Advertisement

Frontiers of Medicine

, Volume 11, Issue 2, pp 161–168 | Cite as

The antibiotic resistome: gene flow in environments, animals and human beings

  • Yongfei Hu
  • George F. Gao
  • Baoli Zhu
Review

Abstract

The antibiotic resistance is natural in bacteria and predates the human use of antibiotics. Numerous antibiotic resistance genes (ARGs) have been discovered to confer resistance to a wide range of antibiotics. The ARGs in natural environments are highly integrated and tightly regulated in specific bacterial metabolic networks. However, the antibiotic selection pressure conferred by the use of antibiotics in both human medicine and agriculture practice leads to a significant increase of antibiotic resistance and a steady accumulation of ARGs in bacteria. In this review, we summarized, with an emphasis on an ecological point of view, the important research progress regarding the collective ARGs (antibiotic resistome) in bacterial communities of natural environments, human and animals, i.e., in the one health settings.We propose that the resistance gene flow in nature is “from the natural environments” and “to the natural environments”; human and animals, as intermediate recipients and disseminators, contribute greatly to such a resistance gene “circulation.”

Keywords

antibiotic resistance resistome microbiome gene flow 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was supported in part by the National Basic Research Program of China (973 Program, No. 2015CB554200), the National Natural Science Foundation of China (Nos. 81401701 and 31471203), the Beijing Municipal Natural Science Foundation (No. 5152019) and the Youth Innovation Promotion Association of Chinese Academy of Sciences (No. 2015069). G.F.G. is a leading principal investigator of the National Natural Science Foundation of China Innovative Research Group (No. 81321063).

