OJSS  Vol.3 No.5 , September 2013
Livestock Antibiotic Effects on Nitrification, Denitrification, and Microbial Community Composition in Soils
ABSTRACT

The broiler (Gallus gallus domesticus) industry in the United States and several other countries routinely includes subtherapeutic levels of antibiotics such as roxarsone, virginiamycin, and bacitracin in the feed to improve bird growth yields. Large fractions of the antibiotics fed to the birds are excreted in manure (litter), which is often applied to soils to improve fertility. Some concerns with this practice are antibiotic-induced alterations in microbially-mediated nutrient cycling, which could influence plant productivity and environmental quality. To investigate this possibility, a series of lab experiments were conducted to determine the effects of increasing levels of the three livestock antibiotics on nitrification, denitrification, and microbial community composition (fatty acid methyl ester profiles) of soils collected along a catena. Roxarsone and virginiamycin significantly influenced microbial community composition and inhibited nitrification in the soils, but only at levels that were several-fold higher than expected in poultry litter-applied soils. Bacitracin did not affect microbial growth, microbial community composition, or nitrification at any concentration tested (up to 500 mg·kg-1). None of the antibiotics influenced denitrification at environmentally-relevant concentrations. Amounts of antibiotics in soil solution were greatly reduced by sorption, which followed Freundlich models in the concentration range of 1 - 500 mg·L-1. Results from this study indicated that addition of roxarsone, virginiamycin, or bacitracin to these soils at environmentally-relevant concentrations would not likely impact microbial community composition, nitrification or denitrification due to intrinsic resistance/insensitivity of microorganisms to these antibiotics and reductions in the bioavailable amounts due to sorption by soil surfaces.


Cite this paper
S. Banerjee and E. D’Angelo, "Livestock Antibiotic Effects on Nitrification, Denitrification, and Microbial Community Composition in Soils," Open Journal of Soil Science, Vol. 3 No. 5, 2013, pp. 203-212. doi: 10.4236/ojss.2013.35024.
References
[1]   M. Mellon, C. Benbrook and K. L. Benbrook, “Hogging It: Estimates of Antimicrobial Abuse in Livestock,” Union of Concerned Scientists, Cambridge, 2001.
http://www.ucsusa.org/assets/documents/food_and_agriculture/hog_chaps.pdf

[2]   K. Kummerer, “Significance of Antibiotics in the Environment,” Journal of Antimicrobial Chemotherapy, Vol. 52, 1, 2003, pp. 5-7. doi:10.1093/jac/dkg293

[3]   A. K. Sarmah, M. T. Meyer and A. B. A Boxall, “A Global Perspective on the Use, Sales, Exposure Pathways, Occurrence, Fate and Effects of Veterinary Antibiotics in the Environment,” Chemosphere, Vol. 65, No. 5, 2006, pp. 725-759. doi:10.1016/j.chemosphere.2006.03.026

[4]   R. A. Swick, “Role of Growth Promotents in Poultry and Swine Feed,” ASA Technical Bulletin, Vol. AN04, 1996. www.asaimsea.com/pdfs/AN04-swick.pdf

[5]   P. Butaye, L. A. Deviese and F. Haesebrouck, “Antimicrobial Growth Promoters Used in Animal Feed: Effects of Less Well-Known Antibiotics on Gram-Positive Bacteria,” American Society for Microbiology, Vol. 16, No. 2, 2003, pp. 175-188. doi:10.1128/CMR.16.2.175-188.2003

[6]   A. A. Pedroso, J. F. Menten, M. R. Lambais, A. M. Racanicci, F. A. Longo and J. O. Sorbara, “Intestinal Bacterial Community and Growth Performance of Chickens Fed Diets Containing Antibiotics,” Poultry Science, Vol. 85, No. 4, 2006, pp. 747-752.

[7]   H. D. Chapman and Z. B. Johnson, “Use of Antibiotics and Roxarsone in Broiler Chickens in the USA: Analysis for the Years 1995 to 2000,” Poultry Science, Vol. 81, No. 3, 2002, pp. 356-364.

[8]   S. Thiele-Bruhn, “Pharmaceutical Antibiotic Compounds in Soils-A Review,” Journal of Plant Nutrition, Vol. 166, No. 2, 2003, pp. 145-16. doi:10.1002/jpln.200390023

[9]   B. Halling-Sorensen, S. N. Nielsen, P. F. Lanzky, F. Ingerslev, H. C. H. Lutzhoft and S. E. Jorgensen, “Occurrence, Fate and Effects of Pharmaceutical Substances in the Environment—A Review,” Chemosphere, Vol. 36, No. 2, 1998, pp. 357-394. doi:10.1016/S0045-6535(97)00354-8

[10]   K. Kim, G. Owens, S. Kwon, K. So, D. Lee and Y. S. Ok, “Occurrence and Environmental Fate of Veterinary Antibiotics in the Terrestrial Environment,” Water Air Soil Pollution, Vol. 214, No. 1-4, 2011, pp. 163-174. doi:10.1007/s11270-010-0412-2

[11]   C. Colinas, E. Ingham and R. Molina, “Population Responses of Target and Nontarget Forest Soil Organisms to Selected Biocides,” Soil Biology & Biochemistry, Vol. 26, No. 1, 1994, pp. 41-47. doi:10.1016/0038-0717(94)90193-7

[12]   K. Westergaard, A. K. Muller, S. Christensen, J. Bloem and S. J. Sorensen, “Effects of Tylosin as a Disturbance on the Soil Microbial Community,” Soil Biology & Biochemistry, Vol. 33, No. 15, 2001, pp. 2061-2071. doi:10.1016/S0038-0717(01)00134-1

[13]   D. K. Patten, D. C. Wolf, W. E. Kunkle and L. W. Douglas, “Effect of Antibiotics in Beef Cattle Feces on Nitrogen and Carbon Mineralization in Soil and on Plant Growth and Composition,” Journal of Environmental Quality, Vol. 9, No. 1, 1980, pp. 167-172.
doi:10.2134/jeq1980.00472425000900010035x

[14]   F. Liu, G. Ying, R. Tao, J. Zhao, J. Yang and L. Zhao, “Effects of Six Selected Antibiotics on Plant Growth and Soil Microbial and Enzymatic Activities,” Environmental Pollution, Vol. 157, No. 5, 2009, pp. 636-1642.
doi:10.1016/j.envpol.2008.12.021

[15]   S. Thiele-Bruhn and I. C. Beck, “Effects of Sulfonamide and Tetracycline Antibiotics on Soil Microbial Activity and Microbial Biomass,” Chemosphere, Vol. 59, No. 4, 2005, pp. 457-465.
doi:10.1016/j.chemosphere.2005.01.023

[16]   D. Pramer, “The Persistence and Biological Effects of Antibiotics in Soil,” Journal of Applied Microbiology, Vol. 6, No. 3, 1958, pp. 221-224.

[17]   B. Chu, K. W. Goyne, S. H. Anderson, C. H. Lin and R. P. Udawatta, “Veterinary Antibiotic Sorption to Agroforestry Buffer, Grass Buffer, and Cropland Soils,” Agroforestry Systems, Vol. 79, No. 1, 2010, pp. 67-80. doi:10.1007/s10457-009-9273-3

[18]   B. L. Brown, A. D. Slaughter and M. E. Schreiber, “Controls on Roxarsone Transport in Agricultural Watersheds,” Applied Geochemistry, Vol. 20, No. 1, 2005, pp. 123-133.
doi:10.1016/j.apgeochem.2004.06.001

[19]   A. Mehlich, “Mehlich 3 Soil Test Extractant: A Modification of Mehlich 2 Extractant,” Communications in Soil Science and Plant Analysis, Vol. 15, No. 12, 1984, pp. 1409-1416.
doi:10.1080/00103628409367568

[20]   W. R. Howarth and E. A. Paul, “Microbial Biomass,” In: Weaver, et al., Eds., Soil Analysis, Part 2: Microbiological and Biochemical Properties, SSSA Book Series No. 5. Madison, 1994, pp. 753-773.

[21]   J. D. Crutchfield and H. R. Burton, “Improved Methods for the Quantification of Nitrate in Plant Materials,” Analytical Letters, Vol. 22, No. 3, 1998, pp. 555-571. doi:10.1080/00032718908051349

[22]   J. R. White and K. R. Reddy, “Influence of Nitrate and Phosphorus Loading on Denitrifying Enzyme Activity in Everglades’s Wetland Soils,” Soil Science Society of America Journal, Vol. 63, No. 6, 1999, pp. 1945-1954. doi:10.2136/sssaj1999.6361945x

[23]   M. E. Schutter and R. P. Dick, “Comparison of Fatty Acid Methyl Ester (FAME) Methods for Characterizing Microbial Communities,” Soil Science Society of America Journal, Vol. 64, No. 5, 2000, pp. 1659-1668. doi:10.2136/sssaj2000.6451659x

