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

T. S. George, C. D. Giles, D. Menezes-Blackburn, L. M. Conron, A. C. Gama-Rodrigues, D. Jaisi, F. Lang, A. L. Neal, M. I. Stutter, D. S. Almeida, et al.

► To cite this version:

T. S. George, C. D. Giles, D. Menezes-Blackburn, L. M. Conron, A. C. Gama-Rodrigues, et al. Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities. Plant and Soil, 2018, 427 (1-2), pp.209-211. 10.1007/s11104-017-3391-x. hal-02625597

HAL Id: hal-02625597

https://hal.inrae.fr/hal-02625597

Submitted on 26 May 2020

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
1 Organic phosphorus in the terrestrial environment: A perspective on the state of the art and future priorities
2

3 ¹*George TS, ¹Giles CD, ²Menezes-Blackburn D, ³Condron LM, ⁴Gama-Rodrigues AC, ⁵Jaisi D, ⁶Lang F, ⁷Neal

4 AL, ¹Stutter MI, ⁸Almeida DS, ⁹Bol R, ¹⁰Cabugao KG, ¹¹Celi L, ¹²Cotner JB, ¹³Feng G, ¹⁴Goll DS, ¹⁵Hallama M,

5 ⁶Krueger J, , ¹⁶Plassard C, ¹⁷Rosling A, ⁷Darch T, ¹⁸Fraser T, ¹⁹Giesler R, ²⁰Richardson AE, ²¹Tamburini F, ¹Shand

6 CA, ¹Lumsdon DG, ²Zhang H, ³Blackwell MSA, ²Wearing C, ¹Mezeli MM, ²²Almås ÅR, ²³Audette Y, ¹⁶Bertrand

7 I, ²⁴Beyhaut E, ³Boitt G, ²⁵Bradshaw N, ²⁶Brearley CA, ²⁷ Bruulsema TW, ¹⁴Ciais P, ²⁸Cozzolino V, ²⁹Cuevas PD,

8 ²⁹Mora ML, ³⁰de Menezes AB, ³¹Dodd RJ, ³²Dunfield K, ³²Engl C, ³³Frazão JJ, ²¹Garland G, ³⁴González Jiménez,

9 JL, ³⁴Graca J, ⁷Granger SJ, ³⁵Harrison AF, ³⁶Heuck C, ³⁷Hou EQ, ³⁸Johnes PJ, ³⁹Kaiser K, ⁴⁰Kjær HA, ¹⁷Klumpp

10 E, ⁴¹Lamb AL, ³²Macintosh KA, ³⁵Mackay EB, ³²McGrath J, ³⁸McIntyre C, ²¹McLaren T, ²¹Mészáros E, ⁹Missong

11 A, ⁴²Mooshammer M, ²⁹Negrón CP, ⁴³Nelson L-A, ⁷Pfahler V, ²⁹Poblete-Grant P, ⁴⁴Randall M, ²⁹Seguel A, ³Seth

12 K, ⁴¹Smith AC, ⁴⁵Smits MM, ²⁹Sobarzo JA, ³⁶Spohn M, ⁴⁶Tawaraya K, ¹⁸Tibbett M, ²³Voroney P, ⁴⁷Wallander H,

13 ⁹Wang L, ⁴⁸Wasaki J, ²Haygarth PM

14 ¹The James Hutton Institute, Dundee DD2 5DA and Aberdeen AB15 8QH, UK, ²Lancaster Environment Centre,

15 Lancaster University, LA1 4YQ, UK, ³Lincoln University, Lincoln 7647, Christchurch, New Zealand,

16 ⁴Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF - Laboratório de Solos), Av. Alberto Lamego

17 2000 Campos dos Goytacazes - RJ, Brasil, ⁵University of Delaware, Plant and Soil Sciences, 160 Townsend Hall,

18 Newark, DE 19716 USA, ⁶University of Freiburg, Faculty of Environment and Natural Resources, Chair of Soil

19 Ecology, Bertoldstraße 17, 79098 Freiburg, Germany, ⁷Rothamsted Research, West Common, Harpenden, Herts.,

20 AL5 2JQ & North Wyke, Okehampton, Devon, EX20 2SB, UK ⁸Sao Paulo State University (UNESP), College

21 of Agricultural Sciences, Department of Crop Science, 1780, Jose Barbosa de Barros st., Botucatu, Sao Paulo,

22 Brazil, ⁹Institute of Bio- and Geosciences, IBG-3: Agrosphere, Forschungszentrum Jülich GmbH 52425 Jülich,

23 Germany, ¹⁰Oak Ridge National Laboratory, P.O.Box 2008, Oak Ridge, TN 37831, USA ¹¹DISAFA, Soil

24 Biogeochemistry, University of Turin, largo Braccini 2, 10095 Grugliasco (TORINO), Italy, ¹²University of

25 Minnesota-Twin Cities, 1479 Gortner Ave. Saint Paul, MN 55108, USA, ¹³China Agricultural University, Beijing,

26 China ¹⁴Le Laboratoire des Sciences du Climat et de l'Environnement, IPSL-LSCE CEA/CNRS/UVSQ Saclay,

27 Gif sur Yvette, France, ¹⁵Institute of Soil Science, University of Hohenheim, Emil Wolff Str. 27, D-70599

28 Stuttgart, Germany, ¹⁶INRA UMR ECO&SOLS, Montpellier, France, ¹⁷Evolutionary Biology Centre, EBC,

29 Kåbovägen 4, house 7, SE-752 36 Uppsala, Sweden, ¹⁸Centre for Agri-environmental Research, School of
30 Agriculture Policy and Development, University of Reading, Whiteknights, PO Box 237, Reading RG6 6AR, UK,
31 ¹⁹Climate Impacts Research Centre, Dep. of Ecology and Environmental Science, Umeå University, 981 07
32 Abisko, Sweden, ²⁰CSIRO Agriculture & Food, Canberra, Australia, ²¹D-USYS, ETH Zurich, Tannenstrasse 1,
33 8092 Zurich Switzerland, ²²Norwegian University of Life Sciences, Department of Environmental Sciences Post
34 Box 5003, 1432 Ås, Norway, ²³University of Guelph, 50 Stone Road East, Guelph, Ontario, N1G 2W1, ²⁴Instituto
35 Nacional de Investigación Agropecuaria (INIA), Uruguay, ²⁵Department of Chemical & Biological Engineering,
36 The University of Sheffield, Mappin Street, S1 3JD, UK, ²⁶School of Biological Sciences, University of East
37 Anglia, Norwich Research Park, Norwich, NR4 7TJ, Norfolk, United Kingdom, ²⁷International Plant Nutrition
38 Institute, 18 Maplewood Drive, Guelph, Ontario, Canada N1G 1L8, ²⁸Centro Interdipartimentale di Ricerca sulla
39 Risonanza Magnetica Nucleare per l'Ambiente, l'Agro-Alimentare ed i Nuovi Materiali (CERMANU), Università
di Napoli Federico II, Via Università 100, 80055 Portici, Italy, ²⁹Universidad de La Frontera, Chile ³⁰School of
40 Environment and Life Sciences, University of Salford, Greater Manchester, The Crescent, M5 4WT, UK,
41 ³¹School of the Environment, Natural Resources and Geography, Bangor University, Gwynedd, LL57 2UW, UK,
42 ³²School of Biological Sciences and Institute for Global Food Security, The Queen's University of Belfast,
43 Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, United Kingdom, ³³CENA,
44 University of Sao Paulo, Avenida Centenario, 303, 13416-000, Piracicaba, SP, Brazil, ³⁴Teagasc, Environmental
45 Research Centre, Johnstown Castle, Co. Wexford, Ireland, ³⁵Centre for Ecology & Hydrology, Library Avenue,
46 Bailrigg, Lancaster, LA1 4AP, UK ³⁶Department of Soil Biogeochemistry, Bayreuth Center of Ecology and
47 Environmental Research (BayCEER), University Bayreuth, Dr.-Hans-Frisch-Str. 1-3, 95448 Bayreuth, Germany,
48 ³⁷Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy
49 of Sciences, 723 Xingke Road, Tianhe District, Guangzhou 510650, China, ³⁸School of Geographical Sciences &
50 School of Chemistry, University of Bristol, University Road, Bristol, BS8 1SS, UK ³⁹Soil Science and Soil
51 Protection, Martin Luther University Halle-Wittenberg, von-Seckendorff-Platz 3, 06120 Halle (Saale), Germany,
52 ⁴⁰Centre for Ice and Climate, Niels Bohr Institute, University of Copenhagen, ⁴¹NERC Isotope Geosciences
53 Facility, British Geological Survey, Nottingham, NG12 5GG, UK., ⁴²Department of Microbiology and Ecosystem
54 Science, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria ⁴³University of Northern British Columbia,
55 3333 University Way, Prince George, BC, V2N 4Z9, Canada, ⁴⁴Brigham Young University, Provo, UT 84602,
56 USA, ⁴⁵Centre for Environmental Sciences, Hasselt University Building D, Agoralaan 3590 Diepenbeek,
57 Belgium, ⁴⁶Yamagata University, Tsuruoka, 997-8555, Japan, ⁴⁷Department of Biology, Lund University, Biology
58
59 Building Sölvegatan 35, 223 62, Lund, Sweden, ⁴⁸Assessment of Microbial Environment, Graduate School of
60 Biosphere Science Hiroshima University, Hiroshima, Japan

