Carbon addition reduces labile soil phosphorus by increasing microbial biomass phosphorus in intensive agricultural systems

Abstract

Accumulation of inorganic and labile organic phosphorus (P) in intensive agricultural systems leads to P loss from soil which can cause serious environmental problems. Soil microbes are important in mobilizing soil non‐available P, however, little is known about the role of soil microbes in immobilizing P to reduce P loss. Here, we test whether stimulating microbial biomass to immobilize P could reduce the amount of labile P available for leaching. The distribution characteristics of Olsen P, organic P and microbial biomass P were determined in three intensive agricultural systems. In addition, we conducted a pot experiment with three P and four carbon (C) levels. CaCl2 extractable P was measured and used to indicate the risk of P leaching. We found that there was a positive relationship between soil organic C and microbial biomass P. Carbon addition drove the process of P immobilization and reduced CaCl2 extractable P. Microbial biomass P increased by 64% (P<0.05) with the addition of C, and Olsen P and CaCl2 extractable P decreased by 28% and 17%, respectively. Our results show that C addition increased microbial immobilization of P and reduced forms of labile P susceptible to leaching. Stimulating microbes to immobilize P by adding C to soils has the potential to reduce P loss from intensive agricultural systems, reducing their environmental impact.

Full text

Soil Use Manage. 2020;00:1–11. wileyonlinelibrary.com/journal/sum
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© 2020 British Society of Soil Science
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INTRODUCTION
Meeting the increasing demand for food by an ever- increasing
world population is one of the biggest challenges in the 21st
century. In recent decades, preserving high crop productivity
has depended mainly on fertilizer inputs and intensive land
use management (Tokatlidis et al., 2011). These measures
lead to a large amount of phosphorus (P) accumulation in the
soil and increase the environmental risks of intensive agricul-
tural systems (George, Hinsinger, & Turner, 2016; Li et al.,
2011; Maharjan, Sanaullah, Razavi, & Kuzyakov, 2017).
Olsen P is used to estimate soil P availability to crops
employing 0.5M NaHCO3 to extract labile soil P (Olsen &
Sommers, 1982). Previous studies have demonstrated that
P accumulation is widespread and soil Olsen P is above the
threshold considered for the onset of P leaching in many in-
tensive agricultural systems (Gao et al., 2014; Li, Liu, Shen,
Bergström, & Zhang, 2015), which has led to environmental
problems and ultimately impacted agricultural sustainability
(Turner, Lambin, & Reenberg, 2007). This problem of exces-
sive addition of P to soil is apparent in China in particular.
According to an investigation of 916 surveyed orchards in
Received: 26 February 2019
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Revised: 13 February 2020
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Accepted: 13 February 2020
DOI: 10.1111/sum.12585
RESEARCH PAPER
Carbon addition reduces labile soil phosphorus by increasing
microbial biomass phosphorus in intensive agricultural systems
ZhenXu1
|
MingshanQu2
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ShenglinLiu3
|
YishengDuan1
|
XiaoWang1
|
Lawrie KBrown4
|
Timothy SGeorge4
|
LinZhang1
|
GuFeng1
1Beijing Key Laboratory of Biodiversity
and Organic Farming, China Agricultural
University, Beijing, China
2Beijing Soil and Fertilizer Work Station,
Beijing, China
3Shandong Academy of Agricultural
Sciences, Jinan, China
4The James Hutton Institute, Dundee, UK
Correspondence
Gu Feng, Beijing Key Laboratory of
Biodiversity and Organic Farming, China
Agricultural University, Beijing, 100193,
China.
Email: fenggu@cau.edu.cn
Funding information
National Key Research and Development
Program of China, Grant/Award Number:
2017YFD0200200; National Natural
Science Foundation of China, Grant/Award
Number: U1703232; NSFC and RS jointly
supported project, Grant/Award Number:
31711530217
Abstract
Accumulation of inorganic and labile organic phosphorus (P) in intensive agricultural
systems leads to P loss from soil which can cause serious environmental problems.
Soil microbes are important in mobilizing soil non- available P, however, little is
known about the role of soil microbes in immobilizing P to reduce P loss. Here, we
test whether stimulating microbial biomass to immobilize P could reduce the amount
of labile P available for leaching. The distribution characteristics of Olsen P, organic
P and microbial biomass P were determined in three intensive agricultural systems.
In addition, we conducted a pot experiment with three P and four carbon (C) levels.
CaCl2 extractableP was measured and used to indicate the risk of P leaching. We
found that there was a positive relationship between soil organic C and microbial
biomass P. Carbon addition drove the process of P immobilization and reduced CaCl2
extractableP. Microbial biomass P increased by 64% (p<.05) with the addition of
C, and Olsen P and CaCl2 extractableP decreased by 28% and 17%, respectively. Our
results show that C addition increased microbial immobilization of P and reduced
forms of labile P susceptible to leaching. Stimulating microbes to immobilize P by
adding C to soils may have the potential to reduce P loss from intensive agricultural
systems, reducing their environmental impact.
KEYWORDS
carbon addition, microbial immobilization, phosphorus accumulation, phosphorus loss

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XU etal.
North China, P application was 2.5–3.0 fold greater than the
P required for optimum fruit yield (Lu, Yan, Chen, & Zhang,
2012). Similarly, in an investigation of vegetable systems in
China, the average soil Olsen P was about 179mg kg−1 in
greenhouses and 100mg kg−1 in open fields, exceeding the
critical level (46.0–58.0mg P kg−1) for optimum vegetable
yield (Yan et al., 2013). Even in cereal systems, Olsen P was
greater than the optimum P level for wheat and maize yield
(Li, Liu, Shen, Bergström, & Zhang, 2015). To avoid soil
P loss to the wider environment from intensive agricultural
systems, it is important to reduce the amount of P going in
to these systems or to reduce the susceptibility of this P to
leaching.
Soil microbes play important roles in the P cycle (Khan,
Zaidi, & Wani, 2007). On one hand, microbes secrete pro-
tons, carboxylates and phosphatases, which mobilize organic
and inorganic P (Jorquera, Hernandez, Rengel, Marschner,
& de la Luz Mora, 2008; Richardson, Barea, McNeill, &
Prigent- Combaret, 2009). On the other hand, microbes can
immobilize soil P into the microbial biomass P (Wu et al.,
2007). The propensity of microbes to immobilize or mobilize
P is dependent on their activity and the inherent carbon (C):P
stoichiometry in the soil (Stutter et al., 2015). Many stud-
ies have focused on the effects of organic fertilizer, biochar
and straw on increasing soil microbial activity, community
composition and biomass in intensive agricultural systems
(Luo, Lin, Durenkamp, & Kuzyakov, 2018; Wang, Xiong, &
Kuzyakov, 2016; Zhu et al., 2010). The commonality in the
effect of these organic amendments is increased microbial
activity driven by C addition (Butterly, Bünemann, McNeill,
Baldock, & Marschner, 2009). Importantly, this addition of C
may promote the transformation of available inorganic P to
microbial biomass P (Zhang, Ding, Peng, George, & Feng,
2018). Microbial activity drives P dynamic transformation
and plays an important role in determining whether P is avail-
able to plants, stored in the soil or available to be lost from
the plant- soil system (Bender & van der Heijden, 2015; van
der Heijden, Bardgett, & van Straalen, 2008). Several stud-
ies have addressed the importance of soil microbes and their
interactions for nutrient mineralization and plant nutrition
(Sharma, Sayyed, Trivedi, & Gobi, 2013).
Recent research has begun to elucidate the mechanism
of microbial mineralization of soil P (Zhang et al., 2014).
However, fewer studies have paid attention to the function of
microbes in immobilizing soil inorganic P into the microbial
biomass P (Oehl et al., 2001; Wu et al., 2007). Many stud-
ies have indicated that the addition of organic matter, plant
rhizodeposition and glucose addition increase soil microbial
biomass P in both laboratory and field conditions (Kouno,
Wu, & Brookes, 2002; Kuzyakova, Friedelb, & Stahr, 2000;
Liu etal., 2009; Lloyd, Ritz, Paterson, & Kirk, 2016). Taken
together, most studies focus on how to use soil microbes to
mobilize soil P (Richardson & Simpson, 2011) and to turn
over microbial biomass P (Schneider et al., 2017), neglect-
ing their potential effect on P immobilization. Increasing the
microbial biomass P pool may decrease excess soil labile
P (Zhang, Ding, Peng, George, & Feng, 2018) suggesting
that there is an opportunity to reduce the risk from excess
P in intensive agricultural systems by encouraging microbial
immobilization.
In the present study, we investigated whether increas-
ing microbial biomass P could reduce labile P which would
imply that leaching of P from the intensive agricultural sys-
tems would also be reduced. We raised the following two
hypotheses: (a) microbes immobilizing soil inorganic P
potentially reduce the risk of P loss, (b) soil organic C is
a driver for enhancing immobilization of P into microbial
biomass P. To test our hypotheses, we collected field soils
from three typical intensive agricultural systems and studied
the status of labile P, and the relationship between microbial
biomass P and CaCl2 extractableP. We further conducted a
pot experiment to assess whether enhancing microbial bio-
mass P induced by C addition would reduce the P content in
leachable forms.
2
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MATERIALS AND METHODS
2.1
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Field investigation
We determined P distribution and characteristics of soil pro-
files in field investigations in 2016. Three intensive agricul-
tural systems including vegetable greenhouse (V), orchard
(O) and grain (G) were sampled as examples of systems with
excessive soil P, based on the data from a long- term moni-
toring site at the Beijing Soil and Fertilizer Work Station in
Daxing district, Beijing, China. The spatial range of sam-
pling was from 39◦26′- 39◦51′N to 116◦13′- 116◦43′E and
the locations of the sampling points are shown in Figure1.
The annual average temperature was 11.6°C and the rainfall
556mm. The soil type was fluvo- aquic according to USDA
soil classification. Top soil samples (0–20cm) from three ag-
ricultural systems were collected separately to measure basic
soil physical and chemical properties (Table1).
The different intensive agricultural systems received dif-
ferent amounts of manure and chemical fertilizer, although
within a system the same amount of manure and chemical
fertilizer was added every year. Manure and chemical fertil-
izer inputs are shown in Table2. For V, vegetables had been
grown for 8years. There were five vegetable species grown,
including long bean, cauliflower, cabbage, crown daisy and
broccoli. For O, fruit had been grown for 20years. There
were three fruit species grown including pear (two variet-
ies), plum (two varieties) and apricot. For G, winter wheat
and summer maize had been grown in rotation for 5years.
Each replicate from the V, O and G systems was an average

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XU etal.
area of 500, 10,000 and 3,000m2, respectively. After crop
and fruit harvest, soil samples were collected in the field.
The treatments were defined as the three intensive systems,
and the five sampling points from each system were treated
as the five replicates. In order to reduce any confounding
effects of spatial location and soil textural composition on
the status of labile P, we selected the same soil type with
similar clay contents (6.7%–14.7%). Five cores from each
replicate were taken in an X configuration and thoroughly
mixed into a bulked soil sample. Each core in the three sys-
tems was separated by 10, 50 and 15m from each other, re-
spectively. Samples were taken to 60cm depth and divided
into three soil layers of 20cm (0–20, 20–40, 40–60 cm).
All soil samples were immediately sieved through a 2mm
mesh and divided into two parts. One part was kept fresh
and stored at 4°C for analysis of microbial biomass P. The
other part was air- dried at room temperature (~25°C) for
measuring Olsen P, organic P, CaCl2 extractableP and soil
organic C.
2.2
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Carbon addition pot experiment
The soil was taken from Changping District in the long- term
fertilizer experiment of Beijing, China Agricultural University
(40◦8′20″N, 116◦10′47″E). The properties of the soil are
shown in Table1. The soil was passed through a 2- mm sieve
before being placed in plastic pots (18cm in height, 16cm in
diameter, 2kg of soil per pot).
The pot experiment was a 3×4 completely factorial de-
sign, there were three P levels (0, 228, 570mg P kg−1 soil as
monopotassium phosphate; 0, 1.0, 2.5g pot−1) and four C lev-
els (0, 1.5, 3, 5g kg−1 as glucose). To test our hypothesis, we
used relatively high P additions, consistent with soil P applica-
tion in intensive agricultural systems. Potassium sulphate was
supplied at the rate of 1.62, 0.97, 0g pot−1, depending on the
P levels to balance the potassium addition. According to the
nutrient demand for cotton, the following mineral nutrients
were added uniformly (per kilogram soil): 200mg of nitrogen
(as potassium nitrate), 50mg of magnesium (as magnesium
FIGURE 1 The locations of sampling
points in three intensive systems. Rhombic
points represent the vegetable greenhouse
system (V), circular points represent the
orchard system (O) and triangles represent
the grain system (G)
Beijing Daxing District
V
N
01020406
08
0
km
O
G
TABLE 1 General soil properties in the field and pot experiment
Experiment Soil type
Soil texture
SOC (g kg−1)
Total N
(g kg−1)
Olsen P
(mg kg−1)
Available K
(mg kg−1) pHSand (%) Silt (%) Clay (%)
Vegetable system Fluvo- aquic 24.0 61.3 14.7 18.8 1.26 218 439.2 7.86
Orchard system Fluvo- aquic 26.3 67.0 6.7 13.8 0.67 60.8 165.4 7.86
Grain system Fluvo- aquic 27.6 63.3 9.1 11.6 0.52 9.6 45.5 8.85
Pot experiment Fluvo- aquic 34.3 44.4 21.4 5.78 0.43 10.5 37.61 6.51
TABLE 2 Crop types, manure and chemical fertilizer inputs in the field
System Crop type
Manure type and application
rate
Chemical fertilizer type and
application rate
Vegetable greenhouse Long bean, Cauliflower, Cabbage Chicken manureaCompound fertilizer
Crown daisy, Broccoli 30,000kg ha−1year−1 15- 15- 15, 675kg ha−1year−1
Orchard Pear species, Plum species Chicken manureaCompound fertilizer
Apricot species 30,000kg ha−1year−1 15- 15- 15, 300kg ha−1year−1
Grain Winter wheat- summer maize – Compound fertilizer
18- 17- 10, 750kg ha−1year−1
aChicken manure composition was 20.1g N kg−1, 7.9g P kg−1, and 14.8g K kg−1.

4
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XU etal.
sulphate), 5mg of zinc (as zinc sulphate) and 2mg of copper
(as copper sulphate). There were four replicates per treatment,
giving 64 pots in total. The pots were arranged in randomized
blocks in the greenhouse, and the position of each block was
re- randomized weekly.
Cotton (cv. Xinluzao90) was grown under greenhouse
conditions in March 2017. Seeds of cotton were surface
sterilized in 10% (v/v) hydrogen peroxide for 10min and
rinsed at least five times in deionized water. Three germi-
nated seeds were sown into each pot and were thinned to
one seedling per pot after emergence. Deionized water was
supplied daily, and the pots were weighed every 3days to
adjust soil moisture content to 20% (w/w); differences in
plant weight between treatments were ignored. The tem-
perature ranged from 25 to 30°C day and night. Plants
were harvested 7 weeks after sowing. Shoot samples
were oven- dried at 60°C, weighed for plant biomass, and
then milled for determination of shoot P concentration.
Shoot P concentration was measured by the molybdo-
vanadophosphate method after samples were digested in
concentrated H2SO4 and H2O2 (Shi, 1986). Soil in the
pot was mixed and collected immediately. After passing
through a 2 mm sieve, soil was divided into two parts.
One part was air- dried to determine soil Olsen P, labile
organic P, organic C and CaCl2 extractableP. The other
part was stored at 4°C before being analysed for microbial
biomass P.
2.3
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Sample analysis
Microbial biomass P was extracted using the chloroform
fumigation- extraction method (Brookes, Powlson, &
Jenkinson, 1982), determined colorimetrically by a modi-
fied ammonium molybdate ascorbic acid method and cal-
culated using a kp value of 0.40, where kp is the fraction
of P extracted after fumigation. Correction of microbial
biomass P was made using recovery of added phosphate
(Brookes etal., 1982). Briefly, fresh soil was adjusted to
a soil moisture ranging from 10% to 15%. Then three in-
dividual portions of 5.63g fresh soil (about 5g dry soil)
were weighed into jars. One portion was fumigated with
chloroform, one portion was left unfumigated and another
was spiked with 0.5M KH2PO4 to assess P recovery. Three
soils were incubated in an evacuated desiccator for 24hr
and then extracted with 100ml of 0.5 M NaHCO3 solu-
tion in the same way. Olsen P was measured by extract-
ing soil samples with 0.5M NaHCO3 at pH 8.5 using the
molybdo- vanadophosphate method (Pierzynski, 2000).
Labile organic P in the solution was calculated by subtract-
ing the Olsen P from the total P (Aspila, Agemian, & Chau,
1976). Soil organic C was determined using the potassium
dichromate volumetric method (Mebius, 1960) using an
automatic analyzer (Multi N/C2100), and calcium chloride
extractable P was obtained by shaking 2.0 g soil sample
with 20ml of 10mM CaCl2 solution for 1hr (Sparks etal.,
1993) followed by analysis with the molybdate blue method
(Murphy & Riley, 1962).
2.4
|
Statistical analyses
The results presented are arithmetic means of five replicates
in the field experiments and four replicates in the pot experi-
ment. In the field experiment, the content of soil Olsen P, la-
bile organic P, microbial biomass P and CaCl2 extractableP
was compared among intensive systems and soil layers using
two- way analysis of variance (ANOVA). In the pot experi-
ment, plant biomass, P uptake, Olsen P, microbial biomass P
and CaCl2 extractableP were compared among P levels and
C additions using two- way analysis of variance (ANOVA) at
a significance level of p<.05 using the statistical software
SAS version 6.12 (SAS Institute). Linear and quadratic re-
gression was used to determine the relationship between soil
organic C and microbial biomass P, CaCl2 extractableP and
the ratio of microbial biomass P to Olsen P. The significance
of temporal trends was analysed by regression analysis using
Sigma Plot 12.5 (Systat).
3
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RESULTS
3.1
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Olsen P, organic P, microbial biomass P
and soil organic C in the three soil layers
The interaction between depth distribution and intensive ag-
ricultural system significantly influenced Olsen P (p<.001)
and organic P (p<.001) extracted by NaHCO3 (Table.3).
Among the three intensive agricultural systems, Olsen P and
organic P were in the order V>O>G (Figure2a,b). Olsen P
under V (204.2mg kg−1) was almost ten times that under O
(20.1mg kg−1) and five times that under G (41.6mg kg−1).
Olsen P was significantly greater in the 0–20cm soil layer
than the other two layers under V (Figure 2a; p <.001).
