Lateral gene transfer, bacterial genome evolution, and the Anthropocene

Annals of the New York Academy of Sciences

Volumn 1389, Issue 1, 2017, Pages 20-36

  Gillings, Michael R ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

antibiotic resistance; horizontal gene transfer; microbial ecology; mobile DNA; resistome

Indexed keywords

ANTHROPOCENE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; GENETIC SELECTION; GEOLOGICAL TIME; HORIZONTAL GENE TRANSFER; HUMAN; HUMAN ACTIVITIES; MOLECULAR EVOLUTION; NONHUMAN; POLLUTION; ANIMAL; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIUM; DRUG EFFECTS; ECOSYSTEM; EVOLUTION; GENETICS; PHENOTYPE;

ANTIINFECTIVE AGENT; BACTERIAL DNA;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; BACTERIA; BACTERIAL INFECTIONS; BIOLOGICAL EVOLUTION; DNA, BACTERIAL; ECOSYSTEM; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GENOME, BACTERIAL; HUMANS; PHENOTYPE;

EID: 84990855002     PISSN: 00778923     EISSN: 17496632     Source Type: Journal    
DOI: 10.1111/nyas.13213     Document Type: Article

References (209)

1. Gogarten, J.P., W.F. Doolittle & J.G. Lawrence. 2002. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19: 2226–2238.
2. Ochman, H., J.G. Lawrence & E.A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299–304.
3. Soucy, S.M., J. Huang & J.P. Gogarten. 2015. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16: 472–482.
4. Cordero, O.X. & M.F. Polz. 2014. Explaining microbial genomic diversity in light of evolutionary ecology. Nat. Rev. Microbiol. 12: 263–273.
5. Doolittle, W.F. 2012. Population genomics: how bacterial species form and why they don't exist. Curr. Biol. 22: R451–R453.
6. Gogarten, J.P. & J.P. Townsend. 2005. Horizontal gene transfer, genome innovation and evolution. Nat. Rev. Microbiol. 3: 679–687.
7. Thompson, C.C., G.R. Amaral, M. Campeão, et al. 2015. Microbial taxonomy in the post-genomic era: rebuilding from scratch? Arch. Microbiol. 197: 359–370.
8. Bapteste, E. & Y. Boucher. 2008. Lateral gene transfer challenges principles of microbial systematics. Trends Microbiol. 16: 200–207.
9. Lukjancenko, O., T.M. Wassenaar & D.W. Ussery. 2010. Comparison of 61 sequenced Escherichia coli genomes. Microb. Ecol. 60: 708–720.
10. Tettelin, H., V. Masignani, M.J. Cieslewicz, et al. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome.” Proc. Natl. Acad. Sci. U.S.A. 102: 13950–13955.
11. Baumdicker, F., W.R. Hess & P. Pfaffelhuber. 2012. The infinitely many genes model for the distributed genome of bacteria. Genome Biol. Evol. 4: 443–456.
12. Bapteste, E., M.A. O'Malley, R.G. Beiko, et al. 2009. Prokaryotic evolution and the tree of life are two different things. Biol. Direct 4: 34.
13. Wolf, Y.I., I.B. Rogozin, N.V. Grishin, et al. 2002. Genome trees and the tree of life. Trends Genet. 18: 472–479.
14. Brown, J.R. 2003. Ancient horizontal gene transfer. Nat. Rev. Genet. 4: 121–132.
15. Fournier, G.P., C.P. Andam & J.P. Gogarten. 2015. Ancient horizontal gene transfer and the last common ancestors. BMC Evol. Biol. 15: 70.
16. Beiko, R.G., T.J. Harlow & M.A. Ragan. 2005. Highways of gene sharing in prokaryotes. Proc. Natl. Acad. Sci. U.S.A. 102: 14332–14337.
17. Jain, R., M.C. Rivera, J.E. Moore, et al. 2003. Horizontal gene transfer accelerates genome innovation and evolution. Mol. Biol. Evol. 20: 1598–1602.
18. Zhaxybayeva, O., P. Lapierre & J.P. Gogarten. 2004. Genome mosaicism and organismal lineages. Trends Genet. 20: 254–260.
19. Andam, C.P. & J.P. Gogarten. 2013. Biased gene transfer contributes to maintaining the tree of life. In Lateral Gene Transfer in Evolution. U. Gophna, Ed.: 263–274. Springer.
20. Swithers, K.S., S.M. Soucy & J.P. Gogarten. 2012. The role of reticulate evolution in creating innovation and complexity. Int. J. Evol. Biol. 2012: 418964.
21. Andam, C.P. & J.P. Gogarten. 2011. Biased gene transfer in microbial evolution. Nat. Rev. Microbiol. 9: 543–555.
22. Polz, M.F., E.J. Alm & W.P. Hanage. 2013. Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 29: 170–175.
23. Jain, R., M.C. Rivera & J.A. Lake. 1999. Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl. Acad. Sci. U.S.A. 96: 3801–3806.
