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

TLDR: In this article, a group of experts consider the global issues associated with phosphorus in the terrestrial environment, methodological strengths and weaknesses, benefits to be gained from understanding the Po cycle, and to set priorities for Po research.

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.

Figures

Table 1 highlights carbon sequestration as a global issue but the trade off between utilization of Po and C is not really discussed? This is alluded to in section 3 when we discuss the use of organic P as a nutrient source and is implicit in the stoichiometry discussion. What about the role of Po in the remediation of contaminated soils - heavy metals inputs etc. This did not come up in any of the discussion groups and therefore did not make it into the consensus statements. Overall this is a very welcome contribution from the P research community and I fully support publication. I have issues with including so many authors but that must be a decision for the editor! Thank you again for the positive review of the paper and the authorship issue is discussed above in response to reviewer #1 and editor comments.

Fig1 Inositol phosphates have not always a "low soil lability" (whatever this means), in some cases inositol phosphates have been shown to be rapidly mineralized or to be absent from soil organic matter.

Fig1 Inositol phosphates have not always a "low soil lability" (whatever this means), in some cases inositol phosphates have been shown to be rapidly mineralized or to be absent from soil organic matter.

FIGURE 1. Organic phosphorus forms with generic and example structures and information on the relative 759 lability and prevalence in soil. (Adapted from Darch et al. (Darch et al. 2014)) 760 761

Full text

Organic phosphorus in the terrestrial environment: A perspective on
the state of the art and future priorities.
George, TS., Giles, CD., Menezes-Blackburn, D., Condron, LM., Gama-Rodrigues, AC., Jaisi, D., Lang, F., Neal,
AL., Stutter, MI., Almeida, DS., Bol, R., Cabugao, KG., Celi, L., Cotner, JB., Feng, G., Goll, DS., Hallama, M.,
Krueger, J., Plassard, C., ... Haygarth, PM. (2017). Organic phosphorus in the terrestrial environment: A
perspective on the state of the art and future priorities.
Plant and Soil
. https://doi.org/10.1007/s11104-017-3391-
x
Published in:
Plant and Soil
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Download date:10. Aug. 2022