61 *Corresponding author: tim.george@hutton.ac.uk, tel: +44 1382 568700; fax:+44 344 9285429

62 **Abstract**

63 **Background:** The dynamics of phosphorus (P) in the environment is important for regulating nutrient cycles in
64 natural and managed ecosystems and an integral part in assessing biological resilience against environmental
65 change. Organic P (P<sub>o</sub>) compounds play key roles in biological and ecosystems function in the terrestrial
66 environment, being critical to cell function, growth and reproduction.

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

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

77 **Keywords**

78 , Ecosystems services, Method development, Microbiome, Modelling, Organic Phosphorus, Stoichiometry.

79 **Abbreviations**

80 δ18OP – oxygen-18 isotope ratio

81 16S rRNA = 16S ribosomal Ribonucleic acid

82 Al = Aluminium

83 ATP = Adenosine triphosphate
84 C = Carbon

85 DNA = Deoxyribonucleic acid

86 Fe = Iron

87 N = Nitrogen

88 P = Phosphorus

89 Pho = Pho regulon transcription factors

90 Pᵢ = Inorganic orthophosphate

91 P₀ = Organic phosphate compounds

92 S = Sulphur

93 **The Importance of Phosphorus and Organic Phosphorus**

94 The dynamics of phosphorus (P) in the terrestrial environment is critical for regulating nutrient cycling in both
95 natural and managed ecosystems. Phosphorus compounds fundamentally contribute to life on earth: being
96 essential to cellular organization as phospholipids, as chemical energy for metabolism in the form of ATP, genetic
97 instructions for growth, development and cellular function as nucleic acids, and as intracellular signalling
98 molecules (Butusov and Jernelöv 2013). Plant growth is limited by soil P availability, so turnover of organic
99 phosphorus (P₀) represents a source of P for ecosystem function and, critically, P supply affects crop production
100 (Runge-Metzger 1995). Phosphorus deficiency constrains the accumulation and turnover of plant biomass and
101 dictates community assemblages and biodiversity in a range of natural ecosystems (Attiwill and Adams 1993;
102 McGill and Cole 1981).

103 Chemically, P is a complex nutrient that exists in many inorganic (Pᵢ) and organic (P₀) forms in the environment.
104 Through the utilization of orthophosphate, plants and other organisms drive the conversion of Pᵢ to P₀. Death,
105 decay and herbivory facilitate the return of both P₀ and Pᵢ in plant materials to soil. Inputs of P to soil through
106 these processes may contribute P₀ directly to soil or indirectly, following decomposition, accumulation, and
107 stabilization of P₀ by microorganisms (Harrison 1982; Lang et al. 2016; Magid et al. 1996; McGill and Cole 1981;
108 Stewart and Tiessen 1987; Tate and Salcedo 1988). In its simplest definition, P₀ is any compound that contains
109 an organic moiety in addition to P, while a wider definition would include phosphate which is associated with
110 organic matter. Such discrete P₀ compounds are categorized into similarly structured forms and these forms and
111 their relative lability in soil is shown in Figure 1, taken from Darch et al. (2014). The P₀ compounds, which are
112 considered to be biologically relevant include monoesters, inositol phosphates, diesters and phosphonates. The
113 relative lability and accumulation of these different groups varies in the environment, but overall the labile
114 monoesters and diesters tend to be less prevalent and the inositol phosphates tend to be less labile and accumulate
115 in the environment (Darch et al. 2014). In general, soil organic P forms have a smaller affinity to the soil solid
116 phase than inorganic P forms and a large proportion of the P forms found in leachate are found to be in organic
117 forms (Chardon & Oenema, 1995; Chardon et al. 1997; Espinosa et al. 1999) and can therefore have large impacts
118 on ecosystem function (Sharma et al. 2017; Toor et al. 2003). All P₀ compounds have a range of chemical bonds,
119 and all require specific catalytic enzymes to make them biologically available in the form of orthophosphate. The
120 hydrolysis of P₀ is mediated by the action of a suite of phosphatase enzymes which may have specificity for single
121 compounds or broad specificity to a range of compounds (George et al. 2007). Unlike for organic nitrogen, there
122 is no evidence for direct uptake of dissolved P₀ compounds by biology, apart from the uptake of phosphonates by
123 bacteria in marine systems (Dyhrman et al. 2006). Plants and microbes possess a range of phosphatases that are
124 associated with various cellular functions, including; energy metabolism, nutrient transport, metabolic regulation
125 and protein activation (Duff et al. 1994). However, it is the extracellular phosphatases released into the soil that
126 are of particular importance for the mineralisation of soil P₀. Extracellular phosphatase activity is induced under
127 conditions of P deficiency and is either associated with root cell walls or released directly into the rhizosphere
128 (Richardson et al. 2009).

129 There have been a number of important advances in our understanding of P₀ dynamics at the ecosystem and
130 rhizosphere scale in the past decade, with particular advancement in understanding of plant-soil-microorganism
131 interactions and concomitant advances in techniques used to assess these dynamics. It is now timely to start to
132 consider how to integrate this information and extract further understanding of the dynamics of P₀ in the managed
133 and natural environment and this will have a number of potentially important impacts on how we tackle some of
134 the most pressing global issues of today. Here we summarise the state of the art of P₀ research and identify
135 priorities for future research, which will help meet these goals.

