Skip to main content
SpringerLink
Log in

Sources of Antibiotic Resistant Bacteria (ARB) and Antibiotic Resistance Genes (ARGs) in the Soil: A Review of the Spreading Mechanism and Human Health Risks

  • Chapter
  • First Online:
Reviews of Environmental Contamination and Toxicology Volume 256

Part of the book series: Reviews of Environmental Contamination and Toxicology ((RECT,volume 256))

Abstract

Soil is an essential part of our ecosystem and plays a crucial role as a nutrient source, provides habitat for plants and other organisms. Overuse of antibiotics has accelerated the development and dissemination of antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARGs). ARB and ARGs are recognized as emerging environmental contaminants causing soil pollution and serious risks to public health. ARB and ARGs are discharged into soils through several pathways. Application of manure in agriculture is one of the primary sources of ARB and ARGs dissemination in the soil. Different sources of contamination by ARB and ARGs were reviewed and analyzed as well as dissemination mechanisms in the soil. The effects of ARB and ARGs on soil bacterial community were evaluated. Furthermore, the impact of different sources of manure on soil microbial diversity as well as the effect of antibiotics on the development of ARB and ARGs in soils was analyzed. Human health risk assessments associated with the spreading of ARB and ARGs in soils were investigated. Finally, recommendations and mitigation strategies were proposed.

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 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 139.99
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

Abbreviations

AS:

Activated sludge

ARB:

Antibiotic resistant bacteria

ARs:

Antibiotic resistomes

EECs:

Emerging environmental contaminants

HGT:

Horizontal gene transfer

LGT:

Lateral gene transfer

MGEs:

Mobile genetic elements

SS:

Sewage sludge

WWTPs:

Wastewater treatment plants

AMRs:

Antimicrobial resistances

STPs:

Sludge treatment plants

References

  • Aarestrup FM, Wegener HC, Collignon P (2008) Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev Anti-Infect Ther 6(5):733–750

    Article  Google Scholar 

  • Ågerstrand M, Berg C, Björlenius B, Breitholtz M, Brunström Br, Fick J, Gunnarsson L, Larsson DJ, Sumpter JP, Tysklind M (2015) Improving environmental risk assessment of human pharmaceuticals. Environ Sci Technol 49(9):5336–5345

    Article  Google Scholar 

  • Ahmed S, Ibrahim M, Waheed R, Azdee ABH, Hashmi MZ, Ahmed S (2017) Genotoxicity and biochemical toxicity of soil antibiotics to earthworms. In: Antibiotics and antibiotics resistance genes in soils. Springer, Cham, pp 327–340

    Chapter  Google Scholar 

  • Almakki A, Jumas-Bilak E, Marchandin H, Licznar-Fajardo P (2019) Antibiotic resistance in urban runoff. Sci Total Environ 667:64–76

    Article  CAS  Google Scholar 

  • Aminov RI (2009) The role of antibiotics and antibiotic resistance in nature. Environ Microbiol 11(12):2970–2988

    Article  CAS  Google Scholar 

  • Arun S, Mukhopadhyay M, Chakraborty P (2017) A review on antibiotics consumption, physico-chemical properties and their sources in Asian soil. In: Antibiotics and antibiotics resistance genes in soils. Springer, Cham, pp 39–53

    Chapter  Google Scholar 

  • Austin D, Anderson R (1999) Studies of antibiotic resistance within the patient, hospitals and the community using simple mathematical models. Philos Trans R Soc Lond B Biol Sci 354(1384):721–738

    Article  CAS  Google Scholar 

  • Bassil RJ, Bashour II, Sleiman FT, Abou-Jawdeh YA (2013) Antibiotic uptake by plants from manure-amended soils. J Environ Sci Health B 48(7):570–574

    Article  CAS  Google Scholar 

  • Berglund B (2015) Environmental dissemination of antibiotic resistance genes and correlation to anthropogenic contamination with antibiotics. Infect Ecol Epidemiol 5(1):28564

    Google Scholar 

  • Boxall AB, Fogg LA, Kay P, Blackwel PA, Pemberton EJ, Croxford A (2003a) Prioritisation of veterinary medicines in the UK environment. Toxicol Lett 142(3):207–218