24. Skippington, E. & M.A. Ragan. 2013. Lateral genetic transfer and cellular networks. In Lateral Gene Transfer in Evolution. U. Gophna, Ed.: 123–135. Springer.
25. Koonin, E.V. & Y.I. Wolf. 2008. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res. 36: 6688–6719.
26. Thomas, C.M. & K.M. Nielsen. 2005. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 3: 711–721.
27. Popa, O., E. Hazkani-Covo, G. Landan, et al. 2011. Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. Genome Res. 21: 599–609.
28. Francis, A.R. & M.M. Tanaka. 2012. Evolution of variation in presence and absence of genes in bacterial pathways. BMC Evol. Biol. 12: 55.
29. Pál, C., B. Papp & M.J. Lercher. 2005. Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat. Genet. 37: 1372–1375.
30. Yano, H., M. Miyakoshi, K. Ohshima, et al. 2010. Complete nucleotide sequence of TOL plasmid pDK1 provides evidence for evolutionary history of IncP-7 catabolic plasmids. J. Bacteriol. 192: 4337–4347.
31. Ochman, H. & N.A. Moran. 2001. Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292: 1096–1099.
32. Raymond, J., O. Zhaxybayeva, J.P. Gogarten, et al. 2002. Whole-genome analysis of photosynthetic prokaryotes. Science 298: 1616–1620.
33. Andam, C.P., S.M. Carver & S.T. Berthrong. 2015. Horizontal gene flow in managed ecosystems. Annu. Rev. Ecol. Evol. Syst. 46: 121–143.
34. Davies, J. & D. Davies. 2010. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74: 417–433.
35. Palumbi, S.R. 2001. Humans as the world's greatest evolutionary force. Science 293: 1786–1790.
36. Steffen, W., P.J. Crutzen & J.R. McNeill. 2007. The Anthropocene: are humans now overwhelming the great forces of nature. Ambio 36: 614–621.
37. Gillings, M.R. & I.T. Paulsen. 2014. Microbiology of the Anthropocene. Anthropocene 5: 1–8.
38. Gillings, M.R., I.T. Paulsen & S.G. Tetu. 2015. Ecology and evolution of the human microbiota: fire, farming and antibiotics. Genes 6: 841–857.
39. Gillings, M.R. & H.W. Stokes. 2012. Are humans increasing bacterial evolvability? Trends Ecol. Evol. 27: 346–352.
40. Stokes, H.W. & M.R. Gillings. 2011. Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiol. Rev. 35: 790–819.
41. Koonin, E.V., K.S. Makarova & L. Aravind. 2001. Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55: 709–742.
42. Lercher, M.J. & C. Pál. 2008. Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Mol. Biol. Evol. 25: 559–567.
43. Pál, C., B. Papp & M.J. Lercher. 2005. Horizontal gene transfer depends on gene content of the host. Bioinformatics 21: ii222–ii223.
44. Carraro, N. & V. Burrus. 2015. The dualistic nature of integrative and conjugative elements. Mob. Genet. Elements 5: 98–102.
45. Chen, I., P.J. Christie & D. Dubnau. 2005. The ins and outs of DNA transfer in bacteria. Science 310: 1456–1460.
46. Chen, I. & D. Dubnau. 2004. DNA uptake during bacterial transformation. Nat. Rev. Microbiol. 2: 241–249.
47. Canchaya, C., G. Fournous, S. Chibani-Chennoufi, et al. 2003. Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6: 417–424.
48. Lang, A.S. & J.T. Beatty. 2007. Importance of widespread gene transfer agent genes in α-proteobacteria. Trends Microbiol. 15: 54–62.
49. Lang, A.S., O. Zhaxybayeva & J.T. Beatty. 2012. Gene transfer agents: phage-like elements of genetic exchange. Nat. Rev. Microbiol. 10: 472–482.
50. Kuchinski, K.S., C.A. Brimacombe, A.B. Westbye, et al. 2016. The SOS response master regulator LexA regulates the gene transfer agent of Rhodobacter capsulatus and represses transcription of the signal transduction protein CckA. J. Bacteriol. 198: 1137–1148.
51. Brimacombe, C.A., H. Ding, J.A. Johnson, et al. 2015. Homologues of genetic transformation DNA import genes are required for Rhodobacter capsulatus gene transfer agent recipient capability regulated by the response regulator CtrA. J. Bacteriol. 197: 2653–2663.
52. McDaniel, L.D., E. Young, J. Delaney, et al. 2010. High frequency of horizontal gene transfer in the oceans. Science 330: 50.
53. Berleman, J. & M. Auer. 2013. The role of bacterial outer membrane vesicles for intra- and interspecies delivery. Environ. Microbiol. 15: 347–354.
54. Biller, S.J., F. Schubotz, S.E. Roggensack, et al. 2014. Bacterial vesicles in marine ecosystems. Science 343: 183–186.
55. Pande, S., S. Shitut, L. Freund, et al. 2015. Metabolic cross-feeding via intercellular nanotubes among bacteria. Nat. Commun. 6: 6238.
56. Dubey, G.P. & S. Ben-Yehuda. 2011. Intercellular nanotubes mediate bacterial communication. Cell 144: 590–600.
57. Dubey, G.P., G.B.M. Mohan, A. Dubrovsky, et al. 2016. Architecture and characteristics of bacterial nanotubes. Dev. Cell 36: 453–461.
58. Leplae, R., G. Lima-Mendez & A. Toussaint. 2010. ACLAME: a CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res. 38: D57–D61.
59. Siefert, J.L. 2009. Defining the mobilome. In Horizontal Gene Transfer: Genomes in Flux. Vol. 532. M.B. Gogarten, J.P. Gogarten & L.C. Olendzenski, Eds.: 13–27. Humana Press.
60. Darmon, E. & D.R. Leach. 2014. Bacterial genome instability. Microbiol. Mol. Biol. Rev. 78: 1–39.
61. Halary, S., J.W. Leigh, B. Cheaib, et al. 2010. Network analyses structure genetic diversity in independent genetic worlds. Proc. Natl. Acad. Sci. U.S.A. 107: 127–132.
62. Osborn, A.M. & D. Böltner. 2002. When phage, plasmids, and transposons collide: genomic islands, and conjugative-and mobilizable-transposons as a mosaic continuum. Plasmid 48: 202–212.
63. Slater, F.R., M.J. Bailey, A.J. Tett, et al. 2008. Progress towards understanding the fate of plasmids in bacterial communities. FEMS Microbiol. Ecol. 66: 3–13.
64. Norman, A., L.H. Hansen & S.J. Sørensen. 2009. Conjugative plasmids: vessels of the communal gene pool. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364: 2275–2289.
65. Smillie, C., M.P. Garcillán-Barcia, M.V. Francia, et al. 2010. Mobility of plasmids. Microbiol. Mol. Biol. Rev. 74: 434–452.
66. Nicolas, E., M. Lambin, D. Dandoy, et al. 2015. The Tn3-family of replicative transposons. Microbiol. Spectr. 3. doi:10.1128/microbiolspec.MDNA3-0060-2014.
67. Siguier, P., E. Gourbeyre, A. Varani, et al. 2015. Everyman's guide to bacterial insertion sequences. Microbiol. Spectr. 3: MDNA3-0030-2014.
68. Penadés, J.R., J. Chen, N. Quiles-Puchalt, et al. 2015. Bacteriophage-mediated spread of bacterial virulence genes. Curr. Opin. Microbiol. 23: 171–178.
69. Burrus, V. & M.K. Waldor. 2004. Shaping bacterial genomes with integrative and conjugative elements. Res. Microbiol. 155: 376–386.
70. Guglielmini, J., L. Quintais, M.P. Garcillán-Barcia, et al. 2011. The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet. 7: e1002222.
71. Johnson, C.M. & A.D. Grossman. 2015. Integrative and conjugative elements (ICEs): what they do and how they work. Annu. Rev. Genet. 49: 577–601.
72. Bellanger, X., S. Payot, N. Leblond-Bourget, et al. 2014. Conjugative and mobilizable genomic islands in bacteria: evolution and diversity. FEMS Microbiol. Rev. 38: 720–760.
73. Dobrindt, U., B. Hochhut, U. Hentschel, et al. 2004. Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2: 414–424.
74. Escudero, J.A., C. Loot, A. Nivina, et al. 2015. The integron: adaptation on demand. Microbiol. Spectr. 3: MDNA3-0019-2014.
75. Gillings, M.R. 2014. Integrons: past, present, and future. Microbiol. Mol. Biol. Rev. 78: 257–277.
76. Gillings, M., Y. Boucher, M. Labbate, et al. 2008. The evolution of class 1 integrons and the rise of antibiotic resistance. J. Bacteriol. 190: 5095–5100.
77. Whitfield, J. 2004. Origins of life: born in a watery commune. Nature 427: 674–676.
78. Kohanski, M.A., D.J. Dwyer, B. Hayete, et al. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797–810.
79. Miller, C., L.E. Thomsen, C. Gaggero, et al. 2004. SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305: 1629–1631.
80. Shapiro, R.S. 2015. Antimicrobial-induced DNA damage and genomic instability in microbial pathogens. PLoS Pathog. 11: e1004678.
81. Jara, L.M., P. Cortés, G. Bou, et al. 2015. Differential roles of antimicrobials in the acquisition of drug resistance through activation of the SOS response in Acinetobacter baumannii. Antimicrob. Agents Chemother. 59: 4318–4320.
82. Erill, I., S. Campoy & J. Barbé. 2007. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev. 31: 637–656.
83. Le-Minh, N., S.J. Khan, J.E. Drewes, et al. 2010. Fate of antibiotics during municipal water recycling treatment processes. Water Res. 44: 4295–4323.
84. Sarmah, A.K., M.T. Meyer & A.B.A. Boxall. 2006. A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65: 725–759.
85. Cabello, F.C., H.P. Godfrey, A.H. Buschmann, et al. 2016. Aquaculture as yet another environmental gateway to the development and globalisation of antimicrobial resistance. Lancet Infect. Dis. 16: e127–e133.
86. Gillings, M.R. 2013. Evolutionary consequences of antibiotic use for the resistome, mobilome and microbial pangenome. Front. Microbiol. 4: 4.
87. Zuccato, E., S. Castiglioni, R. Bagnati, et al. 2010. Source, occurrence and fate of antibiotics in the Italian aquatic environment. J. Hazard. Mater. 179: 1042–1048.
88. Larsson, D.J. 2014. Pollution from drug manufacturing: review and perspectives. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369. pii: 20130571.
89. Michel, B. 2005. After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol. 3: e255.
90. Andersson, D.I. & D. Hughes. 2014. Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol. 12: 465–478.
91. Helfrich, S., E. Pfeifer, C. Krämer, et al. 2015. Live cell imaging of SOS and prophage dynamics in isogenic bacterial populations. Mol. Microbiol. 98: 636–650.
92. Nanda, A.M., K. Thormann & J. Frunzke. 2015. Impact of spontaneous prophage induction on the fitness of bacterial populations and host–microbe interactions. J. Bacteriol. 197: 410–419.
93. Oppenheim, A.B., O. Kobiler, J. Stavans, et al. 2005. Switches in bacteriophage lambda development. Annu. Rev. Genet. 39: 409–429.
94. Beaber, J.W., B. Hochhut & M.K. Waldor. 2004. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427: 72–74.
95. Chow, L., L. Waldron & M.R. Gillings. 2015. Potential impacts of aquatic pollutants: sub-clinical antibiotic concentrations induce genome changes and promote antibiotic resistance. Front. Microbiol. 6: 803.
96. Nagel, M., T. Reuter, A. Jansen, et al. 2011. Influence of ciprofloxacin and vancomycin on mutation rate and transposition of IS256 in Staphylococcus aureus. Int. J. Med. Microbiol. 301: 229–236.
97. Maiques, E., C. Úbeda, S. Campoy, et al. 2006. β-Lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J. Bacteriol. 188: 2726–2729.
98. Úbeda, C., E. Maiques, E. Knecht, et al. 2005. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol. Microbiol. 56: 836–844.
99. Cambray, G., N. Sanchez-Alberola, S. Campoy, et al. 2011. Prevalence of SOS-mediated control of integron integrase expression as an adaptive trait of chromosomal and mobile integrons. Mob. DNA 2: 6.
100. Guerin, E., G. Cambray, N. Sanchez-Alberola, et al. 2009. The SOS response controls integron recombination. Science 324: 1034.
101. Boucher, Y., O.X. Cordero, A. Takemura, et al. 2011. Local mobile gene pools rapidly cross species boundaries to create endemicity within global Vibrio cholerae populations. mBio 2. doi:10.1128/mBio.00335-10.
102. Engelstädter, J., K. Harms & P.J. Johnsen. 2016. The evolutionary dynamics of integrons in changing environments. ISME J. 10:1296–1307.
103. Westbye, A., M. Leung, S. Florizone, et al. 2013. Phosphate concentration and the putative sensor kinase protein CckA modulate cell lysis and release of the Rhodobacter capsulatus gene transfer agent. J. Bacteriol. 195: 5025–5040.
104. Paget, E. & P. Simonet. 1994. On the track of natural transformation in soil. FEMS Microbiol. Ecol. 15: 109–117.
105. Levy-Booth, D.J., R.G. Campbell, R.H. Gulden, et al. 2007. Cycling of extracellular DNA in the soil environment. Soil Biol. Biochem. 39: 2977–2991.
106. Pedersen, M.W., S. Overballe-Petersen, L. Ermini, et al. 2015. Ancient and modern environmental DNA. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370: 20130383.
107. Fuhrman, J.A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399: 541–548.
108. Suttle, C.A. 2007. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5: 801–812.
109. Johnston, C., B. Martin, G. Fichant, et al. 2014. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat. Rev. Microbiol. 12: 181–196.
110. Charpentier, X., P. Polard & J.-P. Claverys. 2012. Induction of competence for genetic transformation by antibiotics: convergent evolution of stress responses in distant bacterial species lacking SOS? Curr. Opin. