Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 10, pp 9283–9292 | Cite as

The influence of heavy metals, polyaromatic hydrocarbons, and polychlorinated biphenyls pollution on the development of antibiotic resistance in soils

  • Andrey Vladimirovich Gorovtsov
  • Ivan Sergeevich Sazykin
  • Marina Alexandrovna Sazykina
Review Article

Abstract

The minireview is devoted to the analysis of the influence of soil pollution with heavy metals, polyaromatic hydrocarbons (PAHs), and the polychlorinated biphenyls (PCBs) on the distribution of antibiotics resistance genes (ARGs) in soil microbiomes. It is shown that the best understanding of ARGs distribution process requires studying the influence of pollutants on this process in natural microbiocenoses. Heavy metals promote co-selection of genes determining resistance to them together with ARGs in the same mobile elements of a bacterial genome, but the majority of studies focus on agricultural soils enriched with ARGs originating from manure. Studying nonagricultural soils would clear mechanisms of ARGs transfer in natural and anthropogenically transformed environments and highlight the role of antibiotic-producing bacteria. PAHs make a considerable shift in soil microbiomes leading to an increase in the number of Actinobacteria which are the source of antibiotics formation and bear multiple ARGs. The soils polluted with PAHs can be a selective medium for bacteria resistant to antibiotics, and the level of ARGs expression is much higher. PCBs are accumulated in soils and significantly alter the specific structure of soil microbiocenoses. In such soils, representatives of the genera Acinetobacter, Pseudomonas, and Alcanivorax dominate, and the ability to degrade PCBs is connected to horizontal gene transfer (HGT) and high level of genomic plasticity. The attention is also focused on the need to study the properties of the soil having an impact on the bioavailability of pollutants and, as a result, on resistome of soil microorganisms.

Keywords

Antibiotic resistance Heavy metals Polyaromatic hydrocarbons Polychlorinated biphenyls Soil resistome 

Notes

Acknowledgements

This study was funded by the Ministry of Education and Science of the Russian Federation (grant № 6.2379.2017/PCh), Russian Foundation for Basic Research (grant № 17-04-00787 A), President of Russian Federation (grant № NSh-3464.2018.11).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adebusuyi AA, Foght JM (2011) An alternative physiological role for the EmhABC efflux pump in Pseudomonas fluorescens cLP6a. BMC Microbiol 11(1):252.  https://doi.org/10.1186/1471-2180-11-252 CrossRefGoogle Scholar
  2. Assiri AM, Banjar WM (2017) The strategic plan for combating antimicrobial resistance in gulf cooperation council states, KSA perspective. J Infect Public Health 10(5):485–486.  https://doi.org/10.1016/j.jiph.2016.09.013 CrossRefGoogle Scholar
  3. Balachandran C, Duraipandiyan V, Balakrishna K, Ignacimuthu S (2012) Petroleum and polycyclic aromatic hydrocarbons (PAHs) degradation and naphthalene metabolism in Streptomyces sp. (ERI-CPDA-1) isolated from oil-contaminated soil. Bioresour Technol 112:83–90.  https://doi.org/10.1016/j.biortech.2012.02.059 CrossRefGoogle Scholar
  4. Berg J, Tom-Petersen A, Nybroe O (2005) Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett Appl Microbiol 40(2):146–151.  https://doi.org/10.1111/j.1472-765X.2004.01650.x CrossRefGoogle Scholar