Similarly, organic P under V (17.6mg kg−1) was more than
five times that under the O (3.0mg kg−1) and G (3.5 mg
kg−1) systems. Organic P in the 0–20cm layer was signifi-
cantly greater than in the 20–40cm layer (5.1mg kg−1) and
40- 60cm layer (2.9mg kg−1) under V (Figure2b).
The interaction between soil depth and intensive agri-
cultural system did not influence the microbial biomass P
significantly (p=.56, Table.3). But the interaction between
soil depth and intensive agricultural system significantly
influenced soil organic C (p <.001, Table.3). Microbial

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XU etal.
biomass P and soil organic C were significantly greater
under V than the other cropping systems for the 20–40cm
layer (Figure2c,d). Microbial biomass P in the 0–20cm layer
(14.4mg kg−1) was significantly greater than in the 20–40cm
layer (8.4mg kg−1) and the 40–60cm layer (4.4mg kg−1)
under G. Microbial biomass P in the 0–20cm layer (22.0mg
kg−1) and the 20–40cm layer (24.1mg kg−1) was signifi-
cantly greater than that in the 40–60cm layer (9.4mg kg−1)
under V. There were no significant differences among three
soil layers under O (Figure2c). Similarly, soil organic C in
the 0–20cm and 20–40cm layer was significantly greater
than in the 40–60cm layer among three intensive systems.
TABLE 3 ANOVA results for soil layer and intensive system treatment as independent variables and their interaction, for Olsen P, organic P,
microbial biomass P and soil organic C as dependent variables in the field experiment
Independent
variable
Olsen P Organic P Microbial biomass P Soil organic C
df F p- Value df F p- Value df F p- value df F p- Value
Soil layer 2 40.1 <.0001 2 23.79 <.0001 2 5.86 .0068 2 10.14 .0004
Intensive system 2 24.49 <.0001 2 19.06 <.0001 2 9.87 .0005 2 37.39 <.0001
Soil layer ×
Intensive system
412.97 <.0001 4 9.74 <.0001 4 0.75 .5626 4 7.39 .0002
FIGURE 2 Olsen P (a), labile organic P (b) extracted by NaHCO3, microbial biomass P (c) and soil organic C (d) in three intensive
agricultural systems. V, O and G represent the vegetable greenhouse system, orchard system and grain system, respectively. Capital letters indicate
a significant difference in Olsen P, organic P, microbial biomass P and soil organic C among the three soil layers (p<.05). Small letters indicate a
significant difference in Olsen P, organic P, microbial biomass P and soil organic C among the three intensive agricultural systems (p<.05). Error
bars represent SEs (n=5)
Soil organic C (mg kg
–1
)
036912 15
Aa
Aa
Aa
Aa
Ba
Bb
Ab
Ab
Ab
(d)
Microbial biomass P (mg kg
–1
)
0102030
Soil layer (cm)
0–20
20–40
40–60
Aa
Aa
Aa
Aa
ABa
Bb
Ab
Ab
Ab
(c)
Organic P (mg kg–1)
0510 15 20
Aa
Ab
Ab
Ba
ABb
Ab
Ba
Bb
Ab
(b)
Olsen P (mg kg–1)
050 100 150 200 250
Soil layer (cm)
0–20
20–40
40–60
G
O
V
Aa
Ab
Ab
Ba
Ab
Bb
Ba
Aa
Ba
(a)

6
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XU etal.
The soil organic C in the 20–40cm layer (10.1g kg−1) was
greatest and significantly greater than the 40–60 cm layer
(2.9g kg−1) under V(Figure2d). Soil organic C showed a
significantly positive linear correlation (R2= .52) with mi-
crobial biomass P (Figure3).
3.2
|
Relationships between CaCl2
extractableP and other pools with depth
Correlations between CaCl2 extractableP and microbial bi-
omass P showed that where there was more microbial bio-
mass P there was less CaCl2 extractableP (Figure4a,b). The
CaCl2 extractableP had a negative linear relationship with the
ratio of microbial biomass P to Olsen P in the 0–20cm layer
(Figure4a; R2=.36) and in the 20–40cm layer (Figure4b;
R2=.25). There was no relationship between CaCl2 extract-
able P and the ratio of microbial biomass P to Olsen P in
40–60cm layer (Figure4c). With the increase of microbial
biomass P, CaCl2 extractableP decreased significantly in the
three intensive systems (Figure4a,b; p<.05), especially in
the 0–20cm soil layer (Table4).
