Soil bacterial community response to sulfadiazine in the soil-root zone

Journal of Plant Nutrition and Soil Science

Volumn 178, Issue 3, 2015, Pages 499-506

  Reichel, Rüdiger ^a   Michelini, Lucia ^b   Ghisi, Rossella ^b   Thiele Bruhn, Sören ^a  

^a UNIVERSITY OF TRIER   (Germany)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

Exoenzymes; Pseudomonas; Salix fragilis L.; Sulfadiazine; Zea mays L

Indexed keywords

BACTERIA (MICROORGANISMS); PSEUDOMONAS; SALIX; SALIX FRAGILIS; ZEA MAYS;

EID: 84930416046     PISSN: 14368730     EISSN: 15222624     Source Type: Journal    
DOI: 10.1002/jpln.201400352     Document Type: Article

References (49)

1. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., Vivanco, J. M. (2006): The role of root exudates in rhizosphere interactions with plants and other organisms. Ann. Rev. Plant Biol. 57, 233-266.
2. Baudoin, E., Benizri, E., Guckert, A. (2001): Metabolic fingerprint of microbial communities from distinct maize rhizosphere compartments. Eur. J. Soil. Biol. 37, 85-93.
3. Berg, G., Grube, M., Schloter, M., Smalla, K. (2014): Unraveling the plant microbiome: looking back and future perspectives. FMICB 5. DOI: 10.3389/fmicb.2014.00148.
4. Berg, G., Smalla, K. (2009): Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1-13.
5. Bergsma-Vlami, M., Prins, M. E., Staats, M., Raaijmakers, J. M. (2005): Assessment of genotypic diversity of antibiotic-producing Pseudomonas species in the rhizosphere by denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 71, 993-1003.
6. Brandt, K. K., Sjøholm, O. R., Krogh, K. A., Halling-Sørensen, B., Nybroe, O. (2009): Increased pollution-induced bacterial community tolerance to sulfadiazine in soil hotspots amended with artificial root exudates. Environ. Sci. Technol. 43, 2963-2968.
7. Brown, G. M. (1962): The biosynthesis of folic acid: II. Inhibition by sulfonamides. J. Biol. Chem. 237, 536-540.
8. Cheng, W. (2009): Rhizosphere priming effect: Its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol. Biochem. 41, 1795-1801.
9. Compant, S., Clément, C., Sessitsch, A. (2010): Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42, 669-678.
10. Costa, R., Gomes, N. C. M., Peixoto, R. S., Rumjanek, N., Berg, G., Mendonca-Hagler, L. C. S., Smalla, K. (2006): Diversity and antagonistic potential of Pseudomonas spp. associated to the rhizosphere of maize grown in a subtropical organic farm. Soil Biol. Biochem. 38, 2434-2447.
11. Demoling, L. A., Bååth, E., Greve, G., Wouterse, M., Schmitt, H. (2009): Effects of sulfamethoxazole on soil microbial communities after adding substrate. Soil Biol. Biochem. 41, 840-848.
12. Ding, G., Radl, V., Schloter-Hai, B., Jechalke, S., Heuer, H., Smalla, K., Schloter, M. (2014): Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS ONE 9. DOI: 10.1371/journal.pone.0092958.
13. Förster, M., Laabs, V., Lamshöft, M., Pütz, T., Amelung, W. (2008): Analysis of aged sulfadiazine residues in soils using microwave extraction and liquid chromatography tandem mass spectrometry. Anal. Bioanal. Chem. 391, 1029-1038.
14. Förster, M., Laabs, V., Lamshöft, M., Groeneweg, J., Zühlke, S., Spiteller, M., Krauss, M., Kaupenjohann, M., Amelung, W. (2009): Sequestration of manure-applied sulfadiazine residues in soils. Environ. Sci. Technol. 43, 1824-1830.
15. Garbeva, P., van Elsas, J. D., van Veen, J. A. (2008): Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302, 19-32.
16. Grote, M., Vockel, A., Schwarze, D., Mehlich, A., Freitag, M. (2004): Fate of antibiotics in food chain and environment originating from pig fattening (part 1). Fresenius Environ. Bull. 13, 449, 1216-1224.
17. Halling-Sørensen, B., Nors Nielsen, S., Lanzky, P. F., Ingerslev, F., Holten Lützhøft, H. C., Jørgensen, S. E. (1998): Occurrence, fate and effects of pharmaceutical substances in the environment-areview. Chemosphere 36, 357-593.
18. Hammesfahr, U., Bierl, R., Thiele-Bruhn, S. (2011a): Combined effects of the antibiotic sulfadiazine and liquid manure on the soil microbial-community structure and functions. J. Plant Nutr. Soil Sci. 174, 614-623.
19. Hammesfahr, U., Kotzerke, A., Lamshöft, M., Wilke, B.-M., Kandeler, E., Thiele-Bruhn, S. (2011b): Effects of sulfadiazine-contaminated fresh and stored manure on a soil microbial community. Eur. J. Soil. Biol. 47, 61-68.
20. Hammesfahr, U., Heuer, H., Manzke, B., Smalla, K., Thiele-Bruhn, S. (2008): Impact of the antibiotic sulfadiazine and pig manure on the microbial community structure in agricultural soils. Soil Biol. Biochem. 40, 1583-1591.
21. Heuer, H., Kroppenstedt, R. M., Lottmann, J., Berg, G., Smalla, K. (2002): Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl. Environ. Microbiol. 68, 1325-1335.
22. Heuer, H., Solehati, Q., Zimmerling, U., Kleineidam, K., Schloter, M., Müller, T., Focks, A., Thiele-Bruhn, S., Smalla, K. (2011): Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl. Environ. Microbiol. 77, 2527-2530.
23. Heuer, H., Krsek, M., Baker, P., Smalla, K., Wellington, E. M. (1997): Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl. Environ. Microbiol. 63, 3233-3241.
24. Kleineidam, K., Sharma, S., Kotzerke, A., Heuer, H., Thiele-Bruhn, S., Smalla, K., Wilke, B.-M., Schloter, M. (2010): Effect of sulfadiazine on abundance and diversity of denitrifying bacteria by determining nirK and nirS genes in two arable soils. Microb. Ecol. 60, 703-707.
25. Kopmann, C., Jechalke, S., Rosendahl, I., Groeneweg, J., Krögerrecklenfort, E., Zimmerling, U., Weichelt, V., Siemens, J., Amelung, W., Heuer, H., Smalla, K. (2012): Abundance and transferability of antibiotic resistance as related to the fate of sulfadiazine in maize rhizosphere and bulk soil. FEMS Microb. Ecol. 83, 125-134.
26. Kotzerke, A., Sharma, S., Schauss, K., Heuer, H., Thiele-Bruhn, S., Smalla, K., Wilke, B.-M., Schloter, M. (2008): Alterations in soil microbial activity and N-transformation processes due to sulfadiazine loads in pig-manure. Environ. Poll. 153, 315-322.
27. Kourtev, P. S., Ehrenfeld, J. G., Häggblom, M. (2003): Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol. Biochem. 35, 895-905.
28. Kuzyakov, Y., Domanski, G. (2000): Carbon input by plants into the soil. Review. J. Plant Nutr. Soil Sci. 163, 421-431.
29. Marschner, P., Crowley, D., Yang, C. H. (2004): Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261, 199-208.
30. Michelini, L., Reichel, R., Werner, W., Ghisi, R., Thiele-Bruhn, S. (2012): Sulfadiazine uptake and effects on Salix fragilis L. and Zea mays L. plants. Water Air Soil Poll. 223, 5243-5257.
31. Milling, A., Smalla, K., Maidl, F. X., Schloter, M., Munch, J. C. (2005): Effects of transgenic potatoes with an altered starch composition on the diversity of soil and rhizosphere bacteria and fungi. Plant Soil 266, 23-39.
32. Ollivier, J., Kleineidam, K., Reichel, R., Thiele-Bruhn, S., Kotzerke, A., Kindler, R., Wilke, B.-M., Schloter, M. (2010): Effect of sulfadiazine-contaminated pig manure on the abundances of genes and transcripts involved in nitrogen transformation in the root-rhizosphere complexes of maize and clover. Appl. Environ. Microbiol. 76, 7903-7909.