136 Establishing Priorities for Organic Phosphorus Research

137 There has been a large increase in the number of publications in the P₀ research field in the last two decades, with
138 ~400 publications in 2016, compared to 150 in 2000. In September 2016 a workshop on Organic Phosphorus was
held (https://op2016.com), gathering together 102 experts in the field of P<sub>o</sub> research from 23 countries to identify research priorities. Contributors were asked, in five groups, to consider the global issues associated with P<sub>o</sub>, methodological strengths and weaknesses, benefits to be gained from understanding the P<sub>o</sub> cycle, and priorities for P<sub>o</sub> research. The information from the five groups was collected and the concepts, where consensus between at least two of the groups was reached, are summarized in Table 1. It is clear from this that research into P<sub>o</sub> has the potential to have impacts on global biogeochemical cycles of P both in natural and managed systems and will therefore potentially impact food security, agricultural sustainability, environmental pollution of both the aquatic and atmospheric environments and will be profoundly affected by environmental change both in geopolitical terms and through man-made climate change. We are well placed to tackle these as there are a number of strengths in the way the research is performed and the weaknesses are well understood. It was considered that P<sub>o</sub> research will have a range of impactful outcomes on our understanding of how natural and agricultural systems work and has the potential to give society a number of important tools to help manage the environment more effectively to either prevent or mitigate against some of the major global threats. A number of research priorities were identified and grouped into specific opportunities which are detailed below. The key opportunities to improve the effectiveness of P<sub>o</sub> research identified here are similar to those highlighted in Turner et al. (2005), although it is clear that some progress has been made since that set of recommendations were made. However, the similarities and consistency between the outcomes of these two studies suggests we still have some progress to make. A number of new priority areas were identified here that were not identified in Turner et al. (2005), including the need for greater understanding of the metagenomics and functional microbial genes involved in organic P turnover, greater understanding of the impact of nanoparticles in the environment on organic P turnover and the need to integrate the system more effectively in the form of models. It is clear that P<sub>o</sub> research field is evolving, but some of the issues of a decade ago still persist.

## 1) Opportunities in organic phosphorus analytical methodologies

The core analytical tools for the P<sub>o</sub> discipline are ³¹P NMR spectroscopy (Cade-Menun and Liu 2014; Cade-Menun 2005; Cade-Menun et al. 2005; Turner et al. 2005), which is used to identify P<sub>o</sub> compounds in several environmental matrices, along with more traditional soil extraction methods, such as those to measure total P<sub>o</sub> and the fractionation method developed by Hedley et al. (Condron and Newman 2011; Hedley et al. 1982; Negassa and Leinweber 2009). There is discussion and debate focused around the suitability of these analytical methodologies for characterizing P<sub>o</sub> in soil and terrestrial systems (Liu et al. 2014; Doolette and Smernik, 2011)
and this debate revolves around the identity of the broad base of the inositol hexaphosphate peak on NMR spectra, which some contest is resolved and other suggest is unidentified (Jarosch et al. 2015). Despite this, research into $P_o$ is still limited methodologically and many methods are operationally-defined. Importantly, there is a need to link the results from these methods to biological and biogeochemical processes in the environment. In the process of achieving this, there is debate over the benefits of (i) standardization or homogenization of analytical methods, versus the merits of (ii) promoting diversity of analytical procedures.

It is critical to develop non-destructive methods to analyse soil pools and their dynamics without the need for extraction. Some solid-state methods, such as solid-state NMR or P-XANES (X-ray Adsorptive Near Edge Structure) spectroscopy are limited by the naturally low concentrations of $P_o$ forms in soils (Liu et al. 2013; 2014; 2015). Visible Near-Infrared Reflectance Spectroscopy (VNIRS) has shown some promise for determining total $P_o$ in soils (Abdi et al, 2016), but further testing is needed. Another priority for $P_o$ methodologies is the development of standard analytical quality controls through the use of standardized reference materials for cross-comparison and checks on analytical methods. These standardized reference materials will include reference soils and chemicals. There is a need for the community to identify standardized natural reference materials such as soils and manures, but a large amount of effort would be needed to put together a collection of appropriate materials as well as a means to share them internationally. Standardization of $P_o$ compounds could be achieved through the use of simple, relatively pure, and inexpensive $P_o$ compounds (e.g. Na-phytate, glucose 1-P) purchased from a single supplier operating in many countries with a guaranteed long-term production commitment. And there is a need to develop a commercial supply of other commonly identified $P_o$ compounds in soils, such as scyllo-inositol hexakisphosphate, to allow the use of appropriate substrates for research fully understand the biological and chemical processes controlling the behaviour of this and other $P_o$ compounds in the environment. It is a priority for researchers to further develop methods, while also refining existing $P_o$ methods and standards, to generate useful and comparable datasets and to build a consensus with respect to $P_o$ dynamics and function in agricultural and natural ecosystems.

## 2) Opportunities from understanding stoichiometry – interactions of organic phosphorus with other element cycles

Comparing element ratios of living organisms and their non-living environment has been at the centre of scientific debate for many years. In oceans, planktonic biomass is characterized by similar C:N:P ratios as marine water (106:16:1) (Redfield 1958). While similar characteristic element ratios also exist for terrestrial ecosystems with
much greater heterogeneity across a range of spatial scales (Cleveland and Liptzin 2007). The comparison of C:N:P ratios in the microbial biomass of soils with that of soil organic matter (SOM) may therefore help to identify the nutrient status of the soil (Redfield 1958). Following this concept, the stoichiometric ratios of resources (e.g., SOM) over the microbial biomass has been calculated as a proxy for nutrient imbalances (Cleveland and Liptzin 2007). An understanding of stoichiometric ratios in soils and their relationship to those in crop plants and for the decomposition of litter and SOM will provide an important indicator of nutrient status in terrestrial ecosystems and better management of systems.

Until now, the large temporal and spatial heterogeneity of soil systems and the heterogeneous distribution of SOM constituents have made the analysis and interpretation of ecosystem stoichiometry a challenge because for microbial decomposers the elemental composition of micro-sites in soils might be more relevant than the overall element ratio of the soil. For example, by analysing the C:N:P ratio of bulk soils only, information on relevant and spatially-dependent processes may be lost (e.g., rhizosphere, soil horizons). The most obvious reason for soil-specificity and heterogeneity among stoichiometric ratios is that part of the SOM is separated from microorganisms and roots via physical and physicochemical barriers. By re-analysing the results of C:N:P:Sulphur (S) analyses of SOM obtained from 2000 globally distributed soil samples, Tipping et al. (2016) demonstrated that there is both nutrient-poor and nutrient-rich SOM, with the latter being strongly sorbed by soil minerals (Tipping et al. 2016). This may be explained by the incorporation of SOM into aggregates (Stewart and Tiessen 1987) or the adsorption of P-containing organic and inorganic molecules to mineral surfaces (Celi et al. 2003; Giaveno et al. 2010). Clay and metal (oxy)hydroxide minerals can sequester $P_o$ and $P_i$ released by microbial- or plant-driven processes and/or affect enzyme activities, while limiting P biocycling (Celi and Barberis 2005). This highlights the need to understand the tight interrelationship between chemical, physical and biological processes and the potential for stoichiometric assessment as an indicator of P and organic matter availability in soils. Modern analytical techniques which enable to analyse the stoichiometry of the soil constituents at a high resolution might help provide this knowledge (Mueller et al. 2012).

There are many known mechanisms by which organisms can improve access to $P_o$ (Richardson et al. 2011), but there are several novel mechanisms being identified that target key components of SOM, such as polyphenols and tannins, to mobilise P (Kohlen et al. 2011). A priority will be to understand the plant and microbial mechanisms involved in the accumulation and mobilization of P from organic matter. It is important to attempt to determine the optimal stoichiometry between C:N:P, and understand the role $P_o$ plays in this, to allow sustainable
226 management of P in arable soils and to identify anthropogenic nutrient imbalances in natural, agricultural and
227 forest ecosystems (Frossard et al. 2015).

