Effects of veterinary medicines on the functional diversity of the microbial biomass in different soil compartments in dependence of varying soil moisture conditions
Final Report Abstract
Veterinary antibiotics are used in the animal husbandry for therapeutic purposes and for growth promotion. By the application of manure from treated animals as fertilizer in agriculture, excreted antibiotics and their associated metabolites enter the soil environment. In the present project, we investigated the effects of the antibiotics sulfadiazine, amoxicillin and difloxacin, used in veterinary medicine, on the activity and functional diversity of microbial communities. Thereby, an especial emphasis was given to nitrogen cycle, due to the relevance of this nutrient to plant growth, crop production and sustainable use of soils. The focus of the study was to test the hypothesis that the fate and effects of antibiotics is highly determined by the i) type of antibiotic, ii) the mode and number of application to soil as well as iii) the abiotic soil properties and the climatic conditions. The degree to which the antibiotics affected microbial functions was to a large extent controlled by the exposure of the soil microbial community to the antibiotics, which, in turn, depended on the compound’s fate. Amoxicillin was so readily degraded that its residues hardly affected microbial community functions. Difloxacin in turn was strongly adsorbed by soil particles, so that it was not bioavailable. Both antibiotics had therefore only low potential to affect microbial processes assessed in the experiments. Larger and lasting effects were only reported for sulfadiazine (SDZ). Yet, since SDZ is a bacteriostatic agent, these effects were only observed following the stimulation of microbial activity by adding manure as a substrate. As expected, the measured effects greatly differed between the investigated soil compartments. While consequences of the application of manure containing antibiotics to microbial communities of bulk soils were relatively low, these were more pronounced in the rhizosphere of maize and clover. Also environmental conditions, like soil moisture, influenced the effect pattern of the applied antibiotics on microbial communities involved in nitrogen transformation. In general, the bacterial communities that carry on the process of nitrification were more sensitive to the application of manure containing antibiotic than those related to denitrification. This might be explained by the fact that denitrification is a facultative process carried out by very diverse group of microorganisms. Yet, nitrification potential was less affected by the antibiotic application due to the functional redundancy between ammonia oxidizing bacterial (AOB) and ammonia oxidizing archaeal (AOA) communities. Repeated applications of SDZ-manure led to progressing changes of the microbial community structure and to long-lasting (permanent) decrease of the soil microbial activity. Yet, as shown for AOB, after many applications the community begins to recover due to the selection of either intrinsically better adapted organisms or development of SDZ resistance. In conclusion, we observed that in order to evaluate the risk of the introduction of antibiotics to soil ecosystems many factors must be considered such as bioavailability of the compound, type of soil, concentration and frequency of application. Besides, the selection of general processes carried out by diverse group of microbes as indicator parameters might mask effects of antibiotics on key soil processes, such as nitrification.