    Article  CAS  Google Scholar 

  • Boxall AB, Kolpin DW, Halling-Sørensen B, Tolls J (2003b) Peer reviewed: are veterinary medicines causing environmental risks? ACS Publications, Washington

    Google Scholar 

  • Breazeal MVR, Novak JT, Vikesland PJ, Pruden A (2013) Effect of wastewater colloids on membrane removal of antibiotic resistance genes. Water Res 47(1):130–140

    Article  Google Scholar 

  • Burkhardt M, Stamm C, Waul C, Singer H, Müller S (2005) Surface runoff and transport of sulfonamide antibiotics and tracers on manured grassland. J Environ Qual 34(4):1363–1371

    Article  CAS  Google Scholar 

  • Cao Y, Chang Z, Wang J, Ma Y, Fu G (2013) The fate of antagonistic microorganisms and antimicrobial substances during anaerobic digestion of pig and dairy manure. Bioresour Technol 136:664–671

    Article  CAS  Google Scholar 

  • Chee-Sanford JC, Aminov RI, Krapac I, 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(4):1494–1502

    Article  CAS  Google Scholar 

  • Chee-Sanford J, Mackie R, Koike S, Krapac I, Maxwell S, Lin YF, Aminov R (2009a) Fate and transport of antibiotic residues and antibiotic resistance genetic determinants during manure storage, treatment, and land application. J Environ Qual 38:1086–1108

    Article  CAS  Google Scholar 

  • Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin Y-F, Yannarell AC, Maxwell S, Aminov RI (2009b) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38(3):1086–1108

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chen B, Liang X, Huang X, Zhang T, Li X (2013) Differentiating anthropogenic impacts on ARGs in the Pearl River estuary by using suitable gene indicators. Water Res 47(8):2811–2820

    Article  CAS  Google Scholar 

  • Chen C, Li J, Chen P, Ding R, Zhang P, Li X (2014) Occurrence of antibiotics and antibiotic resistances in soils from wastewater irrigation areas in Beijing and Tianjin, China. Environ Pollut 193:94–101

    Article  CAS  Google Scholar 

  • Chen Q-L, An X-L, Li H, Zhu Y-G, Su J-Q, Cui L (2017) Do manure-borne or indigenous soil microorganisms influence the spread of antibiotic resistance genes in manured soil? Soil Biol Biochem 114:229–237

    Article  CAS  Google Scholar 

  • Chen C, Pankow CA, Oh M, Heath LS, Zhang L, Du P, Xia K, Pruden A (2019a) 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

    Article  CAS  Google Scholar 

  • Chen Z, Zhang W, Yang L, Stedtfeld RD, Peng A, Gu C, Boyd SA, Li H (2019b) Antibiotic resistance genes and bacterial communities in cornfield and pasture soils receiving swine and dairy manures. Environ Pollut 248:947–957

    Article  CAS  Google Scholar 

  • 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(7365):457–461

    Article  Google Scholar 

  • Davis J, Truman C, Kim S, Ascough J, Carlson K (2006) Antibiotic transport via runoff and soil loss. J Environ Qual 35(6):2250–2260

    Article  CAS  Google Scholar 

  • Ding GC, Radl V, Schloter-Hai B, Jechalke S, Heuer H, Smalla K, Schloter M (2014) Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS One 9(3):e92958

    Google Scholar 

  • Dungan RS, McKinney CW, Leytem AB (2018) Tracking antibiotic resistance genes in soil irrigated with dairy wastewater. Sci Total Environ 635:1477–1483

    Article  CAS  Google Scholar 

  • Fatta-Kassinos D, Kalavrouziotis I, Koukoulakis P, Vasquez M (2011a) The risks associated with wastewater reuse and xenobiotics in the agroecological environment. Sci Total Environ 409(19):3555–3563

    Article  CAS  Google Scholar 

  • Fatta-Kassinos D, Meric S, Nikolaou A (2011b) Pharmaceutical residues in environmental waters and wastewater: current state of knowledge and future research. Anal Bioanal Chem 399(1):251–275

    Article  CAS  Google Scholar 

  • Fick J, Söderström H, Lindberg RH, Phan C, Tysklind M, Larsson DJ (2009) Contamination of surface, ground, and drinking water from pharmaceutical production. Environ Toxicol Chem 28(12):2522–2527

    Article  CAS  Google Scholar 

  • Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, Dantas G (2014a) Bacterial phylogeny structures soil resistomes across habitats. Nature 509(7502):612

    Article  CAS  Google Scholar 

  • Forsberg Z, Mackenzie AK, Sørlie M, Røhr ÅK, Helland R, Arvai AS, Vaaje-Kolstad G, Eijsink VG (2014b) Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases. Proc Natl Acad Sci 111(23):8446–8451

    Article  CAS  Google Scholar 

  • Gao P, Mao D, Luo Y, Wang L, Xu B, Xu L (2012) Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res 46(7):2355–2364

    Article  CAS  Google Scholar 

  • Garner E, Benitez R, von Wagoner E, Sawyer R, Schaberg E, Hession WC, Krometis L-AH, Badgley BD, Pruden A (2017) Stormwater loadings of antibiotic resistance genes in an urban stream. Water Res 123:144–152

    Article  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(6):3529–3538

    Article  CAS  Google Scholar 

  • Graham DW, Bergeron G, Bourassa MW, Dickson J, Gomes F, Howe A, Kahn LH, Morley PS, Scott HM, Simjee S (2019) Complexities in understanding antimicrobial resistance across domesticated animal, human, and environmental systems. Ann N Y Acad Sci 1441(1):17

    Article  Google Scholar 

  • Grenni P, Ancona V, Caracciolo AB (2018) Ecological effects of antibiotics on natural ecosystems: a review. Microchem J 136:25–39

    Article  CAS  Google Scholar 

  • Guo C, Wang K, Hou S, Wan L, Lv J, Zhang Y, Qu X, Chen S, Xu J (2017) H2O2 and/or TiO2 photocatalysis under UV irradiation for the removal of antibiotic resistant bacteria and their antibiotic resistance genes. J Hazard Mater 323:710–718

    Article  CAS  Google Scholar 

  • Hashmi MZ, Mahmood A, Kattel DB, Khan S, Hasnain A, Ahmed Z (2017) Antibiotics and antibiotic resistance genes (ARGs) in soil: occurrence, fate, and effects. In: Xenobiotics in the soil environment. Springer, Cham, pp 41–54

    Chapter  Google Scholar 

  • Ho YB, Zakaria MP, Latif PA, Saari N (2014) Environmental risk assessment for veterinary antibiotics and hormone in Malaysian agricultural soil. Iran J Public Health 43(Supple 3):67–71

    Google Scholar 

  • Holten Lützhøft H-C, Vaes WH, Freidig AP, Halling-Sørensen B, Hermens JL (2000) Influence of pH and other modifying factors on the distribution behavior of 4-quinolones to solid phases and humic acids studied by “negligible-depletion” SPME− HPLC. Environ Sci Technol 34(23):4989–4994

    Article  Google Scholar 

  • Hu X, Zhou Q, 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(9):2992–2998

    Article  CAS  Google Scholar 

  • Iversen A, Kühn I, Franklin A, Möllby R (2002) High prevalence of vancomycin-resistant enterococci in Swedish sewage. Appl Environ Microbiol 68(6):2838–2842

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kay P, Blackwell PA, Boxall AB (2005) Column studies to investigate the fate of veterinary antibiotics in clay soils following slurry application to agricultural land. Chemosphere 60(4):497–507

    Article  CAS  Google Scholar 

  • Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8(1):1–13

    Article  CAS  Google Scholar 

  • Knapp CW, Dolfing J, Ehlert PA, Graham DW (2010a) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44(2):580–587

    Article  CAS  Google Scholar 

  • Knapp CW, Zhang W, Sturm BS, Graham DW (2010b) Differential fate of erythromycin and beta-lactam resistance genes from swine lagoon waste under different aquatic conditions. Environ Pollut 158(5):1506–1512

    Article  CAS  Google Scholar 

  • Knapp CW, McCluskey SM, Singh BK, Campbell CD, Hudson G, Graham DW (2011) Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils. PLoS One 6(11):e27300

