Skip to main content
SpringerLink
Log in

The presence of tetracycline in cow manure changes the impact of repeated manure application on soil bacterial communities

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

The effect of tetracycline (Tc) and cow manure on soil bacterial community composition and antibiotic resistance gene (ARG) abundance in soil was investigated in the present microcosm study. Effects of repeated applications of cow manure spiked with Tc in two concentrations or without Tc on the bacterial communities of a clayey and a sandy soil with different history of anthropogenic pollution by sewer flooding were investigated. Soil samples were taken 60 days after each of three amendments. Denaturing gradient gel electrophoresis (DGGE) fingerprints of 16S rRNA gene amplicons from total community DNA revealed soil type-dependent changes in the bacterial community composition in response to manure and to Tc, which became more pronounced with repeated applications. Repeated manure amendments and Tc, in particular at high concentration, triggered the further increase of ARGs tet(A), tet(O), tet(Q), tet(W), sul1, and mobile genetic elements (MGEs) IncP-1ε plasmids and intI1, in a soil type-dependent manner. In the clay soil with no anthropogenic history, the ARG and MGE abundances were low or not detectable, while manure amendments caused pronounced increases in their relative abundance. In the sandy soil with a history of anthropogenic impact, ARGs and MGEs were already present at a higher level and strong increases were mainly observed for the relative abundances of sul2 and MGEs. Here, we show for the first time that effects of repeated cow manure applications might be dependent on soil type and foregoing anthropogenic soil pollution and that the presence of Tc could further increase the abundance of ARGs and MGEs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alexander TW, Yanke JL, Reuter T, Topp E, Read RR, Selinger BL, McAllister TA (2011) Longitudinal characterization of antimicrobial resistance genes in feces shed from cattle fed different subtherapeutic antibiotics. BMC Microbiol 11:19. doi:10.1186/1471-2180-11-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amos GCA, Hawkey PM, Gaze WH, Wellington EM (2014a) Waste water effluent contributes to the dissemination of CTX-M-15 in the natural environment. J Antimicrob Chemoth 69:1785–1791. doi:10.1093/jac/dku079

    Article  CAS  Google Scholar 

  • Amos GCA, Zhang L, Hawkey PM, Gaze WH, Wellington EM (2014b) Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Vet Microbiol 171:441–447. doi:10.1016/j.vetmic.2014.02.017

    Article  CAS  PubMed  Google Scholar 

  • Amos GCA, Gozzard E, Carter CE, Mead A, Bowes MJ, Hawkey PM, Zhang L, Singer AC, Gaze WH, Wellington EMH (2015) Validated predictive modelling of the environmental resistome. ISME J 9:1467–1476. doi:10.1038/ismej.2014.237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bahl M, Hansen L, Goesmann A, Sørensen S (2007) The multiple antibiotic resistance IncP-1 plasmid pKJK5 isolated from a soil environment is phylogenetically divergent from members of the previously established α, β and δ sub-groups. Plasmid 58:31–43. doi:10.1016/j.plasmid.2006.11.007

    Article  CAS  PubMed  Google Scholar 

  • Barraud O, Baclet MC, Denis F, Ploy MC (2010) Quantitative multiplex real-time PCR for detecting class 1, 2 and 3 integrons. J Antimicrob Chemoth 65:1642–1645. doi:10.1093/jac/dkq167

    Article  CAS  Google Scholar 

  • Binh CT, Heuer H, Kaupenjohann M, Smalla K (2008) Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiol Ecol 66:25–37. doi:10.1111/j.1574-6941.2008.00526.x

    Article  CAS  PubMed  Google Scholar 

  • Chessa L, Pusino A, Garau G, Mangia NP, Pinna MV (2016) Soil microbial response to tetracycline in two different soils amended with cow manure. Environ Sci Pollut R 23:5807–5817. doi:10.1007/s11356-015-5789-4

    Article  CAS  Google Scholar 

  • Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260. doi:10.1128/MMBR.65.2.232-260.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding GC, 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:e92958. doi:10.1371/journal.pone.0092958

    Article  PubMed  PubMed Central  Google Scholar 

  • FDA, Food and Drug Administration (2014) Antimicrobials sold or distributed for use in food-producing animals. Department of Health and Human Services.

