Skip to main content

Soil Microorganisms Can Reduce P Loss from Cropping Systems

  • Chapter
  • First Online:
Sustainable Agriculture Reviews

Part of the book series: Sustainable Agriculture Reviews ((SARV,volume 22))

Abstract

Declining supplies of quality phosphate ore and rising costs for P fertilizer, tripled in last 10 years, are changing the economics of food production and consumption. Simultaneously, P applied in crop production continues to be released as a non-point source pollutant that causes widespread degradation of water resources. Strong motivation thus exists to become more efficient in the use of P for crop production. Applications of P fertilizer to crops are commonly guided by single-point-in-time measurements of inorganic P residing in forms that are relatively easy to chemically extract from the soil. While these easily extractable inorganic P forms often represent P that is immediately available for plant uptake, these same P forms also represent P that is most subject to fixation in the soil (decreasing plant availability) or loss from the system via leaching, surface flow, and erosion. Point-in-time measurements ignore the dynamic nature of soil P, since soil biological activities continually transform P into forms with varying mobility and plant-availability and therefore introduce a kinetic aspect to P retention and plant availability. There is an urgent need for an alternative model for managing soil P fertility that accounts for the activities of soil microorganisms in controlling pools and fluxes of soil P and moderating plant P uptake. In this review, we synthesize the emerging literature from different scientific disciplines to provide a foundational understanding of the principles by which native soil microorganisms can improve the efficiency of P use in crop production systems. Following an introduction, we summarize the dual roles of P as a critical resource for food production and an environmental pollutant responsible for economic damages in billions of dollars. In Sect. 2.3 we outline the use of P in fertilization of cropping systems and its possible fates following application. We point out that commonly used indices of fertilization use efficiency fail to account for loss from the system and there is an alternative method that does account for losses. Sect 2.4 summarizes standard schemes for analytical soil P fractionation, their relationship with conventional soil fertility tests, and the limitations of using conventional soil tests to direct P applications. Section 2.5 describes the mechanisms by which soil microorganisms modify P mobility and bioavailability and surveys the emerging literature that demonstrates that microbial biomass turnover and biologically-catalyzed reactions can create an annual flux of 10–40 kg ha−1 plant available P. Section 2.6 documents the role of an obligate plant symbiont, arbuscular mycorrhizal fungi, in providing P to plant hosts and increasing retention of P in the system. Section 2.7 discusses the relationships between plant and microbial diversity and their influence on soil nutrient dynamics. We conclude with a synthesis of agricultural practices documented to promote soil biomass, diversity, and activities that can improve P retention in crop production systems.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alexander RB, Smith RA, Schwarz GE, Boyer EW, Nolan JV, Brakebill JW (2008) Differences in phosphorus and nitrogen delivery to the Gulf of Mexico from the Mississippi River Basin. Environ Sci Technol 42:822–830

    Article  CAS  PubMed  Google Scholar 

  • Altieri MA (1999) The ecological role of biodiversity in agroecosystems. Agric Ecosyst Environ 74:19–31

    Article  Google Scholar 

  • Barber NA, Kiers ET, Theis N, Hazzard RV, Adler LS (2013) Linking agricultural practices, mycorrhizal fungi, and traits mediating plant–insect interactions. Ecol Appl 23:1519–1530

    Article  PubMed  Google Scholar 

  • Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK (2005) The contribution of species richness and composition to bacterial services. Nature 436:1157–1160

    Article  CAS  PubMed  Google Scholar 

  • Benayas JM, Newton AC, Diaz A, Bullock JM (2009) Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. Science 325:1121–1124

    Article  CAS  Google Scholar 

  • Bittman S, Liu A, Hunt DE, Forge TA, Kowalenko CG, Chantigny MH, Buckley K (2012) Precision placement of separated dairy sludge improves early phosphorus nutrition and growth in corn (Zea mays L.). J Environ Qual 41:582–591

    Article  CAS  PubMed  Google Scholar 

  • Boswell EP, Koide RT, Shumway DL, Addy HD (1998) Winter wheat cover cropping, VA mycorrhizal fungi and maize growth and yield. Agric Ecosyst Environ 67:55–65

    Article  Google Scholar 

  • Brookes PC (2001) The soil microbial biomass: concept, measurement and applications in soil ecosystem research. Microbes Environ 16:131–140

    Article  Google Scholar 

  • Brussaard L, De Ruiter PC, Brown GG (2007) Soil biodiversity for agricultural sustainability. Agric Ecosyst Environ 121:233–244

    Article  Google Scholar 

  • Bunemann E, Smithson PC, Jama B, Frossard E, Oberson A (2004a) Maize productivity and nutrient dynamics in maize-fallow rotations in western Kenya. Plant Soil 264:195–208

    Article  Google Scholar 

  • Bunemann EK, Bossio DA, Smithson PC, Frossard E, Oberson A (2004b) Microbial community composition and substrate use in a highly weathered soil as affected by crop rotation and P fertilization. Soil Biol Biochem 36:889–901

    Article  CAS  Google Scholar 

  • Bünemann EK, Oberson A, Liebisch F, Keller F, Annaheim KE, Huguenin-Elie O, Frossard E (2012) Rapid microbial phosphorus immobilization dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95

    Article  CAS  Google Scholar 

  • Butler SJ, Vickery JA, Norris K (2007) Farmland biodiversity and the footprint of agriculture. Science 315:381–384

    Article  CAS  PubMed  Google Scholar 

  • Cassman KG (1999) Ecological intensification of cereal production systems: Yield potential, soil quality, and precision agriculture. Proc Natl Acad Sci 96:5952–5959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng W (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol Biochem 41:1795–1801

    Article  CAS  Google Scholar 

  • Cheng Y, Ishimoto K, Kuriyama Y, Osaki M, Ezawa T (2012) Ninety-year-, but not single, application of phosphorus fertilizer has a major impact on arbuscular mycorrhizal fungi communities. Plant Soil 365:397–407

    Article  CAS  Google Scholar 

  • Chien SH, Sikora FJ, Gilkes RJ, Mclaughlin MJ (2012) Comparing of the difference and balance methods to calculate percent recovery of fertilizer phosphorus applied to soils: a critical discussion. Nutr Cycl Agroecosyst 92:1–8

    Article  Google Scholar 

  • Condron LM, Newman S (2011) Revisiting the fundamentals of phosphorus fractionation of sediments and soils. J Soils Sediments 11:830–840

    Article  CAS  Google Scholar 

  • Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323

    Google Scholar 

  • Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305

    Article  Google Scholar 

  • Cordell D, White S (2013) Sustainable phosphorus measures: strategies and technologies for achieving phosphorus security. Agronomy 3:86–116

    Article  Google Scholar 

  • Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214

    Article  CAS  Google Scholar 

  • Dai M, Hamel C, Bainard LD, Arnaud MS, Grant CA, Lupwayi NZ, Malhi SS, Lemke R (2014) Negative and positive contributions of arbuscular mycorrhizal fungal taxa to wheat production and nutrient uptake efficiency in organic and conventional systems in the Canadian prairie. Soil Biol Biochem 74:156–166

    Article  CAS  Google Scholar 

  • Davis AS, Hill JD, Chase CA, Johanns AM, Liebman M (2012) Increasing cropping system diversity balances productivity, profitability, and environmental health. PLoS One 7:e47149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson JC, Huggins DR, Jones SJ (2008) Characterizing nitrogen use efficiency in natural and agricultural ecosystems to improved the performance of cereal crops in low-input and organic agricultural systems. Field Crop Res 107:89–101

    Article  Google Scholar 

  • De Deyn GB, Quirk H, Bardgett RD (2011) Plant species richness, identity and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility. Biol Lett 7:75–78

    Article  PubMed  Google Scholar 

  • De Vries FT, Thébault E, Liiri M, Birkhofer K, Tsiafouli MA, Bjørnlund L, Jørgensen HB, Brady MV, Christensen S, De Ruiter PC (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci 110:14296–14301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dias T, Dukes A, Antunes PM (2015) Accounting for soil biotic effects on soil health and crop productivity in the design of crop rotations. J Sci Food Agric 95:447–454

    Google Scholar 

  • Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929

    Article  CAS  PubMed  Google Scholar 

  • Dodds WK, Bouska WW, Eitzmann JL, Pilger TJ, Pitts KL, Riley AJ, Schloesser JT, Thornbrugh DJ (2009) Eutrophication of U.S. freshwaters: analysis of potential economic damages. Environ Sci Technol 43:12–19

    Article  CAS  PubMed  Google Scholar 

  • Douds DD Jr, Millner PD (1999) Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agric Ecosyst Environ 74:77–93

    Article  Google Scholar 

  • Douds DD Jr, Janke RR, Peters SE (1993) VAM fungus spore populations and colonization of roots of maize and soybean under conventional and low-input sustainable agriculture. Agric Ecosyst Environ 43:325–335

