Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Pigs expressing salivary phytase produce low-phosphorus manure

Nature Biotechnology volume 19, pages 741–745 (2001)Cite this article

A Corrigendum to this article was published on 01 October 2001

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Tilman, D. et al. Forecasting agriculturally driven global environmental changes. Science 292, 281–284 (2001).

    Article  CAS  Google Scholar 

  • Smil, V. Phosphorus in the environment: natural flows and human interferences. Annu. Rev. Energy Environ. 25, 53–88 (2000).

    Article  Google Scholar 

  • 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).

    Article  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Jongbloed, A.W. & Lenis, N.P. Environmental concerns of animal manure. J. Anim. Sci. 76, 2641–2648 (1998).

    Article  CAS  Google Scholar 

  • Mallin, M.A. Impacts of industrial animal production on rivers and estuaries. American Scientist Jan–Feb., 26–37 (2000).

    Article  Google Scholar 

  • Naqvi, S.W. et al. Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408, 346–349 (2000).

    Article  CAS  Google Scholar 

  • Poulsen, H. Phosphorus utilization and excretion in pig production. J. Environ. Qual. 29, 24–27 (2000).

    Article  CAS  Google Scholar 

  • 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).

    CAS  Google Scholar 

  • Ridley, R.M. & Baker, H.F. Big decisions based on small numbers: lessons from BSE. Vet. Q. 21, 86–92 (1999).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Abelson, P.H. A potential phosphate crisis. Science 283, 2015 (1999).

    Article  CAS  Google Scholar 

  • Wodzinski, R.J. & Ullah, A.H.J. Phytase. Adv. Appl. Microbiol. 42, 263–302 (1996).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Allen, N.D. et al. Transgenes as probes for active chromosomal domains in mouse development. Nature 333, 852–855 (1988).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Garrick, D., Fiering, S., Martin, D.I.K. & Whitelaw, E. Repeat-induced gene silencing in mammals. Nature Genet. 18, 56–59 (1998).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Chi, T.H. & Crabtree, G.R. Inositol phosphates in the nucleus. Science 287, 1937–1939 (2000).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Driver, J., Lijmbach, D. & Steen, I. Why recover phosphorus for recycling and how? Environmental Technol. 20, 651–662 (2001).

    Article  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Eeckhout, W. & De Paepe, M. Total phosphorus, phytate-phosphorus and phytase activity in plant feedstuffs. Anim. Feed Sci. Technol. 47, 19–29 (1994).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

Download references

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

Author notes

  1. Jesper Laursen

    Present address: DAKO A/S, Immunocytochemistry Department, Produktionsvej 42, Glostrup, DK-2600, Denmark

Authors and Affiliations

  1. Department of Microbiology, University of Guelph, Guelph, N1G 2W1, Ontario, Canada

    Serguei P. Golovan, Michael Cottrill & Cecil W. Forsberg

  2. Department of Molecular Biology and Genetics, University of Guelph, Guelph, N1G 2W1, Ontario, Canada

    Serguei P. Golovan, Roy G. Meidinger & John P. Phillips

  3. Department of Animal and Poultry Science, University of Guelph, Guelph, N1G 2W1, Ontario, Canada

    Ayodele Ajakaiye, Ming Z. Fan & Roger R. Hacker

  4. Arkell Swine Research, University of Guelph, Guelph, N1G 2W1, Ontario, Canada

    Miles Z. Wiederkehr & David J. Barney

  5. Department of Population Medicine, University of Guelph, Guelph, N1G 2W1, Ontario, Canada

    Claire Plante & John W. Pollard

  6. Department of Pathobiology, University of Guelph, Guelph, N1G 2W1, Ontario, Canada

    M. Anthony Hayes

  7. Institute of Molecular and Structural Biology, Aarhus C University, C F Mollers Alle Bldg 130, Aarhus C, DK-800, Denmark

    Jesper Laursen & J. Peter Hjorth

Authors
  1. Serguei P. Golovan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roy G. Meidinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ayodele Ajakaiye
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael Cottrill
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miles Z. Wiederkehr
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David J. Barney
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Claire Plante
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. John W. Pollard
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ming Z. Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. M. Anthony Hayes
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jesper Laursen
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. J. Peter Hjorth
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Roger R. Hacker
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. John P. Phillips
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Cecil W. Forsberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Electronic supplementary material

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/90788

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing