Antibiotic resistance is a global public health issue of growing proportions. All antibiotics are susceptible to resistance. The evidence is now clear that the environment is the single largest source and reservoir of resistance. Soil, aquatic, atmospheric, animal-associated, and built ecosystems are home to microbes that harbor antibiotic resistance elements and the means to mobilize them. The diversity and abundance of resistance in the environment is consistent with the ancient origins of antibiotics and a variety of studies support a long natural history of associated resistance. The implications are clear: Understanding the evolution of resistance in the environment, its diversity, and mechanisms is essential to the management of our existing and future antibiotic resources.

Keyword(s): aquaticbuilt environmentdrugsoil

Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Allen HK, Cloud-Hansen KA, Wolinski JM, Guan C, Greene S. 1.  et al. 2009. Resident microbiota of the gypsy moth midgut harbors antibiotic resistance determinants. DNA Cell Biol 28:3109–17 [Google Scholar]
  2. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J. 2.  2009. Functional metagenomics reveals diverse β-lactamases in a remote Alaskan soil. ISME J 3:2243–51 [Google Scholar]
  3. Andrews-Pfannkoch C, Tenney A, Zeigler-Allen L, Hoffman J, Goll JB. 3.  et al. 2013. A metagenomic framework for the study of airborne microbial communities. PLOS ONE 8:12e81862 [Google Scholar]
  4. Armstrong GL, Conn LA, Pinner RW. 4.  1999. Trends in infectious disease mortality in the United States during the 20th century. JAMA 281:161–66 [Google Scholar]
  5. Arotsker L, Krasnov H, Ben-Dov E. 5.  2014. Richness and diversity in dust stormborne biomes at the southeast Mediterranean. Sci. Rep. 4:5265 [Google Scholar]
  6. Ashbolt NJ, Amézquita A, Backhaus T, Borriello P, Brandt KK. 6.  et al. 2013. Human Health Risk Assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ. Health Perspect. 121:9993–1001 [Google Scholar]
  7. Baker KS, Burnett E, McGregor H, Deheer-Graham A, Boinett C. 7.  et al. 2015. The Murray collection of pre-antibiotic era Enterobacteriaceae: a unique research resource. Genome Med 7:97 [Google Scholar]
  8. Baker S. 8.  2015. A return to the pre-antimicrobial era?. Science 347:62261064–66 [Google Scholar]
  9. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. 9.  2006. Co-selection of antibiotic and metal resistance. Trends Microbiol 14:4176–82 [Google Scholar]
  10. Baltz RH. 10.  2005. Antibiotic discovery from actinomycetes: Will a renaissance follow the decline and fall?. SIMB News 55:5186–96 [Google Scholar]
  11. Barlow M, Hall BG. 11.  2002. Phylogenetic analysis shows that the OXA b-lactamase genes have been on plasmids for millions of years. J. Mol. Evol. 55:3314–21 [Google Scholar]
  12. Benedict K. 12.  2014. Invasive fungal infections after natural disasters. Emerg. Infect. Dis. 20:3349–55 [Google Scholar]
  13. Bengtsson-Palme J, Boulund F, Fick J. 13.  2014. Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India. Front. Microbiol. 5:106648 [Google Scholar]
  14. Bengtsson-Palme J, Larsson DGJ. 14.  2015. Antibiotic resistance genes in the environment: prioritizing risks. Nat. Rev. Microbiol. 13:6396 [Google Scholar]
  15. Benveniste R, Davies J. 15.  1973. Aminoglycoside antibiotic-inactivating enzymes in actinomycetes similar to those present in clinical isolates of antibiotic-resistant bacteria. PNAS 70:82276–80 [Google Scholar]
  16. Berthold T, Centler F, Hübschmann T, Remer R, Thullner M. 16.  et al. 2016. Mycelia as a focal point for horizontal gene transfer among soil bacteria. Sci. Rep. 6:36390 [Google Scholar]
  17. Bérdy J. 17.  2005. Bioactive microbial metabolites. J. Antibiot. 58:11–26 [Google Scholar]