    Article  Google Scholar 

  • Drinkwater LE, Snapp SS (2007) Nutrients in agroecosystems: Rethinking the management paradigm. Adv Agron 92:163–186

    Article  CAS  Google Scholar 

  • Eichler-Lobermann B, Kohne S, Koppen D (2007) Effect of organic, inorganic, and combined organic and inorganic P fertilization on plant uptake and soil P pools. J Plant Nutr Soil Sci 170:623–628

    Article  CAS  Google Scholar 

  • El Fantroussi S, Agathos SN (2005) Is bioaugmentation a feasible strategy for pollutant removal and site remediation? Curr Opin Microbiol 8:268–275

    Article  CAS  PubMed  Google Scholar 

  • FAO, 2006. Plant nutrition for food security: a guide for integrated nutrient management. FAO Fertilizer and Plant Nutrition Bulletin No. 16. Rome.

    Google Scholar 

  • FAO, 2008. Efficiency of soil and fertilizer phosphorus. FAO Fertilizer and Plant Nutrition Bulletin No. 18. Rome.

    Google Scholar 

  • Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’connell C, Ray DK, West PC (2011) Solutions for a cultivated planet. Nature 478:337–342

    Article  CAS  PubMed  Google Scholar 

  • Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29:15–23

    Article  CAS  Google Scholar 

  • Frossard E, Demaria P, Sinaj S, Schärer M (2014) A flow-through reactor to assess potential phosphate release from agricultural soils. Geoderma 219–220:125–135

    Article  CAS  Google Scholar 

  • Galvez L, Douds DD Jr, Drinkwater LE, Wagoner P (2001) Effect of tillage and farming system upon VAM fungus populations and mycorrhizas and nutrient uptake of maize. Plant Soil 228:299–308

    Article  CAS  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet MN, Van Tuinen D, Redecker D, Wipf D (2010) Agroecology: The key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • Gilbert J, Gowing D, Wallace H (2009) Available soil phosphorus in semi-natural grasslands: assessment methods and community tolerances. Biol Conserv 142:1074–1083

    Article  Google Scholar 

  • Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818

    Article  CAS  PubMed  Google Scholar 

  • Harmel RD, Haney RL (2013) Initial field evaluation of the agro-economic effects of determining nitrogen fertilizer rates with a recently-developed soil test methodology. Open Journal of Soil Sciences 3:91–99

    Article  Google Scholar 

  • Hartz TK, Johnstone PR (2006) Relationship between soil phosphorus availability and phosphorus loss potential in runoff and drainage. Commun Soil Sci Plant Anal 37:1525–1536

    Article  CAS  Google Scholar 

  • Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–191

    Article  CAS  PubMed  Google Scholar 

  • Hedley MJ, Stewart JWB (1982) Method to measure microbial phosphate in soils. Soil Biol Biochem 14:377–385

    Article  CAS  Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431–431

    Article  CAS  PubMed  Google Scholar 

  • Hinsinger P, Brauman A, Devau N, Gerard F, Jourdan C, Laclau J-P, Le Cadre E, Jaillard B, Plassard C (2011) Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348:29–61

    Article  CAS  Google Scholar 

  • Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a concensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Horst WJ, Kamh M, Jibrin JM, Chude VO (2001) Agronomic measures for increasing P availability to crops. Plant Soil 237:211–223

    Article  CAS  Google Scholar 

  • Ipni, 2012. A nutrient use system (NuGIS) for the U.S. [online]. International Plant Nutrition Institute. Available from: [Accessed Access Date 2014].

    Google Scholar 

  • Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, Van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202

    Article  CAS  PubMed  Google Scholar 

  • Jansa, J., Wiemken, A. & Frossard, E., 2006. The effects of agricultural practices on arbuscular mycorrhizal fungi. London: Geological Society of London.

