Impact Factor 4.076

The 3rd most cited journal in Microbiology

Opinion ARTICLE

Front. Microbiol., 06 February 2018 | https://doi.org/10.3389/fmicb.2018.00104

Closing the Loop on Phosphorus Loss from Intensive Agricultural Soil: A Microbial Immobilization Solution?

Lin Zhang1, Xiaodong Ding2, Yi Peng1, Timothy S. George3 and Gu Feng1*
  • 1Department of Ecological Science and Technology, College of Resources and Environmental Sciences, China Agricultural University, Beijing, China
  • 2Department of Soil Science and Plant Nutrition, College of Resources and Environment, Qingdao Agricultural University, Qingdao, China
  • 3James Hutton Institute, Dundee, United Kingdom

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 H2PO4- and HPO42-, 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
www.frontiersin.org

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.

Acknowledgments

This study is financially supported by National Key Research and Development Program of China (2017YFD0200200/2017YFD0200203), the National Natural Science Foundation of China (U1403285, 31701998) and NSFC and RS jointly supported project (31711530217). TG contribution to the manuscript is funded by The Royal Society International Exchange 2016 Cost Share (China) grant (IE161327) and the Rural & Environment Science & Analytical Services Division of the Scottish Government. We thank two reviewers for their constructive comments on an earlier version of the manuscript.

References

Bai, Z., Ma, L., Jin, S., Ma, W., Velthof, G. L., Oenema, O., et al. (2016). Nitrogen, phosphorus, and potassium flows through the manure management chain in China. Environ. Sci. Technol. 50, 13409–13418. doi: 10.1021/acs.est.6b03348

PubMed Abstract | CrossRef Full Text | Google Scholar

Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., and Vivanco, J. M. (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233–266. doi: 10.1146/annurev.arplant.57.032905.105159

PubMed Abstract | CrossRef Full Text | Google Scholar

Bender, S. F., Wagg, C., and van der Heijden, M. G. A. (2016). An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31, 440–452. doi: 10.1016/j.tree.2016.02.016

PubMed Abstract | CrossRef Full Text | Google Scholar

Butterly, C. R., Bünemann, E. K., McNeill, A. M., Baldock, J. A., and Marschner, P. (2009). Carbon pulses but not phosphorus pulses are related to decreases in microbial biomass during repeated drying and rewetting of soils. Soil Biol. Biochem. 41, 1406–1416. doi: 10.1016/j.soilbio.2009.03.018

CrossRef Full Text | Google Scholar

Chen, G., and He, Z. (2002). Microbial biomass phosphorus turnover in variable-charge soils in China. Commun. Soil Sci. Plan. 33, 2101–2117, doi: 10.1081/CSS-120005751

CrossRef Full Text | Google Scholar

Chen, M., Chen, J., and Sun, F. (2008). Agricultural phosphorus flow and its environmental impacts in China. Sci. Total Environ. 405, 140–152. doi: 10.1016/j.scitotenv.2008.06.031

PubMed Abstract | CrossRef Full Text | Google Scholar

Cleveland, C. C., and Liptzin, D. (2007). C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85, 235–252. doi: 10.1007/s10533-007-9132-0

CrossRef Full Text | Google Scholar

Cordell, D., Drangert, J. O., and White, S. (2009). The story of phosphorus: global food security and food for thought. Global Environ. Chang. 19, 292–305. doi: 10.1016/j.gloenvcha.2008.10.009

CrossRef Full Text | Google Scholar

Fan, Y. T., Zhang, Y. H., Zhang, S. F., Hou, H. W., and Ren, B. Z. (2006). Efficient conversion of wheat straw wastes into biohydrogen gas by cow dung compost. Bioresour. Technol. 97, 500–505. doi: 10.1016/j.biortech.2005.02.049

PubMed Abstract | CrossRef Full Text | Google Scholar

He, Z., Wu, J., O'Donnell, A. G., and Syers, J. K. (1997). Seasonal responses in microbial biomass carbon, phosphorus and sulphur in soils under pasture. Biol. Fertil. Soils 24, 421–428. doi: 10.1007/s003740050267

