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Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities

A Correction to this article was published on 02 December 2017

This article has been updated

Abstract

Background

The dynamics of phosphorus (P) in the environment is important for regulating nutrient cycles in natural and managed ecosystems and an integral part in assessing biological resilience against environmental change. Organic P (Po) compounds play key roles in biological and ecosystems function in the terrestrial environment being critical to cell function, growth and reproduction.

Scope

We asked a group of experts to consider the global issues associated with Po in the terrestrial environment, methodological strengths and weaknesses, benefits to be gained from understanding the Po cycle, and to set priorities for Po research.

Conclusions

We identified seven key opportunities for Po research including: the need for integrated, quality controlled and functionally based methodologies; assessment of stoichiometry with other elements in organic matter; understanding the dynamics of Po in natural and managed systems; the role of microorganisms in controlling Po cycles; the implications of nanoparticles in the environment and the need for better modelling and communication of the research. Each priority is discussed and a statement of intent for the Po research community is made that highlights there are key contributions to be made toward understanding biogeochemical cycles, dynamics and function of natural ecosystems and the management of agricultural systems.

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Fig. 1

Change history

  • 02 December 2017

    The article “Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities”, written by Timothy S George et al., was originally published with incorrect affiliation information for one of the co-authors, E. Klumpp.

Abbreviations

δ18OP:

Oxygen-18 isotope ratio

16S rRNA:

16S ribosomal Ribonucleic acid

Al:

Aluminium

ATP:

Adenosine triphosphate

C:

Carbon

DNA:

Deoxyribonucleic acid

Fe:

Iron

N:

Nitrogen

P:

Phosphorus

Pho:

Pho regulon transcription factors

Pi :

Inorganic orthophosphate

Po :

Organic phosphorus compounds

S:

Sulphur

References

  • Abdi D, Cade-Menun BJ, Ziadi N, Parent L-É (2014) Long-term impact of tillage practices and phosphorus fertilization on soil phosphorus forms as determined by 31P nuclear magnetic resonance spectroscopy. J Environ Qual 43:1431–1441. https://doi.org/10.2134/jeq2013.10.0424

    PubMed  CAS  Article  Google Scholar 

  • Abdi D, Cade-Menun BJ, Ziadi N, Tremblay GF, Parent LÉ (2016) Visible near infrared reflectance spectroscopy to predict soil phosphorus pools in chernozems of Saskatchewan, Canada. Geoderma Region 7:93–101

    Article  Google Scholar 

  • Adeloju S, Webb B, Smernik R (2016) Phosphorus distribution in soils from Australian dairy and beef rearing pastoral systems. Appl Sci 6:31

    Article  Google Scholar 

  • Ahlgren J, Djodjic F, Börjesson G, Mattsson L (2013) Identification and quantification of organic phosphorus forms in soils from fertility experiments. Soil Use Manag 29:24–35. https://doi.org/10.1111/sum.12014

    Article  Google Scholar 

  • Alegria-Terrazas R, Giles CD, Paterson E, Robertson-Albertyn S, Cesco S, Mimmo T, Pii Y, Bulgarelli D (2016) Plant-microbiota interactions as a driver of the mineral turnover in the rhizosphere. Adv Appl Microbiol. Springer

  • Annaheim KE, Doolette AL, Smernik RJ, Mayer J, Oberson A, Frossard E, Bünemann EK (2015) Long-term addition of organic fertilizers has little effect on soil organic phosphorus as characterized by 31P NMR spectroscopy and enzyme additions. Geoderma 257–258:67–77. https://doi.org/10.1016/j.geoderma.2015.01.014

    CAS  Article  Google Scholar 

  • Attiwill PM, Adams MA (1993) Nutrient cycling in forests. New Phytol 124:561–582. https://doi.org/10.1111/j.1469-8137.1993.tb03847.x

    CAS  Article  Google Scholar 

  • Bergkemper F, Bünemann EK, Hauenstein S, Heuck C, Kandeler E, Krüger J, Marhan S, Mészáros É, Nassal D, Nassal P, Oelmann Y, Pistocchi C, Schloter M, Spohn M, Talkner U, Zederer DP, Schulz S (2016) An inter-laboratory comparison of gaseous and liquid fumigation based methods for measuring microbial phosphorus (Pmic) in forest soils with differing P stocks. J Microbiol Methods 128:66–68. https://doi.org/10.1016/j.mimet.2016.07.006

    PubMed  CAS  Article  Google Scholar 

  • Bol R, Julich D, Brödlin D, Siemens J, Kaiser K, Dippold MA, Spielvogel S, Zilla T, Mewes D, von Blanckenburg F, Puhlmann H, Holzmann S, Weiler M, Amelung W, Lang F, Kuzyakov Y, Feger K-H, Gottselig N, Klumpp E, Missong A, Winkelmann C, Uhlig D, Sohrt J, von Wilpert K, Wu B, Hagedorn F (2016) Dissolved and colloidal phosphorus fluxes in forest ecosystems—an almost blind spot in ecosystem research. J Plant Nutr Soil Sci 179:425–438. https://doi.org/10.1002/jpln.201600079

    CAS  Article  Google Scholar 

  • Borda T, Celi L, Zavattaro L, Sacco D, Barberis E (2011) Effect of agronomic management on risk of suspended solids and phosphorus losses from soil to waters. J Soils Seds 11:440–451. https://doi.org/10.1007/s11368-010-0327-y

    CAS  Article  Google Scholar 

  • Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329. https://doi.org/10.1016/0038-0717(82)90001-3

    CAS  Article  Google Scholar 

  • Brookes PC, Powlson DS, Jenkinson DS (1984) Phosphorus in the soil microbial biomass. Soil Biol Biochem 16:169–175. https://doi.org/10.1016/0038-0717(84)90108-1

    CAS  Article  Google Scholar 

  • Bünemann EK (2015) Assessment of gross and net mineralization rates of soil organic phosphorus – a review. Soil Biology Biochem 89:82–98. https://doi.org/10.1016/j.soilbio.2015.06.026

    CAS  Article  Google Scholar 

  • Butusov M, Jernelöv A (2013) Phosphorus in the organic life: cells, tissues, organisms. Phosphorus: An Element that could have been called Lucifer. Springer New York, New York

  • Cade-Menun BJ (2005) Characterizing phosphorus in environmental and agricultural samples by 31 P nuclear magnetic resonance spectroscopy. Talanta 66:359–371

    PubMed  CAS  Article  Google Scholar 

  • Cade-Menun B, Liu CW (2014) Solution phosphorus-31 nuclear magnetic resonance spectroscopy of soils from 2005 to 2013: a review of sample preparation and experimental parameters. Soil Sci Soc Am J 78:19–37. https://doi.org/10.2136/sssaj2013.05.0187dgs

    CAS  Article  Google Scholar 

  • Cade-Menun BJ, Turner B, Frossard E, Baldwin D (2005) Using phosphorus-31 nuclear magnetic resonance spectroscopy to characterize organic phosphorus in environmental samples. Org Phosphorus Environ:21–44

  • Cade-Menun BJ, He Z, Zhang H, Endale DM, Schomberg HH, Liu CW (2015) Stratification of phosphorus forms from long-term conservation tillage and poultry litter application. Soil Sci Soc Am J 79:504–516. https://doi.org/10.2136/sssaj2014.08.0310

    CAS  Article  Google Scholar 

  • Celi L, Barberis E (2005) Abiotic stabilization of organic phosphorus in the environment. Org Phosphorus Environ CABI Pub pp 113–132

  • Celi L, Barberis E (2007) Abiotic reactions of inositol phosphates in soils. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Oxfordshire

    Google Scholar 

  • Celi L, De Luca G, Barberis E (2003) Effects of interaction of organic and inorganic P with ferrihydrite and kaolinite-iron oxide systems on iron release. Soil Sci 168:479–488

    CAS  Google Scholar 

  • Chardon WJ, Oenema O (1995) Leaching of dissolved organically bound phosphorus. DLO Research Institute for Agrobiology and Soil Fertility

  • Chardon WJ, Oenema O, del Castilho P, Vriesema R, Japenga J, Blaauw D (1997) Organic phosphorus in solutions and leachates from soils treated with animal slurries. J Environ Q 26:372–378