    Article  CAS  Google Scholar 

  • Knapp CW, Callan AC, Aitken B, Shearn R, Koenders A, Hinwood A (2017) Relationship between antibiotic resistance genes and metals in residential soil samples from Western Australia. Environ Sci Pollut Res 24(3):2484–2494

    Article  CAS  Google Scholar 

  • Koike S, Krapac I, Oliver H, Yannarell A, Chee-Sanford J, Aminov R, 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(15):4813–4823

    Article  CAS  Google Scholar 

  • Kovalova L, Siegrist H, Singer H, Wittmer A, McArdell CS (2012) Hospital wastewater treatment by membrane bioreactor: performance and efficiency for organic micropollutant elimination. Environ Sci Technol 46(3):1536–1545

    Article  CAS  Google Scholar 

  • Kreuzig R, Höltge S (2005) Investigations on the fate of sulfadiazine in manured soil: laboratory experiments and test plot studies. Environ Toxicol Chem Int J 24(4):771–776

    Article  CAS  Google Scholar 

  • Kristiansson E, Fick J, Janzon A, Grabic R, Rutgersson C, Weijdegård B, Söderström H, Larsson DJ (2011) Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS One 6(2):e17038

    Article  CAS  Google Scholar 

  • Kumar K, Gupta SC, Chander Y, Singh AK (2005) Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron 87:1–54

    Article  CAS  Google Scholar 

  • Kurwadkar ST, Adams CD, Meyer MT, Kolpin DW (2007) Effects of sorbate speciation on sorption of selected sulfonamides in three loamy soils. J Agric Food Chem 55(4):1370–1376

    Article  CAS  Google Scholar 

  • LaPara TM, Burch TR, McNamara PJ, Tan DT, Yan M, Eichmiller JJ (2011) Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into Duluth-Superior Harbor. Environ Sci Technol 45(22):9543–9549

    Article  CAS  Google Scholar 

  • Larsson DJ, de Pedro C, Paxeus N (2007) Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J Hazard Mater 148(3):751–755

    Article  CAS  Google Scholar 

  • Latare A, Kumar O, Singh S, Gupta A (2014) Direct and residual effect of sewage sludge on yield, heavy metals content and soil fertility under rice–wheat system. Ecol Eng 69:17–24

    Article  Google Scholar 

  • Lebreton F, Manson AL, Saavedra JT, Straub TJ, Earl AM, Gilmore MS (2017) Tracing the enterococci from Paleozoic origins to the hospital. Cell 169(5):849–861.e13

    Article  CAS  Google Scholar 

  • Lee S, Suits M, Wituszynski D, Winston R, Martin J, Lee J (2020) Residential urban stormwater runoff: a comprehensive profile of microbiome and antibiotic resistance. Sci Total Environ 723:138033

    Article  CAS  Google Scholar 

  • Levy S, Marshall B, Schluederberg S, Rowse D, Davis J (1988) High frequency of antimicrobial resistance in human fecal flora. Antimicrob Agents Chemother 32(12):1801–1806

    Article  CAS  Google Scholar 

  • Li D, Yang M, Hu J, Zhang J, Liu R, Gu X, Zhang Y, Wang Z (2009) Antibiotic-resistance profile in environmental bacteria isolated from penicillin production wastewater treatment plant and the receiving river. Environ Microbiol 11(6):1506–1517

    Article  CAS  Google Scholar 

  • Li D, Yu T, Zhang Y, Yang M, Li Z, Liu M, Qi R (2010) Antibiotic resistance characteristics of environmental bacteria from an oxytetracycline production wastewater treatment plant and the receiving river. Appl Environ Microbiol 76(11):3444–3451

    Article  CAS  Google Scholar 

  • Li B, Sun J-Y, Liu Q-Z, Han L-Z, Huang X-H, Ni Y-X (2011) High prevalence of CTX-M β-lactamases in faecal Escherichia coli strains from healthy humans in Fuzhou, China. Scand J Infect Dis 43(3):170–174

