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Cryptic phosphorus in the environment: composition, behavior, and ecological significance
Benjamin L. Turner
Smithsonian Tropical Research Institute
What are cryptic forms of phosphorus?
Cryp·tic, adjective: 1. having a mysterious or hidden meaning
2. not recognized
3. serving to conceal
4. enigmatic
Organic and inorganic phosphorus that is….
• Hidden physically or chemically from organisms in the soil
• Hidden from our thinking about biological availability
Organic phosphorus and its importance in plant nutrition
• Abundant in soil – a large proportion of the phosphorus in
most soils is organic (up to 90% in wetlands)
• Abundant in phosphorus inputs to soil – much of the phosphorus in fresh plant litter
and microbial residues is organic
• Biologically available – organisms have evolved complex ways to
access soil organic phosphorus
Why has organic phosphorus been overlooked?
1. Agronomic perspective – most research has focused on mineral fertilizer and inorganic
phosphate loss
2. Bioavailability – most organisms appear to take up phosphorus only as
dissolved PO4 ions
3. Analytical chemistry – organic phosphorus has conventionally been difficult to
identify and quantify in environmental samples
O
OC
O
H2C
CHR2
C
O
CH2R1 O
CH3N+P
O-
O
O CH2 CH2
CH3
CH3
O
OC
O
H2C
CHR2
C
O
CH2R1 OO
CH3N+P
O-
O
O CH2 CH2
CH3
CH3
Phosphatidyl choline β-Glycerophosphate
HC P
OH
O
O
OH
CH2
CH2HO
HO
HC P
OH
O
O
OH
CH2
CH2HO CH2HO
HO
Phosphomonoesters
D-Glucose 6-phosphate
O OH
OH OH
H
P
OH
O
O HO O
OH
OH OH
H
P
OH
O
O HO
myo-Inositol hexakisphosphate
OPO3H2
OPO3H2 H2O3PO
OPO3H2
OPO3H2
H2O3PO
6 1
5 4
3
2
Adenosine 5’-triphosphate
Phosphoanhydrides
( α ) ( β ) ( γ )
O
OH OH
H H
H H
O P O
O
OH
P
O
OH
N
N N
N
NH
O P HO
O
OH
( α ) ( β ) ( γ )
O
OH OH
H H
H H
O P O
OH
P
N
N N
N
NH
N
N N
N
NH2
O P HO
O
OH
O P
Phosphonates
2-Aminoethyl phosphonic acid
P
O
OH
OH
CH2CH2H2N P
O
OH
OH
CH2CH2H2N
Phosphodiesters
Ribonucleic acid
Behavior of organic phosphorus in soils
• Inositol phosphates (phosphate monoesters)
• Phosphate diesters (DNA, RNA, phospholipids)
O
O C
O
H2C
CH R2
C
O
CH2 R1 O
CH3 N+ P
O-
O
O CH2 CH2
CH3
CH3
Phosphatidyl choline
Two ester bonds
OPO 3 H 2
OPO 3 H 2 H 2 O 3 PO
OPO 3 H 2
OPO 3 H 2
H 2 O 3 PO
6 1
5 4
3
2
myo-Inositol hexakisphosphate
Single ester bonds
The phosphorylated inositol stereoisomers: very cryptic!