    CAS  Article  Google Scholar 

  • Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochem 85:235–252. https://doi.org/10.1007/s10533-007-9132-0

    Article  Google Scholar 

  • Condron LM, Newman S (2011) Revisiting the fundamentals of phosphorus fractionation of sediments and soils. J Soils Seds 11:830–840. https://doi.org/10.1007/s11368-011-0363-2

    CAS  Article  Google Scholar 

  • Courty P-E, Franc A, Garbaye J (2010) Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community. Soil Biol Biochem 42:2022–2025. https://doi.org/10.1016/j.soilbio.2010.07.014

    CAS  Article  Google Scholar 

  • Cui H, Zhou Y, Gu Z, Zhu H, Fu S, Yao Q (2015) The combined effects of cover crops and symbiotic microbes on phosphatase gene and organic phosphorus hydrolysis in subtropical orchard soils. Soil Biol Biochem 82:119–126. https://doi.org/10.1016/j.soilbio.2015.01.003

    CAS  Article  Google Scholar 

  • Darch T, Blackwell MSA, Hawkins JMB, Haygarth PM, Chadwick D (2014) A meta-analysis of organic and inorganic phosphorus in organic fertilizers, soils, and water: implications for water quality. Crit Rev Environ Sci Technol 44:2172–2202. https://doi.org/10.1080/10643389.2013.790752

    CAS  Article  Google Scholar 

  • Dauner M, Storni T, Sauer U (2001) Bacillus Subtilis metabolism and energetics in carbon-limited and excess-carbon Chemostat culture. J Bacteriol 183:7308–7317. https://doi.org/10.1128/JB.183.24.7308-7317.2001

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • de Oliveira CMB, Erich MS, Gatiboni LC, Ohno T (2015) Phosphorus fractions and organic matter chemistry under different land use on humic Cambisols in southern Brazil. Geoderma Regional 5:140–149. https://doi.org/10.1016/j.geodrs.2015.06.001

    Article  Google Scholar 

  • Di HJ, Cameron KC, McLaren RG (2000) Isotopic dilution methods to determine the gross transformation rates of nitrogen, phosphorus, and sulfur in soil: a review of the theory, methodologies, and limitations. Soil Res 38:213–230. https://doi.org/10.1071/SR99005

    CAS  Article  Google Scholar 

  • Dodd RJ, Sharpley AN (2015) Recognizing the role of soil organic phosphorus in soil fertility and water quality. Res Conserv Recycl 105(part B):282–293. https://doi.org/10.1016/j.resconrec.2015.10.001

    Article  Google Scholar 

  • Doolette AL, Smernik RJ (2011) Soil organic phosphorus speciation using spectroscopic techniques. In: Phosphorus in action. Springer, Berlin Heidelberg, pp 3–36

    Chapter  Google Scholar 

  • Duff SM, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800

    CAS  Article  Google Scholar 

  • Dyhrman ST, Chappell PD, Haley ST, Moffett JW, Orchard ED, Waterbury JB, Webb EA (2006) Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439:68

    PubMed  CAS  Article  Google Scholar 

  • Ebuele VO, Santoro A, Thoss V (2016) Phosphorus speciation by 31P NMR spectroscopy in bracken (Pteridium Aquilinum (L.) Kuhn) and bluebell (Hyacinthoides non-Scripta (L.) Chouard ex Rothm.) dominated semi-natural upland soil. Sci Tot Environ 566–567:1318–1328. https://doi.org/10.1016/j.scitotenv.2016.05.192

    CAS  Article  Google Scholar 

  • Espinosa M, Turner B, Haygarth P (1999) Preconcentration and separation of trace phosphorus compounds in soil leachate. J. Environ Q 28:1497–1504

    CAS  Article  Google Scholar 

  • Food and Agricultural Organization of the United Nations (2016). Research and Extension http://www.fao.org/nr/research-extension-systems/res-home/en/. Date Accessed: 13 October 2016

  • Fraser T, Lynch DH, Entz MH, Dunfield KE (2015) Linking alkaline phosphatase activity with bacterial phoD gene abundance in soil from a long-term management trial. Geoderma 257–258:115–122. https://doi.org/10.1016/j.geoderma.2014.10.016

