Skip to main content
SpringerLink
Log in

Antibiotic Resistance in Soil

  • Chapter
  • First Online:
Antibiotic Resistance in the Environment

Part of the book series: The Handbook of Environmental Chemistry ((HEC,volume 91))

Abstract

Exposure to antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) from natural and agricultural ecosystems such as soil can significantly affect the dissemination of resistance determinants to the human microbiome. Soil contains a diverse natural resistome and also serves as an important environmental reservoir for ARB and ARGs derived from water sources, aerosols, and sewage sludge. Soil microbiomes have been impacted worldwide by the use and overuse of antibiotics for anthropogenic activities (clinical use and livestock production) and agricultural practices (manure application and irrigation with wastewater). The dynamics and persistence of ARB and ARGs in soil are affected by soil management and environmental factors. Both abiotic and biotic factors (pH, temperature, organic matter, nutrient availability, and syntrophic, competing or antagonistic organisms) can act as driving forces for ARG fate, evolution, and horizontal gene transfer processes. Meanwhile, ARGs in soil may also be transferred to other environments, such as groundwater and the phytosphere. To tackle the potential threat of ARGs, treatment measures (aerobic composting, anaerobic digestion, and disinfection) have been evaluated to reduce the selective pressure and import of ARGs into soil. Furthermore, the “One Health” approach was put forward to manage the development and dissemination of ARGs in a cross-disciplinary manner, to more holistically reduce human risk to the lowest level.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 349.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 449.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 449.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Tiedje JM, Wang F, Manaia C, Virta M, Sheng H, Ma L, Zhang T, Topp E (2019) Antibiotic resistance genes in the human impacted environment: a One Health perspective. Pedosphere 29:273–282. https://doi.org/10.1016/S1002-0160(18)60062-1

    Article  Google Scholar 

  2. Xie WY, Shen Q, Zhao FJ (2018) Antibiotics and antibiotic resistance from animal manures to soil: a review. Eur J Soil Sci 69:181–195

    Google Scholar 

  3. Nesme J, Simonet P (2015) The soil resistome: a critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria. Environ Microbiol 17:913–930

    Google Scholar 

  4. 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

    CAS  Google Scholar 

  5. Dolejska M, Papagiannitsis CC (2018) Plasmid-mediated resistance is going wild. Plasmid 99:99–111

    CAS  Google Scholar 

  6. Hu J, Zhao F, Zhang XX, Li K, Li C, Ye L, Li M (2018) Metagenomic profiling of ARGs in airborne particulate matters during a severe smog event. Sci Total Environ 615:1332–1340

    CAS  Google Scholar 

  7. Pärnänen KMM et al (2019) Antibiotic resistance in European wastewater treatment plants mirrors the pattern of clinical antibiotic resistance prevalence. Sci Adv 5:eaau9124

    Google Scholar 

  8. Thompson JM, Gundogdu A, Stratton HM, Katouli M (2013) Antibiotic resistant Staphylococcus aureus in hospital wastewaters and sewage treatment plants with special reference to methicillin-resistant Staphylococcus aureus (MRSA). J Appl Microbiol 114:44–54

    CAS  Google Scholar 

  9. Wang F, Xu M, Stedtfeld RD, Sheng H, Fan J, Liu M, Chai B, Soares de Carvalho T, Li H, Li Z, Hashsham SA, Tiedje JM (2018) Long-term effect of different fertilization and cropping systems on the soil antibiotic resistome. Environ Sci Technol 52:13037–13046

    CAS  Google Scholar 

  10. Rodriguez RL, Gunturu S, Tiedje JM, Cole JR, Konstantinidis KT (2018) Nonpareil 3: fast estimation of metagenomic coverage and sequence diversity. mSystems 3:3

    Google Scholar 

  11. Chen B, Yuan K, Chen X, Yang Y, Zhang T, Wang Y, Luan T, Zou S, Li X (2016) Metagenomic analysis revealing antibiotic resistance genes (ARGs) and their genetic compartments in the Tibetan environment. Environ Sci Technol 50:6670–6679

    CAS  Google Scholar 

  12. Leonard AFC, Zhang L, Balfour A, Garside R, Gaze WH (2015) Human recreational exposure to antibiotic resistant bacteria in coastal bathing waters. Environ Int 82:92–100

    CAS  Google Scholar 

  13. Zhu YG, Zhao Y, Zhu D, Gillings M, Penuelas J, Ok YS, Capon A, Banwart S (2019) Soil biota, antimicrobial resistance and planetary health. Environ Int 131:105059

    Google Scholar 

  14. UNEP (2017) Antimicrobial resistance from environmental pollution among biggest emerging health threats, says UN Environment. https://www.unenvironment.org/news-and-stories/press-release/antimicrobial-resistance-environmental-pollution-among-biggest

  15. Robinson DA, Sutcliffe JA, Tewodros W, Manoharan A, Bessen DE (2006) Evolution and global dissemination of macrolide-resistant group a Streptococci. Antimicrob Agents Chemother 50:2903–2911

    CAS  Google Scholar 

  16. Brown MG, Balkwill DL (2009) Antibiotic resistance in bacteria isolated from the deep terrestrial subsurface. Microb Ecol 57:484–493

    CAS  Google Scholar 

  17. D’Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD (2011) Antibiotic resistance is ancient. Nature 477:457

    Google Scholar 

  18. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J (2009) Functional metagenomics reveals diverse beta-lactamases in a remote Alaskan soil. ISME J 3:243–251

    CAS  Google Scholar 

  19. 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(4):e34953

    CAS  Google Scholar 

  20. Mindlin SZ, Soina VS, Ptrova MA, Gorlenko ZM (2008) Isolation of antibiotic resistance bacterial strains from East Siberia permafrost sediments. Genetika 44:36–44

    CAS  Google Scholar 

  21. Wang F, Stedtfeld R, Kim O-S, Chai B, Yang L, Stedtfeld T, Hong SG, Kim D, Lim HS, Hashsham S, Tiedje J, Sul WJ (2016) Influence of soil characteristics and proximity to antarctic research stations on abundance of antibiotic resistance genes in soils. Environ Sci Technol 50(23):12621–12629

    CAS  Google Scholar 

  22. Kevin JF, Alejandro R, Bin W, Elizabeth MS, Morten OAS, Gautam D (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:4

    Google Scholar 

  23. Peterson E, Kaur P (2018) Antibiotic resistance mechanisms in bacteria: relationships between resistance determinants of antibiotic producers, environmental bacteria, and clinical pathogens. Front Microbiol 9:2928

    Google Scholar 

  24. Bengtsson-Palme J, Kristiansson E, Larsson DGJ (2018) Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol Rev 42(1):fux053

    Google Scholar 

  25. 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

    CAS  Google Scholar 

  26. Li L-G, Yin X, Zhang T (2018) Tracking antibiotic resistance gene pollution from different sources using machine-learning classification. Microbiome 6:93–93

    Google Scholar 

  27. Song L, Li L, Yang S, Lan J, He H, McElmurry SP, Zhao Y (2016) Sulfamethoxazole, tetracycline and oxytetracycline and related antibiotic resistance genes in a large-scale landfill, China. Sci Total Environ 551-552:9–15

    CAS  Google Scholar 

  28. Heuer H, Schmitt H, Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243

    CAS  Google Scholar 

  29. Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in Northern Colorado. Environ Sci Technol 40:7445–7450

    CAS  Google Scholar 

  30. Sengelov G, Agerso Y, Halling-Sorensen 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

    CAS  Google Scholar 

  31. Marti R, Scott A, Tien Y-C, 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

    CAS  Google Scholar 

  32. 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

    CAS  Google Scholar 

  33. Popowska M, Rzeczycka M, Miernik A, Krawczyk-Balska A, Walsh F, Duffy B (2012) Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob Agents Chemother 56:1434–1443

    CAS  Google Scholar 

  34. Schmitt H, Stoob K, Hamscher G, Smit E, Seinen W (2006) Tetracyclines and tetracycline resistance in agricultural soils: Microcosm and field studies. Microb Ecol 51:267–276

    Google Scholar 

  35. Pei RT, Kim SC, Carlson KH, Pruden A (2006) Effect of River Landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res 40:2427–2435

    CAS  Google Scholar 

  36. Muurinen J, Stedtfeld R, Karkman A, Parnanen K, Tiedje J, Virta M (2017) Influence of manure application on the environmental resistome under finnish agricultural practice with restricted antibiotic use. Environ Sci Technol 51:5989–5999

    CAS  Google Scholar 

  37. Witte W (1998) Medical consequences of antibiotic use in agriculture. Science 279:996–997

    CAS  Google Scholar 

  38. Moses A, Tomaselli P (2017) Industrial animal agriculture in the United States: concentrated animal feeding operations (CAFOs). In: Steier G, Patel KK (eds) International farm animal, wildlife and food safety law. Springer, Cham, pp 185–214

    Google Scholar 

  39. Yang F, Li R, Cui Y, Duan Y (2010) Utilization and develop strategy of organic fertilizer resources in China. Soil Fert Sci China 4:77–82

    Google Scholar 

  40. 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

    Google Scholar 

  41. Kumar D, Pornsukarom S, Thakur S (2019) Antibiotic usage in poultry production and antimicrobial-resistant Salmonella in poultry. In: Venkitanarayanan K, Thakur S, Ricke SC (eds) Food safety in poultry meat production. Springer, Cham, pp 47–66

    Google Scholar 

  42. Chen C, Pankow CA, Oh M, Heath LS, Zhang L, Du P, Xia K, Pruden A (2019) Effect of antibiotic use and composting on antibiotic resistance gene abundance and resistome risks of soils receiving manure-derived amendments. Environ Int 128:233–243

    CAS  Google Scholar 

  43. You Y, Silbergeld EK (2014) Learning from agriculture: understanding low-dose antimicrobials as drivers of resistome expansion. Front Microbiol 5:284

    Google Scholar 

  44. Xie W-Y, Yang X-P, Li Q, Wu L-H, Shen Q-R, Zhao F-J (2016) Changes in antibiotic concentrations and antibiotic resistome during commercial composting of animal manures. Environ Pollut 219:182–190

    CAS  Google Scholar 

  45. Johnson TA, Stedtfeld RD, Wang Q, Cole JR, Hashsham SA, Looft T, Zhu Y-G, Tiedje JM (2016) Clusters of antibiotic resistance genes enriched together stay together in swine agriculture. MBio 7:e02214–e02215

    CAS  Google Scholar 

  46. Ma L, Li AD, Yin XL, Zhang T (2017) The prevalence of integrons as the carrier of antibiotic resistance genes in natural and man-made environments. Environ Sci Technol 51:5721–5728

    CAS  Google Scholar 

  47. Zhu YG, Gillings M, Simonet P, Stekel D, Banwart S, Penuelas J (2017) Microbial mass movements. Science 357:2

    Google Scholar 

  48. Marti R, Tien Y-C, Murray R, Scott A, Sabourin L, Topp E (2014) Safely coupling livestock and crop production systems: how rapidly do antibiotic resistance genes dissipate in soil following a commercial application of swine or dairy manure? Appl Environ Microbiol 80:3258–3265

    Google Scholar 

  49. Qian X, Sun W, Gu J, Wang XJ, Sun JJ, Yin YN, Duan ML (2016) Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure. J Hazard Mater 315:61–69

    CAS  Google Scholar 

  50. Van Elsas JD, Turner S, Bailey MJ (2003) Horizontal gene transfer in the phytosphere. New Phytol 157:525–537

    Google Scholar 

  51. Flörke M, Kynast E, Bärlund I, Eisner S, Wimmer F, Alcamo J (2013) Domestic and industrial water uses of the past 60 years as a mirror of socio-economic development: A global simulation study. Glob Environ Chang 23:144–156

    Google Scholar 

  52. Mateo-Sagasta J, Raschid-Sally L, Thebo A (2015) Global wastewater and sludge production, treatment and use. In: Drechsel P, Qadir M, Wichelns D (eds) Wastewater: economic asset in an urbanizing world. Springer, Dordrecht, pp 15–38

    Google Scholar 

  53. Gatica J, Cytryn E (2013) Impact of treated wastewater irrigation on antibiotic resistance in the soil microbiome. Environ Sci Pollut Res Int 20:3529–3538

    CAS  Google Scholar 

  54. Pan M, Chu LM (2018) Occurrence of antibiotics and antibiotic resistance genes in soils from wastewater irrigation areas in the Pearl River Delta region, southern China. Sci Total Environ 624:145–152

    CAS  Google Scholar 

  55. Jechalke S, Broszat M, Lang F, Siebe C, Smalla K, Grohmann E (2015) Effects of 100 years wastewater irrigation on resistance genes, class 1 integrons and IncP-1 plasmids in Mexican soil. Front Microbiol 6:163

    Google Scholar 

  56. Kapanen A, Vikman M, Rajasärkkä J, Virta M, Itävaara M (2013) Biotests for environmental quality assessment of composted sewage sludge. Waste Manag 33:1451–1460

    CAS  Google Scholar 

  57. Raheem A, Sikarwar VS, He J, Dastyar W, Dionysiou DD, Wang W, Zhao M (2018) Opportunities and challenges in sustainable treatment and resource reuse of sewage sludge: a review. Chem Eng J 337:616–641

    CAS  Google Scholar 

  58. Yang G, Zhang G, Wang H (2015) Current state of sludge production, management, treatment and disposal in China. Water Res 78:60–73

    Google Scholar 

  59. An X-L, Su J-Q, Li B, Ouyang W-Y, Zhao Y, Chen Q-L, Cui L, Chen H, Gillings MR, Zhang T, Zhu Y-G (2018) Tracking antibiotic resistome during wastewater treatment using high throughput quantitative PCR. Environ Int 117:146–153

    CAS  Google Scholar 

  60. Su JQ, Wei B, Ou-Yang WY, Huang FY, Zhao Y, Xu HJ, Zhu YG (2015) Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol 49:7356–7363

    CAS  Google Scholar 

  61. Zhang J, Sui Q, Tong J, Buhe C, Wang R, Chen M, Wei Y (2016) Sludge bio-drying: Effective to reduce both antibiotic resistance genes and mobile genetic elements. Water Res 106:62–70

    Google Scholar 

  62. Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall AB, Wellington EM (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 5:1253–1261

    CAS  Google Scholar 

  63. Chen H, Zhang M (2013) Occurrence and removal of antibiotic resistance genes in municipal wastewater and rural domestic sewage treatment systems in eastern China. Environ Int 55:9–14

    CAS  Google Scholar 

  64. Threedeach S, Chiemchaisri W, Watanabe T, Chiemchaisri C, Honda R, Yamamoto K (2012) Antibiotic resistance of Escherichia coli in leachates from municipal solid waste landfills: Comparison between semi-aerobic and anaerobic operations. Bioresour Technol 113:253–258

    CAS  Google Scholar 

  65. 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

    CAS  Google Scholar 

  66. 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

    CAS  Google Scholar 

  67. Gao M, Jia R, Qiu T, Han M, Wang X (2017) Size-related bacterial diversity and tetracycline resistance gene abundance in the air of concentrated poultry feeding operations. Environ Pollut 220:1342–1348

    CAS  Google Scholar 

  68. Dungan RS (2010) Fate and transport of bioaerosols associated with livestock operations and manures. J Anim Sci 88:3693–3706

    CAS  Google Scholar 

  69. Morselli L, Olivieri P, Brusori B, Passarini F (2003) Soluble and insoluble fractions of heavy metals in wet and dry atmospheric depositions in Bologna, Italy. Environ Pollut 124:457–469

    CAS  Google Scholar 

  70. Flanner MG, Zender CS, Randerson JT, Rasch PJ (2007) Present-day climate forcing and response from black carbon in snow. J Geophys Res 112(D11)

    Google Scholar 

  71. Xie J, Jin L, Luo X, Zhao Z, Li X (2018) Seasonal disparities in airborne bacteria and associated antibiotic resistance genes in PM2.5 between urban and rural sites. Environ Sci Technol Lett 5:74–79

    CAS  Google Scholar 

  72. Fahrenfeld N, Knowlton K, Krometis LA, Hession WC, Xia K, Lipscomb E, Libuit K, Green BL, Pruden A (2014) Effect of manure application on abundance of antibiotic resistance genes and their attenuation rates in soil: field-scale mass balance approach. Environ Sci Technol 48:2643–2650

    CAS  Google Scholar 

  73. Gou M, Hu HW, Zhang YJ, Wang JT, Hayden H, Tang YQ, He JZ (2018) Aerobic composting reduces antibiotic resistance genes in cattle manure and the resistome dissemination in agricultural soils. Sci Total Environ 612:1300–1310

    CAS  Google Scholar 

  74. Burch TR, Sadowsky MJ, LaPara TM (2014) Fate of antibiotic resistance genes and class 1 integrons in soil microcosms following the application of treated residual municipal wastewater solids. Environ Sci Technol 48:5620–5627

    CAS  Google Scholar 

  75. Zhang J, Sui Q, Tong J, Zhong H, Wang Y, Chen M, Wei Y (2018) Soil types influence the fate of antibiotic-resistant bacteria and antibiotic resistance genes following the land application of sludge composts. Environ Int 118:34–43

    CAS  Google Scholar 

  76. Joy SR, Bartelt-Hunt SL, Snow DD, Gilley JE, Woodbury BL, Parker DB, Marx DB, Li X (2013) Fate and transport of antimicrobials and antimicrobial resistance genes in soil and runoff following land application of swine manure slurry. Environ Sci Technol 47:12081–12088

    CAS  Google Scholar 

  77. Chen Z, Zhang W, Wang G, Zhang Y, Gao Y, Boyd SA, Teppen BJ, Tiedje JM, Zhu D, Li H (2017) Bioavailability of soil-sorbed tetracycline to Escherichia coli under unsaturated conditions. Environ Sci Technol 51:6165–6173

    CAS  Google Scholar 

  78. McKinney CW, Pruden A (2012) Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ Sci Technol 46:13393–13400

    CAS  Google Scholar 

  79. Burch TR, Sadowsky MJ, Lapara TM (2013) Aerobic digestion reduces the quantity of antibiotic resistance genes in residual municipal wastewater solids. Front Microbiol 4:17

    Google Scholar 

  80. 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

    CAS  Google Scholar 

  81. Chee-Sanford JC, Aminov RI, Krapac IJ, Garrigues-Jeanjean N, Mackie RI (2001) Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl Environ Microbiol 67:1494–1502

    CAS  Google Scholar 

  82. Koike S, Krapac IG, Oliver HD, Yannarell AC, Chee-Sanford JC, Aminov RI, Mackie RI (2007) Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period. Appl Environ Microbiol 73:4813–4823

    CAS  Google Scholar 

  83. Kroer N, Barkay T, Sorensen S, Weber D (1998) Effect of root exudates and bacterial metabolic activity on conjugal gene transfer in the rhizosphere of a marsh plant. FEMS Microbiol Ecol 25:375–384