    Article  CAS  Google Scholar 

  • Li N, Sheng G-P, Lu Y-Z, Zeng RJ, Yu H-Q (2017) Removal of antibiotic resistance genes from wastewater treatment plant effluent by coagulation. Water Res 111:204–212

    Article  CAS  Google Scholar 

  • Liu H, Zhou X, Huang H, Zhang J (2019) Prevalence of antibiotic resistance genes and their association with antibiotics in a wastewater treatment plant: process distribution and analysis. Water 11(12):2495

    Article  CAS  Google Scholar 

  • Lloret E, Pascual JA, Brodie EL, Bouskill NJ, Insam H, Juárez MF-D, Goberna M (2016) Sewage sludge addition modifies soil microbial communities and plant performance depending on the sludge stabilization process. Appl Soil Ecol 101:37–46

    Article  Google Scholar 

  • Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP, Stedtfeld RD, Sul WJ, Stedtfeld TM, Chai B, Cole JR (2012) In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci 109(5):1691–1696

    Article  CAS  Google Scholar 

  • Lucas D, Badia-Fabregat M, Vicent T, Caminal G, Rodríguez-Mozaz S, Balcázar J, Barceló D (2016) Fungal treatment for the removal of antibiotics and antibiotic resistance genes in veterinary hospital wastewater. Chemosphere 152:301–308

    Article  CAS  Google Scholar 

  • Luo Y, Mao D, Rysz M, Zhou Q, Zhang H, Xu L, Alvarez JJ, P. (2010) Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environ Sci Technol 44(19):7220–7225

    Article  Google Scholar 

  • Martín J, Santos JL, Aparicio I, Alonso E (2015) Pharmaceutically active compounds in sludge stabilization treatments: anaerobic and aerobic digestion, wastewater stabilization ponds and composting. Sci Total Environ 503:97–104

    Article  Google Scholar 

  • Martínez JL, Coque TM, Baquero F (2015) What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol 13(2):116–123

    Article  Google Scholar 

  • McGrath JW, Hammerschmidt F, Quinn JP (1998) Biodegradation of phosphonomycin by rhizobium huakuii PMY1. Appl Environ Microbiol 64(1):356–358

    Article  CAS  Google Scholar 

  • McKinney CW, Loftin KA, Meyer MT, Davis JG, Pruden A (2010) Tet and sul antibiotic resistance genes in livestock lagoons of various operation type, configuration, and antibiotic occurrence. Environ Sci Technol 44(16):6102–6109

    Article  CAS  Google Scholar 

  • McLain JE, Williams CF (2010) Development of antibiotic resistance in bacteria of soils irrigated with reclaimed wastewater. In: 5th National Decennial Irrigation Conference Proceedings, 5–8 December 2010, Phoenix convention Center, Phoenix, Arizona USA. American Society of Agricultural and Biological Engineers, Michigan, p 1

    Google Scholar 

  • Michael I, Rizzo L, McArdell C, Manaia C, Merlin C, Schwartz T, Dagot C, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: a review. Water Res 47(3):957–995

    Article  CAS  Google Scholar 

  • Michelini L, Gallina G, Capolongo F, Ghisi R (2014) Accumulation and response of willow plants exposed to environmental relevant sulfonamide concentrations. Int J Phytoremediation 16(9):947–961

    Article  CAS  Google Scholar 

  • Munir M, Xagoraraki I (2011) Levels of antibiotic resistance genes in manure, biosolids, and fertilized soil. J Environ Qual 40(1):248–255

    Article  CAS  Google Scholar 

  • Munir M, Wong K, Xagoraraki I (2011) Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Res 45(2):681–693

    Article  CAS  Google Scholar 

  • Nathan SS, Chung PG, Murugan K (2004) Effect of botanical insecticides and bacterial toxins on the gut enzyme of the rice leaffolderCnaphalocrocis medinalis. Phytoparasitica 32(5):433

    Article  CAS  Google Scholar 

  • Negreanu Y, Pasternak Z, Jurkevitch E, Cytryn E (2012) Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environ Sci Technol 46(9):4800–4808

    Article  CAS  Google Scholar 

  • 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(4):913–930

    Article  Google Scholar 

  • Nesme J, Topp E, Simonet P (2015) Antibiotic resistance genes mobility and dissemination during a long-term experiment: fifteen years of farm-soil amendment with antibiotics analyzed with high-throughput sequencing. Indo-French Workshop on Environmental Biotechnology (Molecular Ecology & Environmental Engineering)

    Google Scholar 

  • Novo A, Manaia CM (2010) Factors influencing antibiotic resistance burden in municipal wastewater treatment plants. Appl Microbiol Biotechnol 87(3):1157–1166

    Article  CAS  Google Scholar 

  • Nwosu VC (2001) Antibiotic resistance with particular reference to soil microorganisms. Res Microbiol 152(5):421–430

    Article  CAS  Google Scholar 

  • Oliver JP, Gooch CA, Lansing S, Schueler J, Hurst JJ, Sassoubre L, Crossette EM, Aga DS (2020) Invited review: fate of antibiotic residues, antibiotic-resistant bacteria, and antibiotic resistance genes in US dairy manure management systems. J Dairy Sci 103(2):1051–1071

    Article  CAS  Google Scholar 

  • Pan M, Chu L (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

    Article  CAS  Google Scholar 

  • Pehrsson EC, Tsukayama P, Patel S, Mejía-Bautista M, Sosa-Soto G, Navarrete KM, Calderon M, Cabrera L, Hoyos-Arango W, Bertoli MT (2016a) Interconnected microbiomes and resistomes in low-income human habitats. Nature 533(7602):212

    Article  CAS  Google Scholar 

  • Pehrsson SJ, Eglington BM, Evans DA, Huston D, Reddy SM (2016b) Metallogeny and its link to orogenic style during the Nuna supercontinent cycle. Geol Soc Lond, Spec Publ 424(1):83–94

    Article  Google Scholar 

  • Peng S, Feng Y, Wang Y, Guo X, Chu H, Lin X (2017) Prevalence of antibiotic resistance genes in soils after continually applied with different manure for 30 years. J Hazard Mater 340:16–25

    Article  CAS  Google Scholar 

  • Pepper IL, Brooks JP, Gerba CP (2018) Antibiotic resistant bacteria in municipal wastes: is there reason for concern? Environ Sci Technol 52(7):3949–3959

    Article  CAS  Google Scholar 

  • Perry J, Wright G (2013) The antibiotic resistance “mobilome”: searching for the link between environment and clinic. Front Microbiol 4:138

    Article  Google Scholar 

  • Perry JA, Westman EL, Wright GD (2014) The antibiotic resistome: what’s new? Curr Opin Microbiol 21:45–50

    Article  CAS  Google Scholar 

  • Petrie B, Barden R, Kasprzyk-Hordern B (2015) A review on emerging contaminants in wastewaters and the environment: current knowledge, understudied areas and recommendations for future monitoring. Water Res 72:3–27

    Article  CAS  Google Scholar 

  • Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 40(23):7445–7450

    Article  CAS  Google Scholar 

  • Pruden A, Larsson DG, Amézquita 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(8):878–885

    Google Scholar 

  • Qian X, Gu J, Sun W, Wang X-J, Su J-Q, Stedfeld R (2018) Diversity, abundance, and persistence of antibiotic resistance genes in various types of animal manure following industrial composting. J Hazard Mater 344:716–722

    Article  CAS  Google Scholar 

  • Renou S, Givaudan J, Poulain S, Dirassouyan F, Moulin P (2008) Landfill leachate treatment: review and opportunity. J Hazard Mater 150(3):468–493

    Article  CAS  Google Scholar 

  • Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360

    Article  CAS  Google Scholar 

  • Roig N, Sierra J, Martí E, Nadal M, Schuhmacher M, Domingo JL (2012) Long-term amendment of Spanish soils with sewage sludge: effects on soil functioning. Agric Ecosyst Environ 158:41–48

    Article  Google Scholar 

  • Sabri N, Schmitt H, Van der Zaan B, Gerritsen H, Zuidema T, Rijnaarts H, Langenhoff A (2020) Prevalence of antibiotics and antibiotic resistance genes in a wastewater effluent-receiving river in the Netherlands. J Environ Chem Eng 8(1):102245

