Science in Society Archive

Phosphorus Starvation Threatens the World

The world is running short of phosphate ore for chemical fertilizers; recovering phosphate from waste and reducing phosphate use in phosphate rich countries can alleviate the shortage and simultaneously prevent environmental pollution Prof Joe Cummins

Phosphorus a limiting nutrient

Earth seems to be growing sicker every year along with threats to global food security.  One threat that has been widely ignored is the diminished availability of phosphorous fertilization for crops due to rapidly declining sources of the ore used to produce the fertilizer and rising prices for the fertilizer. Countries across the world fall into three groups: the rich phosphate fertilizer users, the phosphate poor that suffer from food shortages due to low food crop  production and even human disease from phosphorous deficiency and the inability  to purchase expensive phosphate fertilizer, and the few remaining countries that are rapidly  mining out phosphate ore [1].  Organizations dealing with crop yield in Africa tend to focus on introducing varieties with increased yield in optimum soil fertility but such varieties do not do well in the vast areas lacking nutrients such as phosphate [2].  Phosphorous is a   limiting nutrient for humanity. Phosphorous is key to the storage of genetic information in DNA and RNA; it plays a crucial role in cell membranes and in practically all energy transactions through ATP (adenosine triphosphate) and other organic phosphate molecules. Phosphates are ubiquitous in life chemistry as they are involved in just about every function [3].

Phosphate availability declining

Phosphorus scarcity has been gaining increased attention on the research and policy agenda in recent years due to the 800% phosphate rock price spike in 2008.  Actual estimates of phosphate depletion or ‘peak phosphorus’ vary widely, from the critical point occurring in 30–40 years to 300–400 years. These estimates diverge for various reasons, ranging from the uncertainty in volume and quality of the global reserves to the quantity of future demand. The biggest users of phosphates, China and the United States, will have exhausted their own reserves in 50 to 60 years, and by the end of the next century nearly 90 % of all reserves of phosphates, which are important for the production of food, will be controlled by one country – Morocco [4]. Historical sources of phosphorus for use as fertilizers, including manure, human excreta, guano and phosphate rock. The strong addiction to phosphate rock came into force less than 100 years ago and the global   resource   has been hogged by rich countries [5].

Heavy application of phosphate has led to environmental pollution

The extensive use of phosphate fertilizer has led to leakage into waterways and lakes causing eutrophication (nutrient enrichment leading to algal bloom). Algal blooms are dangerous because some algae are toxic and the blooms also remove oxygen from the waterways.  In recent years, there have been record algal blooms in the Great Lake Erie caused by agricultural runoffs along with warming weather trends [6].  In China, which produces more than 50% of the world’s vegetables, excessive use of animal manures and chemical fertilizers has resulted in extensive phosphate pollution of the environment [7]. In the United States, only 5%   of the phosphate extracted from nature for food was found to be  ingested by humans,  while the remainder was lost to the environment [8]. In England, the  phosphates discharge from urban  sewage treatment  plants was  greater than the agricultural discharges into rivers  and the urban  phosphorous discharges  have begun to be remedied  by phosphorous stripping prior to discharge to the environment [9].  While   wealthy countries pollute their waterways and lakes with excess phosphate,   poor   countries in Africa and South America suffer from low crop yields and human illness due to phosphate starvation of soils.

Hypophosphatemia a disease of low phosphate intake

Chronic phosphorus deficiency in humans causes proximal myopathy (muscle disease). Acute hypophosphatemia may precipitate rhabdomyolysis (muscle breakdown). Plasma low phosphorus concentration suppresses erythrocyte synthesis and storage of 2,3-diphosphoglycerate (2,3-DPG), which plays an important role in the affinity of haemoglobin for oxygen. Symptoms of nervous system dysfunction, such as weakness, apathy, a bedridden state, and intention tremors, are also observed in severe hypophosphatemia [10]. Severe malnutrition contributes up to 50 % of childhood mortality in developing countries, and is frequently characterized by electrolyte depletion, including low total body phosphate in children treated at Kenyatta National Hospital with kwashiorkor (protein deficiency). Among children with mild, moderate, and severe hypophosphataemia, 8, 14 and 21 % died respectively [11]. It is safe to say that insufficient phosphate is a serious problem that will worsen as the world’s supply of phosphate ore shrinks.