References

  1. 1.
    Rossolini GM, Arena F, Pecile P, Pollini S. Update on the antibiotic resistance crisis. Curr Opin Pharmacol 2014; 18: 56–60CrossRefPubMedGoogle Scholar
  2. 2.
    O’Neill J. Antimicrobial resistance: tackling a crisis for the health and wealth of nations. Rev Antimicrob Resist 2014; doi:10.1038/510015aGoogle Scholar
  3. 3.
    Laxminarayan R, Amabile-Cuevas CF, Cars O, Evans T, Heymann DL, Hoffman S, Holmes A, Mendelson M, Sridhar D, Woolhouse M, Røttingen JA. UN High-Level Meeting on antimicrobials—what do we need? Lancet 2016; 388(10041): 218–220CrossRefPubMedGoogle Scholar
  4. 4.
    Abraham EP, Chain E. An enzyme from bacteria able to destroy penicillin. Nature 1940; 146(3713): 837CrossRefGoogle Scholar
  5. 5.
    Alanis AJ. Resistance to antibiotics: are we in the post-antibiotic era? Arch Med Res 2005; 36(6): 697–705CrossRefPubMedGoogle Scholar
  6. 6.
    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. Antibiotic resistance is ancient. Nature 2011; 477(7365): 457–461CrossRefPubMedGoogle Scholar
  7. 7.
    Riesenfeld CS, Goodman RM, Handelsman J. Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ Microbiol 2004; 6(9): 981–989CrossRefPubMedGoogle Scholar
  8. 8.
    Sommer MOA, Dantas G, Church GM. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 2009; 325(5944): 1128–1131CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    D’Costa VM, McGrann KM, Hughes DW, Wright GD. Sampling the antibiotic resistome. Science 2006; 311(5759): 374–377CrossRefPubMedGoogle Scholar
  10. 10.
    Wright GD. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 2007; 5(3): 175–186CrossRefPubMedGoogle Scholar
  11. 11.
    Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 2010; 74(3): 417–433CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Martinez JL. Antibiotics and antibiotic resistance genes in natural environments. Science 2008; 321(5887): 365–367CrossRefPubMedGoogle Scholar
  13. 13.
    Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 2010; 8(4): 251–259CrossRefPubMedGoogle Scholar
  14. 14.
    Dantas G, Sommer MO, Oluwasegun RD, Church GM. Bacteria subsisting on antibiotics. Science 2008; 320(5872): 100–103CrossRefPubMedGoogle Scholar
  15. 15.
    Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G. The shared antibiotic resistome of soil bacteria and human pathogens. Science 2012; 337(6098): 1107–1111CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Baquero F, Martinez JL, Canton R. Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 2008; 19(3): 260–265CrossRefPubMedGoogle Scholar
  17. 17.
    Cabello FC. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 2006; 8(7): 1137–1144CrossRefPubMedGoogle Scholar
  18. 18.
    Zhang XX, Zhang T, Fang HH. Antibiotic resistance genes in water environment. Appl Microbiol Biotechnol 2009; 82(3): 397–414CrossRefPubMedGoogle Scholar
  19. 19.
    Hatosy SM, Martiny AC. The ocean as a global reservoir of antibiotic resistance genes. Appl Environ Microbiol 2015; 81(21): 7593–7599CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Yap MN. The double life of antibiotics. Mo Med 2013; 110(4): 320–324PubMedPubMedCentralGoogle Scholar
  21. 21.
    Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA 2013; 110(9): 3435–3440CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Schmidt AS, Bruun MS, Dalsgaard I, Larsen JL. Incidence, distribution, and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among motile aeromonads from a fish farming environment. Appl Environ Microbiol 2001; 67(12): 5675–5682CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Aarestrup FM. Occurrence of glycopeptide resistance among Enterococcus faecium isolates from conventional and ecological poultry farms. Microb Drug Resist 1995; 1(3): 255–257CrossRefPubMedGoogle Scholar
  24. 24.
    Cheng W, Chen H, Su C, Yan S. Abundance and persistence of antibiotic resistance genes in livestock farms: a comprehensive investigation in eastern China. Environ Int 2013; 61: 1–7CrossRefPubMedGoogle Scholar
  25. 25.
    Ibrahim DR, Dodd CE, Stekel DJ, Ramsden SJ, Hobman JL. Multidrug resistant, extended spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from a dairy farm. FEMS Microbiol Ecol 2016; 92(4): fiw013CrossRefPubMedGoogle Scholar
  26. 26.
    Kazimierczak KA, Scott KP, Kelly D, Aminov RI. Tetracycline resistome of the organic pig gut. Appl Environ Microbiol 2009; 75(6): 1717–1722CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Xiao L, Estelle J, Kiilerich P, Ramayo-Caldas Y, Xia Z, Feng Q, Liang S, Pedersen AØ, Kjeldsen NJ, Liu C, Maguin E, Doré J, Pons N, Le Chatelier E, Prifti E, Li J, Jia H, Liu X, Xu X, Ehrlich SD, Madsen L, Kristiansen K, Rogel-Gaillard C, Wang J. A reference gene catalogue of the pig gut microbiome. Nat Microbiol 2016; 1: 16161CrossRefGoogle Scholar
  28. 28.
    Anderson ES. The ecology of transferable drug resistance in the enterobacteria. Annu Rev Microbiol 1968; 22(1): 131–180CrossRefPubMedGoogle Scholar
  29. 29.
    Weinstein L, Goldfield M, Chang TW. Infections occurring during chemotherapy; a study of their frequency, type and predisposing factors. N Engl J Med 1954; 251(7): 247–255CrossRefPubMedGoogle Scholar
  30. 30.
    Salyers AA, Gupta A, Wang Y. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol 2004; 12(9): 412–416CrossRefPubMedGoogle Scholar
  31. 31.
    Hu Y, Yang X, Qin J, Lu N, Cheng G, Wu N, Pan Y, Li J, Zhu L, Wang X, Meng Z, Zhao F, Liu D, Ma J, Qin N, Xiang C, Xiao Y, Li L, Yang H, Wang J, Yang R, Gao GF, Wang J, Zhu B. Metagenomewide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat Commun 2013; 4: 2151PubMedGoogle Scholar
  32. 32.
    Hu Y, Yang X, Lu N, Zhu B. The abundance of antibiotic resistance genes in human guts has correlation to the consumption of antibiotics in animal. Gut Microbes 2014; 5(2): 245–249CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Hu Y, Zhu B. The human gut antibiotic resistome in the metagenomic era: progress and perspectives. Infect Dis Transl Med 2016; 2(1): 41–47Google Scholar
  34. 34.
    Martinez JL, Coque TM, Baquero F. What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol 2015; 13(2): 116–123PubMedGoogle Scholar
  35. 35.
    Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J. Emergence of plasmidmediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 2016; 16(2): 161–168CrossRefPubMedGoogle Scholar
  36. 36.
    Cox G, Wright GD. Intrinsic antibiotic resistance: mechanisms, origins, challenges and solutions. Int J Med Microbiol 2013; 303(6–7): 287–292CrossRefPubMedGoogle Scholar
  37. 37.
    Martinez JL, Baquero F, Andersson DI. Predicting antibiotic resistance. Nat Rev Microbiol 2007; 5(12): 958–965CrossRefPubMedGoogle Scholar
  38. 38.
    Gogarten JP, Townsend JP. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 2005; 3(9): 679–687CrossRefPubMedGoogle Scholar
  39. 39.
    Bennett PM. Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 2008; 153(S1): S347–S357CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Rice LB. Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob Agents Chemother 1998; 42(8): 1871–1877PubMedPubMedCentralGoogle Scholar
  41. 41.
    Rowe-Magnus DA, Mazel D. The role of integrons in antibiotic resistance gene capture. Int J Med Microbiol 2002; 292(2): 115–125CrossRefPubMedGoogle Scholar
  42. 42.
    Hu Y, Zhu Y, Ma Y, Liu F, Lu N, Yang X, Luan C, Yi Y, Zhu B. Genomic insights into intrinsic and acquired drug resistance mechanisms in Achromobacter xylosoxidans. Antimicrob Agents Chemother 2015; 59(2): 1152–1161CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Dobrindt U, Hochhut B, Hentschel U, Hacker J. Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2004; 2(5): 414–424CrossRefPubMedGoogle Scholar
  44. 44.
    Fournier PE, Vallenet D, Barbe V, Audic S, Ogata H, Poirel L, Richet H, Robert C, Mangenot S, Abergel C, Nordmann P, Weissenbach J, Raoult D, Claverie JM. Comparative genomics of multidrug resistance in Acinetobacter baumannii. PLoS Genet 2006; 2(1): 62–72CrossRefGoogle Scholar
  45. 45.
    Hu Y, Yang X, Li J, Lv N, Liu F, Wu J, Lin IYC, Wu N, Weimer BC, Gao GF, Liu Y, Zhu B. The bacterial mobile resistome transfer network connecting the animal and human microbiomes. Appl Environ Microbiol 2016; 82(22): 6672–6681CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Thomas CM, Nielsen KM. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 2005; 3(9): 711–721CrossRefPubMedGoogle Scholar
  47. 47.
    Popa O, Dagan T. Trends and barriers to lateral gene transfer in prokaryotes. Curr Opin Microbiol 2011; 14(5): 615–623CrossRefPubMedGoogle Scholar
  48. 48.
    Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, Dantas G. Bacterial phylogeny structures soil resistomes across habitats. Nature 2014; 509(7502): 612–616CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 2011; 480(7376): 241–244CrossRefPubMedGoogle Scholar
