Prevalence of antibiotic resistance genes in soils after continually applied with different manure for 30 years

Journal of Hazardous Materials

Volumn 340, Issue , 2017, Pages 16-25

  Peng, Shuang ^a   Feng, Youzhi ^a   Wang, Yiming ^a   Guo, Xisheng ^b   Chu, Haiyan ^a   Lin, Xiangui ^a  

^a INSTITUTE OF SOIL SCIENCE   (China)

^b RICE RESEARCH INSTITUTE   (China)

Author keywords

Antibiotic resistance genes; Class 1 integron; Manure; qPCR

Indexed keywords

ANTIBIOTICS; APPLICATION PROGRAMS; FERTILIZERS; GENES; MANURES; POLYMERASE CHAIN REACTION; SOILS;

ANTHROPOGENIC INFLUENCE; ANTIBIOTIC RESISTANCE GENES; CLASS 1; GAMMAPROTEOBACTERIA; LONG TERM EXPOSURE; POSITIVE CORRELATIONS; QPCR; RESISTANCE TO ANTIBIOTICS;

SOIL POLLUTION;

ARSENIC; BETA LACTAM; CADMIUM; COPPER; LEAD; MACROLIDE; MERCURY; QUINOLONE; RNA 16S; SULFANILAMIDE; TETRACYCLINE; ZINC; BACTERIAL DNA; FERTILIZER; HEAVY METAL;

ANTIBIOTIC RESISTANCE; BACTERIUM; CORRELATION; CROPPING PRACTICE; EXPERIMENTAL STUDY; GENE; MANURE; PIG; RELATIVE ABUNDANCE; SOIL POLLUTION; SOYBEAN; STRAW; WHEAT;

ACIDOBACTERIA; ACTINOBACTERIA; ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS ANTHRACIS; BACILLUS MEGATERIUM; BACTEROIDALES; BACTEROIDETES; BORDETELLA PERTUSSIS; BURKHOLDERIA PSEUDOMALLEI; CAMPYLOBACTER; CHLOROFLEXI; CLOSTRIDIOIDES DIFFICILE; CLOSTRIDIUM BEIJERINCKII; CONTROLLED STUDY; ENTEROBACTER CLOACAE; ENTEROCOCCUS FAECIUM; FIRMICUTES; GAMMAPROTEOBACTERIA; GENE SEQUENCE; MANURE; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; PARABURKHOLDERIA XENOVORANS; PLANCTOMYCETES; PREVALENCE; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS SYRINGAE; SALMONELLA; SHIGELLA; SOIL; SOIL AMENDMENT; STAPHYLOCOCCUS SAPROPHYTICUS; ANALYSIS; ANIMAL; BACTERIAL GENE; BACTERIUM; BOVINE; ENVIRONMENTAL MONITORING; GENETICS; MICROBIOLOGY; PIG; SOIL POLLUTANT; WHEAT;

ANIMALIA; BACTEROIDETES; FIRMICUTES; GAMMAPROTEOBACTERIA; GLYCINE MAX; SUIDAE; TRITICUM AESTIVUM;

ANIMALS; BACTERIA; CATTLE; DNA, BACTERIAL; DRUG RESISTANCE, MICROBIAL; ENVIRONMENTAL MONITORING; FERTILIZERS; GENES, BACTERIAL; MANURE; METALS, HEAVY; SOIL MICROBIOLOGY; SOIL POLLUTANTS; SWINE; TRITICUM;

EID: 85023596066     PISSN: 03043894     EISSN: 18733336     Source Type: Journal    
DOI: 10.1016/j.jhazmat.2017.06.059     Document Type: Article

References (67)