Plant and Soil
Organic phosphorus in the terrestrial environment: A perspective on the state of the art
and future priorities
--Manuscript Draft--
Manuscript Number: PLSO-D-17-00622R1
Full Title: Organic phosphorus in the terrestrial environment: A perspective on the state of the art
and future priorities
Article Type: Special Issue S69 – OP2016
Keywords: cosystems services, Method development, Microbiome, Modelling, Organic
Phosphorus, Stoichiometry.
Corresponding Author: Tim S. George, Ph.D.
James Hutton Institute
Dundee, Scotland UNITED KINGDOM
Corresponding Author Secondary
Information:
Corresponding Author's Institution: James Hutton Institute
Corresponding Author's Secondary
Institution:
First Author: Tim S. George, Ph.D.
First Author Secondary Information:
Order of Authors: Tim S. George, Ph.D.
Courtney Giles
Daniel Menezes-Blackburn
Leo Condron
Tony Gama-Rodrigues
Deb Jaisi
Frederike Lang
Andrew Neal
Marc Stutter
Daniel Almeida
Roland Bol
K Carbugao
Luisella Celi
James Cotner
Gu Feng
Daniel Goll
M Hallama
Jaane Krueger
Claude Plassard
Anna Rosling
Tegan Darch
Tandra Fraser
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Reiner Giesler
Alan Richardson
Federica Tamburini
Charles Shand
David Lumsdon
Hao Zhang
Martin Blackwell
Catherine Wearing
Malika Mezeli
Åsgeir Almås
Yuki Audette
Isabelle Bertrand
E Beyhaut
Gustavo Boitt
N Bradshaw
Charles Brearley
Tom Bruulsema
Philippe Ciais
Vincenza Cozzolino
P Cuevas
Mariluz Mora
A de Menezes
Rosalind Dodd
Kari Dunfield
C Engl
J Frazão
Gina Garland
Jose González Jiménez
Jessica Graca
Stephen Granger
Anthony Harrison
Christine Heuck
E Hou
Penny Johnes
Klaus Kaiser
H Kjær
Erwin Klumpp
A Lamb
Katrina Macintosh
E Mackay
John McGrath
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Catherine McIntyre
Timothy McLaren
Eva Mészáros
Anna Missong
M Mooshammer
C Negrón
L Nelson
Verena Pfahler
P Poblete-Grant
Matt Randall
Alex Segeul
Kritarth Seth
Andrew Smith
Mark Smits
J Sobarzo
Marie Spohn
K Tawaraya
Mark Tibbett
P Voroney
Hakan Wallander
Lim Wang
Jun Wasaki
Philip Haygarth
Order of Authors Secondary Information:
Funding Information: Biotechnology and Biological Sciences
Research Council
(BB/K018167/1)
Dr. Tim S. George
Dr Courtney Giles
Dr Daniel Menezes-Blackburn
Dr Marc Stutter
Dr Tegan Darch
Dr Charles Shand
Dr David Lumsdon
Dr Hao Zhang
Dr Martin Blackwell
Ms Catherine Wearing
Prof Philip Haygarth
Biotechnology and Biological Sciences
Research Council
(BB/L025671/2)
Dr Tandra Fraser
Prof Mark Tibbett
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
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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
Response to Reviewers: Rebuttal Major Revisions requested PLSO-D-17-00622
Editor Comments
There are additional comments in the box for the Editor, but I will leave those out
except for one: "I do not like the multi-author list as they will not have all contributed to
this paper. Conference attendees could be listed in an Appendix." Please consider
that option, which makes sense, but I will leave it to you to decide how to proceed.
See response to comments below. We would like to keep the authorship as it is for this
submission.
Reviewer #1
This manuscript is difficult to review for a number of reasons. As an opinion piece it
represents the opinions, presumably, of the first 20 or so authors, and the 'assent' of
the remaining 70-odd (where alphabetical order begins). So, no new science is
presented in the manuscript. And as an opinion piece, the review of the various
identified areas and priorities is incomplete and not comprehensive. At least a third of
each section recapitulates basic facts and then cites some interesting observations
within each of those areas, usually by authors who are listed in the manuscript. As a
reviewer, there is actually little to review.
The written synthesis of the content is the work of the 20 or so of the first authors, but
all authors contributed to the production of the information that was synthesised and
therefore warrant inclusion in the author list. We have decided to keep the author list as
it is, as this authorship was offered to participants in the data collection part of the
process at the start and I would not want to go back on that agreement. There is no
new science presented as it is a synthesis of expert opinion and any perceived
blandness in the observations is down to trying to achieve a consensus statement
between 80+ authors with varying backgrounds and opinions. We are unable to
change the content as we went through a rational process to gather the information
and this is what we got. So the piece should either be considered a worthwhile
contribution as it is or not.
I disagree with a number of the areas listed here, yet, in reality it is irrelevant. For
example, a) a key area of organic P research focus should be on identifying the large,
non-phytate, fraction present, presumably, in the broad peak of NMR studies (Jarosch
et al. 2015); first identified by the chromatography work of Cosgrove half a century ago.
In reality, we don't know what half the organic P in soil actually is, yet that doesn't
seem to have been identified as a priority? b) Furthermore, there was acknowledged
(in the paper) disagreement at the conference about the value of standardised
methodologies and worldwide reference samples, with some arguing that fixing the
standards will advance organic P characterisation and others arguing against that
position. The consensus is oddly described, as many of the authors have published
more advanced deconvolution techniques that are moving the science forward and
allowing the characterisation and correction of methodological over-allocation of
different Po classes. This fluidity may not have occurred if standard methods were
fixed according to old methods. c) A comprehensive review of stoichometric ratios of
C:Po many years ago at a conference I attended made it very clear that the range is
wide, unlikely to be associated with specific compounds that are identifiable, and is
perhaps easily confused by metal-P linkages with P in organic attachments.
Suggesting great leaps can be made in this area struck me as optimistic. d) The land
management section describes reasonably clearly that withdrawing P fertiliser results
in drawdown of inorganic P sources (and some accumulation of Po)(lns 255-266), yet
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Frequently asked questions

Q1. What are the contributions in "Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities" ?

