Abstract
To address the problem of manure-based environmental pollution in the pork industry, we have developed the phytase transgenic pig. The saliva of these pigs contains the enzyme phytase, which allows the pigs to digest the phosphorus in phytate, the most abundant source of phosphorus in the pig diet. Without this enzyme, phytate phosphorus passes undigested into manure to become the single most important manure pollutant of pork production. We show here that salivary phytase provides essentially complete digestion of dietary phytate phosphorus, relieves the requirement for inorganic phosphate supplements and reduces fecal phosphorus output by up to 75%. These pigs offer a unique biological approach to the management of phosphorus nutrition and environmental pollution in the pork industry.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Improvements in pig agriculture through gene editing
CABI Agriculture and Bioscience Open Access 21 June 2022
-
Towards progressive regulatory approaches for agricultural applications of animal biotechnology
Transgenic Research Open Access 09 January 2022
-
Genome Editing in Livestock, Complicity, and the Technological Fix Objection
Journal of Agricultural and Environmental Ethics Open Access 11 May 2021
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout



References
Tilman, D. et al. Forecasting agriculturally driven global environmental changes. Science 292, 281–284 (2001).
Smil, V. Phosphorus in the environment: natural flows and human interferences. Annu. Rev. Energy Environ. 25, 53–88 (2000).
American Society of Agricultural Engineers. Manure production characteristics. In ASAE standards: Standards, engineering practices and data. 663–665 (American Society of Agricultural Engineers, St. Joseph, MI; 1999).
Jongbloed, A.W. & Kemme, P.A. Effect of pelleting mixed feeds on phytase activity and the apparent absorbability of phosphorus and calcium in pigs. Anim. Feed Sci. Technol. 28, 233–242 (1990).
Kornegay, E.T. Digestion of phosphorus and other nutrients: the role of phytases and factors influencing their activity. In Enzymes in Farm animal nutrition. (ed. Bedford, M.R. & Partridge, G.G.) 237–271 (CABI Publishing, Marlborough; 2001).
NRC. Nutrient requirements of swine. (National Academy Press, Washington, DC; 1998).
Correll, D.L. Phosphorus: a rate limiting nutrient in surface waters. Poultry Sci. 78, 674–682 (1999).
Jongbloed, A.W. & Lenis, N.P. Environmental concerns of animal manure. J. Anim. Sci. 76, 2641–2648 (1998).
Mallin, M.A. Impacts of industrial animal production on rivers and estuaries. American Scientist Jan–Feb., 26–37 (2000).
Naqvi, S.W. et al. Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408, 346–349 (2000).
Poulsen, H. Phosphorus utilization and excretion in pig production. J. Environ. Qual. 29, 24–27 (2000).
Jongbloed, A.W. & Kemme, P.A. Apparent digestible phosphorus in the feeding of pigs in relation to availability, equipment and environment. 1. Digestible phosphorus in feedstuffs from plant and animal origin. Neth. J. Agric. Sci. 38, 567–575 (1990).
Ridley, R.M. & Baker, H.F. Big decisions based on small numbers: lessons from BSE. Vet. Q. 21, 86–92 (1999).
Ryder, S.J., Hawkins, S.A., Dawson, M. & Wells, G.A. The neuropathology of experimental bovine spongiform encephalopathy in the pig. J. Comp. Pathol. 122, 131–143 (2000).
Spencer, J.D., Allee, G.L. & Sauber, T. E. Phosphorus bioavailability and digestibility of normal and genetically modified low-phytate corn for pigs. J. Anim. Sci. 78, 675–681 (2000).
Abelson, P.H. A potential phosphate crisis. Science 283, 2015 (1999).
Wodzinski, R.J. & Ullah, A.H.J. Phytase. Adv. Appl. Microbiol. 42, 263–302 (1996).
Golovan, S.P., Hayes, M.A., Phillips, J.P. & Forsberg, C.W. Transgenic mice expressing bacterial phytase as a model for phosphorus pollution control. Nature Biotechnol. 19, 429–433 (2001).
Golovan, S., Wang, G., Zhang, J. & Forsberg, C.W. Characterization and overproduction of the Escherichia coli appA encoded bifunctional enzyme which exhibits both phytase and acid phosphatase activities. Can. J. Microbiol. 46, 59–71 (2000).
Leeson, S., Namkung, H., Cottrill, M. & Forsberg, C.W. Efficacy of a new bacterial phytase in poultry diets. Can. J. Anim. Sci. 80, 527–528 (2000).
Drackley, J.K. Soy in animal nutrition. (Federation of Animal Science Societies, Savoy, IL; 2000).
Ball, W.D. Cell-restricted secretory proteins as markers of cellular phenotype in salivary glands. In Biology of the salivary glands. (ed. Dobrosielski-Vergona, V.) 355–395 (CRC Press, Boca Raton; 1993).
Mirels, L., Miranda, A.J. & Ball, W.D. Characterization of the rat salivary-gland B1-immunoreactive proteins. Biochem. J. 330, 437–444 (1998).
Allen, N.D. et al. Transgenes as probes for active chromosomal domains in mouse development. Nature 333, 852–855 (1988).
Al-Shawi, R., Kinnaird, J., Burke, J. & Bishop, J.O. Expression of a foreign gene in a line of transgenic mice is modulated by a chromosomal position effect. Mol. Cell Biol. 10, 1192–1198 (1990).
Garrick, D., Fiering, S., Martin, D.I.K. & Whitelaw, E. Repeat-induced gene silencing in mammals. Nature Genet. 18, 56–59 (1998).
Robertson, G., Garrick, D., Wilson, M., Martin, D.I. & Whitelaw, E. Age-dependent silencing of globin transgenes in the mouse. Nucleic Acids Res. 24, 1465–1471 (1996).
Greiner, R., Carlsson, N. & Alminger, M.L. Stereospecificity of myo-inositol hexakisphosphate dephosphorylation by a phytate-degrading enzyme of Escherchia coli. J. Biotechnol. 84, 53–62 (2000).
Sakamoto, K., Vucenik, I. & Shamsuddin, A.M. [3H]Phytic acid (inositol hexaphosphate) is absorbed and distributed to various tissues in rats. J. Nutr. 123, 713–720 (1993).
Chi, T.H. & Crabtree, G.R. Inositol phosphates in the nucleus. Science 287, 1937–1939 (2000).
Zhang, Z.B., Kornegay, E.T., Radcliffe, J.S., Wilson, J.H. & Veit, H. P. Comparison of phytase from genetically engineered Aspergillus and canola in weanling pig diets. J. Anim. Sci. 78, 2868–2878 (2000).
Corring, T. Endogenous secretions in the pig. In Current concepts of digestion and absorption in pigs. (eds. Low, A.G. & Partridge, I.G.) 136–150 (National Institute for Research in Dairying, Reading; 1980).
Souffrant, W.B. Endogenous nitrogen losses during digestion in pigs. In Digestive physiology in pigs. (eds. Verstegen, M.W.A., Huisman, J. & den Hartog, L.A.) 147–166 (Pudoc, Wageningen; 1991).
Simons, P.C.M. et al. Improvement of phosphorus availability by microbial phytase in broilers and pigs. Brit. J. Nutr. 64, 525–540 (1990).
Ketaren, P.P., Batterham, E.S., Dettmann, E.B. & Farrell, D.J. Phosphorus studies in pigs. 3. Effect of phytase supplementation on the digestibility and availability of phosphorus in soya-bean meal for grower pigs. Br. J. Nutr. 70, 289–311 (1993).
Mroz, Z., Jongbloed, A.W. & Kemme, P.A. Apparent digestibility and retention of nutrients bound to phytate complexes as influenced by microbial phytase and feeding regimen in pigs. J. Anim. Sci. 72, 126–132 (1994).
Driver, J., Lijmbach, D. & Steen, I. Why recover phosphorus for recycling and how? Environmental Technol. 20, 651–662 (2001).
Wall, R.J., Pursel, V.G., Hammer, R.E. & Brinster, R.L. Development of porcine ova that were centrifuged to permit visualization of pronuclei and nuclei. Biol. Reprod. 32, 645–651 (1985).
Lam, S.J. & Mutharia, L.M. Antigen-antibody reactions. In Methods for general and molecular bacteriology. (eds. Gerhardt, P., Murray, R.G.E., Wood, W.A. & Krieg, N.R.) 104–132 (American Society for Microbiology, Washington; 1994).
Fan, M.Z. et al. Novel methodology allows simultaneous measurement of true phosphorus digestibility and the gastrointestinal endogenous phosphorus outputs in studies with pigs. J. Nutr. 131, (2001).
Eeckhout, W. & De Paepe, M. Total phosphorus, phytate-phosphorus and phytase activity in plant feedstuffs. Anim. Feed Sci. Technol. 47, 19–29 (1994).
Fan, M.Z. & Sauer, W.C. Determination of true ileal amino acid digestibility in feedstuffs for pigs with the linear relationships between distal ileal outputs and dietary inputs of amino acids. J. Sci. Food Agric. 73, 189–199 (1997).
Acknowledgements
We thank the staff at Arkell Swine Research and T. Archbold in the Department of Animal and Poultry Science for their assistance. This research was supported by funding from Ontario Pork, Ontario Ministry of Agriculture, Food and Rural Affairs, Food Systems Biotechnology Centre (University of Guelph) and the Natural Sciences and Engineering Research Council of Canada to C.W.F. and J.P.P.
Author information
Authors and Affiliations
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Golovan, S., Meidinger, R., Ajakaiye, A. et al. Pigs expressing salivary phytase produce low-phosphorus manure. Nat Biotechnol 19, 741–745 (2001). https://doi.org/10.1038/90788
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/90788
This article is cited by
-
Digestion and utilization of plant-based diets by transgenic pigs secreting β-glucanase, xylanase, and phytase in their salivary glands
Transgenic Research (2023)
-
Improvements in pig agriculture through gene editing
CABI Agriculture and Bioscience (2022)
-
Towards progressive regulatory approaches for agricultural applications of animal biotechnology
Transgenic Research (2022)
-
Genome Editing in Livestock, Complicity, and the Technological Fix Objection
Journal of Agricultural and Environmental Ethics (2021)