[24]   E. M. D’Angelo, A. D. Karathanasis, E. J. Sparks, S. A. Ritchey and S. A. Wehr-McChesney, “Soil Carbon and Microbial Communities at Mitigated and Late Successional Bottomland Forest Wetlands,” Wetlands, Vol. 25, No. 1, 2005, pp. 162-175. doi:10.1672/0277-5212(2005)025[0162:SCAMCA]2.0.CO;2

[25]   T. J. Dumonceaux, J. E. Hill, S. M. Hemmingsen and A. G. Van Kessel, “Characterization of Intestinal Microbiota and Response to Dietary Virginiamycin Supplementation in the Broiler Chicken,” Applied and Environmental Microbiology, Vol. 72, No. 4, 2006, pp. 2815-2823. doi:10.1128/AEM.72.4.2815-2823.2006

[26]   M. G. Wise and G. R. Siragusa, “Quantitative Analysis of the Intestinal Bacterial Community in Oneto ThreeWeek-Old Commercially Reared Broiler Chickens Fed Conventional or Antibiotic-Free Vegetable-Based Diets,” Journal of Applied Microbiology, Vol. 102, No. 4, 2007, pp. 1138-1149.
doi:10.1111/j.1365-2672.2006.03153.x

[27]   H. K. Allen, J. Donato, H. H. Wang, K. A. Cloud-Hansen, J. Davies and J. Handelsman, “Call of the Wild: Antibiotic Resistance Genes in Natural Environments,” Nature Reviews Microbiology, Vol. 8, No. 4, 2010, pp. 251-259. doi:10.1038/nrmicro2312

[28]   V. M. D’Costa, E. Griffiths and G. D. Wright, “Expanding the Soil Antibiotic Resistome: Exploring Environmental Diversity,” Current Opinion in Microbiology, Vol. 10, No. 5, 2007, pp. 481-489. doi:10.1016/j.mib.2007.08.009

[29]   N. Esiobu, L. Armenta and J. Ike. “Antibiotic Resistance in Soil and Water Environments,” International Journal of Environmental Health Research, Vol. 12, No. 2, 2002, pp. 133-144.
doi:10.1080/09603120220129292

[30]   C. W. Knapp, J. Dolfing, P. A. Ehlert and D. W. Graham, “Evidence of Increasing Antibiotic Resistance Gene Abundances in Archived Soils Since 1940,” Environmental Science & Technology, Vol. 44, No. 2, 2010, pp. 580-587. doi:10.1021/es901221x

[31]   D. Mazel and J. Davies, “Antibiotic Resistance in Microbes,” Cellular and Molecular Life Sciences, Vol. 56, No. 9-10, 1999, pp. 742-754. doi:10.1007/s000180050021

[32]   E. C. Oldfield, “The Road to Resistance: Antibiotics as Growth Promoters for Animals,” World Literature Review, Vol. 98, No. 2, 2003, p. 499. doi:10.1111/j.1572-0241.2003.07277.x

[33]   L. Onan and T. LaPara, “Tylosin-Resistant Bacteria Cultivated from Agricultural Soil,” FEMS Microbiology Letters, Vol. 220, No. 1, 2003, pp. 15-20. doi:10.1016/S0378-1097(03)00045-4

[34]   J. Gavalchin and S. E. Katz, “The Persistence of Fecal-Borne Antibiotics in Soil,” Journal of the Association of Official Analytical Chemists, Vol. 77, No. 2, 1994, pp. 481-485.

[35]   F. Ingerslev and B. Halling-Sorrensen, “Biodegradability of Metronidazole, Olaquindox, and Tylosin and Formation of Tylosin Degradation Products in Aerobic SoilManure Slurries,” Ecotoxicology and Environmental Safety, Vol. 48, No. 3, 2001, pp. 311-320. doi:10.1006/eesa.2000.2026

[36]   C. A. Weerasinghe and D. Towner, “Aerobic Biodegradation of Virginiamycin in Soil,” Environmental Toxicology and Chemistry, Vol. 16, No. 9, 1997, pp. 1873-1876. doi:10.1002/etc.5620160916

[37]   J. Davison, “Genetic Exchange between Bacteria in the Environment,” Plasmid, Vol. 42, No. 2, 1999, pp. 73-91. doi:10.1006/plas.1999.1421

 
 
Top