    CAS  Google Scholar 

  84. Zhu YG, Zhao Y, Li B, Huang CL, Zhang SY, Yu S, Chen YS, Zhang T, Gillings MR, Su JQ (2017) Continental-scale pollution of estuaries with antibiotic resistance genes. Nat Microbiol 2:16270

    CAS  Google Scholar 

  85. Rahube TO, Romain M, Andrew S, Yuan-Ching T, Roger M, Lyne S, Yun Z, Peter D, Lapen DR, Edward T (2014) Impact of fertilizing with raw or anaerobically digested sewage sludge on the abundance of antibiotic-resistant coliforms, antibiotic resistance genes, and pathogenic bacteria in soil and on vegetables at harvest. Appl Environ Microbiol 80:6898–6907

    Google Scholar 

  86. Xu FL, Wang JP, Guo YC, Fu P, Zeng HW, Li ZG, Pei XY, Liu XM, Wang S (2018) Antibiotic resistance, biochemical typing, and PFGE typing of Bifidobacterium strains commonly used in probiotic health foods. Food Sci Biotechnol 27:467–477

    CAS  Google Scholar 

  87. Chen QL, An XL, Zhu YG, Su JQ, Gillings MR, Ye ZL, Cui L (2017) Application of struvite alters the antibiotic resistome in soil, rhizosphere, and phyllosphere. Environ Sci Technol 51:8149–8157

    CAS  Google Scholar 

  88. Yang L, Liu W, Zhu D, Hou J, Ma T, Wu L, Zhu Y, Christie P (2018) Application of biosolids drives the diversity of antibiotic resistance genes in soil and lettuce at harvest. Soil Biol Biochem 122:131–140

    CAS  Google Scholar 

  89. Hao Z, Li X, Yang Q, Sun L, Yang X, Zhou M, Deng R, Bi L (2017) Plant growth, antibiotic uptake, and prevalence of antibiotic resistance in an endophytic system of pakchoi under antibiotic exposure. Int J Environ Res Public Health 14:1336

    Google Scholar 

  90. Verraes C, Van BS, Van ME, Van CE, Butaye P, Catry B, de Schaetzen MA, Van HX, Imberechts H, Dierick K (2013) Antimicrobial resistance in the food chain: a review. Int J Environ Res Public Health 10:2643–2669

    Google Scholar 

  91. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    CAS  Google Scholar 

  92. Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    CAS  Google Scholar 

  93. Smalla K, Cook K, Djordjevic SP, Kluemper U, Gillings M (2018) Environmental dimensions of antibiotic resistance: assessment of basic science gaps. FEMS Microbiol Ecol 94(12):fiy195

    Google Scholar 

  94. Cruz-Loya M, Kang TM, Lozano NA, Watanabe R, Tekin E, Damoiseaux R, Savage VM, Yeh PJ (2019) Stressor interaction networks suggest antibiotic resistance co-opted from stress responses to temperature. ISME J 13:12–23

    Google Scholar 

  95. Graham DW, Olivares-Rieumont S, Knapp CW, Lima L, Werner D, Bowen E (2011) Antibiotic resistance gene abundances associated with waste discharges to the Almendares river near Havana, Cuba. Environ Sci Technol 45:418–424

    CAS  Google Scholar 

  96. Poole K (2012) Stress responses as determinants of antimicrobial resistance in Gram-negative bacteria. Trends Microbiol 20:227–234

    CAS  Google Scholar 

  97. Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K (2014) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545

    CAS  Google Scholar 

  98. Van Zwieten L, Kimber S, Morris S, Chan KY, Downie A, Rust J, Joseph S, Cowie A (2010) Effects of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant and Soil 327:235–246

    Google Scholar 

  99. Jia M, Wang F, Jin X, Song Y, Bian Y, Boughner LA, Yang X, Gu C, Jiang X, Zhao Q (2016) Metal ion-oxytetracycline interactions on maize straw biochar pyrolyzed at different temperatures. Chem Eng J 304:934–940

    CAS  Google Scholar 

  100. Vithanage M, Rajapaksha AU, Zhang M, Thiele-Bruhn S, Lee SS, Ok YS (2015) Acid-activated biochar increased sulfamethazine retention in soils. Environ Sci Pollut Res 22:2175–2186

    CAS  Google Scholar 

  101. Han XM, Hu HW, Shi XZ, Wang JT, Han LL, Chen D, He JZ (2016) Impacts of reclaimed water irrigation on soil antibiotic resistome in urban parks of Victoria, Australia. Environ Pollut 211:48–57

    CAS  Google Scholar 

  102. Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota – a review. Soil Biol Biochem 43:1812–1836

    CAS  Google Scholar 

  103. Nguyen BT, Lehmann J, Hockaday WC, Joseph S, Masiello CA (2010) Temperature sensitivity of black carbon decomposition and oxidation. Environ Sci Technol 44:3324–3331