    Google Scholar 

  • Johnson D, Ijdo M, Genney DR, Anderson IC, Alexander IJ (2005) How do plants regulate the function, community structure, and diversity of mycorrhizal fungi? J Exp Bot 56:1751–1760

    Article  CAS  PubMed  Google Scholar 

  • Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2004) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515

    Article  Google Scholar 

  • Johnson NC, Copeland PJ, Crookston RK, Pfleger FL (1992) Mycorrhizae: possible explanation for yield decline with continuous corn and soybean. Agron J 84:387–390

    Article  Google Scholar 

  • Johnstone AE, Poulton PR, Fixen PE, Curtin D (2014) Phosphorus: its efficient use in agriculture. Adv Agron 123:177–228

    Article  CAS  Google Scholar 

  • Joner EJ, Jakobsen I (1995) Contribution by two arbuscular mycorrhizal fungi to P-uptake by cucumber (Cucumis sativus L.) from 32P-labeld organic matter during mineralization in soil. Plant Soil 163:203–209

    Article  Google Scholar 

  • Keller M, Oberson A, Annaheim KE, Tamburini F, Mäder P, Mayer J, Frossard E, Bünemann EK (2012) Phosphorus forms and enzymatic hydrolyzability of organic phosphorus in soils after 30 years of organic and conventional farming. J Plant Nutr Soil Sci 175:385–393

    Article  CAS  Google Scholar 

  • Kernaghan G (2005) Mycorrhizal diversity: Cause and effect? Pedobiologia 49:511–520

    Article  Google Scholar 

  • Klironomos JN, Mccune J, Hart M, Neville J (2000) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecol Lett 3:137–141

    Article  Google Scholar 

  • Köhl L, Oehl F, Van Der Heijden MGA (2014) Agricultural practices indirectly influence plant productivity and ecosystem services through effects on soil biota. Ecol Appl 24(7):1842–1853

    Article  Google Scholar 

  • Kuchenbuch RO, Buczko U (2011) Re-visiting potassium- and phosphate-fertilizer responses in field experiments and soil-test interpretations by means of data mining. J Plant Nutr Soil Sci 174:171–185

    Article  CAS  Google Scholar 

  • Lehman RM, Taheri WI, Osborne SL, Buyer JS, Douds DD Jr (2012) Fall cover cropping can increase arbuscular mycorrhizae in soils supporting intensive agricultural production. Appl Soil Ecol 61:300–304

    Article  Google Scholar 

  • Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol 168:189–204

    Article  CAS  PubMed  Google Scholar 

  • Li, L., Li, S., Sun, J., Zhou, L., Bao, X., Zhang, H. & Zhang, F., 2007. Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation in phosphorus-deficient soil. Proc Natl Acad Sci 104:11192–11196.

    Google Scholar 

  • Litke DW (1999) Review of phosphorus control measures in the United States and their effects on water quality. Denver, U.S. Dept. of the Interior

    Google Scholar 

  • Lopez-Hernandez D, Brossard M, Frossard E (1998) P-isotopic exchange values in relation to Po mineralisation in soils with very low P-sorbing capacities. Soil Biol Biochem 30:1663–1670

    Article  CAS  Google Scholar 

  • Macdonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world's croplands. Proc Natl Acad Sci 108:3086–3091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mader P, Fliebbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697

    Article  CAS  PubMed  Google Scholar 

  • Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 277:504–509

    Article  CAS  PubMed  Google Scholar 

  • Mckenzie RH, Bremer E (2003) Relationship of soil phosphorus fractions to phosphorus soil tests and fertilizer response. Can J Soil Sci 83:443–449

    Article  CAS  Google Scholar 

  • Mclaughlin MJ, Mcbeath TM, Smernik R, Stacey SP, Ajiboye B, Guppy C (2011) The chemical nature of P accumulation in agricultural soils - implications for fertiliser management and design: an Australian perspective. Plant Soil 349:69–87

    Article  CAS  Google Scholar 

  • Mengel K (1997) Agronomic measures for better utilization of soil and fertilizer phosphates. Eur J Agron 7:221–233

    Article  Google Scholar 

  • Miller MH (2000) Arbuscular mycorrhizae and the phosphorous nutrition of maize: A review of Guelph studies. Can J Plant Sci 80:47–52

    Article  CAS  Google Scholar 

  • Moonen A, Barberi P (2008) Functional biodiversity: An agroecosystem approach. Agric Ecosyst Environ 127:7–21

    Article  Google Scholar 

  • Mueller ND, Gerber JS, Johnston M, Ray DK, Ramankutty N, Foley JA (2012) Closing yield gaps through nutrient and water management. Nature 490:254–257

    Article  CAS  PubMed  Google Scholar 

  • Oberson A, Besson JM, Maire N, Sticher H (1996) Microbiological processes in soil organic phosphorus transformations in conventional and biological cropping systems. Biol Fertil Soils 21:138–148

    Article  CAS  Google Scholar 

  • Oberson A, Fardeau JC, Besson JM, Sticher H (1993) Soil phosphorus dynamics in cropping systems managed according to conventional and biological agricultural methods. Biol Fertil Soils 16:111–117

