Abstract
Manure application to agricultural soils can increase the abundance of antibiotic-resistance genes and resistant bacterial populations in soil. The aim of this study was to compare the contribution of nutrients and microorganisms of manure in the accumulation of tetracycline resistance in manure-treated soil. Soil microcosms were incubated for 77 days in a bench-scale mesocosm experiment and for 2 years in a greenhouse experiment and treated with manure or sterilized manure. In the manured soil, both aerobic tetracycline-resistant bacteria (TRB) and tetracycline-resistance genes (TRGs) (tetG, tetB(P), tetO, and tetL) were detected. Nutrients and TRGs not carried by live bacteria contribute little to the accumulation of TRB and TRGs, while microorganisms from manure contributed considerably. However, in soil with a long history of manure fertilization, the survival or dissemination of TRB and TRGs were prevented. The native soil microbial communities were probably more competitive than microbial species added with manure for nutrients of colonizing soil niches. Some bacterial species showed a significant negative correlation with the relative abundance of the four TRGs and TRB; probably, these bacterial species might have played a role in inhibiting the survival of TRB or dissemination of TRGs. These findings provide some clues for revealing the mechanisms of how manure application influences the abundance of TRGs and TRB in soil.
Similar content being viewed by others
References
Agersø Y, Wulff G, Vaclavik E, Halling-Sorensen B, Jensen LB (2006) Effect of tetracycline residues in pig manure slurry on tetracycline-resistant bacteria and resistance gene tet(M) in soil microcosms. Environ Int 32:876–882
Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci U S A 105:10583–10588
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
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
D’Costa VM, King CE, Kalan L, Morar M, Sung WW, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD (2011) Antibiotic resistance is ancient. Nature 477:457–461
Delmont TO, Francioli D, Jacquesson S, Laoudi S, Mathieu A, Nesme J, Ceccherini MT, Nannipieri P, Simonet P, Vogel TM (2014) Microbial community development and unseen diversity recovery in inoculated sterile soil. Biol Fertil Soils 50:1069–1076
Durso LM, Harhay GP, Bono JL, Smith TP (2011) Virulence-associated and antibiotic resistance genes of microbial populations in cattle feces analyzed using a metagenomic approach. J Microbiol Methods 84:278–282
Edmeades DC (2003) The long-term effects of manures and fertilisers on soil productivity and quality: a review. Nutr Cycl Agroecosyst 66:165–180
Eitel Z, Sóki J, Urbán E, Nagy E (2013) The prevalence of antibiotic resistance genes in Bacteroides fragilis group strains isolated in different European countries. Anaerobe 21:43–49
Ferens WA, Hovde CJ (2011) Escherichia coli O157:H7: animal reservoir and sources of human infection. Foodborne Pathog Dis 8:465–487
Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107–1111
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
Gibson MK, Forsberg KJ, Dantas G (2015) Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J 9:207–216
Götz A, Smalla K (1997) Manure enhances plasmid mobilization and survival of Pseudomonas putida introduced into field soil. Appl Environ Microbiol 63:1980–1986
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
Heuer H, Schmitt H, Smalla K (2011a) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243
Heuer H, Solehati Q, Zimmerling U, Kleineidam K, Schloter M, Muller 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 Microbiol 77:2527–2530
Jechalke S, Kopmann C, Rosendahl I, Groeneweg J, Weichelt V, Krogerrecklenfort E, Brandes N, Nordwig M, Ding GC, Siemens J, Heuer H, Smalla K (2013) Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Appl Environ Microbiol 79:1704–1711
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
Kyselková M, Kotrbová L, Bhumibhamon G, Chroňáková A, Jirout J, Vrchotová N, Schmitt H, Elhottová D (2015) Tetracycline resistance genes persist in soil amended with cattle feces independently from chlortetracycline selection pressure. Soil Biol Biochem 81:259–265
Lefevre F, Robe P, Jarrin C, Ginolhac A, Zago C, Auriol D, Vogel TM, Simonet P, Nalin R (2008) Drugs from hidden bugs: their discovery via untapped resources. Res Microbiol 159:153–161
Ma Y, Wilson CA, Novak JT, Riffat R, Aynur S, Murthy S, Pruden A (2011) Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons. Environ Sci Technol 45:7855–7861
Marti R, Scott A, Tien YC, Murray R, Sabourin L, Zhang Y, Topp E (2013) Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl Environ Microbiol 79:5701–5709
