Skip to main content
Log in

Soil microbial community responses to antibiotic-contaminated manure under different soil moisture regimes

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Sulfadiazine (SDZ) is an antibiotic frequently administered to livestock, and it alters microbial communities when entering soils with animal manure, but understanding the interactions of these effects to the prevailing climatic regime has eluded researchers. A climatic factor that strongly controls microbial activity is soil moisture. Here, we hypothesized that the effects of SDZ on soil microbial communities will be modulated depending on the soil moisture conditions. To test this hypothesis, we performed a 49-day fully controlled climate chamber pot experiments with soil grown with Dactylis glomerata (L.). Manure-amended pots without or with SDZ contamination were incubated under a dynamic moisture regime (DMR) with repeated drying and rewetting changes of >20 % maximum water holding capacity (WHCmax) in comparison to a control moisture regime (CMR) at an average soil moisture of 38 % WHCmax. We then monitored changes in SDZ concentration as well as in the phenotypic phospholipid fatty acid and genotypic 16S rRNA gene fragment patterns of the microbial community after 7, 20, 27, 34, and 49 days of incubation. The results showed that strongly changing water supply made SDZ accessible to mild extraction in the short term. As a result, and despite rather small SDZ effects on community structures, the PLFA-derived microbial biomass was suppressed in the SDZ-contaminated DMR soils relative to the CMR ones, indicating that dynamic moisture changes accelerate the susceptibility of the soil microbial community to antibiotics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Bapiri A, Bååth E, Rousk J (2010) Drying-rewetting cycles affect fungal and bacterial growth differently in an arable soil. Microb Ecol 60:419–428

    Article  PubMed  Google Scholar 

  • Baughman TA, Shaw DR (1996) Effect of wetting/drying cycles on dissipation patterns of bioavailable imazaquin. Weed Sci 44:380–382

    CAS  Google Scholar 

  • Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12

    Article  CAS  PubMed  Google Scholar 

  • Brown GM (1962) The biosynthesis of folic acid: II Inhibition by sulfonamides. J Biol Chem 237:536–540

    CAS  PubMed  Google Scholar 

  • Costa R, Gomes NCM, Peixoto RS, Rumjanek N, Berg G, Mendonca-Hagler LCS, 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

    Article  CAS  Google Scholar 

  • Davet P (2004) Microbial ecology of the soil and plant growth. Science Publishers Inc, Plymouth, pp 84–85

    Google Scholar 

  • Demoling LA, 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

    Article  CAS  Google Scholar 

  • Evans S, Wallenstein M (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101–116

    Article  Google Scholar 

  • Fierer N, Schimel JP, Holden PA (2003) Influence of drying–rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71

    Article  CAS  PubMed  Google Scholar 

  • 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. Env Sci Technol 43:1824–1830

    Article  Google Scholar 

  • García-Valcárcel AI, Tadeo JL (1999) Influence of soil moisture on sorption and degradation of hexazinone and simazine in soil. J Agric Food Chem 47:3895–3900

    Article  PubMed  Google Scholar 

  • Gomes NCM, Heuer H, Schönfeld J, Costa R, Mendonça-Hagler L, Smalla K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232:167–180

    Article  CAS  Google Scholar 

  • Gordon H, Haygarth PM, Bardgett RD (2008) Drying and rewetting effects on soil microbial community composition and nutrient leaching. Soil Biol Biochem 40:302–311

    Article  CAS  Google Scholar 

  • Gutiérrez I, Watanabe N, Harter T, Glaser B, Radke M (2010) Effect of sulfonamide antibiotics on microbial diversity and activity in a Californian Mollic Haploxeralf. J Soil Sedim 10:537–544

    Article  Google Scholar 

  • Halling-Sørensen B (2001) Inhibition of aerobic growth and nitrification of bacteria in sewage sludge by antibacterial agents. Arch Environ Contam Toxicol 40:451–460

    Article  PubMed  Google Scholar 

  • 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 Soil Sci Plant Nutr 174:614–623

    Article  CAS  Google Scholar 

  • Hammesfahr U, Kotzerke A, Lamshöft M, Wilke B, 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Heuer H, Krsek M, Baker P, Smalla K, Wellington EM (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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heuer H, Schmitt H, Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243

    Article  CAS  PubMed  Google Scholar 

  • Iovieno P, Bååth E (2008) Effect of drying and rewetting on bacterial growth rates in soil. FEMS Microbiol Ecol 65:400–407

    Article  CAS  PubMed  Google Scholar 

  • Kopmann C, Jechalke S, Rosendahl I, Groeneweg J, Krögerrecklenfort E, Zimmerling U, Weichelt V, Siemens J, Amelung W, Heuer H, Smalla K (2013) Abundance and transferability of antibiotic resistance as related to the fate of sulfadiazine in maize rhizosphere and bulk soil. FEMS Microbiol Ecol 83:125–134

    Article  CAS  PubMed  Google Scholar 

  • Kotzerke A, Sharma S, Schauss K, Heuer H, Thiele-Bruhn S, Smalla K, Wilke B, Schloter M (2008) Alterations in soil microbial activity and N-transformation processes due to sulfadiazine loads in pig-manure. Environ Pollut 153:315–322

    Article  CAS  PubMed  Google Scholar 

  • Kotzerke A, Klemer S, Kleineidam K, Horn M, Drake H, Schloter M, Wilke B (2010) Manure contaminated with the antibiotic sulfadiazine impairs the abundance of nirK- and nirS-type denitrifiers in the gut of the earthworm Eisenia fetida. Biol Fertil Soils 46:415–418

    Google Scholar 

  • Kumar K, Gupta SC, Baidoo SK, Chander Y, Rosen CJ (2005) Antibiotic uptake by plants from soil fertilized with animal manure. J Environ Qual 34:2082–2085

    Article  CAS  PubMed  Google Scholar 

  • Landesman W, Dighton J (2011) Shifts in microbial biomass and the bacteria: fungi ratio occur under field conditions within 3 h after rainfall. Microb Ecol 62:228–236

    Article  PubMed  Google Scholar 

  • Larkin R, Honeycutt C, Griffin T (2006) Effect of swine and dairy manure amendments on microbial communities in three soils as influenced by environmental conditions. Biol Fertil Soils 43:51–61

    Article  Google Scholar 

  • Marshall BM, Levy SB (2011) Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24:718–733

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mavrodi DV, Mavrodi OV, Parejko JA, Bonsall RF, Kwak Y, Paulitz TC, Thomashow LS, Weller DM (2012) Accumulation of the antibiotic phenazine-1-carboxylic acid in the rhizosphere of dryland cereals. Appl Environ Microbiol 78:804–812

    Google Scholar 

  • Miller KJ, Kennedy EP, Reinhold VN (1986) Osmotic adaptation by gram-negative bacteria: possible role for periplasmic oligosaccharides. Science 231:48–51

    Article  CAS  PubMed  Google Scholar 

  • Milling A, Smalla K, Maidl FX, Schloter M, Munch JC (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

    Article  Google Scholar 

  • Moyano FE, Manzoni S, Chenu C (2013) Responses of soil heterotrophic respiration to moisture availability: An exploration of processes and models. Soil Biol Biochem 59:72–85

    Article  CAS  Google Scholar 

  • Ok Y, Kim S-C, Kim K-R, Lee S, Moon D, Lim K, Sung J-K, Hur S-O, Yang J (2011) Monitoring of selected veterinary antibiotics in environmental compartments near a composting facility in Gangwon Province, Korea. Environ Monit Assess 174:693–701

    Article  CAS  PubMed  Google Scholar 

  • Ollivier J, Kleineidam K, Reichel R, Thiele-Bruhn S, Kotzerke A, Kindler R, Wilke B, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Orchard VA, Cook FJ (1983) Relationship between soil respiration and soil moisture. Soil Biol Biochem 15:447–453

    Article  Google Scholar 

  • Rosendahl I, Siemens J, Groeneweg J, Linzbach E, Laabs V, Herrmann C, Vereecken H, Amelung W (2011) Dissipation and sequestration of the veterinary antibiotic sulfadiazine and its metabolites under field conditions. Env Sci Technol 45:5216–5222

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sarmah AK, Meyer MT, Boxall ABA (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

    Article  CAS  PubMed  Google Scholar 

  • Schneckenburger T, Schaumann GE, Woche SK, Thiele-Bruhn S (2012) Short-term evolution of hydration effects on soil organic matter properties and resulting implications for sorption of naphthalene-2-ol. J Soils Sediments 12:1269–1279

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Schmitt H, van Beelen P, Tolls J, van Leeuwen CL (2004) Pollution-induced community tolerance of soil microbial communities caused by the antibiotic sulfachloropyridazine. Environ Sci Technol 38:1148–1153

    Article  CAS  PubMed  Google Scholar 

  • Singh BK, Dawson LA, Macdonald CA, Buckland SM (2009) Impact of biotic and abiotic interaction on soil microbial communities and functions: a field study. Appl Soil Ecol 41:239–248

    Article  Google Scholar 

  • Tappe W, Herbst M, Hofmann D, Koeppchen S, Kummer S, Thiele B, Groeneweg J (2013) Degradation of Sulfadiazine by Microbacterium lacus Strain SDZm4, Isolated from Lysimeters Previously Manured with Slurry from Sulfadiazine-Medicated Pigs. Appl Environ Microbiol 79:2572–2577

    Google Scholar 

  • Thiele S (2000) Adsorption of the antibiotic pharmaceutical compound sulfapyridine by a long-term differently fertilized loess Chernozem. Z. Pflanzenernähr. Bodenk 163:589–594

    CAS  Google Scholar 

  • Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils—a review. J Plant Nutr Soil Sci 166:145–167

    Article  CAS  Google Scholar 

  • Thiele‐Bruhn S (2005) Microbial inhibition by pharmaceutical antibiotics in different soils—dose‐response relations determined with the iron (III) reduction test. Environ Toxicol Chem 24:869–876

    Article  PubMed  Google Scholar 

  • Thiele-Bruhn S, Beck I-C (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465

    Article  CAS  PubMed  Google Scholar 

  • Walker A, Moon Y-H, Welch SJ (1992) Influence of temperature, soil moisture and soil characteristics on the persistence of alachlor. Pestic Sci 35:109–116

    Article  CAS  Google Scholar 

  • Wu J, Brookes PC (2005) The proportional mineralisation of microbial biomass and organic matter caused by air-drying and rewetting of a grassland soil. Soil Biol Biochem 37:507–515

    Article  CAS  Google Scholar 

  • Xiang S-R, Doyle A, Holden PA, Schimel JP (2008) Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils special section: enzymes in the environment. Enzymes in the Environment III. Soil Biol Biochem 40:2281–2289

    Article  CAS  Google Scholar 

  • Zelles L, Bai QY (1993) Fractionation of fatty acids derived from soil lipids by solid phase extraction and their quantitative analysis by GC-MS. Soil Biol Biochem 25:495–507

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Elvira Sieberger and Petra Ziegler for the practical support. This project was funded by the German Research Foundation (DFG) within the Research Unit FOR 566 “Veterinary medicines in soil: basic research for risk assessment.”

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sören Thiele-Bruhn.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 18021 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reichel, R., Radl, V., Rosendahl, I. et al. Soil microbial community responses to antibiotic-contaminated manure under different soil moisture regimes. Appl Microbiol Biotechnol 98, 6487–6495 (2014). https://doi.org/10.1007/s00253-014-5717-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-5717-4

Keywords

Navigation