Advertisement

Biology and Fertility of Soils

, Volume 50, Issue 6, pp 939–947 | Cite as

Influence of ciprofloxacin on microbial community structure and function in soils

  • Hao Cui
  • Shu-Ping WangEmail author
  • Jin Fu
  • Zhi-Qiang Zhou
  • Na Zhang
  • Li Guo
Original Paper

Abstract

Microcosm experiments were designed to investigate the effects of the widely used antibiotic ciprofloxacin (CIP) on soil microbial communities by using four different concentrations (0, 1, 5, and 50 mg kg−1 of soil) and five sampling times (1, 3, 9, 22, and 40 days). Untreated controls only received water. The addition of CIP significantly decreased microbial biomass (p < 0.05) but did not affect soil respiration at high doses. Potential nitrification rates were stimulated at low CIP concentrations (1 mg kg−1) and inhibited at high CIP concentrations (50 mg kg−1) after 9 days of incubation. The nitrate and ammonium contents of soil were not altered after CIP addition at any time. The structure of soil microbial communities was assessed by phospholipid fatty acid (PLFA) analysis. The addition of CIP decreased the ratio of bacteria to fungi and increased the ratio of Gram-positive to Gram-negative bacteria. Principal component analysis of the PLFA data clearly distinguished among the different CIP concentrations. Redundancy analysis indicated that the CIP concentration and incubation time explained 33.5 % of the total variance in the PLFA data. These results confirmed that a single addition of CIP can influence structure and function of microbial communities in soil.

Keywords

Ciprofloxacin Soil microbial communities Incubation experiment Phospholipid fatty acids Potential nitrification rate 

Notes

Acknowledgments

This work was supported by the Knowledge Innovation Program of the Chinese Academy of Sciences (No. KZCX2-EW-QN606), the Key Program of the National Natural Science Foundation of China (No. 41230750), and the National Natural Science Foundation of China (No. 40771215). We thank Pei Leng and Lei Sun for their assistance with the sample collection and Yanjie Liu for the data analysis.

References

  1. Anderson JM, Ingram JSI (1993) Colorimetric determination of ammonium. In: Anderson JM, Ingram JSI (eds) Tropical soil biology and fertility, a handbook of methods, 2nd edn. CAB International, Wallingford, pp 73–74Google Scholar
  2. Aust MO, Godlinski F, Travis GR, Hao XY, McAllister TA, Leinweber P, Thiele-Bruhn S (2008) Distribution of sulfamethazine, chlortetracycline and tylosin in manure and soil of Canadian feedlots after subtherapeutic use in cattle. Environ Pollut 156:1243–1251PubMedCrossRefGoogle Scholar
  3. Bååth E, Anderson T-H (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963CrossRefGoogle Scholar
  4. Berlanga M, Montero MT, Hernández-Borrell J, Viñas M (2004) Influence of the cell wall on ciprofloxacin susceptibility in selected wild-type Gram-negative and Gram-positive bacteria. Int J Antimicrob Agents 23:627–630PubMedCrossRefGoogle Scholar
  5. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedCrossRefGoogle Scholar
  6. Cataldo DA, Haroon M, Schrader LE, Young V (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salycilic acid. Commun Soil Sci Plant Anal 6:71–80CrossRefGoogle Scholar
  7. Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499CrossRefGoogle Scholar
  8. Chun S, Lee J, Radosevich M, White DC, Geyer R (2006) Influence of agricultural antibiotics and 17 beta-estradiol on the microbial community of soil. J Environ Sci Health B 41:923–935PubMedCrossRefGoogle Scholar
  9. Córdova-Kreylos AL, Scow KM (2007) Effects of ciprofloxacin on salt marsh sediment microbial communities. ISME J 1:585–595PubMedCrossRefGoogle Scholar
  10. Dalhoff A, Schmitz FJ (2003) In vitro antibacterial activity and pharmacodynamics of new quinolones. Eur J Clin Microbiol Infect Dis 22:203–221PubMedGoogle Scholar
  11. Dantas G, Sommer MOA, Oluwasegun RD, Church GM (2008) Bacteria subsisting on antibiotics. Science 320:100–103PubMedCrossRefGoogle Scholar
  12. Demoling LA, Bååth E, Greve G, Wouterse M, Schmitt H (2009) Effects of sulfamethoxazole on soil microbial communities after adding substrate. Soil Biol Biochem 41:840–848CrossRefGoogle Scholar
  13. Ding C, He J (2010) Effect of antibiotics in the environment on microbial populations. Appl Microbiol Biotechnol 87:925–941PubMedCrossRefGoogle Scholar
  14. Drlica K, Zhao XL (1997) DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61:377–392PubMedCentralPubMedGoogle Scholar
  15. Förster M, Laabs V, Lamshoft M, Groeneweg J, Zuhlke S, Spiteller M, Krauss M, Kaupenjohann M, Amelung W (2009) Sequestration of manure-applied sulfadiazine residues in soils. Environ Sci Technol 43:1824–1830PubMedCrossRefGoogle Scholar
  16. Frostegård Å, Bååth E, Tunlio A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730CrossRefGoogle Scholar
  17. Girardi C, Greve J, Lamshöft M, Fetzer I, Miltner A, Schäffer A, Kästner M (2011) Biodegradation of ciprofloxacin in water and soil and its effects on the microbial communities. J Hazard Mater 198:22–30PubMedCrossRefGoogle Scholar
  18. Gutiérrez IR, 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 Sediment 10:537–544CrossRefGoogle Scholar
  19. Halling-Sørensen B, Lützhoft HCH, Andersen HR, Ingerslev F (2000) Environmental risk assessment of antibiotics: comparison of mecillinam, trimethoprim and ciprofloxacin. J Antimicrob Chemother 46:53–58CrossRefGoogle Scholar
  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 40:1583–1591CrossRefGoogle Scholar
  21. 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 174:614–623CrossRefGoogle Scholar
  22. 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 47:61–68CrossRefGoogle Scholar
  23. Hu XG, Zhou QX, Luo Y (2010) Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China. Environ Pollut 158:2992–2998PubMedCrossRefGoogle Scholar
  24. Hund-Rinke K, Simon M, Lukow T (2004) Effects of tetracycline on the soil microflora: function, diversity, resistance. J Soil Sediment 4:11–16CrossRefGoogle Scholar
  25. Karnjanapiboonwong A, Suski JG, Shah AA, Cai Q, Morse AN, Anderson TA (2011) Occurrence of PPCPs at a wastewater treatment plant and in soil and groundwater at a land application site. Water Air Soil Pollut 216:257–273CrossRefGoogle Scholar
  26. Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999-2000: a national reconnaissance. Environ Sci Technol 36:1202–1211PubMedCrossRefGoogle Scholar
  27. Kong WD, Zhu YG, Fu BJ, Marschner P, He JZ (2006) The veterinary antibiotic oxytetracycline and Cu influence functional diversity of the soil microbial community. Environ Pollut 143:129–137PubMedCrossRefGoogle Scholar
  28. 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 Pollut 153:315–322PubMedCrossRefGoogle Scholar
  29. Kotzerke A, Fulle M, Sharma S, Kleineidam K, Welzl G, Lamshoft M, Schloter M, Wilke B-M (2011a) Alterations in total microbial activity and nitrification rates in soil due to amoxicillin-spiked pig manure. J Plant Nutr Soil Sci 174:56–64CrossRefGoogle Scholar
  30. Kotzerke A, Hammesfahr U, Kleineidam K, Lamshöft M, Thiele-Bruhn S, Schloter M, Wilke B-M (2011b) Influence of difloxacin-contaminated manure on microbial community structure and function in soils. Biol Fertil Soils 47:177–186CrossRefGoogle Scholar
  31. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529PubMedCrossRefGoogle Scholar
  32. Kümmerer K (2009) Antibiotics in the aquatic environment—a review—part I. Chemosphere 75:417–434PubMedCrossRefGoogle Scholar
  33. Kurola J, Salkinoja-Salonen M, Aarnio T, Hultman J, Romantschuk M (2005) Activity, diversity and population size of ammonia-oxidising bacteria in oil-contaminated landfarming soil. FEMS Microbiol Lett 250:33–38PubMedCrossRefGoogle Scholar
  34. Leal RM, Figueira RF, Tornisielo VL, Regitano JB (2012) Occurrence and sorption of fluoroquinolones in poultry litters and soils from São Paulo State, Brazil. Sci Total Environ 432:344–349PubMedCrossRefGoogle Scholar
  35. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809PubMedCrossRefGoogle Scholar
  36. Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, CambridgeGoogle Scholar
  37. Lindberg RH, Bjorklund K, Rendahl P, Johansson MI, Tysklind M, Andersson BAV (2007) Environmental risk assessment of antibiotics in the Swedish environment with emphasis on sewage treatment plants. Water Res 41:613–619PubMedCrossRefGoogle Scholar
  38. Liu F, Ying GG, Tao R, Zhao JL, Yang JF, Zhao LF (2009) Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environ Pollut 157:1636–1642PubMedCrossRefGoogle Scholar
  39. Maul JD, Schuler LJ, Belden JB, Whiles MR, Lydy MJ (2006) Effects of the antibiotic ciprofloxacin on stream microbial communities and detritivorous macroinvertebrates. Environ Toxicol Chem 25:1598–1606PubMedCrossRefGoogle Scholar
  40. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670CrossRefGoogle Scholar
  41. Näslund J, Hedma JE, Agestrand C (2008) Effects of the antibiotic ciprofloxacin on the bacterial community structure and degradation of pyrene in marine sediment. Aquat Toxicol 90:223–227PubMedCrossRefGoogle Scholar
  42. Picó Y, Andreu V (2007) Fluoroquinolones in soil—risks and challenges. Anal Bioanal Chem 387:1287–1299PubMedCrossRefGoogle Scholar
  43. Rousk J, Demoling LA, Bahr A, Bååth E (2008) Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol Ecol 63:350–358PubMedCrossRefGoogle Scholar
  44. Sanchez-Brunete C, Albero B, Tadeo JL (2004) Multiresidue determination of pesticides in soil by gas chromatography–mass spectrometry detection. J Agric Food Chem 52:1445–1451PubMedCrossRefGoogle Scholar
  45. Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele-Bruhn S, Sharma S, Wilke B-M, Matthies M, Smalla K, Munch JC, Amelung W, Kaupenjohann M, Schloter M, Schleper C (2009) Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 11:446–456PubMedCrossRefGoogle Scholar
  46. 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 37:1882–1892CrossRefGoogle Scholar
  47. Schnabel EL, Jones AL (1999) Distribution of tetracycline resistance genes and transposons among phylloplane bacteria in Michigan apple orchards. Appl Environ Microbiol 65:4898–4907PubMedCentralPubMedGoogle Scholar
  48. Sukul P, Spiteller M (2007) Fluoroquinolone antibiotics in the environment. Rev Environ Contam Toxicol 191:131–162PubMedGoogle Scholar
  49. Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils—a review. J Plant Nutr Soil Sci 166:145–167CrossRefGoogle Scholar
  50. Thiele-Bruhn S, Beck I (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465PubMedCrossRefGoogle Scholar
  51. Uslu MO, Yediler A, Balcioglu IA, Schulte-Hostede S (2008) Analysis and sorption behavior of fluoroquinolones in solid matrices. Water Air Soil Pollut 190:55–63CrossRefGoogle Scholar
  52. Weber KP, Mitzel MR, Slawson RM, Legge RL (2011) Effect of ciprofloxacin on microbiological development in wetland mesocosms. Water Res 45:3185–3196PubMedCrossRefGoogle Scholar
  53. Wei RC, Ge F, Huang SY, Chen M, Wang R (2011) Occurrence of veterinary antibiotics in animal wastewater and surface water around farms in Jiangsu Province, China. Chemosphere 82:1408–1414PubMedCrossRefGoogle Scholar
  54. Xia Y, Zhu YG, Gu Q, He JZ (2007) Does long-term fertilization treatment affect the response of soil ammonia-oxidizing bacterial communities to Zn contamination? Plant Soil 301:245–254CrossRefGoogle Scholar
  55. Yang JF, Ying GG, Liu S, Zhou LJ, Zhao JL, Tao R, Peng PA (2012) Biological degradation and microbial function effect of norfloxacin in a soil under different conditions. J Environ Sci Health B 47:288–295PubMedCrossRefGoogle Scholar
  56. 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 38:2372–2380CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Hao Cui
    • 1
    • 2
  • Shu-Ping Wang
    • 1
    Email author
  • Jin Fu
    • 3
  • Zhi-Qiang Zhou
    • 1
  • Na Zhang
    • 1
  • Li Guo
    • 1
  1. 1.College of Resources and EnvironmentUniversity of Chinese Academy of SciencesBeijingChina
  2. 2.Research Unit Microbe–Plant Interactions, Department of Environmental SciencesHelmholtz Zentrum München German Research Center for Environmental HealthNeuherbergGermany
  3. 3.Institute for Meteorology and Climate Research, Atmospheric Environmental Research (IMK-IFU)Karlsruhe Institute of TechnologyGarmisch-PartenkirchenGermany

Personalised recommendations