    CAS  Article  Google Scholar 

  • Fraser TD, Lynch DH, Gaiero J, Khosla K, Dunfield KE (2017) Quantification of bacterial non-specific acid (phoC) and alkaline (phoD) phosphatase genes in bulk and rhizosphere soil from organically managed soybean fields. Appl Soil Ecol 111:48–56

    Article  Google Scholar 

  • Frossard E, Achat DL, Bernasconi SM, Bünemann EK, Fardeau J-C, Jansa J, Morel C, Rabeharisoa L, Randriamanantsoa L, Sinaj S, Tamburini F, Oberson A (2011) The use of tracers to investigate phosphate cycling in soil–plant systems. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer Berlin Heidelberg, Berlin, Heidelberg

    Google Scholar 

  • Frossard E, Buchmann N, Bünemann EK, Kiba DI, Lompo F, Oberson A, Tamburini F, Traoré OY (2015) Soil properties and not inputs control carbon, nitrogen, phosphorus ratios in cropped soils in the long-term. Soil Discuss 2:995–1038

    Article  Google Scholar 

  • Gaind S, Singh YV (2016) Soil organic phosphorus fractions in response to long-term fertilization with composted manures under rice–wheat cropping system. J Plant Nutri 39:1336–1347. https://doi.org/10.1080/01904167.2015.1086795

    CAS  Article  Google Scholar 

  • George TS, Simpson RJ, Gregory PJ, Richardson AE (2007) Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates. Soil Biol Biochem 39:793–803

    CAS  Article  Google Scholar 

  • Giaveno C, Celi L, Richardson AE, Simpson RJ, Barberis E (2010) Interaction of phytases with minerals and availability of substrate affect the hydrolysis of inositol phosphates. Soil Biol Biochem 42:491–498. https://doi.org/10.1016/j.soilbio.2009.12.002

    CAS  Article  Google Scholar 

  • Godwin CM, Cotner JB (2015) Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J 9:2324–2327. https://doi.org/10.1038/ismej.2015.34

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • Gottselig N, Bol R, Nischwitz V, Vereecken H, Amelung W, Klumpp E (2014) Distribution of phosphorus-containing fine colloids and nanoparticles in stream water of a Forest catchment. Vadose Zone J 13. https://doi.org/10.2136/vzj2014.01.0005

  • Harrison AF (1982) 32P-method to compare rates of mineralization of labile organic phosphorus in woodland soils. Soil Biol Biochem 14:337–341. https://doi.org/10.1016/0038-0717(82)90003-7

    CAS  Article  Google Scholar 

  • Haygarth PM, Jarvie HP, Powers SM, Sharpley AN, Elser JJ, Shen J, Peterson HM, Chan NI, Howden NJ, Burt T, Worrall F, Zhang F, Liu X (2014) Sustainable phosphorus management and the need for a long-term perspective: the legacy hypothesis. Environ Sci Technol 48:8417–8419. https://doi.org/10.1021/es502852s

    PubMed  CAS  Article  Google Scholar 

  • Hedley MJ, Stewart JWB, Chauhuan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–976

    CAS  Article  Google Scholar 

  • Jarosch KA, Doolette AL, Smernik RJ, Tamburini F, Frossard E, Bünemann EK (2015) Characterisation of soil organic phosphorus in NaOH-EDTA extracts: a comparison of 31 P NMR spectroscopy and enzyme addition assays. Soil Biol Biochem 91:298–309

    CAS  Article  Google Scholar 

  • Jaspers E, Overmann J (2004) Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 70:4831–4839. https://doi.org/10.1128/AEM.70.8.4831-4839.2004

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • Jiang X, Bol R, Willbold S, Vereecken H, Klumpp E (2015) Speciation and distribution of P associated with Fe and al oxides in aggregate-sized fraction of an arable soil. Biogeosciences 12:6443–6452. https://doi.org/10.5194/bg-12-6443-2015

    Article  Google Scholar 

  • Keller M, Oberson A, Annaheim KE, Tamburini F, Mäder P, Mayer J, Frossard E, Bünemann EK (2012) Phosphorus forms and enzymatic hydrolyzability of organic phosphorus in soils after 30 years of organic and conventional farming. J Plant Nutr Soil Sci 175:385–393. https://doi.org/10.1002/jpln.201100177

    CAS  Article  Google Scholar 

  • Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155:974–987. https://doi.org/10.1104/pp.110.164640

    PubMed  CAS  Article  Google Scholar 

  • Lang F, Bauhus J, Frossard E, George E, Kaiser K, Kaupenjohann M, Krüger J, Matzner E, Polle A, Prietzel J, Rennenberg H, Wellbrock N (2016) Phosphorus in forest ecosystems: new insights from an ecosystem nutrition perspective. J Plant Nutri Soil Sci 179:129–135. https://doi.org/10.1002/jpln.201500541

    CAS  Article  Google Scholar 

  • Lim BL, Yeung P, Cheng C, Hill JE (2007) Distribution and diversity of phytate-mineralizing bacteria. ISME 1:321–330. https://doi.org/10.1038/ismej.2007.40

    CAS  Article  Google Scholar 

  • Liu R, Lal R (2015) Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Sci Total Environ 514:131–139. https://doi.org/10.1016/j.scitotenv.2015.01.104

    PubMed  CAS  Article  Google Scholar 

  • Liu J, Yang J, Cade-Menun BJ, Liang X, Hu Y, Liu CW, Zhao Y, Li L, Shi J (2013) Complementary phosphorus speciation in agricultural soils by sequential fractionation, solution 31P nuclear magnetic resonance, and phosphorus K-edge X-ray absorption near-edge structure spectroscopy. J Environ Qual 42:1763–1770. https://doi.org/10.2134/jeq2013.04.0127

    PubMed  CAS  Article  Google Scholar 

  • Liu J, Hu Y, Yang J, Abdi D, Cade-Menun BJ (2014) Investigation of soil legacy phosphorus transformation in long-term agricultural fields using sequential fractionation, P K-edge XANES and solution P NMR spectroscopy. Environ Sci & Tech 49:168–176

    Article  Google Scholar 

  • Liu J, Hu Y, Yang J, Abdi D, Cade-Menun BJ (2015) Investigation of soil legacy phosphorus transformation in long-term agricultural fields using sequential fractionation, P K-edge XANES and solution P NMR spectroscopy. Environ Sci Technol 49:168–176. https://doi.org/10.1021/es504420n

    PubMed  CAS  Article  Google Scholar 

  • Luo H, Benner R, Long RA, Hu J (2009) Subcellular localization of marine bacterial alkaline phosphatases. PNAS 106:21249–21223

    Google Scholar 

  • Magid J, Tiessen H, Condron LM (1996) Humic substances in terrestrial ecosystems. In: Piccolo A (ed) Dynamics of organic phosphorus in soils under natural and agricultural ecosystems. Elsevier Science, Amsterdam

    Chapter  Google Scholar 

  • Magnacca G, Allera A, Montoneri E, Celi L, Benito DE, Gagliardi LG, Gonzalez MC, Mártire DO, Carlos L (2014) Novel magnetite nanoparticles coated with waste-sourced biobased substances as sustainable and renewable adsorbing materials. ACS Sustain Chem Eng 2:1518–1524. https://doi.org/10.1021/sc500213j

    CAS  Article  Google Scholar 

  • McGill WB, Cole CV (1981) Compartive aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–286

    CAS  Article  Google Scholar 

  • Mueller CW, Kölbl A, Hoeschen C, Hillion F, Heister K, Herrmann AM, Kögel-Knabner I (2012) Submicron scale imaging of soil organic matter dynamics using NanoSIMS–from single particles to intact aggregates. Org Geochem 42:1476–1488

    Article  Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer Berlin Heidelberg, Berlin, Heidelberg

    Google Scholar 

  • Nash DM, Haygarth PM, Turner BL, Condron LM, McDowell RW, Richardson AE, Watkins M, Heaven MW (2014) Using organic phosphorus to sustain pasture productivity: a perspective. Geoderma 221:11–19. https://doi.org/10.1016/j.geoderma.2013.12.004