  18. Bhullar K, Waglechner N, Pawlowski A, Koteva K, Banks ED. 18.  et al. 2012. Antibiotic resistance is prevalent in an isolated cave microbiome. PLOS ONE 7:4e34953 [Google Scholar]
  19. Bonnedahl J, Drobni M, Gauthier-Clerc M, Hernandez J, Granholm S. 19.  et al. 2009. Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellow-legged gulls in the south of France. PLOS ONE 4:6e5958 [Google Scholar]
  20. Bonnedahl J, Drobni P, Johansson A, Hernandez J, Melhus A. 20.  et al. 2010. Characterization, and comparison, of human clinical and black-headed gull (Larus ridibundus) extended-spectrum β-lactamase-producing bacterial isolates from Kalmar, on the southeast coast of Sweden. J. Antimicrob. Chemother. 65:91939–44 [Google Scholar]
  21. Bos KI, Schuenemann VJ, Golding GB, Burbano HA, Waglechner N. 21.  et al. 2011. A draft genome of Yersinia pestis from victims of the Black Death. Nature 478:7370506–10 [Google Scholar]
  22. Brown ED, Wright GD. 22.  2016. Antibacterial drug discovery in the resistance era. Nature 529:7586336–43 [Google Scholar]
  23. Cabello FC, Godfrey HP, Buschmann AH, Dölz HJ. 23.  2016. Aquaculture as yet another environmental gateway to the development and globalisation of antimicrobial resistance. Lancet Infect. Dis. 16:7e127–33 [Google Scholar]
  24. Cameron A, McAllister TA. 24.  2016. Antimicrobial usage and resistance in beef production. J. Anim. Sci. Biotechnol. 7:168 [Google Scholar]
  25. Chen Q, An X, Li H, Su J, Ma Y, Zhu Y-G. 25.  2016. Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ. Int. 92–93:1–10 [Google Scholar]
  26. Clemente JC, Pehrsson EC, Blaser MJ, Sandhu K, Gao Z. 26.  et al. 2015. The microbiome of uncontacted Amerindians. Sci. Adv. 1:3e1500183 [Google Scholar]
  27. Costa D, Poeta P, Sáenz Y, Vinué L, Rojo-Bezares B. 27.  et al. 2006. Detection of Escherichia coli harbouring extended-spectrum β-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. J. Antimicrob. Chemother. 58:61311–12 [Google Scholar]
  28. Cox G, Wright GD. 28.  2013. Intrinsic antibiotic resistance: mechanisms, origins, challenges and solutions. Int. J. Med. Microbiol 3036–7287–92 [Google Scholar]
  29. Creamean JM, Suski KJ, Rosenfeld D, Cazorla A, DeMott PJ. 29.  et al. 2013. Dust and biological aerosols from the Sahara and Asia influence precipitation in the western U.S. Science 339:61271572–78 [Google Scholar]
  30. Culyba MJ, Mo CY, Kohli RM. 30.  2015. Targets for combating the evolution of acquired antibiotic resistance. Biochemistry 54:233573–82 [Google Scholar]
  31. Cundliffe E. 31.  1989. How antibiotic-producing organisms avoid suicide. Annu. Rev. Microbiol. 43:207–33 [Google Scholar]
  32. Dantas G, Sommer MOA, Oluwasegun RD, Church GM. 32.  2008. Bacteria subsisting on antibiotics. Science 320:5872100–3 [Google Scholar]
  33. Davies J. 33.  2006. Are antibiotics naturally antibiotics?. J. Ind. Microbiol. Biotechnol. 33:7496–99 [Google Scholar]
  34. Davies J, Davies D. 34.  2010. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74:3417–33 [Google Scholar]
  35. Devault AM, Golding GB, Waglechner N, Enk JM, Kuch M. 35.  et al. 2014. Second-pandemic strain of Vibriocholerae from the Philadelphia cholera outbreak of 1849. N. Engl. J. Med. 370:4334–40 [Google Scholar]
  36. Dirksen P, Marsh SA, Braker I, Heitland N, Wagner S. 36.  et al. 2016. The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model. BMC Biol 14:138 [Google Scholar]
  37. Dolejska M, Cizek A, Literak I. 37.  2007. High prevalence of antimicrobial‐resistant genes and integrons in Escherichia coli isolates from black‐headed gulls in the Czech Republic. J. Appl. Microbiol. 103:111–19 [Google Scholar]
  38. Drudge CN, Elliott AVC, Plach JM, Ejim LJ, Wright GD. 38.  et al. 2012. Diversity of integron- and culture-associated antibiotic resistance genes in freshwater floc. Appl. Environ. Microbiol. 78:124367–72 [Google Scholar]
  39. D'Costa VM, King CE, Kalan L, Morar M, Sung WWL. 39.  et al. 2011. Antibiotic resistance is ancient. Nature 477:7365457–61 [Google Scholar]
  40. D'Costa VM, McGrann KM, Hughes DW, Wright GD. 40.  2006. Sampling the antibiotic resistome. Science 311:5759374–77 [Google Scholar]
  41. Elbehery AHA, Leak DJ, Siam R. 41.  2017. Novel thermostable antibiotic resistance enzymes from the Atlantis II Deep Red Sea brine pool. Microb. Biotechnol. 10:1189–202 [Google Scholar]
  42. Engel P, Martinson VG. 42.  2012. Functional diversity within the simple gut microbiota of the honey bee. PNAS 109:2711002–7 [Google Scholar]
  43. Fajardo A, Martínez-Martín N, Mercadillo M, Galán JC, Ghysels B. 43.  et al. 2008. The neglected intrinsic resistome of bacterial pathogens. PLOS ONE 3:2e1619 [Google Scholar]
  44. Finland M. 44.  1979. Emergence of antibiotic resistance in hospitals, 1935–1975. Rev. Infect. Dis. 1:14–22 [Google Scholar]
  45. Finley RL, Collignon P, Larsson DGJ, McEwen SA, Li X-Z. 45.  et al. 2013. The scourge of antibiotic resistance: the important role of the environment. Clin. Infect. Dis. 57:5704–10 [Google Scholar]
  46. Fitzpatrick D, Walsh F. 46.  2016. Antibiotic resistance genes across a wide variety of metagenomes. FEMS Microbiol. Ecol. 92:2fiv168 [Google Scholar]
  47. Flach C-F, Johnning A, Nilsson I, Smalla K, Kristiansson E, Larsson DGJ. 47.  2015. Isolation of novel IncA/C and IncN fluoroquinolone resistance plasmids from an antibiotic-polluted lake. J. Antimicrob. Chemother. 70:102709–17 [Google Scholar]
  48. Forsberg KJ, Patel S, Wencewicz TA, Dantas G. 48.  2015. The tetracycline destructases: a novel family of tetracycline-inactivating enzymes. Chem. Biol. 22:7888–97 [Google Scholar]
  49. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G. 49.  2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:60981107–11 [Google Scholar]
  50. Fournier P-E, Vallenet D, Barbe V, Ogata H, Robert C, Raoult D. 50.  2006. Comparative genomics of multidrug resistance in Acinetobacter baumannii. PLOS Genet 2:1e7 [Google Scholar]
  51. Gao M, Jia R, Qiu T, Han M, Wang X. 51.  2016. Size-related bacterial diversity and tetracycline resistance gene abundance in the air of concentrated poultry feeding operations. Environ. Pollut. 220:1342–48 [Google Scholar]
  52. Gao X-L, Shao M-F, Luo Y, Dong Y-F, Ouyang F. 52.  et al. 2016. Airborne bacterial contaminations in typical Chinese wet market with live poultry trade. Sci. Total Environ. 572:681–87 [Google Scholar]
  53. Gaze WH, Krone SM, Larsson DGJ, Li X-Z, Robinson JA. 53.  et al. 2013. Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg. Infect. Dis. 19:7e120871 [Google Scholar]
  54. Gillings MR. 54.  2014. Integrons: past, present, and future. Microbiol. Mol. Biol. Rev. 78:2257–77 [Google Scholar]
  55. Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM, Zhu Y-G. 55.  2015. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J 9:61269–79 [Google Scholar]
  56. Gillings MR, Stokes HW. 56.  2012. Are humans increasing bacterial evolvability?. Trends Ecol. Evol. 27:6346–52 [Google Scholar]
  57. Gilliver MA, Bennett M, Begon M, Hazel SM, Hart CA. 57.  1999. Antibiotic resistance found in wild rodents. Nature 401:6750233–34 [Google Scholar]
  58. Hall BG, Barlow M. 58.  2004. Evolution of the serine β-lactamases: past, present and future. Drug Resist. Updates 7:2111–23 [Google Scholar]
  59. Hall BG, Salipante SJ, Barlow M. 59.  2004. Independent origins of subgroup Bl+B2 and subgroup B3 metallo-β-lactamases. J. Mol. Evol. 59:1133–41 [Google Scholar]
  60. Hall RM. 60.  2012. Integrons and gene cassettes: hotspots of diversity in bacterial genomes. Ann. N. Y. Acad. Sci. 1267:71–78 [Google Scholar]
  61. Hamidian M, Holt KE, Hall RM. 61.  2015. Genomic resistance island AGI1 carrying a complex class 1 integron in a multiply antibiotic-resistant ST25 Acinetobacter baumannii isolate.. J. Antimicrob. Chemother. 70:92519–23 [Google Scholar]
  62. Harbarth S, Balkhy HH, Goossens H, Jarlier V, Kluytmans J. 62.  et al. 2015. Antimicrobial resistance: One world, one fight!. Antimicrob. Resist. Infect. Control 4:49 [Google Scholar]
  63. Hatosy SM, Martiny AC. 63.  2015. The ocean as a global reservoir of antibiotic resistance genes. Appl. Environ. Microbiol. 81:217593–99 [Google Scholar]
  64. Heuer H, Schmitt H, Smalla K. 64.  2011. Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 14:3236–43 [Google Scholar]
  65. Hofreiter M, Serre D, Poinar HN, Kuch M, Pääbo S. 65.  2001. Ancient DNA. Nat. Rev. Genet. 2:5353–59 [Google Scholar]
  66. Hsu T, Joice R, Vallarino J, Abu-Ali G, Hartmann EM. 66.  et al. 2016. Urban transit system microbial communities differ by surface type and interaction with humans and the environment. mSystems 1:3e00018–16 [Google Scholar]
  67. Hu Y, Yang X, Li J, Lv N, Liu F. 67.  et al. 2016. The transfer network of bacterial mobile resistome connecting animal and human microbiome. Appl. Environ. Microbiol. 82:226672–81 [Google Scholar]
  68. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ. 68.  et al. 2016. A new view of the tree of life. Nat. Microbiol. 1:516048 [Google Scholar]
  69. Icgen B. 69.  2016. VanA-type MRSA (VRSA) emerged in surface waters. Bull. Environ. Contam. Toxicol. 97:3359–66 [Google Scholar]
  70. Inglis DO, Binkley J, Skrzypek MS, Arnaud MB, Cerqueira GC. 70.  et al. 2013. Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans. A. fumigatus, A. niger and A. oryzae. BMC Microbiol 13:191 [Google Scholar]
  71. Ishihara S, Bitner JJ, Farley GH, Gillock ET. 71.  2013. Vancomycin-resistant gram-positive cocci isolated from the saliva of wild songbirds. Curr. Microbiol. 66:4337–43 [Google Scholar]
  72. Jacoby GA. 72.  2009. AmpC β-lactamases. Clin. Microbiol. Rev. 22:1161–82 [Google Scholar]
  73. Jansson JK, Taş N. 73.  2014. The microbial ecology of permafrost. Nat. Rev. Microbiol. 12:6414–25 [Google Scholar]
  74. Johnson TA, Stedtfeld RD, Wang Q, Cole JR, Hashsham SA. 74.  et al. 2016. Clusters of antibiotic resistance genes enriched together stay together in swine agriculture. mBio 7:2e02214–15 [Google Scholar]
  75. Jones C, Stanley J. 75.  1992. Salmonella plasmids of the pre-antibiotic era. J. Gen. Microbiol. 138:1189–97 [Google Scholar]
  76. Kadavy DR, Hornby JM, Haverkost T, Nickerson KW. 76.  2000. Natural antibiotic resistance of bacteria isolated from larvae of the oil fly. Helaeomyia petrolei. Appl. Environ. Microbiol. 66:114615–19 [Google Scholar]
  77. Katz L, Baltz RH. 77.  2016. Natural product discovery: past, present, and future. J. Ind. Microbiol. Biotechnol. 43:2–3155–76 [Google Scholar]
  78. Kristiansson E, Fick J, Janzon A, Grabic R, Rutgersson C. 78.  et al. 2011. Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLOS ONE 6:2e17038 [Google Scholar]
  79. Landan G, Cohen G, Aharonowitz Y, Shuali Y, Graur D, Shiffman D. 79.  1990. Evolution of isopenicillin N synthase genes may have involved horizontal gene transfer. Mol. Biol. Evol. 7:5399–406 [Google Scholar]
  80. Larsson DGJ, de Pedro C, Paxeus N. 80.  2007. Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J. Hazard. Mater. 148:3751–55 [Google Scholar]
  81. Lax S, Gilbert JA. 81.  2015. Hospital-associated microbiota and implications for nosocomial infections. Trends Mol. Med. 21:7427–32 [Google Scholar]
  82. Leung MHY, Lee PKH. 82.  2016. The roles of the outdoors and occupants in contributing to a potential pan-microbiome of the built environment: a review. Microbiome 4:21 [Google Scholar]
  83. Li L-G, Xia Y, Zhang T. 83.  2016. Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J 11:651–62 [Google Scholar]