  5. Binková B, Šrám RJ (2004) The genotoxic effect of carcinogenic PAHs, their artificial and environmental mixtures (EOM) on human diploid lung fibroblasts. Mutat Res 547(1-2):109–121.  https://doi.org/10.1016/j.mrfmmm.2003.12.006 CrossRefGoogle Scholar
  6. Bisht S, Kumar V, Kumar M, Sharma S (2014) Innoculant technology in Populus deltoides rhizosphere for effective bioremediation of Polyaromatic hydrocarbons (PAHs) in contaminated soil, Northern India. Emir J Food and Agric 26(9):786.  https://doi.org/10.9755/ejfa.v26i9.18436 CrossRefGoogle Scholar
  7. Blanco A, Salazar MJ, Cid CV, Pignata ML, Rodriguez JH (2017) Accumulation of lead and associated metals (Cu and Zn) at different growth stages of soybean crops in lead-contaminated soils: food security and crop quality implications. Environ Earth Sci 76(4):182.  https://doi.org/10.1007/s12665-017-6508-x CrossRefGoogle Scholar
  8. Bosch C, Andersson A, Kruså M, Bandh C, Hovorková I, Klánová J, Knowles TD, Pancost RD, Evershed RP, Gustafsson O (2015) Source apportionment of polycyclic aromatic hydrocarbons in central European soils with compound-specific triple isotopes (δ13C, Δ14C, and δ2H). Environ Sci Technol 49(13):7657–7665.  https://doi.org/10.1021/acs.est.5b01190 CrossRefGoogle Scholar
  9. Burrus V, Waldor MK (2004) Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol 155(5):376–386.  https://doi.org/10.1016/j.resmic.2004.01.012 CrossRefGoogle Scholar
  10. Cabello FC, Godfrey HP (2016) Even therapeutic antimicrobial use in animal husbandry may generate environmental hazards to human health. Environ Microbiol 18(2):311–313.  https://doi.org/10.1111/1462-2920.13247 CrossRefGoogle Scholar
  11. Campbell JI, Jacobsen CS, Sørensen J (1995) Species variation and plasmid incidence among fluorescent Pseudomonas strains isolated from agricultural and industrial soils. FEMS Microbiol Lett 18(1):51–62.  https://doi.org/10.1111/j.1574-6941.1995.tb00163.x CrossRefGoogle Scholar
  12. Carraro N, Poulin D, Burrus V (2015) Replication and active partition of integrative and conjugative elements (ICEs) of the SXT/R391 family: the line between ICEs and conjugative plasmids is getting thinner. PLoS Genet 11(6):e1005298.  https://doi.org/10.1371/journal.pgen.1005298 CrossRefGoogle Scholar
  13. Chakraborty P, Zhang G, Li J, Selvaraj S, Breivik K, Jones KC (2016) Soil concentrations, occurrence, sources and estimation of air-soil exchange of polychlorinated biphenyls in Indian cities. Sci Total Environ 562:928–934.  https://doi.org/10.1016/j.scitotenv.2016.03.009 CrossRefGoogle Scholar
  14. Chapman JS (2003) Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeterior Biodegrad 51(4):271–276.  https://doi.org/10.1016/S0964-8305(03)00044-1 CrossRefGoogle Scholar
  15. Chaudhary P, Sharma R, Singh SB, Nain L (2011) Bioremediation of PAH by Streptomyces sp. Bull Environ Contam Toxicol 86(3):268–271.  https://doi.org/10.1007/s00128-011-0211-5 CrossRefGoogle Scholar
  16. Chen B, He R, Yuan K, Chen E, Lin L, Chen X, Sha S, Zhong J, Lin L, Yang L, Yang Y, Wang X, Zou S, Luan T (2017) Polycyclic aromatic hydrocarbons (PAHs) enriching antibiotic resistance genes (ARGs) in the soils. Environ Pollut 220(Pt B):1005–1013.  https://doi.org/10.1016/j.envpol.2016.11.047 CrossRefGoogle Scholar
  17. Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR, Schweizer HP (2001) Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob Agents Chemother 45(2):428–432.  https://doi.org/10.1128/AAC.45.2.428-432.2001 CrossRefGoogle Scholar
  18. D'costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science 311(5759):374–377.  https://doi.org/10.1126/science.1120800 CrossRefGoogle Scholar