    CAS  Article  Google Scholar 

  • Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract pseudomonas putida to the rhizosphere. PLoS One 7:e35498. https://doi.org/10.1371/journal.pone.0035498

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • Neal AL, Rossman M, Brearley C, Akkari E, Guyomar C, Clark IM, Allen E (2017) Hirsch PR (2017) land-use influences phosphatase gene microdiversity. Environ Microbiol. https://doi.org/10.1111/1462-2920.13778

  • Negassa W, Leinweber P (2009) How does the Hedley sequential phosphorus fractionation reflect impacts of land use and management on soil phosphorus: a review. J Plant Nutr Soil Sci 172:305–325. https://doi.org/10.1002/jpln.200800223

    CAS  Article  Google Scholar 

  • Nisticò R, Evon P, Labonne L, Vaca-Medina G, Montoneri E, Francavilla M, Vaca-Garcia C, Magnacca G, Franzoso F, Negre M (2016) Extruded poly(ethylene–co–vinyl alcohol) composite films containing biopolymers isolated from municipal biowaste. Chem Select 1:2354–2365. https://doi.org/10.1002/slct.201600335

    CAS  Article  Google Scholar 

  • Plassard C, Louche J, Ali MA, Duchemin M, Legname E, Cloutier-Hurteau B (2011) Diversity in phosphorus mobilisation and uptake in ectomycorrhizal fungi. Ann Forest Sci 68:33–43. https://doi.org/10.1007/s13595-010-0005-7

    Article  Google Scholar 

  • Powers SM, Bruulsema TW, Burt TP, Chan NI, Elser JJ, Haygarth PM, Howden NJK, Jarvie HP, Lyu Y, Peterson HM, Sharpley AN, Shen J, Worrall F, Zhang F (2016) Long-term accumulation and transport of anthropogenic phosphorus in three river basins. Nat Geosci 9:353–356. https://doi.org/10.1038/ngeo2693

    CAS  Article  Google Scholar 

  • Ragot SA, Kertesz MA, Bünemann EK (2015) phoD alkaline phosphatase gene diversity in soil. Appl Environ Microbiol 81:7281–7289. https://doi.org/10.1128/aem.01823-15

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • Ragot SA, Kertesz MA, Mészáros É, Frossard E, Bünemann EK. (2016) Soil phoD and phoX alkaline phosphatase gene diversity responds to multiple environmental factors. FEMS microbiology ecology. 93:fiw212

  • Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46:230A–2221

    Google Scholar 

  • Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimise access to soil phosphorus. Crop Past Sci 60:124–143

    CAS  Article  Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156. https://doi.org/10.1007/s11104-011-0950-4

    CAS  Article  Google Scholar 

  • Rosemarin A, Ekane N (2015) The governance gap surrounding phosphorus. Nutri Cycl Agroecosys:1–15. https://doi.org/10.1007/s10705-015-9747-9

  • Rosling A, Midgley MG, Cheeke T, Urbina H, Fransson P, Phillips RP (2016) Phosphorus cycling in deciduous forest soil differs between stands dominated by ecto- and arbuscular mycorrhizal trees. New Phytol 209:1184–1195. https://doi.org/10.1111/nph.13720

    PubMed  Article  Google Scholar 

  • Runge-Metzger A (1995) Closing the cycle: obstacles to efficient P management for improved global food security. Scope-Scientific Committee on Problems of the Environment International Council of Scientific Unions 54: 27–42

  • Santos-Beneit F (2015) The pho regulon: a huge regulatory network in bacteria. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.00402

  • Schneider KD, Cade-Menun BJ, Lynch DH, Voroney RP (2016) Soil phosphorus forms from organic and conventional forage fields. Soil Sci Soc Am J 80:328–340. https://doi.org/10.2136/sssaj2015.09.0340

    CAS  Article  Google Scholar 

  • Sebastian M, Ammerman JW (2009) The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME 3:563–572. https://doi.org/10.1038/ismej.2009.10

    CAS  Article  Google Scholar 

  • Secco D, Wang C, Shou H, Whelan J (2012) Phosphate homeostasis in the yeast Saccharomyces Cerevisiae, the key role of the SPX domain-containing proteins. FEBS Lett 586:289–295. https://doi.org/10.1016/j.febslet.2012.01.036