228 **3) Opportunities from understanding interactions of organic phosphorus with land management**

229 An ability to utilise P<sub>o</sub> to sustain agronomic productivity with declining conventional fertiliser inputs drives
230 research into interactions among P<sub>o</sub>, land use and management (Nash et al. 2014; Stutter et al. 2012). The
231 conditions to better utilise P<sub>o</sub> may bring benefits for other soil quality factors (e.g., SOM status and microbial
232 cycling), but may require management of potentially adverse effects on wider biological cycles and water quality
233 (Dodd and Sharpley 2015). Societal drivers for food and timber production underpin much of the research into P<sub>o</sub>
234 speciation, biological turnover and integration with agronomic systems. Numerous studies have reported P<sub>o</sub> stocks
235 and changes associated with management; fewer have studied the time-course of transformations and turnover
236 with management change, linked with soil chemical and biological processes. The interactions between P
237 speciation, (bio)availability and SOM are of prime importance since land management greatly affects SOM in
238 space and time (in beneficial or detrimental ways) and exert strong geochemical and microbial controls on P<sub>o</sub>
239 cycling.

240 The interactions of land cover, use and management are important for understanding the role of P<sub>o</sub> across
241 ecosystems. In agricultural systems, the information on soil P<sub>o</sub> stocks is well represented have been quantified by
242 numerous studies in North America (Abdi et al. 2014; Cade-Menun et al. 2015; Liu et al. 2015; Schneider et al.
243 2016), Europe (Ahlgren et al. 2013; Annaheim et al. 2015; Keller et al. 2012; Stutter et al. 2015), China (Liu et
244 al. 2013), South America (de Oliveira et al. 2015), and Australia (Adeloju et al. 2016). In forestry, such
245 information is available in tropical (Zaia et al. 2012) and temperate systems (Slazak et al. 2010) and orchards (Cui
246 et al. 2015). However, an important improvement will be to better understand the reasons as to why particular
247 stocks exist under certain geoclimatic-land cover combinations. Key opportunities exist to understand P<sub>o</sub> dynamics
248 for sustainable P use in tropical systems and for forests growing on marginal soils, both of which depend on
249 effective management of P<sub>o</sub> resources.

250 It is known that both land cover and management factors (tillage, fertilizer type, application rate and timing)
251 interact with abiotic factors in controlling P<sub>o</sub> stocks and cycling, such as SOM, stabilizing surfaces [e.g., Fe- and
252 aluminium (Al)-oxides, calcium (Ca) forms, clays] and soil moisture, (Adeloju et al. 2016; Cade-Menun et al.
253 2015; Stutter et al. 2015). Chemical fractionation studies of P<sub>o</sub> stocks provide a snap-shot in time, missing
254 temporal aspects of cycling associated with management-induced change at seasonal or to longer term
management. As a result, short periods of rapid change in P speciation and turnover may not be appreciated. The utilization of 'legacy P' (Haygarth et al. 2014; Powers et al. 2016), following declining fertiliser inputs or altered cropping practices, has been studied following long-duration manipulations. Often these look at the end point of change (Cade-Menun et al. 2015), but have not 'followed' the dynamic. Although powerful methods for P₀ assessment are developing rapidly, studies that preceded these have the opportunity to incorporate them with archived samples or control soils (Keller et al. 2012; Liu et al. 2015). Long-term understanding of P₀ dynamics in management systems should be pursued, while short-term seasonal observations (for example Ebuele et al. 2016) will be needed to understand the influence of microbial dynamics on P speciation and turnover under various land-use and management scenarios. If studies of short-term perturbations (via management, climate etc) can show benefits for providing greater P₀ resources into available pools then these processes may be beneficially incorporated in future land management.

'Organic' farming brings a commercial stimulus to substitute agro-chemicals (including chemical P fertilisers) with sustainable management, such as use of organic amendments, for example enhancing soil P cycling with the aim of better utilizing P already present and moving towards a 'closed' system (Annaheim et al. 2015; Gaind and Singh 2016; Schneider et al. 2016). The same approaches can be applied to less intensive, or developing, agricultural systems. Canadian pastures managed under an organic regime, had a greater abundance of P₀ (65% vs 52% of total P) compared to conventional pastures and were able to maintain yield without inorganic fertilisers (Schneider et al. 2016). These authors concluded that plants were using Pᵢ rather than P₀ and supported by other studies showing no indication that the greater microbial activity under organic farming caused utilization of stabilized P₀ forms (Keller et al. 2012). Therefore, the management conditions and actions required to promote better acquisition of P₀ pools remain elusive.

The consensus is that a key question remains: How long could the turnover of P₀ sustain crop yields under scenarios of reduced P inputs and maintained or increased outputs and thus contribute to agricultural production and feed supplies? The mechanistic understanding required to answer this question lies in the role of biota (in the context of their abiotic setting) in P₀ turnover and the potential pathways of P₀ loss to be managed (e.g. runoff). In order to progress, a systems approach is needed to fully assess the opportunities and role of P₀, as well as the interactions of soil chemical, physical and biological processes and impacts of land use change that control P availability.

**4a) Opportunities from understanding microbial P₀: functional genes and metagenomics**
As our abilities to analyse and interpret the complexity inherent in the soil microbiome improves, interest is 284 burgeoning around the functional ecology of microorganisms. Organic P dynamics across ecosystems, along with 285 development of many techniques that will aid in this understanding, are beginning to emerge. Scavenging of P 286 from P-containing organic compounds by soil microbes is tightly controlled by intracellular P availability through 287 the Pho pathway in yeast (Secco et al. 2012) and the Pho regulon in bacteria. In both cases, transcription of 288 phosphatase and phytase, which act to release orthophosphate from phosphate esters, and high affinity transporters 289 which transport Pᵢ into the cell, are up-regulated under Pᵢ limitation, affecting the organisms' ability to utilise P₀. 290 The Pho regulon also acts as a major regulator of other cellular processes, including N assimilation and ammonium 291 uptake (Santos-Beneit 2015). The C:N:P elemental ratios of the soil bacterium *Bacillus subtilis* range between 292 C₅₃-125:N₁₂-2₉:P₁ under N- and P-limited culture conditions (Dauner et al. 2001), although environmental 293 assemblages may exhibit greater stoichiometric flexibility (Godwin and Cotner 2015). Given this regulatory cross- 294 talk, nutrient stoichiometry will be important to cellular and community metabolism meaning that the cycling of 295 P must be considered within the context of other biogeochemical cycles, as highlighted earlier. 296

Soil type, nutrient inputs, and plant species have been shown to determine microbiota species composition and 297 function (Alegria-Terrazas et al. 2016). However, plant root exudation drives recruitment of specific microbes 298 and microbial consortia to the rhizosphere and may outweigh the impacts of soil and its management in shaping 299 community composition and function (Tkacz et al. 2015). As yet, there is only limited understanding of how 300 specific root exudates affect microbial recruitment (Neal et al. 2012), let alone specific microbiota responsible for 301 phosphatase expression and production. A better understanding of interactions between plants and microbes would 302 facilitate identification of functional redundancy among them, which could ultimately help manage the availability 303 of P in soils and sediments by selection of the optimal plant rhizosphere compliment. 304