  84. Li X-Z, Plésiat P, Nikaido H. 84.  2015. The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clin. Microbiol. Rev. 28:2337–418 [Google Scholar]
  85. Literak I, Dolejska M, Janoszowska D, Hrusakova J, Meissner W. 85.  et al. 2010. Antibiotic-resistant Escherichia coli bacteria, including strains with genes encoding the extended-spectrum β-lactamase and QnrS, in waterbirds on the Baltic Sea Coast of Poland. Appl. Environ. Microbiol. 76:248126–34 [Google Scholar]
  86. Literak I, Dolejska M, Rybarikova J, Cizek A, Strejckova P. 86.  et al. 2009. Highly variable patterns of antimicrobial resistance in commensal Escherichia coli isolates from pigs, sympatric rodents, and flies. Microb. Drug Resist. 15:3229–37 [Google Scholar]
  87. Locey KJ, Lennon JT. 87.  2016. Scaling laws predict global microbial diversity. PNAS 113:215970–75 [Google Scholar]
  88. Loncaric I, Kübber-Heiss A, Posautz A, Stalder GL, Hoffmann D. 88.  et al. 2013. Characterization of methicillin-resistant Staphylococcus spp. carrying the mecC gene, isolated from wildlife. J. Antimicrob. Chemother. 68:102222–25 [Google Scholar]
  89. Lowe CF, Romney MG. 89.  2011. Bedbugs as vectors for drug-resistant bacteria. Emerg. Infect. Dis. 17:61132–34 [Google Scholar]
  90. Luo W, Xu Z, Riber L, Hansen LH. 90.  2016. Diverse gene functions in a soil mobilome. Soil Biol. Biochem. 101:175–83 [Google Scholar]
  91. Luo Y, Yang F, Mathieu J, Mao D, Wang Q. 91.  2014. Proliferation of multidrug-resistant New Delhi metallo-β-lactamase genes in municipal wastewater treatment plants in northern China. Environ. Sci. Technol. Lett. 1:126–30 [Google Scholar]
  92. Mallon DJP, Corkill JE, Hazel SM, Wilson JS, French NP. 92.  et al. 2002. Excretion of vancomycin-resistant enterococci by wild mammals. Emerg. Infect. Dis. 8:6636–38 [Google Scholar]
  93. Manaia CM. 93.  2016. Assessing the risk of antibiotic resistance transmission from the environment to humans: non-direct proportionality between abundance and risk. Trends Microbiol 25:3173–81 [Google Scholar]
  94. Marshall CG, Lessard IA, Park I, Wright GD. 94.  1998. Glycopeptide antibiotic resistance genes in glycopeptide-producing organisms. Antimicrob. Agents Chemother. 42:92215–20 [Google Scholar]
  95. Martinez JL, Sánchez MB, Martínez-Solano L, Hernandez A, Garmendia L. 95.  et al. 2009. Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS Microbiol. Rev. 33:2430–49 [Google Scholar]
  96. Martiny AC, Martiny JBH, Weihe C, Field A, Ellis JC. 96.  2011. Functional metagenomics reveals previously unrecognized diversity of antibiotic resistance genes in gulls. Front. Microbiol. 2:238 [Google Scholar]
  97. Martínez JL, Coque TM, Baquero F. 97.  2015. What is a resistance gene? Ranking risk in resistomes. Nat. Rev. Microbiol. 13:2116–23 [Google Scholar]
  98. Mazar Y, Cytryn E, Erel Y, Rudich Y. 98.  2016. Effect of dust storms on the atmospheric microbiome in the eastern Mediterranean. Environ. Sci. Technol. 50:84194–202 [Google Scholar]
  99. Mazel D. 99.  2006. Integrons: agents of bacterial evolution. Nat. Rev. Microbiol. 4:8608–20 [Google Scholar]
  100. Middleton JH, Ambrose A. 100.  2005. Enumeration and antibiotic resistance patterns of fecal indicator organisms isolated from migratory Canada geese (Branta canadensis). J. Wildl. Dis. 41:2334–41 [Google Scholar]
  101. Mindlin SZ, Soina VS, Petrova MA, Gorlenko ZM. 101.  2008. Isolation of antibiotic resistance bacterial strains from Eastern Siberia permafrost sediments. Russ. J. Genet. 44:127–34 [Google Scholar]
  102. Mitova MI, Lang G, Wiese J, Imhoff JF. 102.  2008. Subinhibitory concentrations of antibiotics induce phenazine production in a marine Streptomyces sp. J. Nat. Prod. 71:5824–27 [Google Scholar]
