Structural and functional response of the soil bacterial community to application of manure from difloxacin-treated pigs

FEMS Microbiology Ecology

Volumn 87, Issue 1, 2014, Pages 78-88

  Jechalke, Sven ^a   Focks, Andreas ^b   Rosendahl, Ingrid ^c   Groeneweg, Joost ^d   Siemens, Jan ^c   Heuer, Holger ^a   Smalla, Kornelia ^a  

^a INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF BONN   (Germany)

^d FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

DGGE; Difloxacin; Manure; Resistance; Rhizosphere; Soil

Indexed keywords

ANTIBIOTICS; BACTERIUM; COMMUNITY COMPOSITION; COMMUNITY STRUCTURE; DISTURBANCE; FUNCTIONAL RESPONSE; MAIZE; MANURE; MICROBIAL COMMUNITY; PIG; SOIL ECOSYSTEM; SOIL MICROORGANISM;

BACTERIA (MICROORGANISMS); SUIDAE; ZEA MAYS;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CIPROFLOXACIN; DIFLOXACIN; DRUG DERIVATIVE;

ANIMAL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM; CLASSIFICATION; DGGE; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTEGRON; ISOLATION AND PURIFICATION; MAIZE; MANURE; MICROBIOLOGY; RESISTANCE; RHIZOSPHERE; SOIL; SWINE;

DGGE; DIFLOXACIN; MANURE; RESISTANCE; RHIZOSPHERE; SOIL;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL PROTEINS; CIPROFLOXACIN; DRUG RESISTANCE, BACTERIAL; INTEGRONS; MANURE; RHIZOSPHERE; SOIL MICROBIOLOGY; SUS SCROFA; SWINE; ZEA MAYS;

EID: 84891485830     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12191     Document Type: Article

References (41)

1. Aarestrup FM (2005) Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin Pharmacol Toxicol 96: 271-281.
2. Adriaenssens N, Coenen S, Versporten A et al. (2011) European Surveillance of Antimicrobial Consumption (ESAC): outpatient antibiotic use in Europe (1997-2009). J Antimicrob Chemother 66: 3-12.
3. Badri DV & Vivanco JM (2009) Regulation and function of root exudates. Plant, Cell Environ 32: 666-681.
4. Barraud O, Baclet MC, Denis F & Ploy MC (2010) Quantitative multiplex real-time PCR for detecting class 1, 2 and 3 integrons. J Antimicrob Chemother 65: 1642-1645.
5. 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.
6. Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8: 1137-1144.
7. Charpentier X, Polard P & Claverys J-P (2012) Induction of competence for genetic transformation by antibiotics: convergent evolution of stress responses in distant bacterial species lacking SOS? Curr Opin Microbiol 15: 570-576.
8. Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, Maxwell S & Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38: 1086-1108.
9. Collignon P, Powers JH, Chiller TM, Aidara-Kane A & Aarestrup FM (2009) World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies for the use of antimicrobials in food production animals. Clin Infect Dis 49: 132-141.
10. Dalhoff A (2012) Resistance surveillance studies: a multifaceted problem-the fluoroquinolone example. Infection 40: 239-262.
11. Dalkmann P, Broszat M, Siebe C, Willaschek E, Sakinc T, Huebner J, Amelung W, Grohmann E & Siemens J (2012) Accumulation of Pharmaceuticals, Enterococcus, and resistance genes in soils irrigated with wastewater for zero to 100 years in central Mexico. PLoS ONE 7: e45397.
12. Doornbos RF, van Loon LC & Bakker P (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32: 227-243.
13. Drlica K & Zhao XL (1997) DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61: 377-392.
14. Garnier F, Raked N, Gassama A, Denis F & Ploy MC (2006) Genetic environment of quinolone resistance gene qnrB2 in a complex sul1-type integron in the newly described Salmonella enterica serovar Keurmassar. Antimicrob Agents Chemother 50: 3200-3202.
15. Gillings M, Boucher Y, Labbate M, Holmes A, Krishnan S, Holley M & Stokes HW (2008a) The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol 190: 5095-5100.
16. Gillings MR, Krishnan S, Worden PJ & Hardwick SA (2008b) Recovery of diverse genes for class 1 integron-integrases from environmental DNA samples. FEMS Microbiol Lett 287: 56-62.
17. Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D & Andersson DI (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7: e1002158.
18. 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.
19. 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.
20. 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.
21. Heuer H, Kopmann C, Binh CTT, 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.
22. Jechalke S, Kopmann C, Rosendahl I, et al. (2013) Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Appl Environ Microbiol 79: 1704-1711.
23. 14C-difloxacin in soil including simultaneous amendment of pig manure with the focus on non-extractable residues. J Environ Sci Health, Part B 47: 858-868.
24. Kopmann C, Jechalke S, Rosendahl I et al. (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.
25. Kotzerke A, Sharma S, Schauss K, Heuer H, Thiele-Bruhn S, Smalla K, Wilke BM & Schloter M (2008) Alterations in soil microbial activity and N-transformation processes due to sulfadiazine loads in pig-manure. Environ Pollut 153: 315-322.
26. Kotzerke A, Hammesfahr U, Kleineidam K, Lamshöft M, Thiele-Bruhn S, Schloter M & Wilke B-M (2011) Influence of difloxacin-contaminated manure on microbial community structure and function in soils. Biol Fertil Soils 47: 177-186.
27. 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.
28. Lamshöft M, Sukul P, Zühlke S & Spiteller M (2010) Behaviour of C-14-sulfadiazine and C-14-difloxacin during manure storage. Sci Total Environ 408: 1563-1568.
29. Li J, Wang T, Shao B, Shen J, Wang S & Wu Y (2012) Plasmid-mediated quinolone resistance genes and antibiotic residues in wastewater and soil adjacent to swine feedlots: potential transfer to agricultural lands. Environ Health Perspect 120: 1144-1149.
30. Mazel D (2006) Integrons: agents of bacterial evolution. Nat Rev Microbiol 4: 608-620.
31. Nordmann P & Poirel L (2005) Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother 56: 463-469.
32. Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA & Hooper DC (2006) qnr Prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother 50: 2872-2874.
33. Rosendahl I, Siemens J, Kindler R, et al. (2012) Persistence of the fluoroquinolone antibiotic difloxacin in soil and lacking effects on nitrogen turnover. J Environ Qual 41: 1275-1283.
34. Ruiz E, Sáenz Y, Zarazaga M, Rocha-Gracia R, Martínez-Martínez L, Arlet G & Torres C (2012a) Qnr, aac(6)-Ib-cr and qepA genes in Escherichia coli and Klebsiella spp.: genetic environments and plasmid and chromosomal location. J Antimicrob Chemother 67: 886-897.
35. Ruiz J, Pons MJ & Gomes C (2012b) Transferable mechanisms of quinolone resistance. Int J Antimicrob Agents 40: 196-203.
36. Sambrook J, Fritsch EF & Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Stalder T, Barraud O, Casellas M, Dagot C & Ploy M-C (2012) Integron involvement in environmental spread of antibiotic resistance. Front Microbiol 3: 119.
38. Strahilevitz J, Jacoby GA, Hooper DC & Robicsek A (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22: 664-689.
39. Sukul P, Lamshoft M, Kusari S, Zuhlke S & Spiteller M (2009) Metabolism and excretion kinetics of C-14-labeled and non-labeled difloxacin in pigs after oral administration, and antimicrobial activity of manure containing difloxacin and its metabolites. Environ Res 109: 225-231.
40. Van den Brink PJ & Ter Braak CJF (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem 18: 138-148.
41. Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NCM, 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 Microbiol 75: 3859-3865.