The authors asked a group of experts to consider the global issues associated with Poin the terrestrial 69 environment, methodological strengths and weaknesses, benefits to be gained from understanding the Po cycle, 70 and to set priorities for Po research. Po cycles ; the implications of nanoparticles in the environment and the need for better modelling and 75 communication of the research. 

Q2. What is the role of the Pho regulon in the soil microbiome?

The Pho regulon also acts as a major regulator of other cellular processes, including N assimilation 293 and ammonium uptake (Santos-Beneit 2015). 

Q3. How many people are needed to build models with great potential use to predict changes in Po bioava?

The cooperation 400 of modellers and empiricists is essential for building models with great potential use to predict changes in Po 401 bioavailability due to land-use and management change and to infer the sustainability of the system as a whole. 

Q4. What is the priority for researchers to develop methods to determine total Po in soils?

It is a priority for researchers to further develop methods, while 191 also refining existing Po methods and standards, to generate useful and comparable datasets and to build a 192 consensus with respect to Po dynamics and function in agricultural and natural ecosystems. 

Q5. What is the way to determine the availability of P in soils and sediments?

A better understanding of interactions between plants and microbes 305 would facilitate identification of functional redundancy among them, which could ultimately help manage the 306 availability of P in soils and sediments by selection of the optimal plant rhizosphere compliment. 

Q6. What is the need for a central platform for Po research and communications?

Po research and communications is still needed, to connect existing forums to global research networks and 417 would include features such as researcher membership, methodological resources, links to relevant 418 organizations and platforms, and a clearing house of Po data for future meta-analysis and modelling efforts. 

Q7. What is the role of key stakeholder groups in the development of the Po research?

419 Key stakeholder groups such as land managers, farmers and extension services are a natural link between 420 industry, government, and academia (FAO 2016). 

Q8. What is the way to determine total Po in soils?

Visible Near-Infrared Reflectance Spectroscopy (VNIRS) has shown some promise for 179 determining total Po in soils (Abdi et al, 2016), but further testing is needed. 

Q9. What is the need for a commercial supply of other commonly identified Po compounds in soils?

Po compounds in soils, such as scyllo-inositol hexakisphosphate, to allow the use of appropriate 189 substrates for research fully understand the biological and chemical processes controlling the behaviour of this 190 and other Po compounds in the environment. 

Q10. What is the relative lability of the different groups of Po compounds in soil?

The relative lability and accumulation of these different groups varies in the environment, but 115 overall the labile monoesters and diesters tend to be less prevalent and the inositol phosphates tend to be less 116 labile and accumulate in the environment (Darch et al. 2014). 

Q11. What is the importance of a non-destructive method to analyse soil pools?

175It is critical to develop non-destructive methods to analyse soil pools and their dynamics without the need for 176 extraction. 

Q12. What is the main argument for reducing reliance on organic P fertilisers?

The first is that the authors must reduce reliance on traditional inorganic P fertilisers (ie primary P) in the future, and strategies towards reducing reliance on soil inorganic P fertility (ie lowering critical soil P) will increase the relevance of soil organic P for providing available P for general ES provision. 

Q13. What is the need for the community to identify standardized reference materials?

There is a need for the community to identify standardized 183 natural reference materials such as soils and manures, but a large amount of effort would be needed to put 184 together a collection of appropriate materials as well as a means to share them internationally. 

Q14. What are the key opportunities to understand Po dynamics for sustainable P use in tropical systems?

Po dynamics for sustainable P use in tropical systems and for forests growing on marginal soils, both of which 250 depend on effective management of Po resources.