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Do antibiotics have environmental side-effects? Impact of synthetic antibiotics on biogeochemical processes

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Abstract

Antibiotic use in the early 1900 vastly improved human health but at the same time started an arms race of antibiotic resistance. The widespread use of antibiotics has resulted in ubiquitous trace concentrations of many antibiotics in most environments. Little is known about the impact of these antibiotics on microbial processes or “non-target” organisms. This mini-review summarizes our knowledge of the effect of synthetically produced antibiotics on microorganisms involved in biogeochemical cycling. We found only 31 articles that dealt with the effects of antibiotics on such processes in soil, sediment, or freshwater. We compare the processes, antibiotics, concentration range, source, environment, and experimental approach of these studies. Examining the effects of antibiotics on biogeochemical processes should involve environmentally relevant concentrations (instead of therapeutic), chronic exposure (versus acute), and monitoring of the administered antibiotics. Furthermore, the lack of standardized tests hinders generalizations regarding the effects of antibiotics on biogeochemical processes. We investigated the effects of antibiotics on biogeochemical N cycling, specifically nitrification, denitrification, and anammox. We found that environmentally relevant concentrations of fluoroquinolones and sulfonamides could partially inhibit denitrification. So far, the only documented effects of antibiotic inhibitions were at therapeutic doses on anammox activities. The most studied and inhibited was nitrification (25–100 %) mainly at therapeutic doses and rarely environmentally relevant. We recommend that firm conclusions regarding inhibition of antibiotics at environmentally relevant concentrations remain difficult due to the lack of studies testing low concentrations at chronic exposure. There is thus a need to test the effects of these environmental concentrations on biogeochemical processes to further establish the possible effects on ecosystem functioning.

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References

  • Ahmad M, Vithanage M, Kim K, Cho J-S, Lee YH, Joo YK, Lee SS, Ok YS (2014) Inhibitory effect of veterinary antibiotics on denitrification in groundwater: a microcosm approach. ScientificWorldJournal. doi:10.1155/2014/879831

    Google Scholar 

  • Alighardashi A, Pandolfi D, Potier O, Pons MN (2009) Acute sensitivity of activated sludge bacteria to erythromycin. J Hazard Mater 172:685–692. doi:10.1016/j.jhazmat.2009.07.051

    Article  CAS  Google Scholar 

  • Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8:251–259. doi:10.1038/nrmicro2312

    Article  CAS  Google Scholar 

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–69

    CAS  Google Scholar 

  • Andersson DI, Hughes D (2014) Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol 12:465–478. doi:10.1038/nrmicro3270

    Article  CAS  Google Scholar 

  • Baath E, Olsson S, Tunlid A (1988) Growth of bacteria in the rhizoplane and the rhizosphere of rape seedlings. FEMS Microbiol Ecol 53(6):355–360. doi:10.1016/0378-1097(88)90501-0

    Article  Google Scholar 

  • Backhaus T, Altenburger R, Boedeker W, Faust M, Scholze M, Grimme LH (2000) Predictability of the toxicity of a multiple mixture of dissimilarly acting chemicals to Vibrio fischeri. Environ Toxicol Chem 19(9):2348–2356. doi:10.1897/1551-5028(2000)019<2348:pottoa>2.3.co;2

    Article  CAS  Google Scholar 

  • Bell KY, Bandy JJ, Finnegan BJ, Keen O, Mauter MS, Parker AM, Sima LC, Stretz HA (2013) Emerging pollutants - part II: treatment. Water Environ Res 85:2022–2071. doi:10.2175/106143013x13698672323308

    Article  Google Scholar 

  • Bressan CR, Kunz A, Schmidell W, Soares HM (2013) Toxicity of the colistin sulfate antibiotic used in animal farming to mixed cultures of nitrifying organisms. Water Air Soil Pollut 224(3):1–9. doi:10.1007/s11270-013-1441-4

    Article  CAS  Google Scholar 

  • Carlson CA, Ingraham JL (1983) Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa and Pseudomonas denitrificans. Appl Environ Microbiol 45(4):1247–1253

    CAS  Google Scholar 

  • Campos JL, Garrido JM, Mendez R, Lema JM (2001) Effect of two broad-spectrum antibiotics on activity and stability of continuous nitrifying system. Appl Biochem Biotechnol 95:1–10. doi:10.1385/abab:95:1:01

    Article  CAS  Google Scholar 

  • Carucci A, Cappai G, Piredda M (2006) Biodegradability and toxicity of pharmaceuticals in biological wastewater treatment plants. J Environ Sci Health A 41:1831–1842. doi:10.1080/10934520600779000

    Article  CAS  Google Scholar 

  • Claus H, Martin HH, Jantos CA, Konig H (2000) A search for beta-lactamase in chlamydiae, mycoplasmas, planctomycetes, and cyanelles: bacteria and bacterial descendants at different phylogenetic positions and stages of cell wall development. Microbiol Res 155:1–6

    Article  CAS  Google Scholar 

  • Conkle JL, White JR (2012) An initial screening of antibiotic effects on microbial respiration in wetland soils. J Environ Sci Health A 47:1381–1390. doi:10.1080/10934529.2012.672315

    Article  CAS  Google Scholar 

  • Costanzo SD, Murby J, Bates J (2005) Ecosystem response to antibiotics entering the aquatic environment. Mar Pollut Bull 51:218

    Article  CAS  Google Scholar 

  • Crane M, Watts C, Boucard T (2006) Chronic aquatic environmental risks from exposure to human pharmaceuticals. Sci Total Environ 367:23–41. doi:10.1016/j.scitotenv.2006.04.010

    Article  CAS  Google Scholar 

  • Cui H, Wang SP, Fu J, Zhou ZQ, Zhang N, Guo L (2014) Influence of ciprofloxacin on microbial community structure and function in soils. Biol Fertil Soils 50(6):939–947. doi:10.1007/s00374-014-0914-y

    Article  CAS  Google Scholar 

  • Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156(4):457–464. doi:10.1016/j.resmic.2005.01.011

    Article  CAS  Google Scholar 

  • Davies J, Ryan KS (2012) Introducing the parvome: bioactive compounds in the microbial world. ACS Chem Biol 7:252–259. doi:10.1021/cb200337h

    Article  CAS  Google Scholar 

  • Demoling LA, Baath E, Greve G, Wouterse M, Schmitt H (2009) Effects of sulfamethoxazole on soil microbial communities after adding substrate. Soil Biol Biochem 41:840–848. doi:10.1016/j.soilbio.2009.02.001

    Article  CAS  Google Scholar 

  • Ducklow H (2008) Microbial services: challenges for microbial ecologists in a changing world. Aquat Microb Ecol 53:13–19. doi:10.3354/ame01220

    Article  Google Scholar 

  • Fernandez I, Mosquera-Corral A, Campos JL, Mendez R (2009) Operation of an anammox SBR in the presence of two broad-spectrum antibiotics. Process Biochem 44:494–498. doi:10.1016/j.procbio.2009.01.001

    Article  CAS  Google Scholar 

  • Finley RL, Collignon P, Larsson DGJ, McEwen SA, Li XZ, Gaze WH, Reid-Smith R, Timinouni M, Graham DW, Topp E (2013) The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis 57:704–710. doi:10.1093/cid/cit355

    Article  Google Scholar 

  • Fountoulakis M, Drillia P, Stamatelatou K, Lyberatos G (2004) Toxic effect of pharmaceuticals on methanogienesis. Wa Sci Technol 50(5):335–340

    CAS  Google Scholar 

  • Gatica J, Cytryn E (2013) Impact of treated wastewater irrigation on antibiotic resistance in the soil microbiome. Environ Sci Pollut Res 20:3529–3538. doi:10.1007/s11356-013-1505-4

    Article  CAS  Google Scholar 

  • Gu JD (2014) Assessment of ecosystem health and ecotoxicology through chemical analysis and modeling. Ecotoxicology 23:475–479. doi:10.1007/s10646-014-1206-x

    Article  CAS  Google Scholar 

  • Hansen PK, Lunestad BT, Samuelsen OB (1992) Effects of oxytetracycline, oxolinic acid, and flumequine on bacteria in an artificial marine fish farm sediment. Can J Microbiol 38:1307–1312

    Article  CAS  Google Scholar 

  • Hou L, Yin G, Liu M, Zhou J, Zheng Y, Gao J, Zong H, Yang Y, Gao L, Tong C (2015) Effects of sulfamethazine on denitrification and the associated N2O release in estuarine and coastal sediments. Environ Sci Technol 49:326–33. doi:10.1021/es504433r

    Article  CAS  Google Scholar 

  • Ingvorsen K, Nielsen MY, Joulian C (2003) Kinetics of bacterial sulfate reduction in an activated sludge plant. FEMS Microbiol Ecol 46:129–137

    Article  CAS  Google Scholar 

  • Juliastuti SR, Baeyens J, Creemers C (2003) Inhibition of nitrification by heavy metals and organic compounds: the ISO 9509 test. Environ Eng Geosci 20(2):79–90. doi:10.1089/109287503763336511

    Article  CAS  Google Scholar 

  • Klaver AL, Matthews RA (1994) Effects of oxytetracycline on nitrification in a model aquatic system. Aquaculture 123:237–247

    Article  CAS  Google Scholar 

  • Katipoglu-Yazan T, Pala-Ozkok I, Ubay-Cokgor E, Orhon D (2013) Acute impact of erythromycin and tetracycline on the kinetics of nitrification and organic carbon removal in mixed microbial culture. Bioresour Technol 144:410–419. doi:10.1016/j.biortech.2013.06.121

    Article  CAS  Google Scholar 

  • Kleineidam K, Sharma S, Kotzerke A, Heuer H, Thiele-Bruhn S, Smalla K, Wilke BM, 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. doi:10.1007/s00248-010-9691-9

    Article  CAS  Google Scholar 

  • Knapp CW, Engemann CA, Hanson ML, Keen PL, Hall KJ, Graham DW (2008) Indirect evidence of transposon-mediated selection of antibiotic resistance genes in aquatic systems at low-level oxytetracycline exposures. Environ Sci Technol 42:5348–5353. doi:10.1021/es703199g

    Article  CAS  Google Scholar 

  • Kotzerke A, Fulle M, Sharma S, Kleineidam K, Welzl G, Lamshoft M, Schloter M, Wilke BM (2011) Alterations in total microbial activity and nitrification rates in soil due to amoxicillin-spiked pig manure. J Plant Nutr Soil Sci 174:56–64. doi:10.1002/jpln.200900210

    Article  CAS  Google Scholar 

  • 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. doi:10.1016/j.envpol.2007.08.020

    Article  CAS  Google Scholar 

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    Article  CAS  Google Scholar 

  • Kümmerer K (2009a) Antibiotics in the aquatic environment - a review - part I. Chemosphere 75:417–434. doi:10.1016/j.chemosphere.2008.11.086

    Article  CAS  Google Scholar 

  • Kümmerer K (2009b) The presence of pharmaceuticals in the environment due to human use - present knowledge and future challenges. J Environ Manag 90:2354–2366. doi:10.1016/j.jenvman.2009.01.023

    Article  CAS  Google Scholar 

  • Larsson DGJ (2014) Pollution from drug manufacturing: review and perspectives. Philos T Roy Soc B 369:20130571. doi:10.1098/rstb.2013.0571

    Article  CAS  Google Scholar 

  • Liu B, Li Y, Zhang X, Wang J, Gao M (2014) Combined effects of chlortetracycline and dissolved organic matter extracted from pig manure on the functional diversity of soil microbial community. Soil Biol Biochem 74:148–155. doi:10.1016/j.soilbio.2014.03.005

    Article  CAS  Google Scholar 

  • Lotti T, Cordola M, Kleerebezem R, Caffaz S, Lubello C, van Loosdrecht MCM (2012) Inhibition effect of swine wastewater heavy metals and antibiotics on anammox activity. Water Sci Technol 66:1519–1526. doi:10.2166/wst.2012.344

    Article  CAS  Google Scholar 

  • Luczkiewicz A, Felis E, Ziembinska A, Gnida A, Kotlarska E, Olanczuk-Neyman K, Surmacz-Gorska J (2013) Resistance of Escherichia coli and Enterococcus spp. to selected antimicrobial agents present in municipal wastewater. J Water Health 11:600–612. doi:10.2166/wh.2013.130

    Article  CAS  Google Scholar 

  • Murray RE, Knowles R (1999) Chloramphenicol inhibition of denitrifying enzyme activity in two agricultural soils. Appl Environ Microbiol 65(8):3487–3492

  • Nesme J, Cecillon S, Delmont TO, Monier JM, Vogel TM, Simonet P (2014) Large-scale metagenomic-based study of antibiotic resistance in the environment. Curr Biol 24:1096–1100. doi:10.1016/j.cub.2014.03.036

    Article  CAS  Google Scholar 

  • Nordberg M, Templeton DM, Andersen O, Duffus JH (2009) Glossary of terms used in ecotoxicology (IUPAC recommendations 2009). Pure Appl Chem 81:829–970. doi:10.1351/pac-rec-08-07-09

    Article  CAS  Google Scholar 

  • Näslund J, Hedman JE, Agestrand C (2008) Effects of the antibiotic ciprofloxacin on the bacterial community structure and degradation of pyrene in marine sediment. Aquat Toxicol 90:223–227

    Article  CAS  Google Scholar 

  • Philippot L, Hallin S (2005) Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Curr Opin Microbiol 8(3):234–239

    Article  CAS  Google Scholar 

  • Prosser JI (1989) Autotrophic nitrification in bacteria. Adv Microb Physiol 30:125–181

    Article  CAS  Google Scholar 

  • Reichel R, Rosendahl I, Peeters ETHM, Focks E, 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. doi:10.1016/j.soilbio.2013.03.007

    Article  CAS  Google Scholar 

  • Rico A, Dimitrov MR, Van Wijngaarden RPA, Satapornvanit K, Smidt H, Van den Brink PJ (2014) Effects of the antibiotic enrofloxacin on the ecology of tropical eutrophic freshwater microcosms. Aquat Toxicol 147:92–104. doi:10.1016/j.aquatox.2013.12.008

    Article  CAS  Google Scholar 

  • Roose-Amsaleg C, Yan C, Hoang AM, Laverman AM (2013) Chronic exposure of river sediments to environmentally relevant levels of tetracycline affects bacterial communities but not denitrification rates. Ecotoxicology 22:1467–1478. doi:10.1007/s10646-013-1133-2

    Article  CAS  Google Scholar 

  • Rosendahl I, Siemens J, Kindler R, Groeneweg J, Zimmermann J, Czerwinski S, Lamshoeft M, Laabs V, Wilke BM, Vereecken H, Amelung W (2012) Persistence of the fluoroquinolone antibiotic difloxacin in soil and lacking effects on nitrogen turnover. J Environ Qual 41:1275–1283. doi:10.2134/jeq2011.0459

    Article  CAS  Google Scholar 

  • Schauss K, Focks A, Heuer H, Kotzerke A, Schmitt H, Thiele-Bruhn S, Smalla K, Wilke BM, Matthies M, Amelung W, Klasmeier J, Schloter M (2009) Analysis, fate and effects of the antibiotic sulfadiazine in soil ecosystems. Trends Anal Chem 28:612–618

    Article  CAS  Google Scholar 

  • Schmidt S, Winter J, Gallert C (2012) Long-term effects of antibiotics on the elimination of chemical oxygen demand, nitrification, and viable bacteria in laboratory-scale wastewater treatment plants. Arch Environ Contam Toxicol 63:354–364. doi:10.1007/s00244-012-9773-4

    Article  CAS  Google Scholar 

  • Schmieder R, Edwards R (2012) Insights into antibiotic resistance through metagenomic approaches. Future Microbiol 7:73–89. doi:10.2217/fmb.11.135

    Article  CAS  Google Scholar 

  • Servais P, Passerat J (2009) Antimicrobial resistance of fecal bacteria in waters of the Seine river watershed (France). Sci Total Environ 408:365–372. doi:10.1016/j.scitotenv.2009.09.042

    Article  CAS  Google Scholar 

  • Shen T, Stieglmeier M, Dai J, Urich T, Schleper C (2013) Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiol Lett 344:121–129. doi:10.1111/1574-6968.12164

    Article  CAS  Google Scholar 

  • Spieck E, Lipski A (2011) Cultivation, growth physiology, and chemotaxonomy of nitrite-oxidizing bacteria. In Martin G. Klotz, editor: Methods in Enzymology, Vol. 486, Burlington: Academic Press, 2011, pp. 109–130. ISBN: 978-0-12-381294-0 Elsevier Inc. Academic Press

  • Stewart PS (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292:107–113. doi:10.1078/1438-4221-00196

    Article  CAS  Google Scholar 

  • Strous M, Kuenen JG, Jetten MSM (1999) Key physiology of anaerobic ammonium oxidation. Appl Environ Microbiol 65:3248–3250

    CAS  Google Scholar 

  • Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils - a review. J Plant Nutr Soil Sci 166:145–167. doi:10.1002/jpln.200390023

    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  Google Scholar 

  • Toth JD, Feng Y, Dou Z (2011) Veterinary antibiotics at environmentally relevant concentrations inhibit soil iron reduction and nitrification. Soil Biol Biochem 43:2470–2472. doi:10.1016/j.soilbio.2011.09.004

    Article  CAS  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108:8420–8425. doi:10.1073/pnas.1013488108

    Article  Google Scholar 

  • Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7(12):1985–1995

    Article  CAS  Google Scholar 

  • Underwood JC, Harvey RW, Metge DW, Repert DA, Baumgartner LK, Smith RL, Roane TM, Barber LB (2011) Effects of the antimicrobial sulfamethoxazole on groundwater bacterial enrichment. Environ Sci Technol 45:3096–3101. doi:10.1021/es103605e

    Article  CAS  Google Scholar 

  • Wunder DB, Tan DT, LaPara TM, Hozalski RM (2013) The effects of antibiotic cocktails at environmentally relevant concentrations on the community composition and acetate biodegradation kinetics of bacterial biofilms. Chemosphere 90:2261–2266. doi:10.1016/j.chemosphere.2012.10.031

    Article  CAS  Google Scholar 

  • Yamamura S, Watanabe K, Suda W, Tsuboi S, Watanabe M (2014) Effect of antibiotics on redox transformations of arsenic and diversity of arsenite-oxidizing bacteria in sediment microbial mommunities. Environ Sci Technol 48:350–357. doi:10.1021/es403971s

    Article  CAS  Google Scholar 

  • Yan C, Dinh QT, Chevreuil M, Garnier J, Roose-Amsaleg C, Labadie P, Laverman AM (2013) The effect of environmental and therapeutic concentrations of antibiotics on nitrate reduction rates in river sediment. Water Res 47:3654–3662. doi:10.1016/j.watres.2013.04.025

    Article  CAS  Google Scholar 

  • Yergeau E, Sanschagrin S, Waiser MJ, Lawrence JR, Greer CW (2012) Sub-inhibitory concentrations of different pharmaceutical products affect the meta-transcriptome of river biofilm communities cultivated in rotating annular reactors. Environ Microbiol Rep 4(3):350–359. doi:10.1111/j.1758-2229.2012.00341.x

    Article  CAS  Google Scholar 

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616

    CAS  Google Scholar 

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The authors acknowledge the constructive comments of four journal reviewers and Ben Abbott for proofreading the paper.

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Correspondence to Céline Roose-Amsaleg.

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Roose-Amsaleg, C., Laverman, A.M. Do antibiotics have environmental side-effects? Impact of synthetic antibiotics on biogeochemical processes. Environ Sci Pollut Res 23, 4000–4012 (2016). https://doi.org/10.1007/s11356-015-4943-3

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