  19. 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.  https://doi.org/10.1038/nature10388 CrossRefGoogle Scholar
  20. Degrendele C, Audy O, Hofman J, Kučerik J, Kukučka P, Mulder MD, Přibylová P, Prokeš R, Šáňka M, Schaumann GE, Lammel G (2016) Diurnal variations of air-soil exchange of semivolatile organic compounds (PAHs, PCBs, OCPs, and PBDEs) in a central European receptor area. Environ Sci Technol 50(8):4278–4288.  https://doi.org/10.1021/acs.est.5b05671 CrossRefGoogle Scholar
  21. Ding K, Wu Q, Wei H, Yang W, Séré G, Wang S, Echevarria G, Tang Y, Tao J, Morel JL, Qiu R (2018) Ecosystem services provided by heavy metal-contaminated soils in China. J Soils Sediments 18(2):380–390.  https://doi.org/10.1007/s11368-016-1547-6 CrossRefGoogle Scholar
  22. Dror I, Yaron B, Berkowitz B (2017) Microchemical contaminants as forming agents of anthropogenic soils. Ambio 46(1):109–120.  https://doi.org/10.1007/s13280-016-0804-7 CrossRefGoogle Scholar
  23. Duan M, Gu J, Wang X, Li Y, Li P, Yin Y (2017) Combined effects of compost containing sulfamethazine and zinc on pakchoi (Brassica chinensis L.) growth, soil sulfonamide resistance genes, and microbial communities. Arch Agron Soil Sci.  https://doi.org/10.1080/03650340.2017.1342033
  24. Fetzner S, Kolkenbrock S, Parschat K (2007) Catabolic linear plasmids. In: Meinhardt F, Klassen R (eds) Microbial linear plasmids. Springer, Berlin, pp 63–98.  https://doi.org/10.1007/7171_2007_091 CrossRefGoogle Scholar
  25. Field JA, Sierra-Alvarez R (2008) Microbial transformation and degradation of polychlorinated biphenyls. Environ Pollut 155(1):1–12.  https://doi.org/10.1016/j.envpol.2007.10.016 CrossRefGoogle Scholar
  26. Fuentes E, Wickham C, Carbajal C, Lopez C, Jauregui S, Lechler R, Kannan S (2017) Genesis of antibiotic resistance XXVII: action plan for global Union for Antibiotics Research and Development (GUARD) to mitigate AR pandemic (ARP). FASEB J 31:777–779Google Scholar
  27. Gardner CM, Gunsch CK (2017) Adsorption capacity of multiple DNA sources to clay minerals and environmental soil matrices less than previously estimated. Chemosphere 175:45–51.  https://doi.org/10.1016/j.chemosphere.2017.02.030 CrossRefGoogle Scholar
  28. Gillings MR (2014) Integrons: past, present, and future. Microbiol Mol Biol Rev 78(2):257–277.  https://doi.org/10.1128/MMBR.00056-13 CrossRefGoogle Scholar
  29. Giudice AL, Casella P, Bruni V, Michaud L (2013) Response of bacterial isolates from Antarctic shallow sediments towards heavy metals, antibiotics and polychlorinated biphenyls. Ecotoxicology 22(2):240–250.  https://doi.org/10.1007/s10646-012-1020-2 CrossRefGoogle Scholar
  30. Gorovtsov A, Rajput VD, Gorbov S, Vasilchenko N (2017) Bioindication-based approaches for sustainable management of urban ecosystems. In: Singh R, Kumar S (eds) Green technologies and environmental sustainability. Springer, Cham, pp 203–228.  https://doi.org/10.1007/978-3-319-50654-8_9 CrossRefGoogle Scholar
  31. Guo J, Li J, Chen H, Bond P, Yuan Z (2017) Metagenomic analysis reveals wastewater treatment plants as hotspots of antibiotic resistance genes and mobile genetic elements. Water Res 123:468–478.  https://doi.org/10.1016/j.watres.2017.07.002 CrossRefGoogle Scholar
  32. 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: Hashmi M, Kumar V, Varma A (eds) Xenobiotics in the soil environment. Springer International Publishing, Cham, pp 41–54.  https://doi.org/10.1007/978-3-319-47744-2_4 CrossRefGoogle Scholar
