Introduction
Phosphorus (P) fertilizer has been applied profligately across the globe, being particularly
overused in China in the past 30 years in order to pursue high yields (Cordell et
al., 2009; Li et al., 2014). This has greatly increased the P content of soil in various
intensive agricultural systems (including cereals, vegetables, and fruit orchard),
many of which now contain sufficient P to potentially supply P for adequate yields
in these crops for several years (Li et al., 2011; Tóth et al., 2014). For example,
the soil available P in some cereal crop, vegetable and orchard systems in China have
arrived at 24.7, 181, and 43.1 mg kg−1, respectively (Lu, 2009; Li et al., 2011; Kalkhajeh
et al., 2017). Over-application of P fertilizer is in itself wasteful, but the transport
of excessive P from soil solution to the waterbodies by surface runoff and leaching
causes various environmental problems, including eutrophication of lakes, rivers and
near coastal zones, pollution of ground water aquifers, algal blooms, and the loss
of terrestrial and aquatic biodiversity (Chen et al., 2008; Schoumans et al., 2014;
Smith et al., 2015). Consequently, it is imperative to understand how best to immobilize
P in the soil to avoid its loss to the wider environment. This is an urgent environmental
issue that should be considered as a priority in intensive agricultural systems across
the globe, but particularly in China.
Phosphorus immobilization by soil microbes
Soil microbes including bacteria, fungi, and microfauna play important roles in the
biogeochemical cycle of P and are involved in both mineralization and immobilization
of P (Richardson and Simpson, 2011). On the one hand, soil microbes are capable of
mobilizing organic P and non-soluble inorganic P (Jorquera et al., 2008) by exuding
protons, carboxylates and phosphatases to release the orthophosphate, usually H2
PO
4
-
and
HPO
4
2
-
, for their own and root uptake (Rodríguez and Fraga, 1999). The phosphate solubilizing
bacteria usually belong to the genera of Pseudomonas, Bacillus, Rhizobium, Burkholderia,
Achromobacter, Agrobacterium, Microccocus, Aereobacter, Flavobacterium, and Erwinia
(Rodríguez and Fraga, 1999). The phosphate solubilizing fungi usually belong to the
genera of Aspergillus, Trichoderma, and Penicillium (Whitelaw, 1999). On the other
hand, soil microbes can also transform available P into microbial biomass P (MBP)
to allow the use of organic carbon (C) and root exudates for energy (Wu et al., 2007).
The immobilized P can be released to increase available P during the microbial biomass
turnover. The turnover time of MBP in the field can range from tens of days to near
one year (Chen and He, 2002; Kouno et al., 2002; Liebisch et al., 2014), which is
largely dependent on a range of environmental factors, e.g., soil moisture, season,
and application of fertilizers (Patra et al., 1990; He et al., 1997; Butterly et al.,
2009). Liebisch et al. (2014) estimate the flux of P through the microbial biomass
can arrive at 18.1–36.9 kg P ha−1 season−1 (from March to November). Most studies
usually focus on how to use soil microbes to mobilize soil P (Richardson and Simpson,
2011), neglecting how to exert their functions on P immobilization.
Indeed, MBP is negatively related to soil solution P (Figure 1A) and has strong competition
with soil available P (Kouno et al., 2002). However, approaches to manipulate soil
microbes to immobilize more P to reduce P loss have been paid little attention. Among
various abiotic and biotic factors that can influence the dynamics of MBP, soil carbon
(C):P ratio is an important one (Marschner, 2008). However, soil P pools are complex
and different P pools, e.g. total P, available P and organic P can be used to calculate
the C:P (Stevenson, 1986; Cleveland and Liptzin, 2007; Spohn and Widdig, 2017). Which
of these reflects a better relationship with MBP is still unclear and needs further
investigation. Generally, at low C:P ratio, MBP is small because of the C limitation
(Cleveland and Liptzin, 2007). As the C:P ratio increases, MBP will increase through
further microbial immobilization for the input of C (Kouno et al., 2002). At high
C:P ratio, MBP becomes stable because C is in excess and P is relatively limited (Figure
1B). Evidence suggest that soil C:P ratio in the Chinese intensive agricultural system
is less than the equilibrium and P is normally the element in excess compared with
C (Tian et al., 2010). Moreover, due to excessive application of P fertilizer, the
C:P ratio has become even lower in recent years (Xu et al., 2015). This suggests there
is an opportunity to raise the C:P ratio of Chinese soils and lock up some of this
excess P by forcing microbial immobilization.
Figure 1
(A) The relationship between microbial biomass P and soil solution P; (B) the relationship
between soil C:P ratio and microbial biomass P; (C) the measures to increase microbial
biomass P by increasing soil C:P ratio to reduce P lost.
Microbial immobilization of phosphorus is limited by C:P ratio
The comparison of the present and initial value of C:P ratio in the P addition treatment
of 22 long-term field experiments shows that the C:P ratio decreased, on average,
by 13% over the course of the experiments (Xu et al., 2015). In addition, based on
a recent Chinese soil survey, the C:P ratio is generally less than 50 in the north
of China (Tian et al., 2010), which is lower than the C:P ratio (usually 60) in microbial
biomass. In addition, compared to natural systems, e.g., the forest and grassland,
in the same region, the MBP in the intensive agricultural system is usually lower
(Pal et al., 2013), which is related to the lower C:P ratio in the agricultural system.
The intensive agricultural systems differs from the natural systems by having a smaller
C input as the aboveground biomass is usually removed and the C source is mainly from
root deposition and their residues which limit the C input (Oberholzer et al., 2014).
This suggests there is an opportunity to apply some ecological concepts to the cropping
system by enhancing the C input and closing the organic matter cycle (Bender et al.,
2016).
Managing soil C:P ratio to increase P microbial immobilization
Previous studies have demonstrated that adding C compounds to the soil can increase
P microbial immobilization. Under soil conditions, adding glucose, plant residue,
etc. increase MBP significantly in a short time (Kouno et al., 2002). In long term
experiments, organic amendments also increase soil MBP (Liu et al., 2009). Considering
the potential to improve MBP in the intensive agricultural system by increasing C:P
ratio, here, an approach to reduce P loss from soil by enhancing microbial P immobilization
through the addition of C-rich substrates is proposed. Various measures can be taken
to increase the C input (Figure 1C): (1) application of organic fertilizer such as
animal manure, which is the most popular organic fertilizer in China (Bai et al.,
2016). As the poultry and livestock breeding industry has developed the amount of
manure has greatly increased, China annually produces 3.8 billion tons of manure.
This manure not only contains nitrogen and P, but also contains organic C compounds.
However, much of this manure goes to waste in land fill. Applying animal manure to
agricultural soil not only increases soil C, but is also environmentally friendly.
Compost is another popular organic fertilizer in Chinese systems. Crop straw and other
organic wastes are fermented and humified to form the humic compounds, which are easily
utilized by microbes, and applied to soils as compost (Fan et al., 2006). Applying
the organic fertilizer instead of part of chemical fertilizer has a great potential
to increase the soil C content. (2) Retention of crop residues, by returning the crop
straw back to the field, has potential to maintain and enhance the soil C content.
The composition of straw includes a range of mainly C-rich compounds, while this may
not be a useful source of essential nutrients for the crop, the enhanced soil carbon
content will have many benefits. Though the retention of crop residues in cropping
system has increased in recent years, only 31.6% of farmers retain their residues
and the majority of straw is burnt or removed (Li et al., 2007). The straw returning
rate needs to be increased in future. (3) Cover crops: in the non-crop growing season
in the crop fields and in the orchard gardens, the cover plants can be cultivated
and then plowed into soil when they are mature. This biological C fixation is also
a potential approach to increase the soil C content. (4) Application of industrial
byproducts with high C content: for example, in the sugar refining and monosodium
glutamate industries, the byproducts usually contain highly labile C sources such
as sugars and glutamic acid, which commonly detected in root exudates (Bais et al.,
2006). These compounds are easily available C substrates for microbes and are likely
to be potent promoters of microbial immobilization of P. (5) Application of domestic
wastes: kitchen wastes, sewage sludge, and other urban waste streams produced by households
usually contain high amount of organic matter which can also be applied in agriculture
after processing to remove any harmful elements.
Taking these measures may go some way to promoting a circular economy on wastes and
reduce the amount of waste from agriculture, animal husbandry, industry, and domestic
households going to landfill. However, it is important to study how effective these
various sources of C are at priming P immobilization by microbes and what impacts
they have on the availability of P and other essential nutrients for crop productivity.
Conclusions
Extensive application of P fertilizer to pursue high yields has increased soil P content
in various intensive agricultural systems (including cereals, vegetables, and fruit
orchards). Over-application of P fertilizer causes various environmental problems
and it is imperative to understand how best to immobilize P in the soil to avoid its
loss to the wider environment. Using soil microbial immobilization is a potentially
efficient way to do this, but is usually limited by the low soil C:P ratio. Several
measures can be taken to increase the C input: (1) application of organic fertilizer;
(2) retention of crop residues; (3) cover crops; (4) application of industrial byproducts
with high C content; and (5) application of domestic wastes.
Author contributions
LZ, XD, and YP wrote the manuscript. TG and GF helped with writing, editing and finalizing
the manuscript.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.