1. Allen, H.K., Donato, J., Wang, H.H., Cloud-Hansen, K.A., Davies, J., Handelsman, J., Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8 (2010), 251–259.
2. Forsberg, K.J., Reyes, A., Wang, B., Selleck, E.M., Sommer, M.O., Dantas, G., The shared antibiotic resistome of soil bacteria and human pathogens. Science 337 (2012), 1107–1111.
3. Martinez, J.L., Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ. Pollut. 157 (2009), 2893–2902.
4. Berendonk, T.U., Manaia, C.M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., Burgmann, H., Sorum, H., Norstrom, M., Pons, M.N., Kreuzinger, N., Huovinen, P., Stefani, S., Schwartz, T., Kisand, V., Baquero, F., Martinez, J.L., Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 13 (2015), 310–317.
5. D'Costa, V.M., Griffiths, E., Wright, G.D., Expanding the soil antibiotic resistome: exploring environmental diversity. Curr. Opin. Microbiol. 10 (2007), 481–489.
6. Heuer, H., Schmitt, H., Smalla, K., Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 14 (2011), 236–243.
7. Brichta-Harhay, D.M., Arthur, T.M., Bosilevac, J.M., Kalchayanand, N., Shackelford, S.D., Wheeler, T.L., Koohmaraie, M., Diversity of multidrug-Resistant salmonella enterica strains associated with cattle at harvest in the United States. Appl. Environ. Microbiol. 77 (2011), 1783–1796.
8. Pruden, A., Larsson, D.G., Amezquita, A., Collignon, P., Brandt, K.K., Graham, D.W., Lazorchak, J.M., Suzuki, S., Silley, P., Snape, J.R., Topp, E., Zhang, T., Zhu, Y.G., Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ. Health. Perspect. 121 (2013), 878–885.
9. Kang, Y., Hao, Y., Shen, M., Zhao, Q., Li, Q., Hu, J., Impacts of supplementing chemical fertilizers with organic fertilizers manufactured using pig manure as a substrate on the spread of tetracycline resistance genes in soil. Ecotoxicol. Environ. Saf. 130 (2016), 279–288.
10. Byrne-Bailey, K.G., Gaze, W.H., Kay, P., Boxall, A.B., Hawkey, P.M., Wellington, E.M., Prevalence of sulfonamide resistance genes in bacterial isolates from manured agricultural soils and pig slurry in the United Kingdom. Antimicrob. Agents Chemother. 53 (2009), 696–702.
11. Luby, E.M., Moorman, T.B., Soupir, M.L., Fate and transport of tylosin-resistant bacteria and macrolide resistance genes in artificially drained agricultural fields receiving swine manure. Sci. Total Environ. 550 (2016), 1126–1133.
12. Marti, R., Scott, A., Tien, Y.-C., Murray, R., Sabourin, L., Zhang, Y., Topp, E., 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 (2013), 5701–5709.
13. Heuer, H., Solehati, Q., Zimmerling, U., Kleineidam, K., Schloter, M., Muller, T., Focks, A., Thiele-Bruhn, S., Smalla, K., Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl. Environ. Microbiol. 77 (2011), 2527–2530.
14. Jechalke, S., Kopmann, C., Rosendahl, I., Groeneweg, J., Weichelt, V., Krogerrecklenfort, E., Brandes, N., Nordwig, M., Ding, G.C., Siemens, J., Heuer, H., Smalla, K., Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Appl. Environ. Microbiol. 79 (2013), 1704–1711.
15. Zhu, Y.G., Johnson, T.A., Su, J.Q., Qiao, M., Guo, G.X., Stedtfeld, R.D., Hashsham, S.A., Tiedje, J.M., Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 3435–3440.
16. Peng, S., Wang, Y., Zhou, B., Lin, X., Long-term application of fresh and composted manure increase tetracycline resistance in the arable soil of eastern China. Sci. Total Environ. 506-507 (2015), 279–286.
17. Wichmann, F., Udikovic-Kolic, N., Andrew, S., Handelsman, J., Diverse antibiotic resistance genes in dairy cow manure. mBio, 5, 2014, e01017.
18. Fahrenfeld, N., Knowlton, K., Krometis, L.A., Hession, W.C., Xia, K., Lipscomb, E., Libuit, K., Green, B.L., Pruden, A., 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 (2014), 2643–2650.
19. Noyes, N.R., Yang, X., Linke, L.M., Magnuson, R.J., Cook, S.R., Zaheer, R., Yang, H., Woerner, D.R., Geornaras, I., McArt, J.A., Gow, S.P., Ruiz, J., Jones, K.L., Boucher, C.A., McAllister, T.A., Belk, K.E., Morley, P.S., Characterization of the resistome in manure, soil and wastewater from dairy and beef production systems. Sci. Rep., 6, 2016, 24645.
20. Chambers, L., Yang, Y., Littier, H., Ray, P., Zhang, T., Pruden, A., Strickland, M., Knowlton, K., Metagenomic analysis of antibiotic resistance genes in dairy cow feces following therapeutic administration of third generation cephalosporin. PLoS One, 10, 2015, e0133764.
21. Qian, X., Sun, W., Gu, J., Wang, X.J., Sun, J.J., Yin, Y.N., Duan, M.L., Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure. J. Hazard. Mater. 315 (2016), 61–69.