Phosphate starvation in crops

Phosphorous starvation profoundly affects plant growth. Maize is the most widely cultivated crop around the world, and commonly affected by phosphate deficiency, but the underlying molecular basis of response mechanisms is still unknown. The transcriptional response of maize roots to phosphate starvation at 3 days after deprivation revealed a total of 283 responsive genes, 199 and 84 up- and down-regulated respectively by 2-fold or more. Pi-responsive genes were found to be involved in sugar and nitrogen metabolic pathways, ion transport, signal transduction, transcriptional regulation, and other processes related to growth and development. The expression patterns of maize inorganic phosphorus transporters, acid phosphatase, phytase, 2-deoxymugineic acid synthase, POD and MYB transcription factors were validated in root response to low phosphorus stress.  Two genes encoding phytase and acid phosphatase were significantly induced by phosphate deficiency, and play a pivotal role in the absorption and re-utilization of phosphate in maize [12].

Plants   acquire   phosphates from the soil, but phosphate availability is limiting for plant growth and crop yield in more than 30 % of the world’s arable land. The application of fertilizer can compensate for low availability in cropping systems, but high phosphate input causes severe environmental problems. Crop production of the important legume, the common bean Phaseolus vulgaris, is often limited by low phosphorus in the soil. The genotypes, BAT477 and DOR364 of the common bean have contrasting responses to phosphate starvation. Plants with the BAT477 deficiency tolerant genotype showed higher phosphate content and root biomass than DOR364 plants under phosphate starvation.  A gene-signalling pathway controlling the degradation of phosphate-containing proteins was present in the phosphate deficiency-tolerant phenotype and absent in the sensitive phenotype [13].

Poor availability of P in soils and consequent P-deficiency are major constraints to crop production globally. Phosphorus is taken up by plants as  orthophosphate . However, in most cultivated soils, organic phosphorous comprises 30–80 % of the total phosphorous, and approximately 60–80% of organic phosphorous exists in the form of phytate, which is not directly available to plants. Thus, improving phytate  bioavailability is important for plant phosphorous   nutrition, and for sustainable agricultural development as phosphorous ore resources are depleting worldwide [14]. Phytic acid (also known as inositol hexakisphosphate in salt form), a saturated cyclic acid, is the principal storage form of phosphorus in many plant tissues, especially bran and seeds. Phytate is not digestible to humans or non--ruminant animals, so it is not a source of either inositol or phosphate if eaten directly. Moreover, phytic acid chelates and makes unabsorbable important minor minerals such as zinc and iron, and to a lesser extent, also macro minerals such as calcium and magnesium [15]. Phytate is a major storage   form of phosphorous in the seeds of grains and legumes  and during  seed germination  the plant enzyme phytase  is activated releasing orthophosphate  for plant growth [16]. Phytate can be degraded by fungi and bacteria that inhabit compost [17].

Remedies for phosphate ore decline

As the global supply of phosphate ore declines, the world must turn to recycling phosphorous and to more economic use of phosphate in agriculture. There are several ways to recycle phosphorus

Recovery from municipal waste

Urban phosphate discharges are being recycled. In the European Union around 25 % of phosphorus in municipal wastewater is currently recovered and reused, predominantly as sludge. Crop residues (such as straw, husks and stalks) are an important and common source of phosphorus, while organic waste from food processing and production (such as peelings, oil cakes, food preparation and plate waste) can also be productively reused for their phosphorus content. Initially developed by the University of British Columbia in Canada to reduce the occurrence of pipe blockages in advanced wastewater treatment facilitates, the Ostara nutrient recovery technology recovers phosphorus and ammonium from wastewater treatment plants via a fluidized bed reactor [18]. Wastewater centrate (water leaving a centrifuge after most of the solids have been removed) influent from sludge dewatering side-streams enters the reactor from the bottom. Magnesium is added to facilitate the crystallization process. The resultant struvite is then harvested from the reactor, dried and packaged onsite for sale.  The full-scale commercial operation at Portland’s Durham wastewater treatment plant processes 100 % of the wastewater through the reactor at a 90% recovery rate. Currently, much of the urban sewage sludge is incinerated. The Dutch sewage sludge treatment company, N.V. Slibverwerking Noord-Brabant (SNB) recovers phosphorus from sewage sludge ash and sells it to an international phosphate producer.

Driven by the goal of local food security, this phosphorus recovery system in southern Niger involves 700 households (eight villages) in the recycling of nutrients and organic matter from human excreta via simple urinals and waterless toilets.  Yields of vegetables and cereals fertilized with excreta were equal or superior to those receiving equivalent amounts of chemical fertilizer [19]. Phosphate recovery is producing a clear and immediate relief from the growing shortage of phosphate ore.