  33. Hearn EM, Dennis JJ, Gray MR, Foght JM (2003) Identification and characterization of the emhABC efflux system for polycyclic aromatic hydrocarbons in Pseudomonas fluorescens cLP6a. J Bacteriol 185(21):6233–6240.  https://doi.org/10.1128/JB.185.21.6233-6240.2003 CrossRefGoogle Scholar
  34. Hemala L, Zhang D, Margesin R (2014) Cold-active antibacterial and antifungal activities and antibiotic resistance of bacteria isolated from an alpine hydrocarbon-contaminated industrial site. Res Microbiol 165(6):447–456.  https://doi.org/10.1016/j.resmic.2014.05.035 CrossRefGoogle Scholar
  35. Hsu TTD, Mitsch WJ, Martin JF, Lee J (2017) Towards sustainable protection of public health: the role of an urban wetland as a frontline safeguard of pathogen and antibiotic resistance spread. Ecol Eng.  https://doi.org/10.1016/j.ecoleng.2017.02.051
  36. Hu HW, Wang JT, Li J, Shi XZ, Ma YB, Chen D, He JZ (2017) Long-term nickel contamination increases the occurrence of antibiotic resistance genes in agricultural soils. Environ Sci Technol 51(2):790–800.  https://doi.org/10.1021/acs.est.6b03383 CrossRefGoogle Scholar
  37. Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68(1):167–182.  https://doi.org/10.1093/bmb/ldg032 CrossRefGoogle Scholar
  38. 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 235-236:178–185.  https://doi.org/10.1016/j.jhazmat.2012.07.040 CrossRefGoogle Scholar
  39. Jiang Y, Wang X, Zhu K, Wu M, Sheng G, Fu J (2011) Polychlorinated biphenyls contamination in urban soil of shanghai: level, compositional profiles and source identification. Chemosphere 83(6):767–773.  https://doi.org/10.1016/j.chemosphere.2011.02.077 CrossRefGoogle Scholar
  40. Jiang X, Ellabaan MMH, Charusanti P, Munck C, Blin K, Tong Y, Weber T, Sommer MOA, Lee SY (2017) Dissemination of antibiotic resistance genes from antibiotic producers to pathogens. Nat Commun 8:15784.  https://doi.org/10.1038/ncomms15784 CrossRefGoogle Scholar
  41. Kang F, Hu X, Liu J, Gao Y (2015) Noncovalent binding of polycyclic aromatic hydrocarbons with genetic bases reducing the in vitro lateral transfer of antibiotic resistant genes. Environ Sci Technol l49:10340–10348CrossRefGoogle Scholar
  42. 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 Int 24(3):2484–2494.  https://doi.org/10.1007/s11356-016-7997-y CrossRefGoogle Scholar
  43. Lee DG, Chu KH (2013) Effects of growth substrate on triclosan biodegradation potential of oxygenase-expressing bacteria. Chemosphere 93(9):1904–1911.  https://doi.org/10.1016/j.chemosphere.2013.06.069 CrossRefGoogle Scholar
  44. Lin H, Sun W, Zhang Z, Chapman SJ, Freitag TE, Fu J, Zhang X, Ma J (2016) Effects of manure and mineral fertilization strategies on soil antibiotic resistance gene levels and microbial community in a paddy-upland rotation system. Environ Pollut 211:332–337.  https://doi.org/10.1016/j.envpol.2016.01.007 CrossRefGoogle Scholar
  45. Liu J, He XX, Lin XR, Chen WC, Zhou QX, Shu WS, Huang LN (2015) Ecological effects of combined pollution associated with e-waste recycling on the composition and diversity of soil microbial communities. Environ Sci Technol 49(11):6438–6447.  https://doi.org/10.1021/es5049804 CrossRefGoogle Scholar
  46. Luzuriaga AL, Sánchez AM, Maestre FT, Escudero A (2012) Assemblage of a semi-arid annual plant community: abiotic and biotic filters act hierarchically. PLoS One 7:1–9CrossRefGoogle Scholar
  47. Lv G, Li Z, Elliott L, Schmidt MJ, MacWilliams MP, Zhang B (2017) Impact of tetracycline-clay interactions on bacterial growth. J Hazard Mater.  https://doi.org/10.1016/j.jhazmat.2017.09.029