    Article  CAS  Google Scholar 

  • Oberson A, Friesen DK, Rao IM, Bühler S, Frossard E (2001) Phosphorus transformations in an Oxisol under contrasting land-use systems: The role of the soil microbial biomass. Plant Soil 237:197–210

    Article  CAS  Google Scholar 

  • Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin DS (eds) Organic Phosphorus in the Environment. Wallingford, CABI International, pp. 133–165

    Chapter  Google Scholar 

  • Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004a) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36:667–675

    Article  CAS  Google Scholar 

  • Oehl F, Oberson A, Probst M, Fliessbach A, Roth HR, Frossard E (2001) Kinetics of microbial phosphorus uptake in cultivated soils. Biol Fertil Soils 34:31–41

    Article  Google Scholar 

  • Oehl F, Oberson A, Tagmann HU, Besson JM, Dubois D, Mäder P, Roth HR, Frossard E (2002) Phosphorus budget and phosphorus availability in soils under organic and conventional farming. Nutr Cycl Agroecosyst 62:25–35

    Article  CAS  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oehl F, Sieverding E, Mã¤Der P, Dubois D, Ineichen K, Boller T, Wiemken A (2004b) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583

    Article  PubMed  Google Scholar 

  • Oelmann Y, Richter AK, Roscher C, Rosenkranz S, Temperton VM, Weisser WW, Wilcke W (2011) Does plant diversity influence phosphorus cycling in experimental grasslands? Geoderma 167-168:178–187

    Article  CAS  Google Scholar 

  • Pellegrino E, Bedini S (2014) Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol Biochem 68:429–439

    Article  CAS  Google Scholar 

  • Richardson AE (2001) Propects for using soil microorganisms to improve the acquisition of phosphorus by plants. Funct Plant Biol 28:897–906

    Article  Google Scholar 

  • Richardson AE, George TS, Hens M, Simpson RJ (2005) Utilization of soil organic phosphorus by higher plants. In: Turner BL, Frossard E, Baldwin DS (eds) Organic Phosphorus in the Environment. Wallingford, CABI International, pp. 165–184

    Chapter  Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156

    Article  CAS  Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystems processes. Ecol Lett 7:740–754

    Article  Google Scholar 

  • Robertson GP, Swinton SM (2005) Reconciling agricultural productivity and environmental integrity: a grand challenge for agriculture. Front Ecol Environ 3:38–46

    Article  Google Scholar 

  • Rosendahl S, Matzen HB (2008) Genetic structure of arbuscular mycorrhizal populations in fallow and cultivated soils. New Phytol 179:1154–1161

    Article  PubMed  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560

    Article  CAS  PubMed  Google Scholar 

  • Sattari, S.Z., Bouwman, A.F., Giller, K.E. & Van Ittersum, M.K., 2012. Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proc Natl Acad Sci 109:6348–6353.

    Google Scholar 

  • Scavia D, Donnelly KA (2007) Reassessing Hypoxia Forecasts for the Gulf of Mexico. Environ Sci Technol 41:8111–8117

    Article  CAS  PubMed  Google Scholar 

  • Schindler DW, Hecky RE, Findlay DL, Stainton MP, Parker BR, Paterson MJ, Beaty KG, Lyng M, Kasian SEM (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: Results of a 37-year whole-ecosystem experiment. Proc Natl Acad Sci 105:11254–11258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnitzer SA, Klironomos JN, Hillerislambers J, Kinkel LL, Reich PB, Xiao K, Rillig MC, Sikes BA, Callaway RM, Mangan SA (2011) Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92:296–303

    Article  PubMed  Google Scholar 

  • Schwartz RC, Dao TH, Bell JM (2011) Manure and mineral fertilizer effects of seasonal dynamics of bioactive soil phosphorus fractions. Agron J 103:1724–1733

    Article  Google Scholar 

  • Sharpley A, Jarvie HP, Buda A, May L, Spears B, Kleinman P (2013) Phosphorus legacy: overcoming the effects of past management practices to mitigate future water quality impairment. J Environ Qual 42:1308–1326

    Article  CAS  PubMed  Google Scholar 

  • Sharpley AN, Mcdowell RW, Kleinman PJA (2001) Phosphorus loss from land to water: integrating agricultural and environmental management. Plant Soil 237:287–307