Difference in the orientation of a single phosphate group
myo-inositol hexakisphosphate
P2
P3
P1
P4 P5
P6
scyllo-inositol hexakisphosphate
P2
P3
P1
P4 P5
P6
Nuclear magnetic resonance spectroscopy
Phosphonates
Inorganic phosphate
Phospholipids
Phosphate monoesters
Polyphosphate end-groups
Mid-chain polyphosphates
DNA
Pyrophosphate
Chemical shift (ppm)
-20 -10 0 10 20
Solution 31P NMR spectrum of an alkaline extract of a Swedish tundra soil
Differences among soils, climates and land-use
-20 -10 0 10 20
Tundra soil (Abisko, Sweden)
Pasture soil (Yorkshire, UK)
Arable soil (Idaho, USA)
Chemical shift (ppm)
• Loxahatchee NWR • Organic matter 90% • pH 5.8
-4 -2 0 2 4 6
Chemical shift (ppm)
DNA Pyro-P
Monoesters
Chemical shift (ppm) 4 5
α-glycerophosphate
β-glycerophosphate
RNA-derived mononucleotides
Phosphodiesters dominate the soil
organic phosphorus
7 6 5 4
Cryptic phosphorus in a Carolina Bay wetland • Savannah River, South Carolina • Total carbon 31% • pH 3.9
Phosphonates
Inositol phosphates
20 15 10 5 0 -5 -10 -15 -20 Chemical shift (ppm)
OPO3H2
OPO3H2 H2O3PO
OPO3H2
OPO3H2
H2O3PO
P
O
OH
OH
CH2CH2H2N P
O
OH
OH
CH2CH2H2N
Cryptic phosphorus in a tropical ombrotrophic bog
20 10 0 -10 -20
Chemical shift (ppm)
Polyphosphate (25% of total P)
• San San Pond Sak wetland, Panama • Organic matter >90% • pH <4.0
P O
O
OH
P
O
OH
O P HO
O
OH
O
OH
O
Plant strategies for acquiring soil organic phosphorus
• Synthesis of phosphatase enzymes – a ubiquitous response of plants to the
need for phosphorus
• Formation of mycorrhizal symbioses – some are extremely efficient at using
organic phosphates (e.g., ericoids)
• Secretion of organic anions – compounds like citrate can solubilize
large amounts of soil organic phosphorus
0
10
10
20
30
Phosphorus source (0.8 mM)
Plan
t dry
mas
s (m
g)
Root a bc bc cd cd d ab
a
bc
ab ab
b b b
c
d
Shoot
Organic phosphorus utilization by Arabidopsis
Resource partitioning for soil phosphorus?
Inositol phosphates (refractory organic P)
Species A Species B Species C Species D
Dissolved phosphate
Taken up directly from solution by roots or mycorrhizae (no hydrolysis required)
myo-Inositol hexakisphosphate
OPO3H2
OPO3H2 H2O3PO
OPO3H2
OPO3H2
H2O3PO
6 1
5 4
3
2
O
OC
O
H2C
CHR2
C
O
CH2R1 O
CH3N+P
O-
O
O CH2 CH2
CH3
CH3
O
OC
O
H2C
CHR2
C
O
CH2R1 OO
CH3N+P
O-
O
O CH2 CH2
CH3
CH3
Phosphatidyl choline
P
OH
HO
O
OH
Strongly bound to metal oxides, clays, and organic matter; requires both solubilization and hydrolysis by phytase to release free phosphate
Simple phosphate monoesters
(labile organic P)
D-Glucose 6-phosphate
O OH
OH OH
H
P
OH
O
O HO
Weakly sorbed in soil or dissolved in solution; hydrolyzed by phosphomonoesterase to release free phosphate
Phosphate diesters
Two ester bonds to the phosphate group; requires hydrolysis by both a phosphodiesterase and phosphomonoesterase to release free phosphate
Inorganic orthophosphate
Increasing investment in organic phosphorus acquisition
From: Turner (2008) Journal of Ecology 96, 698–702.
Summary
1. Importance in the environment – abundance in soils (especially wetland soils), abundance in
inputs to soils, variety of chemical forms
2. Plant strategies for acquisition of cryptic phosphorus – phosphatase enzymes, organic acids, mycorrhizal symbioses
3. Ecological significance – contribution to plant nutrition – distribution of plant species in nature – particular importance in freshwater wetlands....
Thanks: Alex Cheesman (STRI), Omar Lopez (INDICISAT), Sue Newman (pictured), Ramesh Reddy (UF), Jim Rocca (UF), Sofie Sjögersten (Nottingham), PV Sundareshwar (South Dakota)