  50. 50.
    Gibson MK, Forsberg KJ, Dantas G. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J 2015; 9(1): 207–216CrossRefPubMedGoogle Scholar
  51. 51.
    Smith HW. Transfer of antibiotic resistance from animal and human strains of Escherichia coli to resident E. coli in the alimentary tract of man. Vet Rec 1969; 85(2): 31–33CrossRefPubMedGoogle Scholar
  52. 52.
    Rodriguez-Mozaz S, Chamorro S, Marti E, Huerta B, Gros M, Sànchez-Melsió A, Borrego CM, Barceló D, Balcázar JL. Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res 2015; 69: 234–242CrossRefPubMedGoogle Scholar
  53. 53.
    Korzeniewska E, Korzeniewska A, Harnisz M. Antibiotic resistant Escherichia coli in hospital and municipal sewage and their emission to the environment. Ecotoxicol Environ Saf 2013; 91: 96–102CrossRefPubMedGoogle Scholar
  54. 54.
    Gotz A, Smalla K. Manure enhances plasmid mobilization and survival of Pseudomonas putida introduced into field soil. Appl Environ Microbiol 1997; 63(5): 1980–1986PubMedPubMedCentralGoogle Scholar
  55. 55.
    Winokur PL, Vonstein DL, Hoffman LJ, Uhlenhopp EK, Doern GV. Evidence for transfer of CMY-2 AmpC β-lactamase plasmids between Escherichia coli and Salmonella isolates from food animals and humans. Antimicrob Agents Chemother 2001; 45(10): 2716–2722CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Moubareck C, Bourgeois N, Courvalin P, Doucet-Populaire F. Multiple antibiotic resistance gene transfer from animal to human enterococci in the digestive tract of gnotobiotic mice. Antimicrob Agents Chemother 2003; 47(9): 2993–2996CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    No author listed. Antimicrobial resistance: implications for the food system. An expert report, funded by the IFT Foundation. Compr Rev Food Sci F 2006; 5(3): 71–137CrossRefGoogle Scholar
  58. 58.
    Hu Y, Liu F, Lin IY, Gao GF, Zhu B. Dissemination of the mcr-1 colistin resistance gene. Lancet Infect Dis 2016; 16(2): 146–147CrossRefPubMedGoogle Scholar
  59. 59.
    Graham DW, Collignon P, Davies J, Larsson DG, Snape J. Underappreciated role of regionally poor water quality on globally increasing antibiotic resistance. Environ Sci Technol 2014; 48(20): 11746–11747CrossRefPubMedGoogle Scholar
  60. 60.
    Arnold KE, Williams NJ, Bennett M. ‘Disperse abroad in the land’: the role of wildlife in the dissemination of antimicrobial resistance. Biol Lett 2016; 12(8): 20160137CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Vittecoq M, Godreuil S, Prugnolle F, Durand P, Brazier L, Renaud N, Arnal A, Aberkane S, Jean-Pierre H, Gauthier-Clerc M, Thomas F, Renaud F. Antimicrobial resistance in wildlife. J Appl Ecol 2016; 53(2): 519–529CrossRefGoogle Scholar
  62. 62.
    Martinez JL. Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 2009; 157(11): 2893–2902CrossRefPubMedGoogle Scholar
  63. 63.
    Pruden A, Pei RT, Storteboom H, Carlson KH. Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 2006; 40(23): 7445–7450CrossRefPubMedGoogle Scholar
  64. 64.
    Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, Vlieghe E, Hara GL, Gould IM, Goossens H, Greko C, So AD, Bigdeli M, Tomson G, Woodhouse W, Ombaka E, Peralta AQ, Qamar FN, Mir F, Kariuki S, Bhutta ZA, Coates A, Bergstrom R, Wright GD, Brown ED, Cars O. Antibiotic resistance—the need for global solutions. Lancet Infect Dis 2013; 13(12): 1057–1098CrossRefPubMedGoogle Scholar
  65. 65.
    Nathan C, Cars O. Antibiotic resistance-problems, progress, and prospects. N Engl J Med 2014; 371(19): 1761–1763CrossRefPubMedGoogle Scholar
  66. 66.
    McCullough AR, Parekh S, Rathbone J, Del Mar CB, Hoffmann TC. A systematic review of the public’s knowledge and beliefs about antibiotic resistance. J Antimicrob Chemother 2016; 71(1): 27–33CrossRefPubMedGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of MicrobiologyChinese Academy of SciencesBeijingChina
  2. 2.Beijing Key Laboratory of Microbial Drug Resistance and ResistomeBeijingChina
  3. 3.Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated HospitalZhejiang UniversityHangzhouChina
  4. 4.Research Network of Immunity and Health (RNIH), Beijing Institutes of Life ScienceChinese Academy of SciencesBeijingChina
  5. 5.Office of Director-GeneralChinese Center for Disease Control and Prevention (China CDC)BeijingChina

Personalised recommendations