Monier JM, Demaneche S, Delmont TO, Mathieu A, Vogel TM, Simonet P (2011) Metagenomic exploration of antibiotic resistance in soil. Curr Opin Microbiol 14:229–235
Negreanu Y, Pasternak Z, Jurkevitch E, Cytryn E (2012) Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environ Sci Technol 46:4800–4808
Parham JA, Deng SP, Da HN, Sun HY, Raun WR (2003) Long-term cattle manure application in soil. II. Effect on soil microbial populations and community structure. Biol Fertil Soils 38:209–215
Peng S, Wang Y, Zhou B, Lin X (2015) Long-term application of fresh and composted manure increase tetracycline resistance in the arable soil of eastern China. Sci Total Environ 506–507:279–286
Pietramellara G, Ascher J, Borgogni F, Ceccherini MT, Guerri G, Nannipieri P (2009) Extracellular DNA in soil and sediment: fate and ecological relevance. Biol Fertil Soils 45:219–235
Pruden A, Larsson DG, Amezquita A, Collignon P, Brandt KK, Graham DW, Lazorchak JM, Suzuki S, Silley P, Snape JR, Topp E, Zhang T, Zhu YG (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect 121:878–885
Qiu M, Li S, Zhou X, Cui X, Vivanco JM, Zhang N, Shen Q, Zhang R (2014) De-coupling of root–microbiome associations followed by antagonist inoculation improves rhizosphere soil suppressiveness. Biol Fertil Soils 50:217–224
Rousk J, Brookes PC, Baath E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596
Schmitt H, Stoob K, Hamscher G, Smi E, Seinen W (2006) Tetracyclines and tetracycline resistance in agricultural soils: microcosm and field studies. Microb Ecol 51:267–276
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
Sun R, Zhang XX, Guo X, Wang D, Chu H (2015) Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem 88:9–18
Tolls J (2001) Sorption of veterinary pharmaceuticals in soils: a review. Environ Sci Technol 35:3397–3406
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
van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci U S A 109:1159–1164
Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270
Wei R, Ge F, Huang S, Chen M, Wang R (2011) Occurrence of veterinary antibiotics in animal wastewater and surface water around farms in Jiangsu Province, China. Chemosphere 82:1408–1414
Wichmann F, Udikovic-Kolic N, Andrew S, Handelsman J (2014) Diverse antibiotic resistance genes in dairy cow manure. MBio 5:e01017
Yang Q, Ren S, Niu T, Guo Y, Qi S, Han X, Liu D, Pan F (2014) Distribution of antibiotic-resistant bacteria in chicken manure and manure-fertilized vegetables. Environ Sci Pollut Res Int 21:1231–1241
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 Microbiol 78:3203–3213
Zhang T, Zhang M, Zhang X, Fang HH (2009) Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environ Sci Technol 43:3455–3460
Zhang Y, Snow DD, Parker D, Zhou Z, Li X (2013) Intracellular and extracellular antimicrobial resistance genes in the sludge of livestock waste management structures. Environ Sci Technol 47:10206–10213
Zhang X, Li Y, Liu B, Wang J, Feng C, Gao M, Wang L (2014) Prevalence of veterinary antibiotics and antibiotic-resistant Escherichia coli in the surface water of a livestock production region in northern China. PLoS One 9:e111026
Zhao J, Ni T, Li Y, Xiong W, Ran W, Shen B, Shen Q, Zhang R (2014) Responses of bacterial communities in arable soils in a rice-wheat cropping system to different fertilizer regimes and sampling times. PLoS One 9:e85301
Zhao J, Ni T, Li J, Lu Q, Fang Z, Huang Q, Zhang R, Li R, Shen B, Shen Q (2016) Effects of organic–inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice–wheat cropping system. Appl Soil Ecol 99:1–12
Zhou Z, Raskin L, Zilles JL (2010) Effects of swine manure on macrolide, lincosamide, and streptogramin B antimicrobial resistance in soils. Appl Environ Microbiol 76:2218–2224
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
Acknowledgments
We are very grateful to the anonymous reviewers and the chief editor Paolo Nannipieri for their time and the constructive comments on improving our manuscript. Research in this work was funded by the National Natural Science Foundation of China (21377137, 41501275, and 20607024), Jiangsu Planned Projects for Postdoctoral Research Funds (1501077B) and CAS Strategic Priority Research Program Grant No. XDA05020800.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 20 kb)
Rights and permissions
About this article
Cite this article
Peng, S., Zhou, B., Wang, Y. et al. Bacteria play a more important role than nutrients in the accumulation of tetracycline resistance in manure-treated soil. Biol Fertil Soils 52, 655–663 (2016). https://doi.org/10.1007/s00374-016-1105-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-016-1105-9