    CAS  Google Scholar 

  104. Cui E, Wu Y, Jiao Y, Zuo Y, Rensing C, Chen H (2017) The behavior of antibiotic resistance genes and arsenic influenced by biochar during different manure composting. Environ Sci Pollut Res 24:14484–14490

    CAS  Google Scholar 

  105. Tang X, Lou C, Wang S, Lu Y, Liu M, Hashmi MZ, Liang X, Li Z, Liao Y, Qin W, Fan F, Xu J, Brookes PC (2015) Effects of long-term manure applications on the occurrence of antibiotics and antibiotic resistance genes (ARGs) in paddy soils: Evidence from four field experiments in south of China. Soil Biol Biochem 90:179–187

    CAS  Google Scholar 

  106. Kang K, Ni Y, Li J, Imamovic L, Sarkar C, Kobler MD, Heshiki Y, Zheng T, Kumari S, Wong JCY, Archna A, Wong CWM, Dingle C, Denizen S, Baker DM, Sommer MOA, Webster CJ, Panagiotou G (2018) The environmental exposures and inner- and intercity traffic flows of the metro system may contribute to the skin microbiome and resistome. Cell Rep 24:1190

    CAS  Google Scholar 

  107. Vincent AT, Trudel MV, Paquet VE, Boyle B, Tanaka KH, Dallaire-Dufresne S, Daher RK, Frenette M, Derome N, Charette SJ (2014) Detection of variants of the pRAS3, pAB5S9, and pSN254 plasmids in aeromonas salmonicida subsp salmonicida: multidrug resistance, interspecies exchanges, and plasmid reshaping. Antimicrob Agents Chemother 58:7367–7374

    Google Scholar 

  108. Bragazza L, Bardgett RD, Mitchell EAD, Buttler A (2015) Linking soil microbial communities to vascular plant abundance along a climate gradient. New Phytol 205:1175–1182

    Google Scholar 

  109. Gomez-Sagasti MT, Alkorta I, Becerril JM, Epelde L, Anza M, Garbisu C (2012) Microbial monitoring of the recovery of soil quality during heavy metal phytoremediation. Water Air Soil Pollut 223:3249–3262

    CAS  Google Scholar 

  110. Xiao K-Q, Li B, Ma L, Bao P, Zhou X, Zhang T, Zhu Y-G (2016) Metagenomic profiles of antibiotic resistance genes in paddy soils from South China. FEMS Microbiol Ecol 92(3):fiw023

    Google Scholar 

  111. Wu N, Qiao M, Zhang B, Cheng W-D, Zhu Y-G (2010) Abundance and Diversity of Tetracycline Resistance Genes in Soils Adjacent to Representative Swine Feedlots in China. Environ Sci Technol 44:6933–6939

    CAS  Google Scholar 

  112. Hunter PR, Wilkinson DC, Catling LA, Barker GC (2008) Meta-analysis of experimental data concerning antimicrobial resistance gene transfer rates during conjugation. Appl Environ Microbiol 74:6085

    CAS  Google Scholar 

  113. Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, King CJ, McArthur JV (2006) Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ Microbiol 8:1510–1514

    CAS  Google Scholar 

  114. Yazdankhah S, Rudi K, Bernhoft A (2014) Zinc and copper in animal feed – development of resistance and co-resistance to antimicrobial agents in bacteria of animal origin. Microb Ecol Health Dis 25:25862

    Google Scholar 

  115. Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, Wu M (2012) Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater 235:178–185

    Google Scholar 

  116. Zhao Y, Cocerva T, Cox S, Tardif S, Su JQ, Zhu YG, Brandt KK (2019) Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils. Sci Total Environ 656:512–520

    CAS  Google Scholar 

  117. Wright MS, Peltier GL, Stepanauskas R, McArthur JV (2006) Bacterial tolerances to metals and antibiotics in metal-contaminated and reference streams. FEMS Microbiol Ecol 58:293–302

    CAS  Google Scholar 

  118. Ding C, Pan J, Jin M, Yang D, Shen Z, Wang J, Zhang B, Liu W, Fu J, Guo X, Wang D, Chen Z, Yin J, Qiu Z, Li J (2016) Enhanced uptake of antibiotic resistance genes in the presence of nanoalumina. Nanotoxicology 10:1051–1060

    CAS  Google Scholar 

  119. Qiu Z, Yu Y, Chen Z, Jin M, Yang D, Zhao Z, Wang J, Shen Z, Wang X, Qian D, Huang A, Zhang B, Li J-W (2012) Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proc Natl Acad Sci U S A 109:6