  103. Mora M, Mahnert A, Koskinen K, Pausan MR, Oberauner-Wappis L. 103.  et al. 2016. Microorganisms in confined habitats: microbial monitoring and control of intensive care units, operating rooms, cleanrooms and the international space station. Front. Microbiol. 7:1573 [Google Scholar]
  104. Moree WJ, Phelan VV, Wu C-H, Bandeira N, Cornett DS. 104.  et al. 2012. Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. PNAS 109:3413811–16 [Google Scholar]
  105. Nazni WA, Luke H, Wan Rozita WM, Abdullah AG, Sa'diyah I. 105.  et al. 2005. Determination of the flight range and dispersal of the house fly, Musca domestica (L.) using mark release recapture technique. Trop. Biomed. 22:153–61 [Google Scholar]
  106. Nelson M, Jones SH, Edwards C, Ellis JC. 106.  2008. Characterization of Escherichia coli populations from gulls, landfill trash, and wastewater using ribotyping. Dis. Aquat. Org. 81:153–63 [Google Scholar]
  107. Nesme J, Cécillon S, Delmont TO, Monier J-M, Vogel TM, Simonet P. 107.  2014. Large-scale metagenomic-based study of antibiotic resistance in the environment. Curr. Biol. 24:101096–100 [Google Scholar]
  108. Nikaido H. 108.  2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67:4593–656 [Google Scholar]
  109. O'Brien J, Wright GD. 109.  2011. An ecological perspective of microbial secondary metabolism. Curr. Opin. Biotechnol. 22:4552–58 [Google Scholar]
  110. O'Neill J. 110.  2016. Tackling drug-resistance infections globally: final report and recommendations Wellcome Trust & HM Gov London:
  111. Österblad M, Norrdahl K, Korpimäki E, Huovinen P. 111.  2001. Antibiotic resistance: How wild are wild mammals?. Nature 409:681637–38 [Google Scholar]
  112. Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DGJ. 112.  2016. The structure and diversity of human, animal and environmental resistomes. Microbiome 4:54 [Google Scholar]
  113. Pawlowski AC, Wang W, Koteva K, Barton HA, McArthur AG, Wright GD. 113.  2016. A diverse intrinsic antibiotic resistome from a cave bacterium. Nat. Comm. 7:13803 [Google Scholar]
  114. Perron GG, Whyte L, Turnbaugh PJ, Goordial J, Hanage WP. 114.  et al. 2015. Functional characterization of bacteria isolated from ancient arctic soil exposes diverse resistance mechanisms to modern antibiotics. PLOS ONE 10:3e0069533 [Google Scholar]
  115. Perry J, Waglechner N, Wright G. 115.  2016. The prehistory of antibiotic resistance. Cold Spring Harb. Perspect. Med. 6:6a025197 [Google Scholar]
  116. Perry JA, Westman EL, Wright GD. 116.  2014. The antibiotic resistome: What's new?. Curr. Opin. Microbiol. 21:45–50 [Google Scholar]
  117. Perry JA, Wright GD. 117.  2014. Forces shaping the antibiotic resistome. BioEssays 36:121179–84 [Google Scholar]
  118. Poeta P, Radhouani H, Igrejas G, Goncalves A, Carvalho C. 118.  et al. 2008. Seagulls of the Berlengas Natural Reserve of Portugal as carriers of fecal Escherichia coli harboring CTX-M and TEM extended-spectrum β-lactamases. Appl. Environ. Microbiol. 74:237439–41 [Google Scholar]
  119. Poirel L, Potron A, La Cuesta De C, Cleary T, Nordmann P, Munoz-Price LS. 119.  2012. Wild coastline birds as reservoirs of broad-spectrum-β-lactamase-producing Enterobacteriaceae in Miami Beach, Florida. Antimicrob. Agents Chemother. 56:52756–58 [Google Scholar]
  120. Poirel L, Rodriguez-Martinez JM, Mammeri H, Liard A, Nordmann P. 120.  2005. Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob. Agents Chemother. 49:83523–25 [Google Scholar]
  121. Power ML, Emery S, Gillings MR. 121.  2013. Into the wild: dissemination of antibiotic resistance determinants via a species recovery program. PLOS ONE 8:5e63017 [Google Scholar]
  122. Radimersky T, Frolkova P, Janoszowska D, Dolejska M, Svec P. 122.  et al. 2010. Antibiotic resistance in faecal bacteria (Escherichia coli, Enterococcus spp.) in feral pigeons. J. Appl. Microbiol. 109:51687–95 [Google Scholar]