  • Durso LM, Cook KL (2014) Impacts of antibiotic use in agriculture: what are the benefits and risks? Curr Opin Microbiol 19:37–44. doi:10.1016/j.mib.2014.05.019

    Article  PubMed  Google Scholar 

  • EC (1831/2003) Regulation (EC) No 1831/2003 of the European Parliament and of the Council of 22 September 2003 on additives for use in animal nutrition. Official Journal of the European Union.

  • Fulthorpe RR, McGowan C, Maltseva OV, Holben WE, Tiedje JM (1995) 2,4-Dichlorophenoxyacetic acid-degrading bacteria contain mosaics of catabolic genes. Appl Environ Microb 61:3274–3281

    CAS  Google Scholar 

  • Ghosh S, LaPara TM (2007) The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J 1:191–203. doi:10.1038/ismej.2007.31

    Article  CAS  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. doi:10.1023/A:1010350406708

  • Gu C, Karthikeyan KG, Sibley SD, Pedersen JA (2007) Complexation of the antibiotic tetracycline with humic acid. Chemosphere 66:1494–1501. doi:10.1016/j.chemosphere.2006.08.028

    Article  CAS  PubMed  Google Scholar 

  • Hammer TJ, Fierer N, Hardwick B, Simojoki A, Slade E, Taponen J, Viljanen H, Roslin T (2016) Treating cattle with antibiotics affects greenhouse gas emissions, and microbiota in dung and dung beetles. Proc Biol Sci. 283. doi: 10.1098/rspb.2016.0150.

  • 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. doi:10.1016/j.soilbio.2008.01.010

    Article  CAS  Google Scholar 

  • Hamscher G, Sczesny S, Höper H, Nau H (2002) Determination of persistent tetracycline residues in soil fertilized with liquid manure by high-performance liquid chromatography with electrospray ionization tandem mass spectrometry. Anal Chem 74:1509–1518. doi:10.1021/ac015588m

    Article  CAS  PubMed  Google Scholar 

  • Hamscher G, Pawelzick HT, Höper H, Nau H (2005) Different behavior of tetracyclines and sulfonamides in sandy soils after repeated fertilization with liquid manure. Environ Toxicol Chem 24:861–868. doi:10.1897/04-182R.1

    Article  CAS  PubMed  Google Scholar 

  • Hassan R, Ryu K-S (2012) Naturally derived probiotic supplementation effects on physiological properties and manure gas emission of broiler chickens. J Agric Life Sci 46:119–127. doi:10.3382/ps.2013-03314

    Google Scholar 

  • Heuer H, Smalla K (2007) Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environ Microbiol 9:657–666. doi:10.1111/j.1462-2920.2006.01185.x

    Article  CAS  PubMed  Google Scholar 

  • Heuer H, Smalla K (2012) Plasmids foster diversification and adaptation of bacterial populations in soil. FEMS Microbiol Rev 36:1083–1104. doi:10.1111/j.1574-6976.2012.00337.x

    Article  CAS  PubMed  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 Microb 63:3233–3241

    CAS  Google Scholar 

  • Heuer H, Weiland G, Schönfeld J, Schönwälder A, Gomes N, Smalla K (2001) Bacterial community profiling using dgge or tgge analysis. In: Rochelle PA (ed) Environmental molecular microbiology: protocols and applications. Horizon Scientific Press, Wymondham,UK 177–190

  • Heuer H, Focks A, Lamshöft M, Smalla K, Matthies M, Spiteller M (2008) Fate of sulfadiazine administered to pigs and its quantitative effect on the dynamics of bacterial resistance genes in manure and manured soil. Soil Biol Biochem 40:1892–1900. doi:10.1016/j.soilbio.2008.03.014