Alkaline phosphatase and phytase genes are distributed across a broad phylogenetic range and display a high 305 degree of microdiversity (Jaspers and Overmann 2004; Lim et al. 2007; Zimmerman et al. 2013), where closely 306 related organisms exhibit different metabolic activities. It is therefore not possible to determine community 307 functional potential from 16S rRNA gene abundance – functional gene abundance information is required and 308 this can be provided by employing sequencing techniques to assess the soil metagenome. In marine systems, there 309 is evidence from metagenomic sequencing of environmental DNA that alkaline phosphatase genes phoD and 310 phoX are more abundant than phoA (Luo et al. 2009; Sebastian and Ammerman 2009) and the β-propeller phytase 311 is the most abundant phytase gene (Lim et al. 2007). The dominant alkaline phosphatase gene in terrestrial 312
ecosystems is also phoD (Tan et al. 2013), which is more abundant in soils than other environments (Courty et al. 2010; Ragot et al. 2015; Fraser et al. 2017). From a functional standpoint, abundance of phoD-like sequences correlate well with estimates of potential alkaline phosphatase activity (Fraser et al. 2015), although this is not always the case (Ragot et al. 2015). Moreover, in soils there is little information regarding other phosphatases and little is known about the distribution and abundance of bacterial acid phosphatases, but there is some information related to phoX (Ragot et al. 2016). In contrast, fungi are well known for their capacity to secrete acid phosphatases (Plassard et al. 2011; Rosling et al. 2016), especially ectomycorrhizal fungi. Since only a small percentage of soil microorganisms are cultivable, research will need to rely upon culture-independent approaches to generate a thorough understanding of the abundance and diversity of genes associated with P<sub>o</sub> turnover. Environmental metagenomic sequencing can form the basis of an efficient molecular toolkit for studying microbial gene dynamics and processes relevant to P<sub>o</sub> mineralization (Neal et al., 2017). Such an approach will need to prioritize generating comprehensive understanding of the distribution of alkaline and acid phosphatase and phytase genes within soils, coupled with activity measurements, and a sense of their relative sensitivities to edaphic factors. This will allow explicit incorporation of microbial P<sub>o</sub> turnover in the new generation of soil models, as well as allowing rapid assessment of a soil's capabilities for P<sub>o</sub> cycling. Improved knowledge will allow the exploitation of microbial activity to sustain and improve soil fertility and allow the tailoring of new fertilizers based upon the capacity of microbes to exploit P<sub>o</sub>.

**4b) Opportunities from understanding microbial P<sub>o</sub>: measuring stocks, mineralisation and dynamics of turnover**

The apparently large diversity of genes associated with P<sub>o</sub>-hydrolysing enzymes suggests that changes in community composition are unlikely to result in a loss of ecosystem function. This confers resilience to P-cycling processes, although many of these genes have very specific functions intracellularly. However, trait differences are likely to have significant implications for community function in soils, e.g., the contrasting effects of arbuscular and ectomycorrhizal fungi upon the cycling of P in forest soils, where it has been shown that P<sub>o</sub> is more labile in ectomycorrhizal dominated systems than arbuscular mycorrhizal systems (Rosling et al. 2016). The fact that enzyme activity in soil appears to be disconnected from soil P status is at odds with the apparent influence of the Pho regulon or pathway upon gene expression and indicates that much of the observed activity derives from multiple enzyme sources, which have been stabilised by soil colloids (Nannipieri et al. 2011). This also suggests that soil enzyme activity does not directly represent microbial activity or simply reflects the complexity in current
P requirements of different microbial species. However, visualization of acid and alkaline phosphatase activity associated with roots by zymography (Spohn and Kuzyakov 2013) does provide an exciting means to determine regulation of soil phosphatase activity with P availability and illustrates the clear spatial separation among the activities of physiologically different enzymes. It is a priority to develop and couple techniques that resolve the distribution of active enzymes in soil with estimates of gene expression derived from functional genes or meta-transcriptomic studies.

The stock of microbial P is an easy-to-determine component in soils, which is widely used to characterize the P status of microbial communities and ecosystems (Brookes et al. 1982; 1984). Nevertheless, its analysis relies on many different protocols (Bergkemper et al. 2016). Building on the previous work, further insights into both microbial-mediated and enzyme-mediated P transformations in soils may now be gained from measurement of the isotopic composition of oxygen associated with phosphate (δ¹⁸OP) (Tamburini et al. 2014; von Sperber et al. 2014) and the use of radiolabelled (³²P or ³³P) P₀ compounds to measure mineralisation and immobilisation rates directly (Harrison 1982). A powerful tool for quantifying soil P pools and transformation rates is the isotope dilution technique [reviewed in Bünemann 2015; Di et al. 2000; Frossard et al. 2011]. The decrease in radioactivity with time is caused by the exchange of the added radiolabelled P (either ³²P or ³³P) with ³¹P from the sorbed/solid phase and by the release of inorganic ³¹P from the organic pool via hydrolysing enzymes (Bünemann 2015). Determination of gross P₀ mineralization rates from P₀ to Pᵢ remains a critical approach, helping understand the processes and rates of P cycling in different soils and under different environmental conditions (Frossard et al. 2011). These techniques present new opportunities to link P cycling to other biogeochemical cycles, such as C and N.

## 5) Opportunities in the emerging area of interactions between P₀ dynamics and nanoparticles

Reactive nanoparticles can take the form of natural soil colloids or man-made particles and are potential P₀ carriers, sources and sinks in ecosystems. Up to 90% of P in stream water and runoff is present in nano- and colloidal sized materials (Borda et al. 2011; Gottselig et al. 2014; Uusitalo et al. 2003; Withers et al. 2009). Colloidal P may comprise nano-sized aggregates (Jiang et al. 2015) bound to Fe, Al and SOM (Celi and Barberis 2005; Celi and Barberis 2007), including inositol phosphates. However, the influence of nanoparticles on the dynamics and bioavailability of P in soil-plant systems is unclear (Bol et al. 2016). Nanoparticles such as C-magnetite, which adsorb and retain Pᵢ and P₀, are used to enhance the recovery and recycling of P from P-rich wastes (Magnacca et al. 2014; Nisticò et al. 2016). It may also be possible to enhance soil enzyme activity with
amendments containing mesoporous nanoparticle materials (Zhou and Hartmann 2012). Phytase encapsulated in nanoparticles was shown to be resistant to inhibitors and proteases and to promote the hydrolysis of phytate for P uptake by *Medicago truncatula* (Trouillefou et al. 2015). Nanotechnology has also been used to develop new fertilizers and plant-growth-enhancing materials (Liu and Lal 2015), representing one potentially effective option for enhancing global food production. A better understanding of the P₀ nanoparticle interaction may improve our understanding on P fluxes in natural and agricultural systems, and provide innovative technologies for fertilizer production and environmental remediation.

## 6) Opportunities to use modelling of P₀ in soil and ecosystems

The use of all types of modelling approaches to study P₀ is generally overlooked and there is a dearth of P₀ based models, but development of such models would be extremely beneficial. Modelling should facilitate the development of a systems-based perspective and help to identify knowledge gaps in the current understanding of P₀. Models of all types are needed including those that are conceptual, mechanistic or empirical in nature and in general there is a lack of focus on all the types of models that exist for P₀. The potential benefits of advances in modelling for P₀ include:

* Prediction of the relationship between soil P₀ and plant uptake, which should be developed in both conceptual and mechanistic models of P dynamics in the environment.

* Application at different scales to determine the relationship between P₀ with land use and management should be possible by building empirical models based on existing data.

* Application of modelling to help understand the role of microbial traits in soil (Wieder et al. 2015), which may determine the effects of gene expression, enzyme activities and the stoichiometric ratio of C:N:P in the microbial biomass relative to that of SOM

* Application of complete Life-Cycle Analysis for relying on the run-down of soil P₀ as a replacement to inorganic fertilisers will help us develop adequate conceptual models for management of the system.

* Modelling could also be used to help in the quantification of soil P pools for estimating flow among P₀ pools. In general, there is a great opportunity for the development of modelling in all areas of P₀ research and this will be of considerable benefit to the subject if this can be developed and integrated with all areas. The cooperation of modellers and empiricists is essential for building models with great potential use to predict changes in P₀ bioavailability due to land-use and management change and to infer the sustainability of the system as a whole.
400 **7) Opportunities to better communicate and translate research**

401 Organic P represents a small, albeit critical component of biogeochemical research. The marginal nature of the
402 subject to date creates a need to communicate the importance of this science for the future of P sustainability. As
403 for other scientific disciplines, communication priorities include (1) strengthening communication among
404 scientists within and outside of the P<sub>o</sub> research community; (2) engagement with stakeholders; and (3)
405 dissemination of knowledge to the public and specific end-users.