Recovery from bone

It has been suggested that the phosphate fertilizer gap in developing countries can be immediately relieved. Animal bone products (derived from the grinding or thermal treatment of raw bone) contain a greater concentration of plant-available phosphorus than commercial phosphate rock fertilizer. For instance, between 2008 and 2011 the livestock herd in Ethiopia comprised more than 50 million cattle, 23 million sheep and 22 million goats, and would have yielded approximately 192 000 to 330 000 tonnes of bone waste annually. Recycling of these bones would have yielded around 28 to 58 % of annual phosphorus fertilizer supplies to Ethiopia over the same period. Importing an equivalent amount of phosphorus fertilizer costs approximately US$ 50 to 104 million. Developing countries already have access to an indigenous supply of phosphate fertilizer, in the form of organic waste products. By tapping into this resource, these countries can secure a significant fraction of their phosphorus demands without relying on international markets or the benevolence of rich countries [20]. It is also true that developed countries would benefit greatly from recovering bone meal from food waste on a scale much larger than the current production of bone meal.

Recovery through green manure

Green manure consists of growing a crop, such as clover or grass, which is ploughed under the soil to improve fertility. Deep rooted legumes will extract phosphate from deep soil strata that are not available to the roots of food crops. Crotalaria (rattlepods) proved to be a suitable green manure in maize and bean cropping systems in Uganda [21]. Vetch (Vicia) and oat green manures are effective in relieving nutrient deficiency in the soil of central Mexico [22]. Using green manures provides some immediate relief to the soil nutrient deficiency in developing countries, but in the long run, may require some phosphate fertilizer to maintain food crop productivity.

Genetic engineering in phosphorus starvation

Crop and microbial genetic engineering is being promoted for relieving the global shortage of phosphate ore. However, most of that research appears to be focused on phytate reduction in grains.  Such research is not likely to provide improvements that effectively compensate for the global consumption of phosphate ore [3]. Examples of current genetic engineering research include comparing transgenic maize containing bacterial  phytase genes with the maize treated with phytase  enzymes  purified from bacteria in the diet of chickens, which like humans, excrete undigested phytate when fed maize grain.  The transgenic chickens digested transgenic maize phytate comparably to the phytase treated grain [23].  

Low phytate rice was produced by transforming rice with a small RNA (RNAi) gene driven by a promoter from rice, which reduced production of phytate in rice grain. Silencing the phytate synthesis gene led to a substantial reduction in seed phytate levels without hampering the growth and development of transgenic rice plants [24]. Chinese researchers found that a gene Ta-PHR1-A1 is involved in phosphate signalling in wheat and, when over-expressed, it increased phosphate uptake and grain yield of wheat [25]. Several publications deal with transgenic modifications leading to improvements in phosphate uptake and utilization in food crops. However, those modified crops do not have the ability to fabricate phosphorus to replace that required for human nutrition in the long run.

To conclude

The world is facing an immediate crisis in the decline in the availability of phosphate ore to provide for the food needs of globe. There is a critical need to recover the phosphate leaking from sewers and farm lands and polluting the environment. That should be the primary step to protect the health of the human population, at the same time protecting the environment.  Secondarily, selecting food crops that thrive on land devoid of phosphate is an important objective so long as the phosphorus needs of humans and animals is met, and not compromised by consuming crops containing minimal phosphate.