  48. Lyall K, Croen LA, Sjödin A, Yoshida CK, Zerbo O, Kharrazi M, Windham GC (2017) Polychlorinated biphenyl and organochlorine pesticide concentrations in maternal mid-pregnancy serum samples: association with autism spectrum disorder and intellectual disability. Environ Health Perspect 125:474CrossRefGoogle Scholar
  49. MacNaughton SJ, Stephen JR, Venosa AD, Davis GA, Chang YJ, White DC (1999) Microbial population changes during bioremediation of an experimental oil spill. Appl Environ Microbiol 65(8):3566–3574Google Scholar
  50. Marrugo-Negrete J, Pinedo-Hernández J, Díez S (2017) Assessment of heavy metal pollution, spatial distribution and origin in agricultural soils along the Sinú River Basin, Colombia. Environ Res 154:380–388.  https://doi.org/10.1016/j.envres.2017.01.021 CrossRefGoogle Scholar
  51. Martinez JL, Sánchez MB, Martínez-Solano L, Hernandez A, Garmendia L, Fajardo A, Alvarez-Ortega C (2009) Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS Microbiol Rev 33(2):430–449.  https://doi.org/10.1111/j.1574-6976.2008.00157.x CrossRefGoogle Scholar
  52. Máthé I, Benedek T, Táncsics A, Palatinszky M, Lányi S, Márialigeti K (2012) Diversity, activity, antibiotic and heavy metal resistance of bacteria from petroleum hydrocarbon contaminated soils located in Harghita County (Romania). Int Biodeterior Biodegrad 73:41–49.  https://doi.org/10.1016/j.ibiod.2012.05.018 CrossRefGoogle Scholar
  53. Mindlin S, Minakhin L, Petrova M, Kholodii G, Minakhina S, Gorlenko Z, Nikiforov V (2005) Present-day mercury resistance transposons are common in bacteria preserved in permafrost grounds since the Upper Pleistocene. Res Microbiol 156(10):994–1004.  https://doi.org/10.1016/j.resmic.2005.05.011 CrossRefGoogle Scholar
  54. Muangchinda C, Yamazoe A, Polrit D, Thoetkiattikul H, Mhuantong W, Champreda V, Pinyakong O (2017) Biodegradation of high concentrations of mixed polycyclic aromatic hydrocarbons by indigenous bacteria from a river sediment: a microcosm study and bacterial community analysis. Environ Sci Pollut Res Int 24(5):4591–4602.  https://doi.org/10.1007/s11356-016-8185-9 CrossRefGoogle Scholar
  55. Novick RP, Morse SI (1967) In vivo transmission of drug resistance factors between strains of Staphylococcus aureus. J Exp Med 125(1):45–59.  https://doi.org/10.1084/jem.125.1.45 CrossRefGoogle Scholar
  56. Ohtsubo Y, Ishibashi Y, Naganawa H, Hirokawa S, Atobe S, Nagata Y, Tsuda M (2012) Conjugal transfer of polychlorinated biphenyl/biphenyl degradation genes in Acidovorax sp. strain KKS102, which are located on an integrative and conjugative element. J Bacteriol 194(16):4237–4248.  https://doi.org/10.1128/JB.00352-12 CrossRefGoogle Scholar
  57. Pérez-Pantoja D, Nikel PI, Chavarría M, de Lorenzo V (2013) Endogenous stress caused by faulty oxidation reactions fosters evolution of 2,4-dinitrotoluene-degrading bacteria. PLoS Genet 9(8):e1003764.  https://doi.org/10.1371/journal.pgen.1003764 CrossRefGoogle Scholar
  58. Pils JR, Laird DA (2007) Sorption of tetracycline and chlortetracycline on K-and Ca-saturated soil clays, humic substances, and clay-humic complexes. Environ Sci Technol 41(6):1928–1933.  https://doi.org/10.1021/es062316y CrossRefGoogle Scholar
  59. Pires D, de Kraker MEA, Tartari E, Abbas M, Pittet D (2017) ‘Fight antibiotic resistance—It’s in your hands’: call from the World Health Organization for 5th May 2017. Clin Infect Dis 64(12):1780–1783.  https://doi.org/10.1093/cid/cix226 CrossRefGoogle Scholar
  60. Poole K (2017) At the nexus of antibiotics and metals: the impact of Cu and Zn on antibiotic activity and resistance. Trends Microbiol 25(10):820–832.  https://doi.org/10.1016/j.tim.2017.04.010 CrossRefGoogle Scholar