CrossRef Full Text | Google Scholar

Jorquera, M. A., Hernandez, M. T., Rengel, Z., Marschner, P., and de la Luz Mora, M. (2008). Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in a volcanic soil. Biol. Fert. Soils 44, 1025–1034. doi: 10.1007/s00374-008-0288-0

CrossRef Full Text | Google Scholar

Kalkhajeh, Y. K., Huang, B., Hu, W., Holm, P. E., and Hansen, H. C. (2017). Phosphorus saturation and mobilization in two typical Chinese greenhouse vegetable soils. Chemosphere 172, 316–324. doi: 10.1016/j.chemosphere.2016.12.147

PubMed Abstract | CrossRef Full Text | Google Scholar

Kouno, K., Wu, J., and Brookes, P. C. (2002). Turnover of biomass C and P in soil following incorporation of glucose or ryegrass. Soil Biol. Biochem. 34, 617–622. doi: 10.1016/S0038-0717(01)00218-8

CrossRef Full Text | Google Scholar

Li, H., Huang, G., Meng, Q., Ma, L., Yuan, L., Wang, F., et al. (2011). Integrated soil and plant phosphorus management for crop and environment in China. A review. Plant Soil 349, 157–167. doi: 10.1007/s11104-011-0909-5

CrossRef Full Text | Google Scholar

Li, X., Wang, S., Duan, L., Hao, J., Li, C., Chen, Y., et al. (2007). Particulate and trace gas emissions from open burning of wheat straw and corn stover in China. Environ. Sci. Technol. 41, 6052–6058. doi: 10.1021/es0705137

PubMed Abstract | CrossRef Full Text | Google Scholar

Li, Y., Zhang, W., Ma, L., Huang, G., Oenema, O., Zhang, F., et al. (2014). An analysis of China's fertilizer policies: impacts on the industry, food security, and the environment. J. Environ. Qual. 42, 972–981. doi: 10.2134/jeq2012.0465

PubMed Abstract | CrossRef Full Text | Google Scholar

Liebisch, F., Keller, F., Huguenin-Elie, O., Frossard, E., Oberson, A., and Bünemann, E. K. (2014). Seasonal dynamics and turnover of microbial phosphorusin a permanent grassland. Biol. Fert. Soils 50, 465–475. doi: 10.1007/s00374-013-0868-5

CrossRef Full Text | Google Scholar

Liu, M., Hu, F., Chen, X., Huang, Q., Jiao, J., Zhang, B., et al. (2009). Organic amendments with reduced chemical fertilizer promote soil microbial development and nutrient availability in a subtropical paddy field: the influence of quantity, type and application time of organic amendments. Appl. Soil Ecol. 42, 166–175. doi: 10.1016/j.apsoil.2009.03.006

CrossRef Full Text | Google Scholar

Lu, S. (2009). Characteristics of Nutrients Input and the Influences on Soil Quality in Intensive orchards of China. PhD's thesis. Beijing: China Agricultural University.

Marschner, P. (2008). “The role of rhizosphere microorganisms in relation to P uptake by plants,” in The Ecophysiology of Plant-Phosphorus Interactions, eds P. J. White, and J. P. Hammond (Heidelberg: Springer), 165–176.

Google Scholar

Oberholzer, H. R., Leifeld, J., and Mayer, J. (2014). Changes in soil carbon and crop yield over 60 years in the Zurich Organic Fertilization Experiment, following land-use change from grassland to cropland. J. Plant Nutr. Soil Sci. 177, 696–704. doi: 10.1002/jpln.201300385

CrossRef Full Text | Google Scholar

Pal, S., Panwar, P., and Bhardwaj, D. R. (2013). Soil quality under forest compared to other landuses in acid soil of North Western Himalaya, India. Ann. For. Res. 56, 187–198.

Google Scholar

Patra, D. D., Brookes, P. C., Coleman, K., and Jenkinson, D. S. (1990). Seasonal changes of soil microbial biomass in an arable and a grassland soil which have been under uniform management for many years. Soil Biol. Biochem. 22, 739–742. doi: 10.1016/0038-0717(90)90151-O

CrossRef Full Text | Google Scholar

Richardson, A. E., and Simpson, R. J. (2011). Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol. 156, 989–996. doi: 10.1104/pp.111.175448

PubMed Abstract | CrossRef Full Text | Google Scholar

Rodríguez, H., and Fraga, R. (1999). Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17, 319–339. doi: 10.1016/S0734-9750(99)00014-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Schoumans, O. F., Chardon, W. J., Bechmann, M. E., Gascuel-Odoux, C., Hofman, G., Kronvang, B., et al. (2014). Mitigation options to reduce phosphorus losses from the agricultural sector and improve surface water quality: a review. Sci. Total Environ. 468–469, 1255–1266. doi: 10.1016/j.scitotenv.2013.08.061

PubMed Abstract | CrossRef Full Text | Google Scholar

Smith, D. R., King, K. W., Johnson, L., Francesconi, W., Richards, P., Baker, D., et al. (2015). Surface runoff and tile drainage transport of phosphorus in the Midwestern United States. J. Environ. Qual. 44, 495–502. doi: 10.2134/jeq2014.04.0176

PubMed Abstract | CrossRef Full Text | Google Scholar

Spohn, M., and Widdig, M. (2017). Turnover of carbon and phosphorus in the microbial biomass depending on phosphorus availability. Soil Biol. Biochem. 113, 53–59. doi: 10.1016/j.soilbio.2017.05.017

CrossRef Full Text | Google Scholar

Stevenson, F. J. (1986). Cycles of Soil Carbon, Nitrogen, Phosphorus, Sulfur, Micronutrients. New York, NY: Wiley.

Tian, H., Chen, G., Zhang, C., Melillo, J. M., and Hall, C. A. (2010). Pattern and variation of C: N: P ratios in China's soils: a synthesis of observational data. Biogeochemistry 98, 139–151. doi: 10.1007/s10533-009-9382-0

CrossRef Full Text | Google Scholar

Tóth, G., Guicharnaud, R. A., Tóth, B., and Hermann, T. (2014). Phosphorus levels in croplands of the European Union with implications for P fertilizer use. Eur. J. Agron. 55, 42–52. doi: 10.1016/j.eja.2013.12.008

CrossRef Full Text | Google Scholar

Whitelaw, M. A. (1999). Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv. Agron. 69, 99–151. doi: 10.1016/S0065-2113(08)60948-7

CrossRef Full Text | Google Scholar

Wu, J., Huang, M., Xiao, H., Su, Y., Tong, C., Huang, D., et al. (2007). Dynamics in microbial immobilization and transformations of phosphorus in highly weathered subtropical soil following organic amendments. Plant Soil 290, 333–342. doi: 10.1007/s11104-006-9165-5

CrossRef Full Text | Google Scholar

Xu, M., Zhang, W., and Huang, S. (2015). Soil Fertility Evolution in China, 2nd Edn. Beijing, China: Chinese Agricultural Science and Technology Press.

Keywords: agricultural soil, carbon: phosphorus ratio, increase carbon input, microbial biomass phosphorus, phosphorus pollution

Citation: Zhang L, Ding X, Peng Y, George TS and Feng G (2018) Closing the Loop on Phosphorus Loss from Intensive Agricultural Soil: A Microbial Immobilization Solution? Front. Microbiol. 9:104. doi: 10.3389/fmicb.2018.00104

Received: 26 September 2017; Accepted: 17 January 2018;
Published: 06 February 2018.

Edited by:

Michael Sauer, University of Natural Resources and Life Sciences, Vienna, Austria

Reviewed by:

Min Li, Beijing Forestry University, China
Elżbieta Wołejko, Białystok Technical University, Poland

Copyright © 2018 Zhang, Ding, Peng, George and Feng. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Gu Feng, fenggu@cau.edu.cn