Article first published 22/01/14


References

  1. Obersteiner M, Penuelas J, Ciais P, van der Velde M.  The phosphorus trilemma  Nature Geoscience 2013, 6(11), 897-8.
  2. Sabchez P. Tripling crop yields in tropical Africa. Nature Geoscience 2010. 3, 299 – 300
  3. Elser JJ. Phosphorus: a limiting nutrient for humanity? Curr Opin Biotechnol 2012, 23(6), 833-8. doi: 10.1016/j.copbio.2012.03.001
  4. Cordell D, Neset TS, Prior T. The phosphorus mass balance: identifying 'hotspots' in the food system as a roadmap to phosphorus security.  Curr Opin Biotechnol 2012 23(6):839-45. doi: 10.1016/j.copbio.2012.03.010
  5. Cordell D, Drangert J and White S.   The story of phosphorus: global food security and food for thought. Global Environmental Change 2009, 19, 292–305.
  6. Michalak AM, Anderson EJ, Beletsky D, Boland S, Bosch NS, Bridgeman TB, Chaffin JD, Cho K, Confesor R, Daloglu I, Depinto JV, Evans MA, Fahnenstiel GL, He L, Ho JC, Jenkins L, Johengen TH, Kuo KC, Laporte E, Liu X, McWilliams MR, Moore MR, Posselt DJ, Richards RP, Scavia D, Steiner AL, Verhamme E, Wright DM, Zagorski MA.Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proc Natl Acad Sci U S A  2013 110(16),6448-52. doi: 10.1073/pnas.1216006110
  7. Yan Z, Liu P, Li Y, Ma L, Alva A, Dou Z, Chen Q, Zhang F. Phosphorus in China's Intensive Vegetable Production Systems:Overfertilization, Soil Enrichment, and Environmental Implications. J Environ Qual 2013, 42(4),982-9. doi: 10.2134/jeq2012.0463.
  8. Suh S, Yee S. Phosphorus use-efficiency of agriculture and food system in the US. Chemosphere 2011, 84(6), 806-13. doi: 10.1016/j.chemosphere.2011.01.051
  9. Jarvie HP, Neal C and Withers PJ. Sewage-effluent phosphorus: a greater risk to river eutrophication than agricultural phosphorus? Sci Total Environ 2006, 360(1-3), 246-53.
  10. Takeda E, Ikeda S, Nakahashi O. Lack of phosphorus intake and nutrition. Clin Calcium 2012, 22(10), 1487-91
  11. Kimutai D, Maleche-Obimbo E, Kamenwa R, Murila F.Hypo-phosphataemia in children under five years with kwashiorkor and marasmic kwashiorkor. East Afr Med J 2009, 86(7), 330-6.
  12. Lin HJ, Gao J, Zhang ZM, Shen YO, Lan H, Liu L, Xiang K, Zhao M, Zhou S, Zhang YZ, Gao SB, Pan GT. Transcriptional responses of maize seedling root to phosphorus starvation. Mol Biol Rep 2013, 5359-79. doi: 10.1007/s11033-013-2636-x.
  13. Ramírez M, Flores-Pacheco G, Reyes JL, Luzlvarez A, Drevon JJ, Girard L, Hernández G Two Common Bean Genotypes with Contrasting Response to Phosphorus Deficiency Show Variations in the microRNA 399-Mediated PvPHO2 Regulation within the PvPHR1 Signaling Pathway. Int J Mol Sci 2013,14(4):8328-44. doi: 10.3390/ijms14048328.
  14. Wang Y, Ye X, Ding G and Xu F. Overexpression of phyA and appA genes improves soil organic phosphorus utilisation and seed phytase activity in Brassica napus. PLoS One, 2013, 8(4), e60801. doi: 10.1371/journal.pone.0060801
  15. Phytic acid. Wikipedia,  2013  http://en.wikipedia.org/wiki/Phytic_acid
  16. Kyriakidis KB, GaliotouPanayotou M, ]Stavropoulou A and Athanasopoulos P. Increase in phytase activity and decrease in phytate during germination of four common legumes. Biotechnology Letters 1998, 20, 5,  475-8.
  17. Fathallh Eida M, Nagaoka T, Wasaki J and Kouno K. Phytate degradation by fungi and bacteria that inhabit sawdust and coffee residue composts. Microbes Environ 2013, 28(1), 71-80.
  18. Cordell D, Rosemarin A, Schröder JJ and Smit AL. Towards global phosphorus security: a systems framework for phosphorus recovery and reuse options. Chemosphere 2011 Aug;84(6):747-58. doi: 10.1016/j.chemosphere.2011.02.032
  19. Simons,A, Solomon,D,Chibssa,W,Blalock,G,Lehmann,J.Filling the phosphorus fertilizer gap in developing countries Nature Geoscience 2014  7, 3 doi:10.1038/ngeo2049
  20. Fischler, M.; Wortmann, C.S.; Feil, B. Crotalaria (C. ochroleuca G. Don.) as a green manure in maize-bean cropping systems in Uganda  Field Crops Research,1999 , 61 2,  97-107
  21. Astier,M, Maass,J,Etchevers-Barra,J,Peña,J, de León González,F. Short-term green manure and tillage management effects on maize yield and soil quality in an Andisol  Soil & Tillage Research 2006, 88,  1, 153-159.
  22. Gao CQ, Ji C, Zhao LH, Zhang JY, Ma QG. Phytase transgenic corn in nutrition of laying hens: residual phytase activity and phytate phosphorus content in the astrointestinal tract. Poult Sci 2013, 92(11), 2923-9. doi: 10.3382/ps.2013-03226.
  23. Ali N, Paul S, Gayen D, Sarkar SN, Datta K and Datta SK. Development of low phytate rice by RNAi mediated seed-specific silencing of inositol 1,3,4,5,6-pentakisphosphate 2-kinase gene (IPK1). PLoS One 2013, 8(7):e68161. doi: 10.1371/journal.pone.0068161.
  24. Wang J, Sun J, Miao J, Guo J, Shi Z, He M, Chen Y, Zhao X, Li B, Han F, Tong Y and  Li Z. A phosphate starvation response regulator Ta-PHR1 is involved in phosphate signalling and increases grain yield in wheat. Ann Bot 2013,111(6),1139-53. doi: 10.1093/aob/mct080.