    Article  CAS  Google Scholar 

  • 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(7):587–595

    Article  Google Scholar 

  • Séveno NA, Kallifidas D, Smalla K, van Elsas JD, Collard J-M, Karagouni AD, Wellington EM (2002) Occurrence and reservoirs of antibiotic resistance genes in the environment. Rev Med Microbiol 13(1):15–27

    Article  Google Scholar 

  • Singh RP, Singh P, Ibrahim MH, Hashim R (2012) Land application of sewage sludge: physicochemical and microbial response. In: Reviews of environmental contamination and toxicology. Springer, Cham, pp 41–61

    Chapter  Google Scholar 

  • Smith MS, Yang RK, Knapp CW, Niu Y, Peak N, Hanfelt MM, Galland JC, Graham DW (2004) Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl Environ Microbiol 70(12):7372–7377

    Article  CAS  Google Scholar 

  • Storteboom HN, Kim S-C, Doesken KC, Carlson KH, Davis JG, Pruden A (2007) Response of antibiotics and resistance genes to high-intensity and low-intensity manure management. J Environ Qual 36(6):1695–1703

    Article  CAS  Google Scholar 

  • Storteboom H, Arabi M, Davis J, Crimi B, Pruden A (2010) Identification of antibiotic-resistance-gene molecular signatures suitable as tracers of pristine river, urban, and agricultural sources. Environ Sci Technol 44(6):1947–1953

    Article  CAS  Google Scholar 

  • Sui Q, Zhang J, Chen M, Tong J, Wang R, Wei Y (2016) Distribution of antibiotic resistance genes (ARGs) in anaerobic digestion and land application of swine wastewater. Environ Pollut 213:751–759

    Article  CAS  Google Scholar 

  • Taylor V-J, Verner-Jeffreys DW, Baker-Austin C (2011) Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance. Trends Ecol Evol 26:278–284

    Article  Google Scholar 

  • Thevenon F, Adatte T, Wildi W, Poté J (2012) Antibiotic resistant bacteria/genes dissemination in lacustrine sediments highly increased following cultural eutrophication of Lake Geneva (Switzerland). Chemosphere 86(5):468–476

    Article  CAS  Google Scholar 

  • Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils–a review. J Plant Nutr Soil Sci 166(2):145–167

    Article  CAS  Google Scholar 

  • Urra J, Alkorta I, Mijangos I, Epelde L, Garbisu C (2019) Application of sewage sludge to agricultural soil increases the abundance of antibiotic resistance genes without altering the composition of prokaryotic communities. Sci Total Environ 647:1410–1420

    Article  CAS  Google Scholar 

  • Vaz-Moreira I, Varela AR, Pereira TV, Fochat RC, Manaia CM (2016) Multidrug resistance in quinolone-resistant gram-negative bacteria isolated from hospital effluent and the municipal wastewater treatment plant. Microb Drug Resist 22(2):155–163

    Article  CAS  Google Scholar 

  • Wallace JS, Garner E, Pruden A, Aga DS (2018) Occurrence and transformation of veterinary antibiotics and antibiotic resistance genes in dairy manure treated by advanced anaerobic digestion and conventional treatment methods. Environ Pollut 236:764–772

    Article  CAS  Google Scholar 

  • Wang FH, Qiao M, Chen Z, Su JQ, Zhu YG (2015) Antibiotic resistance genes in manure-amended soil and vegetables at harvest. J Hazard Mater 299:215–221

    Article  CAS  Google Scholar 

  • Wang F, Stedtfeld RD, Kim O-S, Chai B, Yang L, Stedtfeld TM, Hong SG, Kim D, Lim HS, Hashsham SA (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

    Article  CAS  Google Scholar 

  • Wang M, Shen W, Yan L, Wang X-H, Xu H (2017) Stepwise impact of urban wastewater treatment on the bacterial community structure, antibiotic contents, and prevalence of antimicrobial resistance. Environ Pollut 231:1578–1585

    Article  CAS  Google Scholar 

  • Wang M, Liu P, Xiong W, Zhou Q, Wangxiao J, Zeng Z, Sun Y (2018) Fate of potential indicator antimicrobial resistance genes (ARGs) and bacterial community diversity in simulated manure-soil microcosms. Ecotoxicol Environ Saf 147:817–823