    PubMed  CAS  Article  Google Scholar 

  • Sharma R, Bella RW, Wong MTF (2017) Dissolved reactive phosphorus played a limited role in phosphorus transport via runoff, throughflow and leaching on contrasting cropping soils from southwest Australia. Sci Tot Env 577:33–44

    CAS  Article  Google Scholar 

  • Sharpley AN, Bergström L, Aronsson H, Bechmann M, Bolster CH, Börling K, Djodjic F, Jarvie HP, Schoumans OF, Stamm C, Tonderski KS, Ulén B, Uusitalo R, Withers PJA (2015) Future agriculture with minimized phosphorus losses to waters: research needs and direction. Ambio 44:163–179. https://doi.org/10.1007/s13280-014-0612-x

    PubMed Central  CAS  Article  Google Scholar 

  • Slazak A, Freese D, da Silva ME, Hüttl RF (2010) Soil organic phosphorus fraction in pine–oak forest stands in northeastern Germany. Geoderma 158:156–162

    CAS  Article  Google Scholar 

  • Spohn M, Kuzyakov Y (2013) Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation – coupling soil zymography with 14C imaging. Soil Biol Biochem 67:106–113. https://doi.org/10.1016/j.soilbio.2013.08.015

    CAS  Article  Google Scholar 

  • Stewart JWB, Tiessen H (1987) Dynamics of soil organic phosphorus. Biogeochem 4:41–60. https://doi.org/10.1007/bf02187361

    CAS  Article  Google Scholar 

  • Stutter MI, Shand CA, George TS, Blackwell MSA, Bol R, MacKay RL, Richardson AE, Condron LM, Turner BL, Haygarth PM (2012) Recovering phosphorus from soil: a root solution? Environ Sci Technol 46:1977–1978. https://doi.org/10.1021/es2044745

    PubMed  CAS  Article  Google Scholar 

  • Stutter MI, Shand CA, George TS, Blackwell MSA, Dixon L, Bol R, MacKay RL, Richardson AE, Condron LM, Haygarth PM (2015) Land use and soil factors affecting accumulation of phosphorus species in temperate soils. Geoderma 257–258:29–39. https://doi.org/10.1016/j.geoderma.2015.03.020

    CAS  Article  Google Scholar 

  • Tamburini F, Pfahler V, von Sperber C, Frossard E, Bernasconi SM (2014) Oxygen isotopes for unraveling phosphorus transformations in the soil–plant system: a review. Soil Sci Soc Am J 78:38–46. https://doi.org/10.2136/sssaj2013.05.0186dgs

    CAS  Article  Google Scholar 

  • Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A, Griffiths B, O’Gara F (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fertil Soils 49:661–672. https://doi.org/10.1007/s00374-012-0755-5

    CAS  Article  Google Scholar 

  • Tate KR, Salcedo I (1988) Phosphorus control of soil organic matter accumulation and cycling. Biogeochem 5:99–107. https://doi.org/10.1007/bf02180319

    CAS  Article  Google Scholar 

  • Tipping E, Somerville CJ, Luster J (2016) The C:N:P:S stoichiometry of soil organic matter. Biogeochem 130:117–131. https://doi.org/10.1007/s10533-016-0247-z

    CAS  Article  Google Scholar 

  • Tkacz A, Cheema J, Chandra G, Grant A, Poole PS (2015) Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition. ISME J 9:2349–2359. https://doi.org/10.1038/ismej.2015.41

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • Toor GS, Condron LM, Di HJ, Cameron KC, Cade-Menun BJ (2003) Characterization of organic phosphorus in leachate from a grassland soil. Soil Biol Biochem 35:1317–1323

    CAS  Article  Google Scholar 

  • Trouillefou CM, Le Cadre E, Cacciaguerra T, Cunin F, Plassard C, Belamie E (2015) Protected activity of a phytase immobilized in mesoporous silica with benefits to plant phosphorus nutrition. J Sol-Gel Sci Technol 74:55–65. https://doi.org/10.1007/s10971-014-3577-0

