Abstract
The use of animal manure as organic fertilizer is a common agricultural practice that can improve soil health and crop yield. However, antibiotics and their metabolites are often present in animal manure and, hence, in manure-amended soil. The aim of this study was to assess the induced development of oxytetracycline (OTC) tolerance in soil bacterial communities as a result of the addition of OTC to soil amended with well-aged cow manure. To this purpose, soil amended with well-aged cow manure was repeatedly – three times – spiked with different OTC concentrations (0, 2, 20, 60, 150, and 500 mg OTC kg−1 dry weight soil, each time) according to a pollution-induced community tolerance (PICT) assay. The PICT detection phase was conducted in Biolog EcoPlatesTM in the presence of the following OTC concentration gradient in the wells: 0, 5, 20, 40, 60, and 100 mg L−1. For all treatments, the application of OTC in the PICT selection phase resulted in lower values of bacterial metabolic activity (i.e., lower values of average well color development) in the PICT detection phase. A significant increase in OTC tolerance was observed in soil bacterial communities that had been exposed three times to ≥ 20 mg OTC kg−1 DW soil during the PICT selection phase. In general, higher levels of OTC exposure during the PICT selection phase resulted in bacterial tolerance to higher OTC concentrations during the PICT detection phase, pointing to a dose-dependent induced tolerance. It is important to (i) rationalize the amount of antibiotics administered to livestock, and (ii) treat properly the antibiotic-containing manure before its application to agricultural soil as fertilizer.
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Aliasgharzad N, Molaei A, Oustan S (2011) Pollution induced community tolerance (PICT) of microorganisms in soil incubated with different levels of PB. Int J Environ Chem Ecol Geo Geophys Eng 5:838–842. https://doi.org/10.5281/zenodo.1332260
Andersson DI, Hughes D (2012) Evolution of antibiotic resistance at non-lethal drug concentration. Drug Resist Updat 15:162–172. https://doi.org/10.1016/j.drup.2012.03.005
Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182. https://doi.org/10.1016/J.TIM.2006.02.006
Berendonk TU, Manaia CM, Merlin C, Fatta-Kassinos D, Cytryn E, Walsh F, Bürgmann H, Sørum H, Noström M, Pons MN, Kreuzinger N, Huovinen P, Stefani S, Schwartz T, Kisand V, Baquero F, Martinez JL (2015) Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol 13:310–317. https://doi.org/10.1038/nrmicro3439
Bhullar K, Waglechner N, Pawlowski A, Koteva K, Banks ED, Johnston MD, Barton HA, Wright GD (2012) Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS One 7:e34953. https://doi.org/10.1371/journal.pone.0034953
Blanck H, Wängberg SA, Molander S (1988) Pollution-induced community tolerance—a new ecotoxicological tool. In: J. Cairns, J.R. Pratt (ed) Functional testing of aquatic biota for estimating hazards of chemicals. American Society for Testing and Materials, Philadelphia, pp 219–230.
Borchers HW (2021) pracma: practical numerical math functions. R package version 2.3.3. https://CRAN.R-project.org/package=pracma.
Brandt KK, Sjøholm OR, Krogh KA, Halling-Sørensen B, Nybroe O (2009) Increased pollution-induced bacterial community tolerance to sulfadiazine in soil hotspots amended with artificial root exudates. Environ Sci Technol 43:2963–2968. https://doi.org/10.1021/es803546y
Braschi I, Blasioli S, Fellet C, Lorenzini R, Garelli A, Pori M, Giacomini D (2013) Persistence and degradation of new β-lactam antibiotics in the soil and water environment. Chemosphere 93:152–159. https://doi.org/10.1016/j.chemosphere.2013.05.016
Brodersen DE, Clemons WM, Carter AP, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V (2000) The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103:1143–1154. https://doi.org/10.1016/S0092-8674(00)00216-6
Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22. https://doi.org/10.1016/j.geoderma.2004.03.005