3.3
|
Plant biomass and P uptake in the
pot experiment
Plant shoot biomass did not vary in response to P addition,
but was affected by C addition (p=.002). Plant P uptake
was significantly affected by P (p =.003) and C addi-
tion (p<.001) (Figure5). Plant biomass significantly de-
creased from 14.1 to 4.8g pot−1 with increasing C addition
(Figure5a; p <.05). Plant P uptake as measured per pot
increased on average by 0.02 and 0.04 g pot−1 under the
P228 and P570 treatment, respectively, compared to the P0
FIGURE 3 Correlation between soil organic C and microbial
biomass P. Each dot represents the average of each sampling plot
in three intensive agricultural systems. Rhombic points represent
vegetable greenhouse system (V), circular points represent orchard
system (O) and triangles represent grain system (G). ** means the
regression relationship is significant at the p<.01 level
Soil organic C (g kg
–1
)
036912 15
Microbial biomass P (mg kg
–1
)
0
10
20
30
40
50
G
O
V
y = 2.6123x – 2.4242
R
2
= .525**
N = 45
FIGURE 4 The relationship between CaCl2 extractable P and
the ratio of microbial biomass P (MBP) and Olsen P on the 0–20cm
layer (a), 20–40cm layer (b), 40–60cm layer (c). ** means regression
relationship is significant at p<.01 level. Rhombic points represent
the vegetable greenhouse system (V), circular points represent the
orchard system (O) and triangles represent the grain system (G). Each
point represents a soil sample from the field. ** means the regression
relationship is significant at the p<.01 level
Microbial Biomass P/Olsen P
0.0 .5 1.01.5 2.0
CaCl2 extractable P (mg kg–1)
0.0
.1
.2
.3
.4
.5
.6
N = 15
40-60 cm (c)
0.0 1.5 3.04.5 6.0
CaCl2 extractable P (mg kg–1)
0.0
.1
.2
.3
.4
.5
.6
20-40 cm (b)
y = 0.0049x
2
– 0.0554x + 0.1523
R
2
= .26**
N = 15
0.0 .5 1.01.5 2.0
CaCl2 extractable P (mg kg–1)
0.0
.1
.2
.3
.4
.5
.6
G
O
V
y = 0.1081x
2
– 0.3314x + 0.304
R
2
= 0.39**
N = 15
0-20 cm (a)

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XU etal.
treatment (Figure5b). Compared to the C0 treatment, plant
P uptake under the C1.5 and C3.0 treatment did not vary
significantly. When C addition was 5.0g kg−1, plant P up-
take decreased significantly compared to the C0 treatment
(p<.05).
3.4
|
Microbial biomass P, Olsen P and
CaCl2 extractableP in pot experiment
The interaction between P level and C addition sig-
nificantly influenced Olsen P (p <.001), microbial bio-
mass P (p <.001) and CaCl2 extractable P (p <.001)
(Table4). Microbial biomass P increased significantly in
the treatments with C addition, ranging from 13% to 136%
(Figure6a; p<.05). In the absence of cotton, there was a C
priming effect, and the increase of microbial biomass P ac-
centuated by the addition of C, ranging from 81% to 103%.
Carbon addition decreased Olsen P (Figure6b) and CaCl2
extractable P consistently (Figure 6c). Carbon addition
increased microbial biomass P by an average of 2.4 mg
kg−1 under the P0 treatment and by 12.8mg kg−1 under the
P570 treatment. Meanwhile, soil Olsen P decreased signifi-
cantly by an average of 4.7mg kg−1 under the P0 treatment
and by 28.1mg kg−1 under the P570 treatment (p<.05).
Similarly, CaCl2 extractable P decreased significantly by
FIGURE 5 Plant biomass (a), plant P uptake (b) for cotton
grown in the pot experiment and treated with four C levels (0, 1.5, 3.0,
5.0g kg- 1 glucose) and three P levels (0, 228 and 570mg kg- 1 P).
Different lower case letters under the same P level indicate a
significant difference at different C addition rates (p<.05). Bars
represent means +SE
Plant P uptake (g pot–1)
0.00
.02
.04
.06
.08
a
aa
b
a
a
a
b
ab
ab
a
b
(b)
P228 P570P0
Plant biomass (g pot–1)
0
5
10
15
20
ab
a
b
c
a
b
c
d
b
b
a
c
C0
C1.5
C3.0
C5.0
(a)
FIGURE 6 Microbial biomass P (a), Olsen P (b) and CaCl2
extractable P (c) in soils taken from the pot experiment following
growth and treatment with four C levels (0, 1.5, 3.0, 5.0g kg- 1 glucose)
and three P levels (0, 228 and 570mg kg- 1 P). P0* represents the no
cotton plant and no P addition treatment. Different lower case letters
under the same P level indicate a significant difference at different C
addition rates (p<.05). Bars represent means +SE
CaCl2 extrectable P (mg kg–1)
0
2
4
20
40
60
aaaaabbb
ab
cc
a
bc
c
P0* P0 P228 P570
Olsen P (mg kg–1)
0
5
10
15
100
150
200
250
300
a
bbba
b
cbc
abbb
abbb
Microbial biomass P (mg kg–1)
0
10
20
30
40
50
60
baaabaaa
b
ab a
ab
b
b
a
a
C0
C1.5
C3.0
C5.0
(a)
(b)
(c)

8
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XU etal.