406 Conferences and workshops on the topic of organic P promote the exchange of ideas and forging of new research
407 partnerships (Sharpley et al. 2015; Turner et al. 2015). Online platforms are also powerful tools to connect
408 researchers and stakeholders on issues of global P sustainability (e.g., European Sustainable Phosphorus Platform,
409 www.phosphorusplatform.eu, North America Partnership for Phosphorus Sustainability) (Rosemarin and Ekane
410 2015). The ‘Soil Phosphorus Forum’ (www.soilforum.com) provides a platform for the exchange of information
411 relating to P<sub>o</sub>. Specific protocols and conference presentations are also featured in archived YouTube channels
412 (https://www.youtube.com/channel/UCtGI3eUZscCgByewafsQKdw). A central platform for P<sub>o</sub> research and
413 communications is still needed, to connect existing forums to global research networks and would include features
414 such as researcher membership, methodological resources, links to relevant organizations and platforms, and a
415 clearing house of P<sub>o</sub> data for future meta-analysis and modelling efforts.

416 Key stakeholder groups such as land managers, farmers and extension services are a natural link between industry,
417 government, and academia (FAO 2016). These key groups hold traditional knowledge on sustainable farming
418 techniques, which serve as a potential basis for future P<sub>o</sub> research. Industry initiatives such as the 4R Nutrient
419 Stewardship framework provide feedback from end users and practitioners on research priorities associated with
420 the management of agricultural nutrients (Vollmer-Sanders et al. 2016). The engagement of P<sub>o</sub> researchers with
421 existing nutrient initiatives such as these will be critical for bolstering public understanding of P<sub>o</sub> and its important
422 role in global P dynamics.

423

424 **Conclusion - Statement of intent for the P<sub>o</sub> research community**

425 Organic P research has a critical role to play in tackling a number of important global challenges and there are
426 key contributions to be made toward understanding biogeochemical cycles, dynamics and function of natural
427 ecosystems and the management of agricultural systems. In particular, we must reduce our reliance on inorganic
428 P fertilisers and strategies to do this will increase the relevance of soil P<sub>o</sub> for plant nutrition. Secondly, there is a
need to develop a circular P economy and close the P cycle which will likely lead to an increase in the amounts of organic P “waste” products being recycled to land shifting the P₀/Pᵢ balance in the soil. To address these global environmental changes and challenges, we should concentrate our efforts on understanding the biological significance of P₀ by considering its interactions with other elements in SOM, soil microorganisms and active soil surfaces. We should consider these interactions with respect to changes in land use and management and as a function of geochemical conditions in the wider biophysical and socio-economic environment. We need to integrate this understanding through the production of models for P₀, which capture both whole systems and fine-scale mechanisms. In addition, we need to develop novel and standardised methodologies that can integrate the dynamics and function of P₀ on appropriate scales in a non-invasive manner. To achieve a step-change in the impact of P₀ research, we need to engage with researchers outside of the discipline, align the research with pressing societal issues, and become more global, collaborative, inclusive, interdisciplinary, and longer-term in nature. The key to fostering this change will depend on logically communicating the importance of P₀ to society at large, engaging with stakeholders on important global issues, and ultimately pushing this important area of research up the agenda of policy makers and funding bodies on a global scale.

## 443 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.

## 451 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. doi: 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.
458 Adeloju S, Webb B, Smernik R (2016) Phosphorus Distribution in Soils from Australian Dairy and Beef
459 Rearing Pastoral Systems. Appl Sci 6: 31.

460 Ahlgren J, Djodjic F, Börjesson G, Mattsson L (2013) Identification and quantification of organic phosphorus
461 forms in soils from fertility experiments. Soil Use and Management 29: 24-35. doi:
462 10.1111/sum.12014.

463 Alegria-Terrazas R, Giles CD, Paterson E, Robertson-Albertyn S, Cesco S, Mimmo T, Pii Y, Bulgarelli D
464 (2016) Plant-Microbiota Interactions as a Driver of the Mineral Turnover in the Rhizosphere. Adv
465 Appl Microbiol. Springer.

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

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

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

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

482 Borda T, Celi L, Zavattaro L, Sacco D, Barberis E (2011) Effect of agronomic management on risk of
483 suspended solids and phosphorus losses from soil to waters. J Soils Seds 11: 440-451. doi:
484 10.1007/s11368-010-0327-y.

485 Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil
486 Biol Biochem 14: 319-329. doi: http://dx.doi.org/10.1016/0038-0717(82)90001-3.
487 Brookes PC, Powlson DS, Jenkinson DS (1984) Phosphorus in the soil microbial biomass. Soil Biol Biochem 16: 169-175. doi: http://dx.doi.org/10.1016/0038-0717(84)90108-1.

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

491 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, NY.

493 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. doi: 10.2136/sssaj2013.05.0187dgs.

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

498 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. doi: 10.2136/sssaj2014.08.0310.

501 Cade-Menun BJ, Turner B, Frossard E, Baldwin D (2005) Using phosphorus-31 nuclear magnetic resonance spectroscopy to characterize organic phosphorus in environmental samples. Organic phosphorus in the environment: 21-44.

504 Celi L, Barberis E (2005) Abiotic stabilization of organic phosphorus in the environment. Organic phosphorus in the environment. CABI Pub pp 113-132.

506 Celi L, Barberis E (2007) Abiotic reactions of inositol phosphates in soils. In: BL Turner, AE Richardson, EJ Mullaney (eds) Inositol Phosphates: Linking Agriculture and the Environment. CAB International, Oxfordshire, UK.

509 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.

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

513 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.

515 Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a "Redfield ratio" for the microbial biomass? Biogeochem 85: 235-252. doi: 10.1007/s10533-007-9132-0.
517 Condron LM, Newman S (2011) Revisiting the fundamentals of phosphorus fractionation of sediments and soils. J Soils Seds 11: 830-840. doi: 10.1007/s11368-011-0363-2.

519 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. doi: 10.1016/j.soilbio.2010.07.014.

521 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 Biology and Biochemistry 82: 119-126. doi: 10.1016/j.soilbio.2015.01.003.

524 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. doi: 10.1080/10643389.2013.790752.

527 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. doi: 10.1128/JB.183.24.7308-7317.2001.

530 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. doi: http://dx.doi.org/10.1016/j.geodrs.2015.06.001.

533 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. doi: http://dx.doi.org/10.1071/SR99005.

536 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. doi: 10.1016/j.resconrec.2015.10.001.

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

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

542 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.

544 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. doi: 10.1016/j.scitotenv.2016.05.192.
547 Espinosa M, Turner B, Haygarth P (1999) Preconcentration and separation of trace phosphorus compounds in
soil leachate. J. Environ Q 28: 1497-1504.

549 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.

551 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. doi:
10.1016/j.geoderma.2014.10.016.

554 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. Applied Soil Ecology 111:48-56.

557 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: E Bünemann, A Oberson, E Frossard (eds) Phosphorus in
Action: Biological Processes in Soil Phosphorus Cycling. Springer Berlin Heidelberg, Berlin,
Heidelberg.

562 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.

565 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. doi:
10.1080/01904167.2015.1086795.

568 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.

571 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.
doi: 10.1016/j.soilbio.2009.12.002.

574 Godwin CM, Cotner JB (2015) Aquatic heterotrophic bacteria have highly flexible phosphorus content and
biomass stoichiometry. ISME J 9: 2324-2327. doi: 10.1038/ismej.2015.34.
576 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. doi: 10.2136/vzj2014.01.0005.