Campagnolo ER, Johnson KR, Karpati A, Rubin CS, Kolpin DW, Meyer MT, Esteban JE, Currier RW, Smith K, Thu KM, McGeehin M (2002) Antimicrobial residues in animal waste and water resources proximal to large-scale swine and poultry feeding operations. Sci Total Environ 299:89–95. https://doi.org/10.1016/S0048-9697(02)00233-4
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. https://doi.org/10.2134/jeq2008.0128
Chen Y, Zhang H, Luo Y, Song J (2012) Occurrence and assessment of veterinary antibiotics in swine manures: a case study in East China. Chin Sci Bull 57:606–614. https://doi.org/10.1007/s11434-011-4830-3
D’Costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science 311:374–377. https://doi.org/10.1126/science.1120800
De Liguoro M, Cibin V, Capolongo F, Halling-Sørensen B, Montesissa C (2003) Use of oxytetracycline and tylosin in intensive calf farming: evaluation of transfer to manure and soil. Chemosphere 52:203–212. https://doi.org/10.1016/S0045-6535(03)00284-4
de Mendiburu F (2020) agricolae: statistical procedures for agricultural research. R package version 1:3–3. https://CRAN.R-project.org/package=agricolae
Delgado-Baquerizo M et al. (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541
Demoling LA, Bååth E (2008) No long-term persistence of bacterial pollution-induced community tolerance in tylosin-polluted soil. Environ Sci Technol 42:6917–6921. https://doi.org/10.1021/es8004706
Epelde L, Becerril JM, Hernández-Allica J, Barrutia O, Garbisu C (2008) Functional diversity as indicator of the recovery of soil health derived from Thlaspi caerulescens growth and metal phytoextraction. Appl Soil Ecol 39:299–310. https://doi.org/10.1016/j.apsoil.2008.01.005
Epelde L, Becerril JM, Kowalchuk GA, Deng Y, Zhou J, Garbisu C (2010) Impact of metal pollution and Thlaspi caerulescens growth on soil microbial communities. Appl Environ Microbiol 76:7843–7853. https://doi.org/10.1128/AEM.01045-10
Epelde L, Jauregi L, Urra J, Ibarretxe L, Romo J, Goikoetxea I, Garbisu C (2018) Characterization of composted organic amendments for agricultural use. Front Sustain Food Syst 2:44. https://doi.org/10.3389/fsufs.2018.00044
European Medicines Agency, European Surveillance of Veterinary Antimicrobial Consumption (2020) Sales of veterinary antimicrobial agents in 31 European countries in 2018 (EMA/24309/2020).
Fang H, Han L, Cui Y, Xue Y, Cai L, Yu Y (2016) Changes in soil microbial community structure and function associated with degradation and resistance of carbendazim and chlortetracycline during repeated treatments. Sci Total Environ 572:1203–1212. https://doi.org/10.1016/j.scitotenv.2016.08.038
Fang H, Han L, Zhang H, Deng Y, Ge Q, Mei J, Long Z, Yu Y (2018) Repeated treatments of ciprofloxacin and kresoxim-methyl alter their dissipation rates, biological function and increase antibiotic resistance in manured soil. Sci Total Environ 628–629:661–671. https://doi.org/10.1016/j.scitotenv.2018.02.116
Fang H, Han Y, Yin Y, Pan X, Yu Y (2014) Variations in dissipation rate, microbial function and antibiotic resistance due to repeated introductions of manure containing sulfadiazine and chlortetracycline to soil. Chemosphere 96:51–56. https://doi.org/10.1016/j.chemosphere.2013.07.016
Garbisu C, Alkorta I, Epelde L (2011) Assessment of soil quality using microbial properties and attributes of ecological relevance. Appl Soil Ecol 49:1–4. https://doi.org/10.1016/j.apsoil.2011.04.018
Han L, Cai L, Zhang H, Long Z, Yu Y, Fang H (2019) Development of antibiotic resistance genes in soils with ten successive treatments of chlortetracycline and ciprofloxacin. Environ Pollut 253:152–160. https://doi.org/10.1016/j.envpol.2019.07.031
Ince B, Coban H, Turker G, Ertekin E, Ince O (2013) Effect of oxytetracycline on biogas production and active microbial populations during batch anaerobic digestion of cow manure. Bioprocess Biosyst Eng 36:541–546. https://doi.org/10.1007/s00449-012-0809-y
Insam H (1997) A new set of substrates proposed for community characterization in environmental samples. In: Insam H, Rangger A (ed) Microbial Communities: Functional versus structural approaches. Springer, Berlin, p 259–260.
Jauregi L, Epelde L, Alkorta I, Garbisu C (2021) Agricultural soils amended with thermally-dried anaerobically-digested sewage sludge showed increased risk of antibiotic resistance dissemination. Front Microbiol 12:666854. https://doi.org/10.3389/fmicb.2021.666854
Jiang WQ, Gao J, Cheng Z, Wang P, Zhou ZQ, Liu DH (2018) The effect of antibiotics on the persistence of herbicides in the soil under the combined pollution. Chemosphere 204:303–309. https://doi.org/10.1016/j.chemosphere.2018.04.046
Jutkina J, Rutgersson C, Flach CF, Larsson J (2016) An assay for determining minimal concentrations of antibiotics that drive horizontal transfer of resistance. Sci Total Environ 548–549:131–138. https://doi.org/10.1016/j.scitotenv.2016.01.044
Kim S, Yun Z, Ha UH, Lee S, Park H, Kwon EE, Cho Y, Choung S, Oh J, Medriano CA, Chandran K (2014) Transfer of antibiotic resistance plasmids in pure and activated sludge cultures in the presence of environmentally representative micro-contaminant concentrations. Sci Total Environ 468–469:813–820. https://doi.org/10.1016/j.scitotenv.2013.08.100
Kong W, Li C, Dolhi JM, Li S, He J, Qiao M (2012) Characteristics of oxytetracycline sorption and potential bioavailability in soils with various physical-chemical properties. Chemosphere 87:542–548. https://doi.org/10.1016/j.chemosphere.2011.12.062
Kuchta SL, Cessna AJ, Elliott JA, Peru KM, Headley JV (2009) Transport of lincomycin to surface and ground water from manure-amended cropland. J Environ Qual 38:1719–1727. https://doi.org/10.2134/jeq2008.0365
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. https://doi.org/10.2134/jeq2005.0026
Li Y, Liu B, Zhang X, Gao M, Wang J (2015) Effects of Cu exposure on enzyme activities and selection for microbial tolerances during swine-manure composting. J Hazard Mater 283:512–518. https://doi.org/10.1016/j.jhazmat.2014.09.061
Lindstrom JE, Barry RP, Braddock JF (1998) Microbial community analysis: a kinetic approach to constructing potential C source utilization patterns. Soil Biol Biochem 30:231–239. https://doi.org/10.1016/S0038-0717(97)00113-2
Liu B, Li Y, Gao S, Chen X (2017) Copper exposure to soil under single and repeated application: selection for the microbial community tolerance and effects on the dissipation of antibiotics. J Hazard Mater 325:129–135. https://doi.org/10.1016/j.jhazmat.2016.11.072
Liu B, Li Y, Zhang X, Wang J, Gao M (2015) Effects of chlortetracycline on soil microbial communities: comparisons of enzyme activities to the functional diversity via Biolog EcoPlates™. Eur J Soil Biol 68:69–76. https://doi.org/10.1016/j.ejsobi.2015.01.002
Liu W, Pan N, Chen W, Jiao W, Wang M (2012) Effect of veterinary oxytetracycline on functional diversity of soil microbial community. Plant Soil Environ 58:295–301
Loke ML, Tjornelund J, Halling-Sørensen B (2002) Determination of the distribution coefficient (log Kd) of oxytetracycline, tylosin A, olaquindox and metronidazole in manure. Chemosphere 48:351–361. https://doi.org/10.1016/S0045-6535(02)00078-4
Loreau M (2001) Microbial diversity, producer–decomposer interactions and ecosystem processes: a theoretical model. Proc Biol Sci 268:303–309. https://doi.org/10.1098/rspb.2000.1366
Ma T, Pan X, Chen L, Liu W, Christie P, Luo Y, Wu L (2016) Effects of different concentrations and application frequencies of oxytetracycline on soil enzyme activities and microbial community diversity. Eur J Soil Biol 76:53–60. https://doi.org/10.1016/j.ejsobi.2016.07.004
MAPA (1994) Métodos oficiales de análisis de suelos y aguas para riego. In: Horwitz W (ed) Métodos Oficiales de Análisis, Vol. III. Ministerio de Agricultura, Pesca y Alimentación, Madrid.
Marques AC, Fuinhas JA, Pais DF (2018) Economic growth, sustainable development and food consumption: Evidence across different income groups of countries. J Clean Prod 196:245–258. https://doi.org/10.1016/j.jclepro.2018.06.011
McGrath SP, Cunliffe CH (1985) A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn from soils and sewage sludges. J Sci Food Agric 36:794–798. https://doi.org/10.1002/jsfa.2740360906
Nannipieri P, Ascher J, Ceccherini M, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670. https://doi.org/10.1111/ejss.4_12398
Ohore OE, Addo FG, Zhang S, Han N, Anim-Larbi K (2019) Distribution and relationship between antimicrobial resistance genes and heavy metals in surface sediments of Taihu Lake, China. J Environ Sci 77:323–335. https://doi.org/10.1016/j.jes.2018.09.004
Pan M, Chu LM (2016) Adsorption and degradation of five selected antibiotics in agricultural soil. Sci Total Environ 545–546:48–56. Environ Sci 77:323–335. https://doi.org/10.1016/j.scitotenv.2015.12.040
Reichel R, Rosendahl I, Peeters ETHM, 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. https://doi.org/10.1016/j.soilbio.2013.03.007
Rozman KK, Doull J, Hayes WJ (2010) Chapter 1: Dose and time determining, and other factors influencing, toxicity. In: Hayes (ed) Handbook of Pesticide Toxicology, Elsevier Inc, pp 1–101. https://doi.org/10.1016/B978-0-12-374367-1.00001-X.