    Article  CAS  Google Scholar 

  • Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349:89–120

    Article  CAS  Google Scholar 

  • Smith FA, Smith SE (2011) What is the significance of the arbuscular mycorrhizal colonization of many economically important crop plants. Plant Soil 348:63–79

    Article  CAS  Google Scholar 

  • Smith RG, Gross KL, Robertson GP (2008) Effects of crop diversity on agroecosystem function: crop yield response. Ecosystems 11:355–366

    Article  Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London

    Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524

    Article  Google Scholar 

  • Symstad AJ, Chapin FS, Wall DH, Gross KL, Huenneke LF, Mittelbach GG, Peters DPC, Tilman D (2003) Long-Term and large-scale perspectives on the relationship between biodiversity and ecosystem functioning. Bioscience 53:89–98

    Article  Google Scholar 

  • Tarafdar JC, Marschner H (1994) Phosphatase activity in the rhizosphere and hydrosphere of a VA mycorrhizal wheat supplied with inorganic and organic phosphorus. Soil Biol Biochem 26:3897–3395

    Article  Google Scholar 

  • Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc Natl Acad Sci 96:5995–6000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    Article  CAS  PubMed  Google Scholar 

  • Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632

    Article  CAS  PubMed  Google Scholar 

  • Toljander JF, Santos-Gonzalez JC, Tehler A, Finlay RD (2008) Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol 65:323–338

    Article  CAS  PubMed  Google Scholar 

  • Tomich TP, Brodt S, Ferris H, Galt R, Horwath WR, Kebreab E, Leveau JHJ, Liptzin D, Lubell M, Merel P, Michelmore R, Rosenstock T, Scow KM, Six J, Williams N, Yang L (2011) Agroecology: a review from a global-change perspective. Annu Rev Environ Resour 36:193–222

    Article  Google Scholar 

  • USGS (1999) The quality of our nation's waters - nutrients and pesticides. U.S.Geological Survey Circular 1225, Reston

    Google Scholar 

  • Valkama E, Uusitalo R, Ylivainio K, Virkajarvi P, Turtola E (2009) Phosphorus fertilization: a meta-analysis of 80 years of research in Finland. Agric Ecosyst Environ 130:75–85

    Article  CAS  Google Scholar 

  • Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Van Der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  CAS  Google Scholar 

  • Van Vuuren DP, Bouwman AF, Beusen AHW (2010) Phosphorus demand for the 1970-2100 period: A scenario analysis of resource depletion. Glob Environ Chang 20:428–439

    Article  Google Scholar 

  • Verbruggen E, Kiers ET, Bakelaar PC, Röling WM, Van Der Heijden MA (2012) Provision of contrasting ecosystem services by soil communities from different agricultural fields. Plant Soil 350:43–55

    Article  CAS  Google Scholar 

  • Verbruggen E, Röling WFM, Gamper HA, Kowalchuk GA, Verhoef HA, Van Der Heijden MGA (2010) Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol 186:968–979

    Article  CAS  PubMed  Google Scholar 

  • Wagg C, Bender SF, Widmer F, Van Der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci 111:5266–5270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wardle DA (1998) Controls of temporal variability of the soil microbial biomass: a global-scale synthesis. Soil Biol Biochem 30:1627–1637

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van Der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  PubMed  Google Scholar 

  • Watson CJ, Smith RV, Matthews DI (2007) Increase in phosphorus losses from grassland in response to Olsen-P accumulation. J Environ Qual 36:1452–1460

    Article  CAS  PubMed  Google Scholar 

  • White CM, Weil RR (2010) Forage radish and cereal rye cover crop effects on mycorrhizal fungus colonization of maize roots. Plant Soil 328:507–521

    Article  CAS  Google Scholar 

  • Withers PJA, Sylvester-Bradley R, Jones DL, Healey JR, Talboys PJ (2014) Feed the crop not the soil: rethinking phosphorus management in the food chain. Environ Sci Technol 48:6523–6530

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8:2907–2916

    Article  CAS  Google Scholar 

  • Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Shannon Osborne and Dr. Randy Anderson for improving the manuscript by critical review.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Michael Lehman .

Editor information

Editors and Affiliations

Additional information

Disclaimer

“Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.”

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Lehman, R.M., Taheri, W.I. (2017). Soil Microorganisms Can Reduce P Loss from Cropping Systems. In: Lichtfouse, E. (eds) Sustainable Agriculture Reviews. Sustainable Agriculture Reviews, vol 22. Springer, Cham. https://doi.org/10.1007/978-3-319-48006-0_2

Download citation

Publish with us

Policies and ethics