  123. Riesenfeld CS, Goodman RM, Handelsman J. 123.  2004. Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ. Microbiol. 6:9981–89 [Google Scholar]
  124. Robinson TP, Bu DP, Carrique-Mas J, Fèvre EM, Gilbert M. 124.  et al. 2016. Antibiotic resistance is the quintessential One Health issue. Trans. R. Soc. Trop. Med. Hyg 1107377–80 [Google Scholar]
  125. Rodriguez MM, Power P, Radice M, Vay C, Famiglietti A. 125.  et al. 2004. Chromosome-encoded CTX-M-3 from Kluyvera ascorbata: a possible origin of plasmid-borne CTX-M-1-derived cefotaximases. Antimicrob. Agents Chemother. 48:124895–97 [Google Scholar]
  126. Rolland RM, Hausfater G, Marshall B, Levy SB. 126.  1985. Antibiotic-resistant bacteria in wild primates: increased prevalence in baboons feeding on human refuse. Appl. Environ. Microbiol. 49:4791–94 [Google Scholar]
  127. Rutgersson C, Fick J, Marathe N. 127.  2014. Fluoroquinolones and qnr genes in sediment, well water, soil and human fecal flora in an Indian environment polluted by drug manufacturing. Environ. Sci. Technol. 48:147825–32 [Google Scholar]
  128. Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL. 128.  2008. Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv. Biol. 22:61600–7 [Google Scholar]
  129. Rybarikova J, Dolejska M, Materna D, Literak I, Cizek A. 129.  2010. Phenotypic and genotypic characteristics of antimicrobial resistant Escherichia coli isolated from symbovine flies, cattle and sympatric insectivorous house martins from a farm in the Czech Republic (2006–2007). Res. Vet. Sci. 89:2179–83 [Google Scholar]
  130. Santiago-Rodriguez TM, Fornaciari G, Luciani S, Dowd SE, Toranzos GA. 130.  et al. 2015. Gut microbiome of an 11th century A.D. pre-Columbian Andean mummy. PLOS ONE 10:9e0138135 [Google Scholar]
  131. Sender R, Fuchs S, Milo R. 131.  2016. Revised estimates for the number of human and bacteria cells in the body. PLOS Biol 14:8e1002533 [Google Scholar]
  132. Simões RR, Poirel L, Da Costa PM, Nordmann P. 132.  2009. Seagulls and beaches as reservoirs for multidrug-resistant Escherichia coli. Emerg. Infect. Dis. 16:1110–12 [Google Scholar]
  133. Sjölund M, Bonnedahl J, Hernandez J, Bengtsson S, Cederbrant G. 133.  et al. 2008. Dissemination of multidrug-resistant bacteria into the Arctic. Emerg. Infect. Dis. 14:170–72 [Google Scholar]
  134. Skurnik D, Ruimy R, Andremont A, Amorin C, Rouquet P. 134.  et al. 2006. Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J. Antimicrob. Chemother. 57:61215–19 [Google Scholar]
  135. Soucy SM, Huang J, Gogarten JP. 135.  2015. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16:8472–82 [Google Scholar]
  136. Surette MG. 136.  2013. Concentration-dependent activity of antibiotics in natural environments. Front. Microbiol. 4:20 [Google Scholar]
  137. Thaller MC, Migliore L, Marquez C, Tapia W, Cedeño V. 137.  et al. 2010. Tracking acquired antibiotic resistance in commensal bacteria of Galápagos land iguanas: no man, no resistance. PLOS ONE 5:2e8989 [Google Scholar]
  138. Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C. 138.  et al. 2016. Diversity, structure and convergent evolution of the global sponge microbiome. Nat. Comm. 7:11870 [Google Scholar]
  139. Tian B, Fadhil NH, Powell JE, Kwong WK, Moran NA. 139.  2012. Long-term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees. mBio 3:6e00377–12 [Google Scholar]
  140. Torres-Cortés G, Millán V, Ramírez-Saad HC, Nisa-Martínez R, Toro N, Martínez-Abarca F. 140.  2011. Characterization of novel antibiotic resistance genes identified by functional metagenomics on soil samples. Environ. Microbiol. 13:41101–14 [Google Scholar]
  141. Traxler MF, Watrous JD, Alexandrov T, Dorrestein PC, Kolter R. 141.  2013. Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. mBio 4:4e00459–13 [Google Scholar]
  142. Tsui WHW, Yim G, Wang HH, McClure JE, Surette MG, Davies J. 142.  2004. Dual effects of MLS antibiotics: transcriptional modulation and interactions on the ribosome. Chem. Biol. 11:91307–16 [Google Scholar]
  143. Ushida K, Segawa T, Kohshima S, Takeuchi N, Fukui K. 143.  et al. 2010. Application of real-time PCR array to the multiple detection of antibiotic resistant genes in glacier ice samples. J. Gen. Appl. Microbiol. 56:143–52 [Google Scholar]
  144. Veldman K, van Tulden P, Kant A, Testerink J, Mevius D. 144.  2013. Characteristics of cefotaxime-resistant Escherichia coli from wild birds in the Netherlands. Appl. Environ. Microbiol. 79:247556–61 [Google Scholar]
  145. Wagner DM, Klunk J, Harbeck M, Devault A. 145.  2014. Yersinia pestis and the plague of Justinian 541–543 AD: a genomic analysis. Lancet Infect. Dis. 14:4319–26 [Google Scholar]
  146. Waksman SA. 146.  1941. Antagonistic relations of microorganisms. Bacteriol. Rev. 5:3231–91 [Google Scholar]
  147. Waksman SA. 147.  1945. Microbial Antagonisms and Antibiotic Substances New York: Commonw. Fund
  148. Walsh F, Duffy B. 148.  2013. The culturable soil antibiotic resistome: a community of multi-drug resistant bacteria. PLOS ONE 8:6e65567 [Google Scholar]
  149. Warinner C, Rodrigues JFM, Vyas R, Trachsel C, Shved N. 149.  et al. 2014. Pathogens and host immunity in the ancient human oral cavity. Nat. Genet. 46:4336–44 [Google Scholar]
  150. Watrous J, Roach P, Alexandrov T. 150.  2012. Mass spectral molecular networking of living microbial colonies. PNAS 109:26e1743–52 [Google Scholar]
  151. Wichmann F, Udikovic-Kolic N, Andrew S, Handelsman J. 151.  2014. Diverse antibiotic resistance genes in dairy cow manure. mBio 5:2e01017–13 [Google Scholar]
  152. Winpisinger KA, Ferketich AK, Berry RL, Moeschberger ML. 152.  2005. Spread of Musca domestica (Diptera: Muscidae), from two caged layer facilities to neighboring residences in rural Ohio. J. Med. Entomol 425732–38 [Google Scholar]
  153. Wolters B, Widyasari-Mehta A, Kreuzig R, Smalla K. 153.  2016. Contaminations of organic fertilizers with antibiotic residues, resistance genes, and mobile genetic elements mirroring antibiotic use in livestock?. Appl. Microbiol. Biotechnol. 100:219343–53 [Google Scholar]
  154. Wright GD. 154.  2007. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5:3175–86 [Google Scholar]
  155. Wright GD. 155.  2010. Antibiotic resistance in the environment: A link to the clinic?. Curr. Opin. Microbiol. 13:5589–94 [Google Scholar]
  156. Xie W-Y, McGrath SP, Su J-Q, Hirsch PR, Clark IM. 156.  et al. 2016. Long-term impact of field applications of sewage sludge on soil antibiotic resistome. Environ. Sci. Technol. 50:2312602–11 [Google Scholar]
  157. Yim G, Huimi Wang H, Davies J. 157.  2006. The truth about antibiotics. Int. J. Med. Microbiol 2962–3163–70 [Google Scholar]
  158. Yim G, Huimi Wang H, Davies J. 158.  2007. Antibiotics as signalling molecules. Philos. Trans. R. Soc. B 362:14831195–200 [Google Scholar]
  159. Young IM. 159.  2004. Interactions and self-organization in the soil-microbe complex. Science 304:56771634–37 [Google Scholar]
  160. Zalasiewicz J, Williams M, Haywood A, Ellis M. 160.  2011. The Anthropocene: a new epoch of geological time?. Philos. Trans. R. Soc. A 369:1938833–34 [Google Scholar]
  161. Zhang Q-Q, Ying G-G, Pan C-G, Liu Y-S, Zhao J-L. 161.  2015. 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. 49:116772–82 [Google Scholar]
  162. Zhang X-X, Zhang T, Fang HHP. 162.  2009. Antibiotic resistance genes in water environment. Appl. Microbiol. Biotechnol. 82:3397–414 [Google Scholar]
  163. Zurek L, Ghosh A. 163.  2014. Insects represent a link between food animal farms and the urban environment for antibiotic resistance traits. Appl. Environ. Microbiol. 80:123562–67 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error