    Article  CAS  Google Scholar 

  • Heuer H, Kopmann C, Binh CT, Top EM, Smalla K (2009) Spreading antibiotic resistance through spread manure: characteristics of a novel plasmid type with low %G + C content. Environ Microbiol 11:937–949. doi:10.1111/j.1462-2920.2008.01819.x

    Article  CAS  PubMed  Google Scholar 

  • Heuer H, Schmitt H, Smalla K (2011a) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243. doi:10.1016/j.mib.2011.04.009

    Article  CAS  PubMed  Google Scholar 

  • Heuer H, Solehati Q, Zimmerling U, Kleineidam K, Schloter M, Müller T, Focks A, Thiele-Bruhn S, Smalla K (2011b) Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl Environ Microb 77:2527–2530. doi:10.1128/AEM.02577-10

    Article  CAS  Google Scholar 

  • Heuer H, Binh CT, Jechalke S, Kopmann C, Zimmerling U, Krögerrecklenfort E, Ledger T, Gonzalez B, Top E, Smalla K (2012) IncP-1epsilon plasmids are important vectors of antibiotic resistance genes in agricultural systems: diversification driven by class 1 integron gene cassettes. Front Microbiol 3:2. doi:10.3389/fmicb.2012.00002

    Article  PubMed  PubMed Central  Google Scholar 

  • Ho A, El-Hawwary A, Kim SY, Meima-Franke M, Bodelier P (2015) Manure-associated stimulation of soil-borne methanogenic activity in agricultural soils. Biol Fert Soils 51:511–516. doi:10.1007/s00374-015-0995-2

    Article  CAS  Google Scholar 

  • Hund-Rinke R, Simon M, Lukow T (2004) Effects of tetracycline on the soil microflora: function, diversity, resistance. J Soil Sediment 4:11–16

    Article  CAS  Google Scholar 

  • Jechalke S, Focks A, Rosendahl I, Groeneweg J, Siemens J, Heuer H, Smalla K (2014a) Structural and functional response of the soil bacterial community to application of manure from difloxacin-treated pigs. FEMS Microbiol Ecol 87:78–88. doi:10.1111/1574-6941.12191

    Article  CAS  PubMed  Google Scholar 

  • Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K (2014b) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545. doi:10.1016/j.tim.2014.05.005

    Article  CAS  PubMed  Google Scholar 

  • Jia DA, Zhou DM, Wang YJ, Zhu HW, Chen JL (2008) Adsorption and cosorption of Cu(II) and tetracycline on two soils with different characteristics. Geoderma 146:224–230. doi:10.1016/j.geoderma.2008.05.023

    Article  CAS  Google Scholar 

  • Jindal A, Kocherginskaya S, Mehboob A, Robert M, Mackie RI, Raskin L, Zilles JL (2006) Antimicrobial use and resistance in swine waste treatment systems. Appl Environ Microb 72:7813–7820. doi:10.1128/AEM.01087-06

    Article  CAS  Google Scholar 

  • Kim KR, Owens G, Kwon SI, So KH, Lee DB, Ok YS (2011) Occurrence and environmental fate of veterinary antibiotics in the terrestrial environment. Water Air Soil Poll 214:163–174. doi:10.1007/s11270-010-0412-2

    Article  CAS  Google Scholar 

  • Kong WD, Li CG, Dolhi JM, Li SY, He JZ, Qiao M (2012) Characteristics of oxytetracycline sorption and potential bioavailability in soils with various physical-chemical properties. Chemosphere 87:542–548. doi:10.1016/j.chemosphere.2011.12.062

    Article  CAS  PubMed  Google Scholar 

  • Kreuzig R, Höltge S (2005) Investigations on the fate of sulfadiazine in manured soil: laboratory experiments and test plot studies. Environ Toxicol Chem 24:771–776. doi:10.1897/03-582R.1