    Article  CAS  Google Scholar 

  • Wen X, Mi J, Wang Y, Ma B, Zou Y, Liao X, Liang JB, Wu Y (2019) Occurrence and contamination profiles of antibiotic resistance genes from swine manure to receiving environments in Guangdong Province southern China. Ecotoxicol Environ Saf 173:96–102

    Article  CAS  Google Scholar 

  • Wenzel RP, Edmond MB (2000) Managing antibiotic resistance. Mass Medical Society, Waltham

    Book  Google Scholar 

  • Winckler C, Grafe A (2001) Use of veterinary drugs in intensive animal production. J Soils Sediments 1(2):66

    Article  CAS  Google Scholar 

  • 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(18):6933–6939

    Article  CAS  Google Scholar 

  • Yang Y, Li B, Zou S, Fang HH, Zhang T (2014) Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res 62:97–106

    Article  CAS  Google Scholar 

  • Zervos MJ, Hershberger E, Nicolau DP, Ritchie DJ, Blackner LK, Coyle EA, Donnelly AJ, Eckel SF, Eng RH, Hiltz A (2003) Relationship between fluoroquinolone use and changes in susceptibility to fluoroquinolones of selected pathogens in 10 United States teaching hospitals, 1991–2000. Clin Infect Dis 37(12):1643–1648

    Article  CAS  Google Scholar 

  • 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(18):7771–7779

    Article  CAS  Google Scholar 

  • Zhang C, Li Y, Wang C, Niu L, Cai W (2016) Occurrence of endocrine disrupting compounds in aqueous environment and their bacterial degradation: a review. Crit Rev Environ Sci Technol 46(1):1–59

    Article  CAS  Google Scholar 

  • Zhao X, Wang J, Zhu L, Ge W, Wang J (2017) Environmental analysis of typical antibiotic-resistant bacteria and ARGs in farmland soil chronically fertilized with chicken manure. Sci Total Environ 593:10–17

    Article  Google Scholar 

  • Zhou Y, Niu L, Zhu S, Lu H, Liu W (2017) Occurrence, abundance, and distribution of sulfonamide and tetracycline resistance genes in agricultural soils across China. Sci Total Environ 599:1977–1983

    Article  Google Scholar 

  • Zhu Y-G, Johnson TA, Su J-Q, Qiao M, Guo G-X, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci 110(9):3435–3440

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation of China (No. 31570504), the Natural Science Foundation of Tianjin (No. 16JCYBJC22900), and the Ministry of Education of China as an innovative team project (grant No. IRT13024).

Declaration

The authors declare no conflict of interests regarding this paper.

Credit Authorship Contribution

Brim Stevy Ondon: Conceptualization, Methodology, Software, Writing, review and editing – Original draft. Shengnan Li: Software and review. Qixing Zhou: Review and editing. Fengxiang Li: Supervision, Writing – review and editing, Project administration.

Author information

Authors and Affiliations

  1. Key Laboratory of Pollution Processes and Environmental Criteria at Ministry of Education, Tianjin Key Laboratory of Environmental Remediation and Pollution Control, College of Environmental Science and Engineering, Nankai University, Tianjin, People’s Republic of China

    Brim Stevy Ondon, Shengnan Li, Qixing Zhou & Fengxiang Li

Authors
  1. Brim Stevy Ondon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shengnan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qixing Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fengxiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fengxiang Li .

Editor information

Editors and Affiliations

  1. University of Amsterdam, Amsterdam, The Netherlands

    Pim de Voogt

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ondon, B.S., Li, S., Zhou, Q., Li, F. (2021). Sources of Antibiotic Resistant Bacteria (ARB) and Antibiotic Resistance Genes (ARGs) in the Soil: A Review of the Spreading Mechanism and Human Health Risks. In: de Voogt, P. (eds) Reviews of Environmental Contamination and Toxicology Volume 256. Reviews of Environmental Contamination and Toxicology, vol 256. Springer, Cham. https://doi.org/10.1007/398_2020_60

Download citation

Publish with us

Policies and ethics

Search

Navigation