    CAS  Article  Google Scholar 

  • Turner BL, Cade-Menun BJ, Condron LM, Newman S (2005a) Extraction of soil organic phosphorus. Talanta 66:294–306. https://doi.org/10.1016/j.talanta.2004.11.012

    PubMed  CAS  Article  Google Scholar 

  • Turner BL, Frossard E, Baldwin DS, editors. (2005b) Organic phosphorus in the environment. CABI Pub.pp 377–380

  • Turner BL, Cheesman AW, Condron LM, Reitzel K, Richardson AE (2015) Introduction to the special issue: developments in soil organic phosphorus cycling in natural and agricultural ecosystems. Geoderma 257–258:1–3. https://doi.org/10.1016/j.geoderma.2015.06.008

    Article  Google Scholar 

  • Uusitalo R, Turtola E, Puustinen M, Paasonen-Kivekas M, Uusi-Kamppa J (2003) Contribution of particulate phosphorus to runoff phosphorus bioavailability. J Environ Qual 32:2007–2016

    PubMed  CAS  Article  Google Scholar 

  • Vollmer-Sanders C, Allman A, Busdeker D, Moody LB, Stanley WG (2016) Building partnerships to scale up conservation: 4R nutrient stewardship certification program in the Lake Erie watershed. J Great Lakes Res. https://doi.org/10.1016/j.jglr.2016.09.004

  • von Sperber C, Kries H, Tamburini F, Bernasconi SM, Frossard E (2014) The effect of phosphomonoesterases on the oxygen isotope composition of phosphate. Geochim Cosmochim Acta 125:519–527. https://doi.org/10.1016/j.gca.2013.10.010

    CAS  Article  Google Scholar 

  • Wieder WR, Grandy AS, Kallenbach CM, Taylor PG, Bonan GB (2015) Representing life in the earth system with soil microbial functional traits in the MIMICS model. Geosci Model Dev 8:1789–1808. https://doi.org/10.5194/gmd-8-1789-2015

    Article  Google Scholar 

  • Withers PJA, Hartikainen H, Barberis E, Flynn NJ, Warren GP (2009) The effect of soil phosphorus on particulate phosphorus in land runoff. Euro J Soil Sci 60:994–1004. https://doi.org/10.1111/j.1365-2389.2009.01161.x

    CAS  Article  Google Scholar 

  • Zaia FC, Gama-Rodrigues AC, Gama-Rodrigues EF, Moço MKS, Fontes AG, Machado RCR, Baligar VC (2012) Carbon, nitrogen, organic phosphorus, microbial biomass and N mineralization in soils under cacao agroforestry systems in Bahia, Brazil. Agroforest Sys 86:197–212. https://doi.org/10.1007/s10457-012-9550-4

    Article  Google Scholar 

  • Zhou Z, Hartmann M (2012) Recent progress in biocatalysis with enzymes immobilized on mesoporous hosts. Topics Catalysis 55:1081–1100. https://doi.org/10.1007/s11244-012-9905-0

    CAS  Article  Google Scholar 

  • Zimmerman AE, Martiny AC, Allison SD (2013) Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. ISME 7:1187–1199. https://doi.org/10.1038/ismej.2012.176

    CAS  Article  Google Scholar 

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Acknowledgements

This work was performed with the financial support of the Organic Phosphorus Utilisation in Soils (OPUS) project, funded by Biotechnology and Biological Sciences Research Council (BBSRC – BBSRC - BB/K018167/1) in the UK and the Rural & Environment Science & Analytical Services Division of the Scottish Government. Fraser and Tibbett acknowledge the support of BBSRC SARISA programme BB/L025671/2. We also acknowledge the contribution to the output of the OP2016 workshop of all the attendees of the meeting who chose not be named as an author on this paper. In particular, the authors would like to thank Barbara Cade-Menun and Ben Turner and acknowledge there contribution to drafts of this manuscript.

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Correspondence to T. S. George.

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George, T.S., Giles, C.D., Menezes-Blackburn, D. et al. Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities. Plant Soil 427, 191–208 (2018). https://doi.org/10.1007/s11104-017-3391-x

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Keywords

  • Ecosystems services
  • Method development
  • Microbiome
  • Modelling
  • Organic phosphorus
  • Stoichiometry