  61. Pyrchenkova IA, Gafarov AB, Puntus IF, Filonov AE, Boronin AM (2006) Selection and characterization of active psychrotrophic microbial oil-degrading microorganisms. Appl Biochem Microbiol 42(3):263–269.  https://doi.org/10.1134/S0003683806030070 CrossRefGoogle Scholar
  62. Rosewarne CP, Pettigrove V, Stokes HW, Parsons YM (2010) Class 1 integrons in benthic bacterial communities: abundance, association with Tn 402-like transposition modules and evidence for co selection with heavy-metal resistance. FEMS Microbiol Ecol 72(1):35–46.  https://doi.org/10.1111/j.1574-6941.2009.00823.x CrossRefGoogle Scholar
  63. Rostami I, Juhasz AL (2011) Assessment of persistent organic pollutant (POP) bioavailability and bioaccessibility for human health exposure assessment: a critical review. Crit Rev Environ Sci Technol 41(7):623–656.  https://doi.org/10.1080/10643380903044178 CrossRefGoogle Scholar
  64. Sazykin IS, Sazykina MA, Khmelevtsova LE, Khammami MI, Karchava SK, Zhuravlevа MV, Kudeevskaya EM (2016) Expression of SOD and production of reactive oxygen species in Acinetobacter calcoaceticus caused by hydrocarbons oxidation. Ann Microbiol 66(3):1039–1045.  https://doi.org/10.1007/s13213-015-1188-9 CrossRefGoogle Scholar
  65. Sinegani AAS, Younessi N (2017) Antibiotic resistance of bacteria isolated from heavy metal-polluted soils with different land uses. J Glob Antimicrob Resist 10:247–255.  https://doi.org/10.1016/j.jgar.2017.05.012 CrossRefGoogle Scholar
  66. Stancu MM (2014) Physiological cellular responses and adaptations of Rhodococcus erythropolis IBB Po1 to toxic organic solvents. J Environ Sci (China) 26(10):2065–2075.  https://doi.org/10.1016/j.jes.2014.08.006 CrossRefGoogle Scholar
  67. Stancu MM, Grifoll M (2011) Multidrug resistance in hydrocarbon-tolerant Gram-positive and Gram-negative bacteria. J Gen Appl Microbiol 57(1):1–18.  https://doi.org/10.2323/jgam.57.1 CrossRefGoogle Scholar
  68. Su HC, Pan CG, Ying GG, Zhao JL, Zhou LJ, Liu YS, Tao R, Zhang RQ, He LY (2014) Contamination profiles of antibiotic resistance genes in the sediments at a catchment scale. Sci Total Environ 490:708–714.  https://doi.org/10.1016/j.scitotenv.2014.05.060 CrossRefGoogle Scholar
  69. Suenaga H, Fujihara H, Kimura N, Hirose J, Watanabe T, Futagami T, Goto M, Shimodaira J, Furukawa K (2017) Insights into the genomic plasticity of Pseudomonas putida KF715, a strain with unique biphenyl-utilizing activity and genome instability properties. Environ Microbiol Rep 9(5):589–598.  https://doi.org/10.1111/1758-2229.12561 CrossRefGoogle Scholar
  70. Sun K, Liu J, Li X, Ling W (2014) Isolation, identification, and performance of two pyrene-degrading endophytic bacteria. Acta Ecol Sin 34(4):853–861.  https://doi.org/10.5846/stxb201210091393 CrossRefGoogle Scholar
  71. Sun M, Ye M, Wu J, Feng Y, Wan J, Tian D, Shen F, Liu K, Hu F, Li H Jiang X, Yang L, Kengara FO (2015) Positive relationship detected between soil bioaccessible organic pollutants and antibiotic resistance genes at dairy farms in Nanjing, Eastern China. Environ Pollut 206:421–428.  https://doi.org/10.1016/j.envpol.2015.07.022 CrossRefGoogle Scholar
  72. Surette M, Wright GD (2017) Lessons from environmental antibiotic resistome. Ann Rev Microbiol 71(1):309–329.  https://doi.org/10.1146/annurev-micro-090816-093420 CrossRefGoogle Scholar
  73. Takeuchi N, Kaneko K, Koonin EV (2014) Horizontal gene transfer can rescue prokaryotes from Muller’s ratchet: benefit of DNA from dead cells and population subdivision. G3 (Bethesda) 4(2):325–339.  https://doi.org/10.1534/g3.113.009845 CrossRefGoogle Scholar