0.2mg kg−1 under P0 treatment and by 20.5mg kg−1 under
the P570 treatment, with C addition (p<.05).
4
|
DISCUSSION
4.1
|
Phosphorus accumulation in three
intensive agricultural systems
P accumulation in the 0–20cm layer was large (Figure2) and
led to high concentrations of CaCl2 extractableP (Figure4).
Such results suggest that these soils are at high risk of P
leaching which poses a threat to the quality of the aquatic
environment (Khan et al., 2018; Li, Shen, Bergström, &
Zhang, 2015). Cotton biomass did not increase in response
to P application because of the relatively high background
of 10.5mg kg−1 Olsen P (Figure4a). Nevertheless, when
excessive P was applied under the P228 and P570 treat-
ments, P accumulated in the soil. In previous studies, the P
leaching change- points of inorganic P ranged from 39.9 to
90.2mg kg−1, above which soil CaCl2 extractableP greatly
increased with increasing soil Olsen P (Bai et al., 2013).
Soil microbes immobilizing P to microbial biomass and
turnover of the microbial biomass are considered to be dy-
namic transformation processes (Wu et al., 2007). We hy-
pothesized that microbes immobilizing P provided a novel
possibility to reduce the excessive P in intensive agricul-
tural systems. We found that microbial biomass P in V was
greater than that in O and G (Figure2). CaCl2 extractableP
in V was less than that in G. Despite the largest content of la-
bile P in V (Figure2a,b), CaCl2 extractableP was no greater
than the other systems (Figure4a,b). This may attributed to
the increase of microbial biomass P. Djodjic, Börling, and
Bergström (2004) suggest that the capacity of soil to absorb
P was also an important factor influencing P leaching. We
believe that the decrease of CaCl2 extractableP in V may
be partly because of the higher (14.7%) clay content in the
soil. Therefore, our observation suggested that increasing
microbial immobilization of labile P into microbial biomass
may reduce excessive labile P in the topsoil. It is critical to
know how to manage soil microbial activities to maximize
the immobilization of labile P.
4.2
|
Regulation of microbial
P immobilization by increasing
soil organic carbon
The present study showed that soil organic C was positively
related to microbial biomass P (R2=.52, Figure3) and organic
C drove the microbial immobilization of P process, as reported
in a previous study (Stutter et al., 2015). Heterotrophic soil
microbes take advantage of low- molecular weight organic
substrates or labile C for nourishment (Dennis, Miller, &
Hirsch, 2010; Pausch & Kuzyakov, 2018). Several studies
have found that incorporation of biochar and organic amend-
ments increases the relative abundance of soil microbes (Liu
et al., 2009; Luo, Lin, Durenkamp, & Kuzyakov, 2018), stimu-
lating soil microbial activities (Kouno, Wu, & Brookes, 2002;
Wang, Xiong, & Kuzyakov, 2016) and enhancing microbial
biomass P (Meier, Finzi, & Phillips, 2017). In these situations,
increasing soil microbial biomass was mainly due to greater C
availability (Huang et al., 2016). Similarly, our study indicates
that C (in the form of glucose) addition significantly increased
microbial biomass P ranging from 15% to 136% (Figure6a).
In our pot experiment, especially, soil CaCl2 extractableP
declined with plant growth which suggests that the potential
risk of leaching was greater without a plant present (Figure6,
Table4). Microbial biomass P increased in the range 60% to
111% under no cotton and P treatment. Importantly, we found
C addition decreased Olsen P significantly by 36% without
plant growth and P application by an average of 10% with
570mg kg−1 P (Figure6b; p<.05).
Phosphorus extracted by CaCl2 solution is usually used to
predict P leaching risk (Hesketh & Brookes, 2000) and pro-
vides a reliable criteria for identifying soils at a high risk of
P loss to the environment (Jalali & Jalali, 2017). In the pot
experiment, we found that C addition significantly decreased
CaCl2 extractableP by 37% with 228mg kg−1 P and 21% with
570mg kg−1 P (Figure6c; p<.05). It confirmed that increas-
ing the ratio of microbial biomass P and Olsen P significantly
reduces CaCl2 extractableP (R2 = .36, p <.05; Figure 5a).