    Google Scholar 

  120. Zhu D, Zheng F, Chen QL, Yang XR, Christie P, Ke X, Zhu YG (2018) Exposure of a soil collembolan to Ag nanoparticles and AgNO3 disturbs its associated microbiota and lowers the incidence of antibiotic resistance genes in the gut. Environ Sci Technol 52:12748–12756

    CAS  Google Scholar 

  121. Li J, Zhang K, Zhang H (2018) Adsorption of antibiotics on microplastics. Environ Pollut 237:460–467

    CAS  Google Scholar 

  122. Sun M, Ye M, Jiao W, Feng Y, Yu P, Liu M, Jiao J, He X, Liu K, Zhao Y, Wu J, Jiang X, Hu F (2018) Changes in tetracycline partitioning and bacteria/phage-comediated ARGs in microplastic-contaminated greenhouse soil facilitated by sophorolipid. J Hazard Mater 345:131–139

    CAS  Google Scholar 

  123. Arias-Andres M, Kluemper U, Rojas-Jimenez K, Grossart H-P (2018) Microplastic pollution increases gene exchange in aquatic ecosystems. Environ Pollut 237:253–261

    CAS  Google Scholar 

  124. Crofts TS, Gasparrini AJ, Dantas G (2017) Next-generation approaches to understand and combat the antibiotic resistome. Nat Rev Microbiol 15:422–434

    CAS  Google Scholar 

  125. Graham DW, Knapp CW, Christensen BT, McCluskey S, Dolfing J (2016) Appearance of beta-lactam resistance genes in agricultural soils and clinical isolates over the 20th century. Sci Rep 6:21550

    CAS  Google Scholar 

  126. Lau CH-F, Van Engelen K, Gordon S, Renaud J, Topp E (2017) Novel antibiotic resistance determinants from agricultural soil exposed to antibiotics widely used in human medicine and animal farming. Appl Environ Microbiol 83:e00989–e00917

    CAS  Google Scholar 

  127. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107–1111

    CAS  Google Scholar 

  128. Luby E, Ibekwe AM, Zilles J, Pruden A (2016) Molecular methods for assessment of antibiotic resistance in agricultural ecosystems: prospects and challenges. J Environ Qual 45:441–453

    CAS  Google Scholar 

  129. Martinez JL, Coque TM, Baquero F (2015) What is a resistance gene? ranking risk in resistomes. Nat Rev Microbiol 13:116–123

    CAS  Google Scholar 

  130. Ghaly TM, Chow L, Asher AJ, Waldron LS, Gillings MR (2017) Evolution of class 1 integrons: Mobilization and dispersal via food-borne bacteria. Plos One 12:e0179169

    Google Scholar 

  131. Blau K, Bettermann A, Jechalke S, Fornefeld E, Vanrobaeys Y, Stalder T, Top EM, Smalla K (2018) The transferable resistome of produce. MBio 9:e01300–e01318

    Google Scholar 

  132. Carnevali C, Morganti M, Scaltriti E, Bolzoni L, Pongolini S, Casadei G (2016) Occurrence of mcr-1 in colistin-resistant Salmonella enterica isolates recovered from humans and animals in Italy, 2012 to 2015. Antimicrob Agents Chemother 60:7532–7534

    CAS  Google Scholar 

  133. Roberts KD, Azad MA, Wang J, Horne AS, Thompson PE, Nation RL, Velkov T, Li J (2015) Antimicrobial activity and toxicity of the major lipopeptide components of polymyxin B and colistin: last-line antibiotics against multidrug-resistant gram-negative bacteria. ACS Infect Dis 1:568–575

    CAS  Google Scholar 

  134. Hu Y, Liu F, Lin IYC, Gao GF, Zhu B (2016) Dissemination of the mcr-1 colistin resistance gene. Lancet Infect Dis 16:146–147

    Google Scholar 

  135. Arnold S, Gassner B, Giger T, Zwahlen R (2004) Banning antimicrobial growth promoters in feedstuffs does not result in increased therapeutic use of antibiotics in medicated feed in pig farming. Pharmacoepidemiol Drug Saf 13:323–331

    Google Scholar 

  136. Edgar R, Friedman N, Molshanski-Mor S, Qimron U (2012) Reversing bacterial resistance to antibiotics by phage-mediated delivery of dominant sensitive genes. Appl Environ Microbiol 78:744–751

    CAS  Google Scholar 

  137. Jang HM, Lee J, Kim YB, Jeon JH, Shin J, Park MR, Kim YM (2018) Fate of antibiotic resistance genes and metal resistance genes during thermophilic aerobic digestion of sewage sludge. Bioresour Technol 249:635–643

    CAS  Google Scholar 

  138. Ghosh S, Ramsden SJ, LaPara TM (2009) The role of anaerobic digestion in controlling the release of tetracycline resistance genes and class 1 integrons from municipal wastewater treatment plants. Appl Microbiol Biotechnol 84:791–796