  74. Vane CH, Kim AW, Beriro DJ, Cave MR, Knights K, Moss-Hayes V, Nathanail PC (2014) Polycyclic aromatic hydrocarbons (PAH) and polychlorinated biphenyls (PCB) in urban soils of Greater London, UK. Appl Geochem 51:303–314.  https://doi.org/10.1016/j.apgeochem.2014.09.013 CrossRefGoogle Scholar
  75. Wang X, Zhang C, Qiu B, Ashraf U, Azad R, Wu J, Ali S (2017) Biotransfer of Cd along a soil-plant-mealybug-ladybird food chain: a comparison with host plants. Chemosphere 168:699–706.  https://doi.org/10.1016/j.chemosphere.2016.11.005 CrossRefGoogle Scholar
  76. World Health Organization (2015) Global action plan on antimicrobial resistance. WHO Document Production Services, GenevaGoogle Scholar
  77. Xiao Y, Li L (2016) China’s national plan to combat antimicrobial resistance. Lancet Infect Dis 16(11):1216–1218.  https://doi.org/10.1016/S1473-3099(16)30388-7 CrossRefGoogle Scholar
  78. Xie WY, McGrath SP, Su JQ, Hirsch PR, Clark IM, Shen Q, Zhu YG, Zhao FJ (2016) Long-term impact of field applications of sewage sludge on soil antibiotic resistome. Environ Sci Technol 50(23):12602–12611.  https://doi.org/10.1021/acs.est.6b02138 CrossRefGoogle Scholar
  79. Xiong X, Yanxia L, Wei L, Chunye L, Wei H, Ming Y (2010) Copper content in animal manures and potential risk of soil copper pollution with animal manure use in agriculture. Resour Conserv Recycl 54:985–990.  https://doi.org/10.1016/j.resconrec.2010.02.005 CrossRefGoogle Scholar
  80. Yang S, Wen X, Zhao L, Shi Y, Jin H (2014) Crude oil treatment leads to shift of bacterial communities in soils from the deep active layer and upper permafrost along the China-Russia crude oil pipeline route. PLoS One 9(5):e96552.  https://doi.org/10.1371/journal.pone.0096552 CrossRefGoogle Scholar
  81. Ye M, Sun M, Wan J, Feng Y, Zhao Y, Tian D, Hu F Jiang X (2016) Feasibility of lettuce cultivation in sophoroliplid-enhanced washed soil originally polluted with Cd, antibiotics, and antibiotic-resistant genes. Ecotoxicol Environ Saf 124:344–350.  https://doi.org/10.1016/j.ecoenv.2015.11.013 CrossRefGoogle Scholar
  82. Yergeau E, Sanschagrin S, Maynard C, St-Arnaud M, Greer CW (2014) Microbial expression profiles in the rhizosphere of willows depend on soil contamination. ISME J 8(2):344–358.  https://doi.org/10.1038/ismej.2013.163 CrossRefGoogle Scholar
  83. Yu B, Tian J, Feng L (2017) Remediation of PAH polluted soils using a soil microbial fuel cell: influence of electrode interval and role of microbial community. J Hazard Mater 336:110–118.  https://doi.org/10.1016/j.jhazmat.2017.04.066 CrossRefGoogle Scholar
  84. Zhou B, Wang C, Zhao Q, Wang Y, Huo M, Wang J, Wang S (2016) Prevalence and dissemination of antibiotic resistance genes and coselection of heavy metals in Chinese dairy farms. J Hazard Mater 320:10–17.  https://doi.org/10.1016/j.jhazmat.2016.08.007 CrossRefGoogle Scholar
  85. 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 599-600:1977–1983.  https://doi.org/10.1016/j.scitotenv.2017.05.152 CrossRefGoogle Scholar
  86. Zhu F, Storey S, Ashaari MM, Clipson N, Doyle E (2017) Benzo (a) pyrene degradation and microbial community responses in composted soil. Environ Sci Pollut Res Int 24(6):5404–5414.  https://doi.org/10.1007/s11356-016-8251-3 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Andrey Vladimirovich Gorovtsov
    • 1
  • Ivan Sergeevich Sazykin
    • 1
  • Marina Alexandrovna Sazykina
    • 1
  1. 1.Southern Federal UniversityRostov-on-DonRussia

Personalised recommendations