Therefore, using C to stimulate immobilization of P by mi-
crobes is another potential tool that can be deployed to better
manage the dynamics of P. In the long run, reinforcing the
process of microbial immobilization may reduce excessive
TABLE 4 ANOVA results with P level and C level as independent variables and their interaction, for Olsen P, microbial biomass P and
CaCl2 extractable P as dependent variables in the pot experiment
Independent variable
Olsen P Microbial biomass P CaCl2 extractable P
df F p-Value df F p-Value df F p-Value
P level 2 4,327.7 <.0001 2 686.37 <.0001 2 1,896 <.0001
C level 3 26.97 <.0001 3 29.5 <.0001 3 27.63 <.0001
P*C 3 4.21 .0005 3 11.44 <.0001 3 11.03 <.0001

|
9
XU etal.
labile P in the soil and enhance agricultural sustainability in
intensive systems.
4.3
|
Ecological significance of
microbial immobilization in intensive
agricultural systems
Conventional measures to reduce P loss from agriculture in-
clude drainage, reduced tillage, cover crops and exogenous
addition of lime (Andersson, Bergström, Djodjic, Ulén,
& Kirchmann, 2016; Aronsson, Ringselle, Andersson, &
Bergkvist, 2015; Šaulys & Bastienė, 2007). However, little is
known about the use of native microbial resources in inten-
sive agricultural systems to reduce excessive labile P in the
soil. Microbes are an increasingly important biological source
of innovation for global agricultural systems and represent an
enormous untapped resource (Kothamasi, Spurlock, & Kiers,
2011). Many studies have shown that soil native microbes in-
cluding bacteria and fungi can reduce P leaching to the en-
vironment (Bender & van der Heijden, 2015; Wagg, Bender,
Widmer, & van der Heijden, 2014) and enriched soil microbial
communities have been shown to significantly reduce P leach-
ing losses in some systems (Bender & van der Heijden, 2015).
In contrast, decreasing soil biodiversity and microbial popula-
tion could increase P leaching loss (Wagg, Bender, Widmer,
& van der Heijden, 2014). Our results found that there was
a positive relationship between soil organic C and microbial
biomass P (Figure3). We also tested the impact of C addition
and found that it increased microbial biomass P and decreased
Olsen P and CaCl2 extractableP (Figure6, Table4) in a pot
experiment. Rhizodeposition and root turnover account for up
to 40% of the C input into soil and are the major drivers for soil
microbiological processes (Jones, Nguyen, & Finlay, 2009;
Richardson, Barea, McNeill, & Prigent-Combaret, 2009). In
the P0 treatment, C addition increased microbial biomass P by
an average of 81% without cotton grown and 103% with cotton
growth (Figure6). Root exudates from cotton are likely to be an
additional C source for soil microbes and potentially stimulate
soil microbial process. We presume that the 22% increase in
microbial biomass P because of cotton was C priming. Soil C
rhizodeposition supports greater microbial biomass in organic
farming (Maharjan, Sanaullah, Razavi, & Kuzyakov, 2017).
Our results indicated that the increase of microbial biomass P
may be driven by C addition within the range 1.5–3.0g kg−1.
Compared to the C0 treatment, plant P uptake decreased under
C5.0g kg−1 which suggests that the competition between soil
microbes and plants took over (Figure5b). When regulating
microbial immobilization to reduce P loss with C addition, the
type and concentration of C should be taken into considera-
tion. This suggests crop residues, industrial by- products with
high C content may be applied to regulate soil microbial ac-
tivities to reduce P loss (Zhang, Ding, Peng, George, & Feng,
2018). Our findings suggest the potential of microbial solu-
tions to reduce soil CaCl2 extractableP at the risk of leaching
in intensive systems.
5
|
CONCLUSION
Our results showed that there was excessive labile P accu-
mulating in intensive agricultural systems which increases
the risk of P leaching Soil organic C drove microbes to im-
mobilize soil P into microbial biomass P. Promoting soil mi-
crobes to immobilize P may be a possible solution to decrease
excessive labile P in soil and reduce the risk of P leaching.
We suggest that C addition decreased soil Olsen P, enhanced
microbial biomass P, and reduced the potential of P to be
leached. The results reported here provide a new insight for
recognizing the role of microbes and a novel measure to pro-
tect the environment against P leaching in intensive agricul-
tural systems with excessive P.
ACKNOWLEDGEMENTS
This study is financially supported by the National
Key Research and Development Program of China
(2017YFD0200200), National Natural Science Foundation
of China (U1703232) and NSFC and RS jointly supported
project (31711530217). We are grateful Mr Yongzhi Zhao
from Beijing Soil and Fertilizer Work Station for his invalu-
able technical support. The contribution of TSG and LKB
was supported by a Royal Society International Exchange
Program grant and the Rural & Environment Science &
Analytical Services Division of the Scottish Government.
ORCID
Gu Feng https://orcid.org/0000-0002-1052-5009
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How to cite this article: Xu Z, Qu M, Liu S, etal.
Carbon addition reduces labile soil phosphorus by
increasing microbial biomass phosphorus in intensive
agricultural systems. Soil Use Manage. 2020;00:1–11.
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