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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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
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
Adeloju S, Webb B, Smernik R (2016) Phosphorus distribution in soils from Australian dairy and beef rearing pastoral systems. Appl Sci 6:31
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Doolette AL, Smernik RJ (2011) Soil organic phosphorus speciation using spectroscopic techniques. In: Phosphorus in action. Springer, Berlin Heidelberg, pp 3–36
Duff SM, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800
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
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
Espinosa M, Turner B, Haygarth P (1999) Preconcentration and separation of trace phosphorus compounds in soil leachate. J. Environ Q 28:1497–1504
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Luo H, Benner R, Long RA, Hu J (2009) Subcellular localization of marine bacterial alkaline phosphatases. PNAS 106:21249–21223
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
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
McGill WB, Cole CV (1981) Compartive aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–286
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
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
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
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
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
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
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
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
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
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
Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimise access to soil phosphorus. Crop Past Sci 60:124–143
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
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
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
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
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
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
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
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
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
Stewart JWB, Tiessen H (1987) Dynamics of soil organic phosphorus. Biogeochem 4:41–60. https://doi.org/10.1007/bf02187361
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
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
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
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
Tate KR, Salcedo I (1988) Phosphorus control of soil organic matter accumulation and cycling. Biogeochem 5:99–107. https://doi.org/10.1007/bf02180319
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
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
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
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
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
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
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
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
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
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
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
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
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
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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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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DOI: https://doi.org/10.1007/s11104-017-3391-x