579 Harrison AF (1982) 32P-method to compare rates of mineralization of labile organic phosphorus in woodland soils. Soil Biol Biochem14: 337-341. doi: 10.1016/0038-0717(82)90003-7.

581 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. doi: 10.1021/es502852s.

584 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.

586 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 Biology and Biochemistry 91:298-309.

589 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. doi: 10.1128/AEM.70.8.4831-4839.2004.

592 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. Biogeosci 12: 6443-6452. doi: 10.5194/bg-12-6443-2015.

595 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. Journal of Plant Nutrition and Soil Science 175: 385-393. doi: 10.1002/jpln.201100177.

599 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 physiol155: 974-987. doi: 10.1104/pp.110.164640.

603 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. doi: 10.1002/jpln.201500541.
606 Lim BL, Yeung P, Cheng C, Hill JE (2007) Distribution and diversity of phytate-mineralizing bacteria. ISME 1: 321-330. doi: 10.1038/ismej.2007.40.

608 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. doi: 10.1021/es504420n.

611 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. doi: 10.2134/jeq2013.04.0127.

615 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. 49:168-76.

618 Liu R, Lal R (2015) Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Science of The Total Environment 514: 131-139. doi: 10.1016/j.scitotenv.2015.01.104.

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

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

625 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 Sustainable Chemistry & Engineering 2: 1518-1524. doi: 10.1021/sc500213j.

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

631 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.
634 Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of Phosphatase Enzymes in Soil. In: E Bünemann, A

635 Oberson, E Frossard (eds) Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling.

636 Springer Berlin Heidelberg, Berlin, Heidelberg.

637 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.

639 doi: 10.1016/j.geoderma.2013.12.004.

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

642 Neal AL, Rossman M, Brearley C, Akkari E, Guyomar C, Clark IM, Allen E, Hirsch PR (2017) Land-use
643 influences phosphatase gene microdiversity. Environ. Microbiol. (in press doi:10.1111/1462-
644 2920.13778)

645 Negassa W, Leinweber P (2009) How does the Hedley sequential phosphorus fractionation reflect impacts of
646 land use and management on soil phosphorus: A review. J Plant Nutr Soil Sci-Z Pflanzenernahr
647 Bodenkd 172: 305-325. doi: 10.1002/jpln.200800223.

648 Nisticò R, Evon P, Labonne L, Vaca-Medina G, Montoneri E, Francavilla M, Vaca-Garcia C, Magnacca G,
649 Franzoso F, Negre M (2016) Extruded Poly(ethylene-co-vinyl alcohol) Composite Films Containing
650 Biopolymers Isolated from Municipal Biowaste. ChemistrySelect 1: 2354-2365. doi:
651 10.1002/slct.201600335.

652 Plassard C, Louche J, Ali MA, Duchemin M, Legname E, Cloutier-Hurteau B (2011) Diversity in phosphorus
653 mobilisation and uptake in ectomycorrhizal fungi. Ann Forest Sci 68: 33-43. doi: 10.1007/s13595-010-
654 0005-7.

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

658 Ragot SA, Kertesz MA, Bünemann EK (2015) phoD Alkaline Phosphatase Gene Diversity in Soil. Appl
659 Environ Microbiol 81: 7281-7289. doi: 10.1128/aem.01823-15.

660 Ragot SA, Kertesz MA, Mészáros É, Frossard E, Bünemann EK. (2016) Soil phoD and phoX alkaline
661 phosphatase gene diversity responds to multiple environmental factors. FEMS microbiology ecology.
662 93:fiw212.
663 Redfield AC (1958) The biological control of chemical factors in the environment American Scientist 46: 230A-
664 221.

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

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

670 Rosemarin A, Ekane N (2015) The governance gap surrounding phosphorus. Nutri Cycl Agroecosys: 1-15. doi:
671 10.1007/s10705-015-9747-9.

672 Rosling A, Midgley MG, Cheeke T, Urbina H, Fransson P, Phillips RP (2016) Phosphorus cycling in deciduous
673 forest soil differs between stands dominated by ecto- and arbuscular mycorrhizal trees. New Phytol
674 209: 1184-1195. doi: 10.1111/nph.13720.

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

678 Santos-Beneit F (2015) The Pho regulon: a huge regulatory network in bacteria. Frontiers in Microbiology 6.
679 doi: 10.3389/fmicb.2015.00402.

680 Schneider KD, Cade-Menun BJ, Lynch DH, Voroney RP (2016) Soil Phosphorus Forms from Organic and
681 Conventional Forage Fields. Soil Sci Soc Am J 80: 328-340. doi: 10.2136/sssaj2015.09.0340.

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

684 Secco D, Wang C, Shou H, Whelan J (2012) Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the
685 key role of the SPX domain-containing proteins. FEBS letters 586: 289-295. doi:
686 10.1016/j.febslet.2012.01.036.

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

690 Sharpley AN, Bergström L, Aronsson H, Bechmann M, Bolster CH, Börling K, Djodjic F, Jarvie HP,
691 Schoumans OF, Stamm C, Tonderski KS, Ulén B, Uusitalo R, Withers PJA (2015) Future agriculture
692 with minimized phosphorus losses to waters: Research needs and direction. AMBIO 44: 163-179. doi:
693 10.1007/s13280-014-0612-x.

694 Slazak A, Freese D, da Silva Matos E, Hüttl RF (2010) Soil organic phosphorus fraction in pine-oak forest stands in Northeastern Germany. Geoderma 158: 156-162.

696 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. doi: http://dx.doi.org/10.1016/j.soilbio.2013.08.015.

699 Stewart JWB, Tiessen H (1987) Dynamics of soil organic phosphorus. Biogeochem 4: 41-60. doi:
700 10.1007/bf02187361.

701 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 SciTechnol 46: 1977-1978. doi: 10.1021/es2044745.

704 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. doi: 10.1016/j.geoderma.2015.03.020.

707 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. doi: 10.2136/sssaj2013.05.0186dgs.

710 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. doi: 10.1007/s00374-012-0755-5.

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

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

718 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. doi: 10.1038/ismej.2015.41.
721 Toor GS, Condron LM, Di HJ, Cameron KC, Cade-Menun BJ (2003) Characterization of organic phosphorus in
722 leachate from a grassland soil. Soil Biol. Biochem. 35:1317-23.

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

726 Turner BL, Cade-Menun BJ, Condron LM, Newman S (2005) Extraction of soil organic phosphorus. Talanta
727 66: 294-306. doi: 10.1016/j.talanta.2004.11.012.

728 Turner BL, Cheesman AW, Condron LM, Reitzel K, Richardson AE (2015) Introduction to the special issue:
729 Developments in soil organic phosphorus cycling in natural and agricultural ecosystems. Geoderma
730 257-258: 1-3. doi: http://dx.doi.org/10.1016/j.geoderma.2015.06.008. Turner BL, Frossard E, Baldwin
731 DS, editors. (2005) Organic phosphorus in the environment. CABI Pub.pp 377-380.

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

734 Vollmer-Sanders C, Allman A, Busdeker D, Moody LB, Stanley WG (2016) Building partnerships to scale up
735 conservation: 4R Nutrient Stewardship Certification Program in the Lake Erie watershed. J Great
736 Lakes Res. doi: http://dx.doi.org/10.1016/j.jglr.2016.09.004.

737 von Sperber C, Kries H, Tamburini F, Bernasconi SM, Frossard E (2014) The effect of phosphomonoesterases
738 on the oxygen isotope composition of phosphate. Geochimica et Cosmochimica Acta 125: 519-527.
739 doi: 10.1016/j.gca.2013.10.010.

740 Wieder WR, Grandy AS, Kallenbach CM, Taylor PG, Bonan GB (2015) Representing life in the Earth system
741 with soil microbial functional traits in the MIMICS model. Geosci Model Dev 8: 1789-1808. doi:
742 10.5194/gmd-8-1789-2015.