Publications
- (2008): Alterations in soil microbial activity and N-transformation processes due to Sulfadiazine loads in pig-manure. Environmental Pollution 153, 315–322
Kotzerke, A, Sharma, S, Schauss, K, Heuer, H, Thiele-Bruhn, S, Smalla, K, Wilke, M, Schloter, M
(See online at https://doi.org/10.1016/j.envpol.2007.08.020) - (2009): Dynamics and functional relevance of ammonia-oxidizing archaea in agricultural soils. Environmental Microbiology 11, 446–456
Schauss, K, Focks, A, Leininger, S, Kotzerke, A, Heuer, H, Thiele-Bruhn, S, Sharma, S, Wilke, BM, Matthies, M, Smalla, K, Munch, JC, Amelung, W, Kaupenjohann, M, Schleper, C, Schloter, M
(See online at https://doi.org/10.1111/j.1462-2920.2008.01783.x) - (2010): Effect of sulfadiazine on abundance and diversity of denitrifying bacteria by determining nirK and nirS genes in two arable soils. Microbial Ecology 60, 703-707
Kleineidam K, Sharma S, Kotzerke A, Heuer H, Thiele-Bruhn S, Smalla K, Wilke BM, Schloter M
(See online at https://doi.org/10.1007/s00248-010-9691-9) - (2010): Effect of sulfadiazine-contaminated pig manure on abundance of genes and transcripts involved in nitrogen transformation in the root-rhizosphere complexes of maize and clover. Applied Environmental Microbiology 76, 7903–7909
Ollivier, J, Kleineidam, K, Reichel, T, Thiele-Bruhn, S, Kotzerke, A, Wilke, BM, Schloter, M
(See online at https://doi.org/10.1128/AEM.01252-10) - (2010): Manure contaminated with the antibiotic sulfadiazine impairs the abundance of nirK- and nirS-type denitrifiers in the gut of the earthworm Eisenia fetida. Biology Fertility of Soils 46, 415–418
Kotzerke, A, Kleineidam, K, Horn, M, Drake, H, Wilke, BM, Schloter, M
(See online at https://doi.org/10.1007/s00374-009-0434-3) - (2011): Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Applied Environmental Microbiology 77, 2527–2530
Heuer, H, Solehati, Q, Zimmerling, U, Kleineidam, K, Schloter, M, Müller, T, Focks, A, Thiele-Bruhn, S, Smalla, K
(See online at https://doi.org/10.1128/AEM.02577-10) - (2011): Alterations in total microbial activity and nitrification rates in soil due to amoxicillin spiked pig manure. Plant Nutrition and Soil Science 174, 56–64
Kotzerke, A, Kleineidam, K, Wilke, BM, Schloter, M
(See online at https://doi.org/10.1002/jpln.200900210) - (2011): Effects of veterinary antibiotics on the activity and functional diversity of microorganisms in different soils. Dissertation. TU Berlin, 134 pp.
Kotzerke, A.
- (2011): Influence of difloxacin-contaminated manure on microbial community structure and function in soils. Biology and Fertility of Soils 47, 177–186
Kotzerke A, Hammesfahr, U, Kleineidam, K, Lamshöft, M, Thiele Bruhn, S, Wilke, BM, Schloter, M
(See online at https://doi.org/10.1007/s00374-010-0517-1) - (2011): Nitrogen turnover in soil and global change. FEMS Microbiology Ecology 78, 3–16
Ollivier, J, Töwe, S, Bannert, A, Hai, B, Kastl, EM, Meyer, A, Su, MX, Kleineidam, K, Schloter, M
(See online at https://doi.org/10.1111/j.1574-6941.2011.01165.x) - (2012): Persistence of the fluoroquinolone antibiotic difloxacin in soil and lacking effects on nitrogen turnover, Journal of Environmental Quality 41, 1275–1283
Rosendahl, I, Siemens, J, Kindler, R, Groeneweg, J, Zimmermann J, Czerwinski, S, Lamshöft, M, Laabs V, Wilke, BM, Vereecken, H, Amelung, W
(See online at https://doi.org/10.2134/jeq2011.0459) - (2013): Diversity, abundance and activity of microbes involved in nitrogen turnover in the rhizosphere of different plants grown on sites contaminated with the antibiotic sulfadiazine or heavy metals. Dissertation, TU Munich, 147 pp.
Ollivier, J.
- (2013): Effects of repeated application of sulfadiazine-contaminated pig manure on the abundance and diversity of ammonia- and nitrite oxidizers in the root-rhizosphere complex of pasture plants under field conditions. Frontiers in Microbiology 4, 22/1
Ollivier, J, Schacht, D, Kindler, R, Groneweg, J, Engel, M, Wilke, BM, Kleineidam, K, Schloter, M
(See online at https://doi.org/10.3389/fmicb.2013.00022) - (2014): Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS ONE 9, e92958
Ding, G.C., Radl, V., Hai, B., Jechalke, S., Heuer, H., Smalla, K., Schloter, M.
(See online at https://doi.org/10.1371/journal.pone.0092958)