    Article  CAS  PubMed  Google Scholar 

  • Kropf S, Heuer H, Grüning M, Smalla K (2004) Significance test for comparing complex microbial community fingerprints using pairwise similarity measures. J Microbiol Methods 57:187–195. doi:10.1016/j.mimet.2004.01.002

    Article  CAS  PubMed  Google Scholar 

  • Kümmerer K (2003) Significance of antibiotics in the environment. J Antimicrob Chemother 52:5–7. doi:10.1093/jac/dkg293

    Article  PubMed  Google Scholar 

  • Kyselková M, Jirout J, Chroňáková A, Vrchotová N, Bradley R, Schmitt H, Elhottová D (2013) Cow excrements enhance the occurrence of tetracycline resistance genes in soil regardless of their oxytetracycline content. Chemosphere 93:2413–2418. doi:10.1016/j.chemosphere.2013.08.058

    Article  PubMed  Google Scholar 

  • Kyselková M, Jirout J, Vrchotová N, Schmitt H, Elhottová D (2015a) Spread of tetracycline resistance genes at a conventional dairy farm. Front Microbiol 6;536. doi: 10.3389/fmicb.2015.00536

  • Kyselková M, Jirout J, Vrchotová N, Schmitt H, Elhottová D (2015a) Spread of tetracycline resistance genes at a conventional dairy farm. Front Microbiol 6:536. doi:10.3389/fmicb.2015.00536

    Article  PubMed  PubMed Central  Google Scholar 

  • Lanz R, Kuhnert P, Boerlin P (2003) Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Vet Microbiol 91:73–84

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Chang PH, Jean JS, Jiang WT, Wang CJ (2010) Interaction between tetracycline and smectite in aqueous solution. J Colloid Interface Sci 341:311–319. doi:10.1016/j.jcis.2009.09.054

    Article  CAS  PubMed  Google Scholar 

  • Marschner P, Kandeler E, Marschner B (2003) Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461. doi:10.1016/S0038-0717(02)00297-3

    Article  CAS  Google Scholar 

  • Montforts MH, Kalf DF, van Vlaardingen PL, Linders JB (1999) The exposure assessment for veterinary medicinal products. Sci Total Environ. 225:119–133. doi: 10.1016S0048-9697(98)00338-6

  • Nelson ML, Levy SB (2011) The history of the tetracyclines. Ann N Y Acad Sci 1241:17–32. doi:10.1111/j.1749-6632.2011.06354.x

    Article  CAS  PubMed  Google Scholar 

  • Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209–215. doi:10.1006/mcpr.2001.0363

    Article  CAS  PubMed  Google Scholar 

  • Nguyen F, Starosta AL, Arenz S, Sohmen D, Donhofer A, Wilson DN (2014) Tetracycline antibiotics and resistance mechanisms. Biol Chem 395:559–575. doi:10.1515/hsz-2013-0292

    Article  CAS  PubMed  Google Scholar 

  • O’Connor S, Aga DS (2007) Analysis of tetracycline antibiotics in soil: advances in extraction, clean-up, and quantification. Trac-Trend Anal Chem 26:456–465. doi:10.1016/j.trac.2007.02.007

    Article  Google Scholar 

  • Pils JR, Laird DA (2007) Sorption of tetracycline and chlortetracycline on K- and Ca-saturated soil clays, humic substances, and clay-humic complexes. Environ Sci Technol 41:1928–1933. doi:10.1021/es062316y

  • Popowska M, Rzeczycka M, Miernik A, Krawczyk-Balska A, Walsh F, Duffy B (2012) Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob Agents Chemother 56:1434–1443. doi:10.1128/AAC.05766-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao M, Chen W, Su J, Zhang B, Zhang C (2012) Fate of tetracyclines in swine manure of three selected swine farms in China. J Environ Sci 24:1047–1052. doi:10.1016/S1001-0742(11)60890-5