Got something to say about this page? Comment

Comment on this article

Comments may be published. All comments are moderated. Name and email details are required.

Name:
Email address:
Your comments:
Anti spam question:
How many legs on a duck?

There are 6 comments on this article so far. Add your comment above.

James Cooley Comment left 23rd January 2014 06:06:11
The article doesn't mention directly another source of phosphorus pollution, namely phosphorus in laundry and dish detergents. Some progress has been achieved in reducing the amount going into wast water treatment systems, but more can be done, especially in developed and rapidly developing societies.

Todd Millions Comment left 26th January 2014 09:09:38
I think that the recovery of human(and other domesticated beasts) excreted should be the highest priority-best done with on site or close too -waterless composter or biogas systems.No reason this can't or shouldn't be done throughout the world now(as in 30 years ago),one further item is a caveat.Like the so called 'nitrate shortage',since the 1890's,as well as a speculators(and Mafias) boom-The shortfall wasn't agricultural per say-it was munitions.The pin head Kaiser wasn't going too get his(just like gradmas) empire,if the nitrates needed for explosives were embargoed.Thus the Fritz Haber ammonia from air process,was his Manhattan project.The poisoning of vast tracts via ammonia/urea fertilizer was a peace dividend of this effort.Need one point too recent shellings using phosphorus incenderiy/poison gas rounds?'Needed for night fighting'-fired at close too local noon.Concern is justified on more than food security.

Richard Dunwell Comment left 29th January 2014 18:06:56
With decades of fertilisation there are massive amounts of phosphate already in the ground, but the problem is that it is not plant-available. The other thing you do not mention is cadmium contamination and it is already a big problem, with some areas of New Zealand, for example, already exceeding internationally-accepted levels. This is the reason that by law in NZ, offal (livers/kidneys) from cattle older than 18 months and sheep older than 6 months cannot be sold for human consumption. Lower-grade phosphates also contain uranium, so much of it, in fact, that when traditional sources of the uranium run out it will be extracted from phosphate. Meanwhile the phosphate continues to be applied to farmland. The NZ government's solution to the cadmium problem is to monitor soil cadmium levels and hope they will not exceed maximum permissible levels for the next 100 years. I.e. do nothing useful. Where permissible levels are in danger of being breached, phosphate application will be restricted on a sliding scale or completely forbidden. Yes, phosphate fertilisation-addicted farmers are screaming. The government's idea of remediation consists of mixing the soil horizons... which is rather pathetic and hellishly expensive. There are, however, ways to make the phosphate plant-available and deal with the cadmium. The same technology can also be applied in the treatment of sewage to make it safe to use as a source of phosphate (which it is not without removing the heavy metals). If you are interesting in taking this further please contact me.

Jan Metcalf Comment left 29th November 2014 06:06:37
Waste water from sewage treatment plants is a significant source of phosphates in UK rivers. You cite one Dutch Company who recovers the phosphorus and sells it. Perhaps water companies managing UK sewage could do likewise - it could be of commercial as well as environmental benefit. A win, win situation?

Dr Mrinalini Menon Comment left 2nd May 2015 05:05:15
Would this not be an opportunity in the area of research into acid phosphatases/phytases? I am extremely keen & am currently working in this area & look forward to interactions & valuable inputs from the scientific fraternity.

Robert Vincin Comment left 7th March 2016 19:07:06
Where did Mother Nature gain phosphate from before Man and indeed deliver it globally. Like so many essential elements to sustain and grow soil food fodder forestry supplied by Nature we are advised are pests. Mother Nature the receiver of the Plants base assets soil water vegetation atmosphere bees is sending signals restore assets 100% working order or----