743 Withers PJA, Hartikainen H, Barberis E, Flynn NJ, Warren GP (2009) The effect of soil phosphorus on
744 particulate phosphorus in land runoff. Euro J Soil Sci 60: 994-1004. doi: 10.1111/j.1365-
745 2389.2009.01161.x.

746 Zaia FC, Gama-Rodrigues AC, Gama-Rodrigues EF, Moço MKS, Fontes AG, Machado RCR, Baligar VC
747 (2012) Carbon, nitrogen, organic phosphorus, microbial biomass and N mineralization in soils under
748 cacao agroforestry systems in Bahia, Brazil. Agroforest Sys 86: 197-212. doi: 10.1007/s10457-012-
749 9550-4.
750 Zhou Z, Hartmann M (2012) Recent Progress in Biocatalysis with Enzymes Immobilized on Mesoporous Hosts.

751 Topics Catalysis 55: 1081-1100. doi: 10.1007/s11244-012-9905-0.

752 Zimmerman AE, Martiny AC, Allison SD (2013) Microdiversity of extracellular enzyme genes among

753 sequenced prokaryotic genomes. ISME 7: 1187-1199. doi: 10.1038/ismej.2012.176.

Generic structure:

<figure><img src="image_2.png" /></figure>

e.g.

<figure><img src="image_3.png" /></figure>

Adenosine diphosphate (ADP)

Generic structure:

<figure><img src="image_4.png" /></figure>

e.g.

<figure><img src="image_5.png" /></figure>

2-aminoethylphosphonic acid

<figure><img src="image_6.png" /></figure>

* The 'R' in chemical formulae denotes an organic group
755 FIGURE 1. Organic phosphorus forms with generic and example structures and information on the relative lability
756 and prevalence in soil. (Adapted from Darch et al. (Darch et al. 2014))

757

758

759

760 Table Legend

761

762 Table 1: Synthesis of expert opinions on the global issues associated with organic phosphorus, how the research
763 community can potentially contribute to solutions to such issues, and identification of opportunities for research
764 to allow this to happen.

765
<table><thead><tr><th>What are the global issues associated with P<sub>o</sub>?</th><th>What are the methodological strengths and weaknesses?</th><th>What are benefits of understanding dynamics of P<sub>o</sub>?</th><th>What are the priorities for P<sub>o</sub> research?</th><th>Opportunities in P<sub>o</sub> research</th></tr></thead><tbody><tr><td><strong>Food Security and agricultural sustainability</strong><br>P<sub>o</sub> has a role as a source of P for agricultural crops</td><td><strong>Strengths</strong><br>Strong collection of well-developed methods</td><td>Management of plant P nutrition</td><td><ul><li>Use existing datasets more effectively</li><li>Avoid repeating experiments by being aware of past research</li><li>Better access to shared facilities</li><li>Training programmes in P<sub>o</sub> related techniques and concepts</li><li>Interdisciplinary and long term research</li></ul></td><td>General advances in the research model</td></tr><tr><td><strong>Nutrient cycling in natural ecosystems</strong><br>P<sub>o</sub> buffers ecosystem function with effects on ecosystem resilience and biodiversity</td><td>Wide range of techniques<br>Capacity for multi-disciplinarity<br>Strong international networks</td><td>Assessment of soil P availability<br>Understanding biological system function<br>Input into climate and biogeochemical models<br>Potential to close the P cycle<br>Manage ecosystem services and resilience</td><td><ul><li>Link operationally-defined pools with biological processes</li><li>Some standardisation of protocols</li><li>Development of in situ, non-destructive techniques for P<sub>o</sub></li><li>Develop a minimum dataset and an accessible database</li></ul></td><td>Opportunities in organic phosphorus analytical methodologies</td></tr><tr><td><strong>Renewable resources</strong><br>Use of wastes containing P<sub>o</sub> as fertilisers to close the loop</td><td>Potential for commercialisation of techniques<br>Range of field based applications</td><td>Understand the role of soil biology – fungal vs bacterial dominated systems<br>Assess stability of P forms in soil</td><td><ul><li>Link the P<sub>o</sub> cycle with other biogeochemical cycles</li><li>Optimise stoichiometry between P<sub>o</sub> and other elements for system function</li><li>Integrate soil physics, chemistry and biology to understand P<sub>o</sub> and how it fits with wider soil fertility</li></ul></td><td>Opportunities from understanding stoichiometry – interactions with other element cycles</td></tr><tr><td><strong>C storage in soils</strong><br>Utilisation of soil P<sub>o</sub> may be counter to our need to store C in organic matter</td><td><strong>Weaknesses</strong></td><td></td><td><ul><li>Design tailored systems for specific managed environments that optimise use of P<sub>o</sub></li><li>Optimise P<sub>o</sub> utilisation over loss</li><li>Improve soil P testing</li><li>Develop a P credits system</li><li>Utilise P<sub>o</sub> more effectively by using what's in soil, what's added to soil and what's lost</li></ul></td><td>Opportunities from understanding interactions with land management</td></tr><tr><td><strong>Environmental pollution</strong></td><td></td><td></td><td></td><td></td></tr></tbody></table>
<table><tr><td>Need to manage the balance of food security vs environmental P pollution</td><td>'Snap-shot' rather than dynamic techniques</td><td>Identify mechanisms from natural systems that can be applied in managed systems</td><td><ul><li>Understand which genes and transcripts control the microbial response to P<sub>o</sub></li><li>Understand microbial impacts on P<sub>o</sub> cycles</li><li>Understand the P limits to plants and microbes</li><li>Produce a molecular toolkit for studying microbial structure and function</li></ul></td><td>Opportunities from understanding Microbial Po: Function and dynamics</td></tr><tr><td><strong>Environmental change</strong><br>Warmer temperatures will shift the biogeochemical cycle of P<sub>o</sub></td><td>Operational methodologies lack biological relevance</td><td>Separate plant and microbial contributions to soil functions</td><td><ul><li>Understand P<sub>o</sub> interaction with natural and manmade nanoparticles</li><li>Assess the utility of nanoparticles to help manage the system</li></ul></td><td>Opportunities from interactions with nanoparticles</td></tr><tr><td><strong>Biogeochemical cycling from global to cellular scales</strong><br>P<sub>o</sub> compounds are vital for cell function and are moved globally as part of biogeochemical cycles and in the food chain</td><td>Lack of standardisation and quality control</td><td>Develop indicators for tipping points in ecosystem function – identify conditions of resistance, resilience and “points of no return”</td><td><ul><li>Model P dynamics in the environment</li><li>Develop conceptual models of cycling at a range of scales</li><li>Build empirical models using existing data</li><li>Produce a life cycle analysis of P<sub>o</sub></li></ul></td><td>Opportunities to use modelling of Po in soil and ecosystems</td></tr><tr><td><strong>Geopolitical stability</strong><br>P<sub>o</sub> as an alternative to mined P resources</td><td>Methodological limitations (matrix issues)</td><td>Allow scaling up in time and space through input to models</td><td><ul><li>Promote discussion of P<sub>o</sub> within the scientific community</li><li>Better communication with stakeholders and the public on the importance of P<sub>o</sub></li><li>Develop a central platform for knowledge exchange</li><li>Understand the needs and motivations of land managers and policy makers with respect to P<sub>o</sub></li><li>Emphasise educating the public in issues associated with P<sub>o</sub></li><li>Understand the socio-economic factors influencing P<sub>o</sub> dynamics</li><li>Improve the translation of research in P<sub>o</sub> to impactful outcomes</li></ul></td><td>Opportunities to better communicate and translate research</td></tr></table>