    Article  CAS  Google Scholar 

  • Roberts MC (2011) Mechanisms of bacterial antibiotic resistance and lessons learned from environmental tetracycline-resistant bacteria, first edition John Wiley & Sons, Inc, Hoboken, NJ USA

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, vol 1. Cold Spring Harbor laboratory Press, USA

    Google Scholar 

  • Sarmah AK, Meyer MT, Boxall AB (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. doi:10.1016/j.chemosphere.2006.03.026

    Article  CAS  PubMed  Google Scholar 

  • Schmitt H, Stoob K, Hamscher G, Smit E, Seinen W (2006) Tetracyclines and tetracycline resistance in agricultural soils: microcosm and field studies. Microb Ecol 51:267–276. doi:10.1007/s00248-006-9035-y

    Article  PubMed  Google Scholar 

  • Selvam A, Xu D, Zhao Z, Wong JW (2012) Fate of tetracycline, sulfonamide and fluoroquinolone resistance genes and the changes in bacterial diversity during composting of swine manure. Bioresour Technol 126:383–390. doi:10.1016/j.biortech.2012.03.045

    Article  CAS  PubMed  Google Scholar 

  • Sengeløv G, Agersø Y, Halling-Sørensen B, Baloda SB, Andersen JS, Jensen LB (2003) Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ Int 28:587–595

    Article  PubMed  Google Scholar 

  • Smalla K, Heuer H, Götz A, Niemeyer D, Krögerrecklenfort E, Tietze E (2000) Exogenous isolation of antibiotic resistance plasmids from piggery manure slurries reveals a high prevalence and diversity of IncQ-like plasmids. Appl Environ Microb 66:4854–4862

    Article  CAS  Google Scholar 

  • 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 Microb 67:4742–4751. doi:10.1128/aem.67.10.4742-4751.2001

    Article  CAS  Google Scholar 

  • Smith MS, Yang RK, Knapp CW, Niu Y, Peak N, Hanfelt MM, Galland JC, Graham DW (2004) Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl Environ Microb 70:7372–7377. doi:10.1128/AEM.70.12.7372-7377.2004

    Article  CAS  Google Scholar 

  • Sun HY, Deng SP, Raun WR (2004) Bacterial community structure and diversity in a century-old manure-treated agroecosystem. Appl Environ Microb 70:5868–5874. doi:10.1128/AEM.70.10.5868-5874.2004

    Article  CAS  Google Scholar 

  • Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl Environ Microb 66:4605–4614

    Article  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, Beck IC (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465. doi:10.1016/j.chemosphere.2005.01.023

    Article  CAS  PubMed  Google Scholar 

  • Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci U S A 111:15202–15207. doi:10.1073/pnas.1409836111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A 112:5649–5654. doi:10.1073/pnas.1503141112

    Article  PubMed  PubMed Central  Google Scholar 

  • Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NC, Schloter M, Berg G, Smalla K (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microb 75:3859–3865. doi:10.1128/AEM.00414-09

    Article  CAS  Google Scholar 

  • Winckler C, Grafe A (2001) Use of veterinary drugs in intensive animal production. J Soil Sediment 1:66–70

    Article  CAS  Google Scholar 

  • Wolters B, Kyselková M, Krögerrecklenfort E, Kreuzig R, Smalla K (2015) Transferable antibiotic resistance plasmids from biogas plant digestates often belong to the IncP-1ε subgroup. Front Microbiol. 6. doi:10.3389/fmicb.2014.00765

  • Wolters B, Ding GC, Kreuzig R, Smalla K (2016) Full-scale mesophilic biogas plants using manure as C-source: bacterial community shifts along the process cause changes in the abundance of resistance genes and mobile genetic elements. FEMS Microbiol Ecol 92:1–17. doi:10.1093/femsec/fiv163

    Google Scholar 

  • Wu K, Yuan S, Wang L, Shi J, Zhao J, Shen B, Shen Q (2014) Effects of bio-organic fertilizer plus soil amendment on the control of tobacco bacterial wilt and composition of soil bacterial communities. Biol Fert Soils 50:961–971. doi:10.1007/s00374-014-0916-9

    Article  Google Scholar 

  • You Y, Hilpert M, Ward MJ (2012) Detection of a common and persistent tet(L)-carrying plasmid in chicken-waste-impacted farm soil. Appl Environ Microb 78:3203–3213. doi:10.1128/AEM.07763-11

    Article  CAS  Google Scholar 

  • Zhang Y, Boyd SA, Teppen BJ, Tiedje JM, Li H (2014) Role of tetracycline speciation in the bioavailability to escherichia coli for uptake and expression of antibiotic resistance. Environ Sci Technol 48:4893–4900. doi:10.1021/es5003428

  • Zhao S, Liu D, Ling N, Chen F, Fang W, Shen Q (2014) Bio-organic fertilizer application significantly reduces the Fusarium oxysporum population and alters the composition of fungi communities of watermelon Fusarium wilt rhizosphere soil. Biol Fert Soils 50:765–774. doi:10.1007/s00374-014-0898-7

    Article  Google Scholar 

  • Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci U S A 110:3435–3440. doi:10.1073/pnas.1222743110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Luigi Chessa gratefully acknowledges Sardinia Regional Government for the financial support of his PhD scholarship (P.O.R. Sardegna F.S.E. Operational Programme of the Autonomous Region of Sardinia, European Social Fund 2007–2013 - Axis IV Human Resources, Objective l.3, Line of Activity l.3.1.). Sven Jechalke was funded by the Federal Environment Agency (Umweltbundesamt) (FKZ 3713 63 402). The authors would like to thank Dr. Martina Kyselková to provide us positive controls for qPCR reactions.

Author information

Author notes

  1. Sven Jechalke

    Present address: Institute for Phytopathology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 (IFZ), 35392, Giessen, Germany

  2. Guo-Chun Ding

    Present address: College of Resources and Environmental Sciences, China Agricultural University, Yuanmingyuan xilu No 2, Haidian District, 100193, Beijing, China

Authors and Affiliations

  1. Department of Agriculture, University of Sassari, Viale Italia 39, 07100, Sassari, Italy

    Luigi Chessa, Alba Pusino & Nicoletta Pasqualina Mangia

  2. Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Messeweg 11-12, 38104, Braunschweig, Germany

    Luigi Chessa, Sven Jechalke, Guo-Chun Ding & Kornelia Smalla

Authors
  1. Luigi Chessa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sven Jechalke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guo-Chun Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alba Pusino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicoletta Pasqualina Mangia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kornelia Smalla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luigi Chessa.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Bacterial 16S rRNA gene amplicons of CL and SA soil 60 days after the first amendment. Four replicates for each soil treatment were performed. M: manure; Tc100: 100 mg Tc kg−1 soil dry weight; Tc500: 500 mg Tc kg−1 soil dry weight

High resolution image (TIF 11470 kb)

Fig. S2

Bacterial 16S rRNA gene amplicons of CL and SA soil 60 days after the second amendment. Four replicates for each soil treatment were performed. M manure; Tc100 100 mg Tc kg−1 soil dry weight; Tc500 500 mg Tc kg−1 soil dry weight

High resolution image (TIF 11301 kb)

Fig. S3

Bacterial 16S rRNA gene amplicons of CL and SA soil 60 days after the third amendment. Four replicates for each soil treatment were performed. M manure; Tc100 100 mg Tc kg−1soil dry weight; Tc500 500 mg Tc kg−1 soil dry weight

High resolution image (TIF 12867 kb)

ESM 4

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chessa, L., Jechalke, S., Ding, GC. et al. The presence of tetracycline in cow manure changes the impact of repeated manure application on soil bacterial communities. Biol Fertil Soils 52, 1121–1134 (2016). https://doi.org/10.1007/s00374-016-1150-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-016-1150-4

Keywords

Search

Navigation