22. Kyselková, M., Jirout, J., Chroňáková, A., Vrchotová, N., Bradley, R., Schmitt, H., Elhottová, D., Cow excrements enhance the occurrence of tetracycline resistance genes in soil regardless of their oxytetracycline content. Chemosphere 93 (2013), 2413–2418.
23. Kyselková, M., Kotrbová, L., Bhumibhamon, G., Chroňáková, A., Jirout, J., Vrchotová, N., Schmitt, H., Elhottová, D., Tetracycline resistance genes persist in soil amended with cattle feces independently from chlortetracycline selection pressure. Soil. Biol. Biochem. 81 (2015), 259–265.
24. Domingo-Olivé, F., Bosch-Serra, À.D., Yagüe, M.R., Poch, R.M., Boixadera, J., Long term application of dairy cattle manure and pig slurry to winter cereals improves soil quality. Nutr. Cycl. Agroecosyst. 104 (2016), 39–51.
25. Verma, S., Sharma, P.K., Long-term effects of organics, fertilizers and cropping systems on soil physical productivity evaluated using a single value index (NLWR). Soil Tillage Res. 98 (2008), 1–10.
26. Polthanee, A., Tre-loges, V., Promsena, K., Effect of rice straw management and organic fertilizer application on growth and yield of dry direct-seeded rice. Paddy Water Environ. 6 (2008), 237–241.
27. Sun, R., Zhang, X.-X., Guo, X., Wang, D., Chu, H., Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil. Biol. Biochem. 88 (2015), 9–18.
28. Rousk, J., Brookes, P.C., Baath, E., Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl. Environ. Microbiol. 75 (2009), 1589–1596.
29. Griffiths, R.I., Thomson, B.C., James, P., Bell, T., Bailey, M., Whiteley, A.S., The bacterial biogeography of British soils. Environ. Microbiol. 13 (2011), 1642–1654.
30. Gillings, M.R., Gaze, W.H., Pruden, A., Smalla, K., Tiedje, J.M., Zhu, Y.G., Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 9 (2015), 1269–1279.
31. Zhang, T., Zhang, M., Zhang, X., Fang, H.H., Tetracycline resistance genes and tetracycline resistant Lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environ. Sci. Technol. 43 (2009), 3455–3460.
32. Biddle, J.F., Fitz-Gibbon, S., Schuster, S.C., Brenchley, J.E., House, C.H., Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 10583–10588.
33. Qian, M., Wu, H., Wang, J., Zhang, H., Zhang, Z., Zhang, Y., Lin, H., Ma, J., Occurrence of trace elements and antibiotics in manure-based fertilizers from the Zhejiang Province of China. Sci. Total Environ. 559 (2016), 174–181.
34. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 (2010), 335–336.
35. Chen, Q., An, X., Li, H., Su, J., Ma, Y., Zhu, Y.G., Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ. Int. 92-93 (2016), 1–10.
36. Fang, H., Wang, H., Cai, L., Yu, Y., Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey. Environ. Sci. Technol. 49 (2015), 1095–1104.
37. Li, B., Ju, F., Cai, L., Zhang, T., Profile and fate of bacterial pathogens in sewage treatment plants revealed by high-throughput metagenomic approach. Environ. Sci. Technol. 49 (2015), 10492–10502.
38. Zhang, Y., Zhang, C., Parker, D.B., Snow, D.D., Zhou, Z., Li, X., Occurrence of antimicrobials and antimicrobial resistance genes in beef cattle storage ponds and swine treatment lagoons. Sci. Total Environ. 463–464 (2013), 631–638.
39. Sandberg, K.D., LaPara, T.M., The Fate of antibiotic resistance genes and class 1 integrons following the application of swine and dairy manure to soils. FEMS Microbiol. Ecol. 92 (2016), 1–10.
40. Partridge, S.R., Tsafnat, G., Coiera, E., Iredell, J.R., Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol. Rev. 33 (2009), 757–784.
41. Tang, X., Lou, C., Wang, S., Lu, Y., Liu, M., Hashmi, M.Z., Liang, X., Li, Z., Liao, Y., Qin, W., Fan, F., Xu, J., Brookes, P.C., 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 (2015), 179–187.
42. Liu, L., Liu, C., Zheng, J., Huang, X., Wang, Z., Liu, Y., Zhu, G., Elimination of veterinary antibiotics and antibiotic resistance genes from swine wastewater in the vertical flow constructed wetlands. Chemosphere 91 (2013), 1088–1093.
43. Koike, S., Krapac, I.G., Oliver, H.D., Yannarell, A.C., Chee-Sanford, J.C., Aminov, R.I., Mackie, R.I., 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 (2007), 4813–4823.
44. Wu, N., Qiao, M., Zhang, B., Cheng, W.D., Zhu, Y.G., Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environ. Sci. Technol. 44 (2010), 6933–6939.
45. Roberts, M.C., Acquired tetracycline resistance genes. Antibiot. Discov. Dev., 2012, 543–568.