Santás-Miguel V, Arias-Estévez M, Díaz-Raviña M, Fernández-Sanjurjo MJ, Álvarez-Rodríguez E, Núñez-Delgado A, Fernández-Calviño D (2020) Bacterial community tolerance to tetracycline antibiotics in Cu polluted soils. Agronomy 10:1220. https://doi.org/10.3390/agronomy10091220
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. https://doi.org/10.1016/j.chemosphere.2006.03.026
Schar D, Klein EY, Laxminarayan R, Gilbert M, Van Boeckel TP (2020) Global trends in antimicrobial use in aquaculture. Sci Rep 10:21878. https://doi.org/10.1038/s41598-020-78849-3
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. https://doi.org/10.1016/j.soilbio.2005.02.022
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. https://doi.org/10.1021/es034685p
Smalla K, Wachtendorf U, Heuer H, Liu W, Forney L (1998) Analysis of BIOLOG GN substrate utilization patterns by microbial communities. Appl Environ Microbiol 64:1220–1225. https://doi.org/10.1128/AEM.64.4.1220-1225.1998
Stefanowicz AM, Niklińska M, Laskowski R (2009) Pollution-induced community tolerance of soil bacterial communities in meadow and forest ecosystems polluted with heavy metals. Eur J Soil Biol 45:363–369. https://doi.org/10.1016/j.ejsobi.2009.05.005
Thiele-Bruhn S, Beck IC (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465. https://doi.org/10.1016/j.chemosphere.2005.01.023
Tlili A, Berard A, Blanck H, Bouchez A, Cássio F, Eriksson KM, Morin S, Montuelle B, Navarro E, Pascoal C, Pesce S, Schmitt-Jansen M, Behra R (2015) Pollution-induced community tolerance (PICT): towards an ecologically relevant risk assessment of chemicals in aquatic systems. Freshwater Biol 61:2141–2151. https://doi.org/10.1111/fwb.12558
Urra J, Alkorta I, Lanzén A, Mijangos I, Garbisu C (2019) The application of fresh and composted horse and chicken manure affects soil quality, microbial composition and antibiotic resistance. Appl Soil Ecol 135:73–84. https://doi.org/10.1016/j.apsoil.2018.11.005
Urra J, Mijangos I, Epelde L, Alkorta I, Garbisu C (2020) Impact of the application of commercial and farm-made fermented liquid organic amendments on corn yield and soil quality. Appl Soil Ecol 153:103643. https://doi.org/10.1016/j.apsoil.2020.103643
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 112:5649–5654. https://doi.org/10.1073/pnas.1503141112
Wakelin S, Gerard E, Black A, Hamonts K, Condron L, Yuan T, van Nostrand J, Zhou J, O’Callaghan M (2014) Mechanisms of pollution induced community tolerance in a soil microbial community exposed to Cu. Environ Pollut 190:1–9. https://doi.org/10.1016/j.envpol.2014.03.008
Walters E, McClellan K, Halden RU (2010) Occurrence and loss over three years of 72 pharmaceuticals and personal care products from biosolids-soil mixtures in outdoor mesocosms. Water Res 44:6011–6020. https://doi.org/10.1016/j.watres.2010.07.051.
Zabaloy MC, Garland JL, Gómez MA (2010) Assessment of the impact of 2,4- dichlorophenoxyacetic acid (2,4-D) on indigenous herbicide-degrading bacteria and microbial community function in an agricultural soil. Appl Soil Ecol 46:240–246. https://doi.org/10.1016/j.apsoil.2010.08.006
Acknowledgements
The authors thank Dr. Itziar Alkorta, Coordinator of the Euskampus JRL - Environmental Antibiotic Resistance, for helpful discussions.
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LJ: Formal analysis, Investigation, Writing-original draft. LE: Conceptualization, Writing: Review & Editing. MA: Formal analysis, Investigation. FB: Methodology. CG: Conceptualization, Writing: Review & Editing.
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This work was financially supported by the Basque Government (URAGAN 18-00044 and KONTRAE-Elkartek-KK-2020-0000 projects) and the Spanish Ministry of Science and Innovation (PRADA PID2019-110055RB-C21 project). LJ was the recipient of a predoctoral fellowship from the Basque Government.
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Jauregi, L., Epelde, L., Artamendi, M. et al. Induced development of oxytetracycline tolerance in bacterial communities from soil amended with well-aged cow manure. Ecotoxicology 32, 418–428 (2023). https://doi.org/10.1007/s10646-023-02650-x
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DOI: https://doi.org/10.1007/s10646-023-02650-x