    CAS  Google Scholar 

  139. Zhang J, Chen M, Sui Q, Wang R, Tong J, Wei Y (2016) Fate of antibiotic resistance genes and its drivers during anaerobic co-digestion of food waste and sewage sludge based on microwave pretreatment. Bioresour Technol 217:28–36

    CAS  Google Scholar 

  140. Qian X, Sun W, Gu J, Wang XJ, Zhang YJ, Duan ML, Li HC, Zhang RR (2016) Reducing antibiotic resistance genes, integrons, and pathogens in dairy manure by continuous thermophilic composting. Bioresour Technol 220:425–432

    CAS  Google Scholar 

  141. Zhang CM, Xu LM, Wang XC, Zhuang K, Liu QQ (2017) Effects of ultraviolet disinfection on antibiotic-resistant Escherichia coli from wastewater: inactivation, antibiotic resistance profiles and antibiotic resistance genes. J Appl Microbiol 123:295–306

    CAS  Google Scholar 

  142. Zhang T, Yang Y, Pruden A (2015) Effect of temperature on removal of antibiotic resistance genes by anaerobic digestion of activated sludge revealed by metagenomic approach. Appl Microbiol Biotechnol 99:7771–7779

    CAS  Google Scholar 

  143. Guo A, Gu J, Wang X, Zhang R, Yin Y, Sun W, Tuo X, Zhang L (2017) Effects of superabsorbent polymers on the abundances of antibiotic resistance genes, mobile genetic elements, and the bacterial community during swine manure composting. Bioresour Technol 244:658–663

    CAS  Google Scholar 

  144. Cui E, Wu Y, Zuo Y, Chen H (2016) Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Bioresour Technol 203:11–17

    CAS  Google Scholar 

  145. Zhang Y, Li H, Gu J, Qian X, Yin Y, Li Y, Zhang R, Wang X (2016) Effects of adding different surfactants on antibiotic resistance genes and intI1 during chicken manure composting. Bioresour Technol 219:545–551

    CAS  Google Scholar 

  146. Peng S, Li H, Song D, Lin X, Wang Y (2018) Influence of zeolite and superphosphate as additives on antibiotic resistance genes and bacterial communities during factory-scale chicken manure composting. Bioresour Technol 263:393–401

    CAS  Google Scholar 

  147. Zhang J, Wang Z, Wang Y, Zhong H, Sui Q, Zhang C, Wei Y (2017) Effects of graphene oxide on the performance, microbial community dynamics and antibiotic resistance genes reduction during anaerobic digestion of swine manure. Bioresour Technol 245:850–859

    CAS  Google Scholar 

  148. Neshat SA, Mohammadi M, Najafpour GD, Lahijani P (2017) Anaerobic co-digestion of animal manures and lignocellulosic residues as a potent approach for sustainable biogas production. Renew Sustain Energy Rev 79:308–322

    CAS  Google Scholar 

  149. Sun W, Gu J, Wang X, Qian X, Peng H (2019) Solid-state anaerobic digestion facilitates the removal of antibiotic resistance genes and mobile genetic elements from cattle manure. Bioresour Technol 274:287–295

    CAS  Google Scholar 

  150. Zhang H, Chang F, Shi P, Ye L, Zhou Q, Pan Y, Li A (2019) Antibiotic resistome alteration by different disinfection strategies in a full-scale drinking water treatment plant deciphered by metagenomic assembly. Environ Sci Technol 53:2141–2150

    CAS  Google Scholar 

  151. Dodd MC (2012) Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. J Environ Monit 14:1754–1771

    CAS  Google Scholar 

  152. Guo M-T, Yuan Q-B, Yang J (2015) Distinguishing effects of ultraviolet exposure and chlorination on the horizontal transfer of antibiotic resistance genes in municipal wastewater. Environ Sci Technol 49:5771–5778

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China

    Fang Wang

  2. University of Chinese Academy of Sciences, Beijing, China

    Fang Wang

  3. Department of Plant, Soil and Microbial Sciences, Center for Microbial Ecology, Michigan State University, East Lansing, MI, USA

    James M. Tiedje

Authors
  1. Fang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James M. Tiedje
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fang Wang .

Editor information

Editors and Affiliations

  1. Universidade Católica Portuguesa, Porto, Portugal

    Célia M. Manaia

  2. University of South Australia, South Australia, Australia

    Erica Donner

  3. Universidade Católica Portuguesa, Porto, Portugal

    Ivone Vaz-Moreira

  4. King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia

    Peiying Hong

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Wang, F., Tiedje, J.M. (2020). Antibiotic Resistance in Soil. In: Manaia, C., Donner, E., Vaz-Moreira, I., Hong, P. (eds) Antibiotic Resistance in the Environment . The Handbook of Environmental Chemistry, vol 91. Springer, Cham. https://doi.org/10.1007/698_2020_562

Download citation

Publish with us

Policies and ethics

Search

Navigation