46. Mu, Q., Li, J., Sun, Y., Mao, D., Wang, Q., Luo, Y., Occurrence of sulfonamide-, tetracycline-, plasmid-mediated quinolone- and macrolide-resistance genes in livestock feedlots in Northern China, Environ. Sci. Pollut. Res. 22 (2015), 6932–6940.
47. Zhang, Q.Q., Ying, G.G., Pan, C.G., Liu, Y.S., Zhao, J.L., Comprehensive evaluation of antibiotics emission and fate in the river basins of china: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ. Sci. Technol. 49 (2015), 6772–6782.
48. Kyselková, M., Jirout, J., Vrchotová, N., Schmitt, H., Elhottová, D., Spread of tetracycline resistance genes at a conventional dairy farm. Front. Microbiol., 6, 2015, 536.
49. Zhou, B., Wang, C., Zhao, Q., Wang, Y., Huo, M., Wang, J., Wang, S., Prevalence and dissemination of antibiotic resistance genes and coselection of heavy metals in Chinese dairy farms. J. Hazard. Mater. 320 (2016), 10–17.
50. Peng, S., Zhou, B., Wang, Y., Lin, X., Wang, H., Qiu, C., Bacteria play a more important role than nutrients in the accumulation of tetracycline resistance in manure-treated soil. Biol. Fertil. Soils 52 (2016), 655–663.
51. Leclercq, S.O., Wang, C., Sui, Z., Wu, H., Zhu, B., Deng, Y., Feng, J., A multiplayer game: species of Clostridium, Acinetobacter, and Pseudomonas are responsible for the persistence of antibiotic resistance genes in manure-treated soils. Environ. Microbiol. 18 (2016), 3494–3508.
52. Gibson, M.K., Forsberg, K.J., Dantas, G., Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J. 9 (2015), 207–216.
53. Ghosh, S., LaPara, T.M., The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J. 1 (2007), 191–203.
54. Liu, M., Zhang, Y., Yang, M., Tian, Z., Ren, L., Zhang, S., Abundance and distribution of tetracycline resistance genes and mobile elements in an oxytetracycline production wastewater treatment system. Environ. Sci. Technol. 46 (2012), 7551–7557.
55. Luo, Y., Mao, D., Rysz, M., Zhou, Q., Zhang, H., xu, L., Alvarez, P.J.J., Trends in antibiotic resistance genes occurrence in the Haihe river, China. Environ. Sci. Technol. 44 (2010), 7220–7225.
56. Jechalke, S., Schreiter, S., Wolters, B., Dealtry, S., Heuer, H., Smalla, K., Widespread dissemination of class 1 integron components in soils and related ecosystems as revealed by cultivation-independent analysis. Front. Microbiol., 4, 2014, 420.
57. Hsu, J.T., Chen, C.Y., Young, C.W., Chao, W.L., Li, M.H., Liu, Y.H., Lin, C.M., Ying, C., Prevalence of sulfonamide-resistant bacteria, resistance genes and integron-associated horizontal gene transfer in natural water bodies and soils adjacent to a swine feedlot in northern Taiwan. J. Hazard. Mater. 277 (2014), 34–43.
58. Wang, F.H., Qiao, M., Lv, Z.E., Guo, G.X., Jia, Y., Su, Y.H., Zhu, Y.G., Impact of reclaimed water irrigation on antibiotic resistance in public parks Beijing, China. Environ. Pollut. 184 (2014), 247–253.
59. Ma, Y., Wilson, C.A., Novak, J.T., Riffat, R., Aynur, S., Murthy, S., Pruden, A., Effect of various sludge digestion conditions on sulfonamide macrolide, and tetracycline resistance genes and class I integrons. Environ. Sci. Technol. 45 (2011), 7855–7861.
60. Heuer, H., Smalla, K., Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environ. Microbiol. 9 (2007), 657–666.
61. Gillings, M.R., Krishnan, S., Worden, P.J., Hardwick, S.A., Recovery of diverse genes for class 1 integron-integrases from environmental DNA samples. FEMS Microbiol. Lett. 287 (2008), 56–62.
62. Wang, N., Guo, X., Yan, Z., Wang, W., Chen, B., Ge, F., Ye, B., A comprehensive analysis on spread and distribution characteristic of antibiotic resistance genes in livestock farms of southeastern China. PLoS One, 11, 2016, e0156889.
63. Lin, H., Sun, W., Zhang, Z., Chapman, S.J., Freitag, T.E., Fu, J., Zhang, X., Ma, J., 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 (2016), 332–337.
64. Ji, X., Shen, Q., Liu, F., Ma, J., Xu, G., Wang, Y., Wu, M., 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 (2012), 178–185.
65. Knapp, C.W., McCluskey, S.M., Singh, B.K., Campbell, C.D., Hudson, G., Graham, D.W., Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived scottish soils. PLoS One, 6, 2011, e27300.
66. Negreanu, Y., Pasternak, Z., Jurkevitch, E., Cytryn, E., Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environ. Sci. Technol. 46 (2012), 4800–4808.
67. Cai, L., Zhang, T., Detecting human bacterial pathogens in wastewater treatment plants by a high-throughput shotgun sequencing technique. Environ. Sci. Technol. 47 (2013), 5433–5441.