33. Reichel, R., Rosendahl, I., Peeters, E., Focks, A., Groeneweg, J., Bierl, R., Schlichting, A., Amelung, W., Thiele-Bruhn, S. (2013): Effects of slurry from sulfadiazine- (SDZ) and difloxacin- (DIF) medicated pigs on the structural diversity of microorganisms in bulk and rhizosphere soil. Soil Biol. Biochem. 62, 82-91.
34. Reichel, R., Patzelt, D., Barleben, C., Rosendahl, I., Ellerbrock, R. H., Thiele-Bruhn, S. (2014a): Soil microbial community responses to sulfadiazine-contaminated manure in different soil microhabitats. Appl. Soil Ecol. 80, 15-25.
35. Reichel, R., Radl, V., Rosendahl, I., Albert, A., Amelung, W., Schloter, M., Thiele-Bruhn, S. (2014b): Soil microbial community responses to antibiotic-contaminated manure under different soil moisture regimes. Appl. Microbiol. Biotechnol. 98, 6487-6495.
36. Sarmah, A. K., Meyer, M. T., Boxall, A. B. A. (2006): A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65, 725-759.
37. Schauss, K., Focks, A., Heuer, H., Kotzerke, A., Schmitt, H., Thiele-Bruhn, S., Smalla, K., Wilke, B.-M., Matthies, M., Amelung, W., Klasmeier, J., Schloter, M. (2009): Analysis, fate and effects of the antibiotic sulfadiazine in soil ecosystems. TRAC-Trend Anal. Chem. 28, 612-618.
38. Schmitt, H., Haapakangas, H., van Beelen, P. (2005): Effects of antibiotics on soil microorganisms: time and nutrients influence pollution-induced community tolerance. Soil Biol. Biochem. 37, 1882-1892.
39. Schmitt, H., Martinali, B., Stoob, K., Hamscher, G., Van Beelen, P., Smit, E., Van Leeuwen, K., Seinen, W. (2006): Antibiotics as environmental pollutants: Effects on soil microorganisms. Environ. Sci. Eur. 18, 110-118.
40. Schmitt, H., van Beelen, P., Tolls, J., van Leeuwen, C. L. (2004): Pollution-induced community tolerance of soil microbial communities caused by the antibiotic sulfachloropyridazine. Environ. Sci. Technol. 38, 1148-1153.
41. Smalla, K., Wieland, G., Buchner, A., Zock, A., Parzy, J., Kaiser, S., Roskot, N., Heuer, H., Berg, G. (2001): Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl. Environ. Microbiol. 67, 4742-4751.
42. Sørensen, J. (1997): The Rizosphere as a Habitat for Soil Microorganisms, in Van Elsas, J. D., Trevors, J. T., Wellington, E. M. H. (eds.): Modern Soil Microbiology. Marcel Dekker, Inc., New York, NY, USA, pp. 21-45.
43. Thiele-Bruhn, S. (2003): Pharmaceutical antibiotic compounds in soils-a review. J. Plant Nutr. Soil Sci. 166, 145-167.
44. Thiele-Bruhn, S., Bloem, J., de Vries, F. T., Kalbitz, K., Wagg, C. (2012): Linking soil biodiversity and agricultural soil management. Curr. Opin. Environ. Sustain. 4, 1-6.
45. Thiele-Bruhn, S., Beck, I.-C. (2005): Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59, 457-465.
46. Vaclavik, E., Halling-Sørensen, B., Ingerslev, F. (2004): Evaluation of manometric respiration tests to assess the effects of veterinary antibiotics in soil. Chemosphere 56, 667-676.
47. Westergaard, K., Müller, A. K., Christensen, S., Bloem, J., Sørensen, S. J. (2001): Effects of tylosin as a disturbance on the soil microbial community. Soil Biol. Biochem. 33, 2061-2071.
48. Zahar Haichar, F., Marol, C., Berge, O., Rangel-Castro, J. I., Prosser, J. I., Balesdent, J., Heulin, T., Achouak, W. (2008): Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2, 1221-1230.
49. Zielezny, Y., Groeneweg, J., Vereecken, H., Tappe, W. (2006): Impact of sulfadiazine and chlorotetracycline on soil bacterial community structure and respiratory activity. Soil Biol. Biochem. 38, 2372-2380.