultsPeriplasmic class B NSAPs are poorly represented in marine and terrestrial environments, reflecting their association with enteric and pathogenic bacteria. Periplasmic class A and outer membrane-associated class C NSAPs are cosmopolitan. NSAPs are more abundant in marine than terrestrial ecosystems and class C more abundant than class A genes, except in an acidic peat where class A genes dominate. A clear effect of land management upon gene abundance was identified.ConclusionsNSAP genes are cosmopolitan. Class C genes are more widely distributed: their association with the outer-membrane of cells gives them a clear role in the cycling of organic phosphorus, particularly in soils.

Soil phoD and phoX alkaline phosphatase gene diversity responds to multiple environmental factors.

Alkaline phosphatases such as PhoD and PhoX are important in organic phosphorus cycling in soil. We identified the key organisms harboring the phoD and phoX genes in soil and explored the relationships between environmental factors and the phoD- and phoX-harboring community structures across three land uses located in arid to temperate climates on two continents using 454-sequencing. phoD was investigated using recently published primers, and new primers were designed to study phoX in soil. phoD was found in 1 archaeal, 13 bacterial and 2 fungal phyla, and phoX in 1 archaeal and 16 bacterial phyla. Dominant phoD-harboring phyla were Actinobacteria, Cyanobacteria, Deinococcus-Thermus, Firmicutes, Gemmatimonadetes, Planctomycetes and Proteobacteria, while abundant phoX-harboring phyla were Acidobacteria, Actinobacteria, Chloroflexi, Planctomycetes, Proteobacteria and Verrucomicrobia. Climate, soil group, land use and soil nutrient concentrations were the common environmental drivers of both community structures. In addition, the phoX-harboring community structure was affected by pH. Despite differences in environmental factors, the dominant phyla in the phoD-harboring community remained similar in all samples, while the composition of phoX differed substantially between the samples. This study shows that the composition of phoD and phoX is governed by the same environmental drivers but that phoD and phoX occur partly in different phyla.

Microbial Biomass and Community Composition Involved in Cycling of Organic Phosphorus in Sediments of Lake Dianchi, Southwest China

ABSTRACTOrganic phosphorus (Po) was a major fraction of phosphorus (P) in sediments of lakes, and microbes were involved in most of its relevant biogeochemical cycling. Forms and quantification of Po were investigated by sequential fractionation in 18 sediments of Lake Dianchi, Southwest China. Microbial biomass and community structure in these sediments were determined by phospholipid fatty acids (PLFAs). Distribution of Po fractions were in the rank order that humic Po > nucleic acid and polyphosphate > residual P > Ca-Al-Po > Fe-Po > sugar Po > acid soluble Po > H2O-Po. The recoveries of Po and Pi in these detailed sequential fractions including residual P shows that the total contents of Po in sediments of lakes were overestimated by the Standards, Measurements and Testing (SMT) protocol (ignition method). Microbial biomass including Gram-positive bacteria (14.4–20.0%), Gram-negative bacteria (32.7–38.4%), microeukaryotes (14.9–24.4%), aerobic bacteria (43.6–55.8%), anaerobic bacteria (0–2.9%) and type І methanotrophs (17.6–24.4%) were assigned. Microbial mass and their composition were strongly correlated with H2O-Po, Fe-Po, nucleic acid and polyphosphate, and humic Po, though residual P was likely inert for microbes in sediments. The formation and degradation of Po was closely related with microbial activities in sediments. These findings have implications for understanding the role of microbes on cycling of Po and organic matter in sediments of lakes.

Total and active microbial communities and phoD as affected by phosphate depletion and pH in soil

Soil microbial communities contribute to organic phosphorus cycling in a variety of ways, including secretion of the PhoD alkaline phosphatase. We sampled a long-term grassland fertilization trial in Switzerland characterized by a natural pH gradient. We examined the effects of phosphate depletion and pH on total and active microbial community structures and on the structure and composition of the total and active phoD-harboring community. Archaeal, bacterial and fungal communities were investigated using T-RFLP and phoD-harboring members of these communities were identified by 454-sequencing. Phosphate depletion decreased total, resin-extractable and organic phosphorus and changed the structure of all active microbial communities, and of the total archaeal and phoD-harboring communities. Organic carbon, nitrogen and phosphorus increased with pH, and the structures of all total and active microbial communities except the total fungal community differed between the two pH levels. phoD-harboring members were affiliated to Actinomycetales, Bacilliales, Gloeobacterales, Planctomycetales and Rhizobiales. Our results suggest that pH and associated soil factors are important determinants of microbial and phoD-harboring community structures. These associated factors include organic carbon and total nitrogen, and to a lesser degree phosphorus status, and active communities are more responsive than total communities. Key players in organic P mineralization are affiliated to phyla that are known to be important in organic matter decomposition.

The Behavior of Organic Phosphorus under Non-Point Source Wastewater in the Presence of Phototrophic Periphyton

To understand the role of ubiquitous phototrophic periphyton in aquatic ecosystem on the biogeochemical cycling of organic phosphorus, the conversion and removal kinetic characteristics of organic phosphorus (Porg) such as adenosine triphosphate (ATP) were investigated in the presence of the periphyton cultured in artificial non-point source wastewater. The preliminary results showed that the periphyton was very powerful in converting Porg evidenced by the fact that inorganic phosphorus (Pinorg) content in solution increased from about 0.7 to 14.3 mg P L−1 in 48 hours in the presence of 0.6 g L−1 periphyton. This was because the periphyton could produce abundant phosphatases that benefited the conversion of Porg to Pinrog. Moreover, this conversion process was described more suitable by the pseudo-first-order kinetic model. The periphyton was also effective in removing Porg, which showed that the Porg can be completely removed even when the initial Porg concentration was as high as 13 mg P L−1 in 48 hours in the presence of 1.6 g L−1 periphyton. Furthermore, it was found that biosorption dominated the Porg removal process and exhibited the characteristics of physical adsorption. However, this biosorption process by the periphyton was significantly influenced by biomass (absorbent dosage) and temperature. This work provides insights into Porg biogeochemical circulation of aquatic ecosystem that contained the periphyton or similar microbial aggregates.

Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres

Despite similar physical properties, the Northern and Southern Atlantic subtropical gyres have different biogeochemical regimes. The Northern subtropical gyre, which is subject to iron deposition from Saharan dust1, is depleted in the nutrient phosphate, possibly as a result of iron-enhanced nitrogen fixation2. Although phosphate depleted, rates of carbon fixation in the euphotic zone of the North Atlantic subtropical gyre are comparable to those of the South Atlantic subtropical gyre3, which is not phosphate limited. Here we use the activity of the phosphorus-specific enzyme alkaline phosphatase to show potentially enhanced utilization of dissolved organic phosphorus occurring over much of the North Atlantic subtropical gyre. We find that during the boreal spring up to 30% of primary production in the North Atlantic gyre is supported by dissolved organic phosphorus. Our diagnostics and composite map of the surface distribution of dissolved organic phosphorus in the subtropical Atlantic Ocean reveal shorter residence times in the North Atlantic gyre than the South Atlantic gyre. We interpret the asymmetry of dissolved organic phosphorus cycling in the two gyres as a consequence of enhanced nitrogen fixation in the North Atlantic Ocean4, which forces the system towards phosphorus limitation. We suggest that dissolved organic phosphorus utilization may contribute to primary production in other phosphorus-limited ocean settings as well.

Fatores que afetam a disponibilidade do fósforo e o manejo da adubação fosfatada em solos sob sistema plantio direto

A compreensão dos fenômenos básicos da dinâmica do fósforo no solo é importante para a tomada de decisão sobre a necessidade de adição e para a definição das doses e dos modos de aplicação de fertilizantes fosfatados. As formas e o grau de labilidade do fósforo variam com as características e propriedades do solo. Em solos jovens, os fosfatos de cálcio são os principais fornecedores de fósforo aos organismos vivos. Por outro lado, em solos altamente intemperizados, a biociclagem dos fosfatos orgânicos assume grande importância na manutenção da biodisponibilidade, embora não seja suficiente para a obtenção da máxima produtividade econômica das culturas comerciais. Nos solos tropicais e subtropicais cultivados, o controle dos teores de fósforo em solução é feito predominantemente pelo fosfato adsorvido aos grupos funcionais dos colóides inorgânicos. O diagnóstico da disponibilidade de fósforo é feito pela análise de solos por diferentes metodologias, cada uma com suas vantagens e limitações. A tomada de decisão em adicionar ou não fosfatos ao solo e a definição da dose a ser aplicada dependem muito mais da calibração, baseada na relação entre os teores de fósforo extraídos e a produtividade das plantas, do que do método de extração. A elevação dos níveis de disponibilidade de fósforo até a faixa ótima pode ser feita de forma corretiva ou gradativa. A adubação corretiva com incorporação em todo o volume de solo é mais eficiente e, talvez, a única alternativa para a correção da carência de fósforo do solo das camadas subsuperficias. A aplicação superficial de fertilizantes fosfatados no sistema plantio direto parece não ser uma boa alternativa econômica e pode se tornar um problema ambiental. Desse modo, devem-se intensificar as pesquisas enfocando, entre outras: (a) as frações de fósforo no solo e a produtividade das culturas; (b) as formas de aplicação dos fertilizantes fosfatados no solo sob sistema plantio direto; (c) as relações entre a disponibilidade de fósforo nas camadas subsuperficiais (abaixo de 10cm), a presença de alumínio trocável e de camadas compactadas e (d) o monitoramento constante das transferências de fósforo dos solos aos sistemas aquáticos.

Phosphonates and particulate organic phosphorus cycling in an anoxic marine basin

Total particulate phosphorus (TPP), particulate inorganic P (PIP), and particulate organic P (POP) concentrations were measured in a year‐long series of sediment trap samples collected throughout the oxic‐anoxic water column (275 m, 455 m, 930 m, and 1,255 m) of the Cariaco Basin. TPP, PIP, and POP fluxes varied seasonally and decreased significantly with depth, from 65 to 19 µmol TPP m−2 d−1, 43 to 8 µmol PIP m−2 d−1, and 22 to 11 µmol POP m−2 d−1. Significant flux relationships (p < 0.001) were found between POP and particulate organic carbon (POC) and particulate organic nitrogen (PON). The lack of a relationship between POC and PIP fluxes and the large fraction of TPP associated with the PIP pool in both oxic and anoxic traps suggests that future analyses must separate PIP and POP when evaluating biological relationships between C, N, and P. The strong relationships between POC, PON, and POP also suggest that POP is not preferentially remineralized relative to PON and POC with increasing depth in this anoxic environment. P composition was also determined using solid state 31P nuclear magnetic resonance (NMR), and it was found that phosphonates, chemically and thermally inert compounds, are a significant fraction of the TPP pool. Furthermore, these compounds were preferentially removed relative to more bioavailable P esters during a low flux event. Their selective removal suggests that these compounds may be an unrecognized source of bioavailable P under anoxic conditions.

Marine organic phosphorus cycling; novel insights from nuclear magnetic resonance

In vast regions of the ocean, a significant fraction of the vital nutrient phosphorus (P) in surface waters is associated with dissolved organic matter (DOM). Oceanic biological productivity in these regions is potentially dependent on the regeneration of bioavailable forms of P from DOM. Using tangential-flow ultrafiltration, high molecular weight (HMW) DOM samples were collected for chemical analysis and 31 P Nuclear Magnetic Resonance (NMR) studies. In a profile of HMW DOP from the Pacific, depth related changes in dissolved organic P (DOP) concentration and C/N/P ratios indicate that DOP is preferentially regenerated from HMW DOM relative to dissolved organic car- bon and dissolved organic nitrogen. NMR studies of these samples show that P esters (75 percent) and phosphonates (25 percent) were the major compound classes present in HMW DOP. HMW DOP appears to be highly enriched in phosphonates relative to marine organisms, where phosphonates comprise a very small fraction of total P. The origin of phosphonates in the marine environ- ment is largely unknown, and the biogeochemical dynamics by which phospho- nates become a major fraction of HMW DOP are not well understood. To explore possible sources of phosphonates in the marine environment, HMW DOM and particulate organic matter (POM) from cultures of four marine primary produc- ers, as well as particulates from heterotrophic bacterial cultures, were examined by 31 P NMR. P esters were observed in all cultures, and phosphonates were detected in only two of the heterotrophic bacterial cultures. Several processes may be acting to produce the observed abundance of phosphonate-P in marine HMW DOP, including (1) selective preservation of phosphonates, and (2) produc- tion by an unrecognized source of phosphonates.

Rhizosphere phosphatase activity and phosphatase hydrolyzable organic phosphorus in two forested spodosols

The cycling of organic phosphorus has a large effect on P availability in forest ecosystems. Organic P must be hydrolyzed to inorganic P before it can be utilized by plants. We examined the acid phosphatase activity in the rhizosphere of slash pine (Pinus elliottii) growing in A and Bh horizon soil from two forested Spodosols; and determined the amount of soluble organic P in these soils that could be hydrolyzed following the addition of an acid phosphomonoesterase. Significant acid phosphatase activity was observed in the A and Bh horizons of the two soils. Acid phosphatase activity was greater in the rhizosphere of the Leon A and Bh horizons and the Pomona Bh horizon soil. Phosphorus fertilization decreased the phosphatase activity in the rhizosphere soil. Soluble organic P comprised 15–25% of the total soluble P in the two A horizon soils and over 75% in the Bh horizon soils. Between 20 and 30% of the water-soluble organic P in the A and Bh horizons of the two soils was hydrolyzed when an acid phosphomonoesterase was added. Our results suggest that organic P may contribute to the P nutrition of slash pine growing on these soils.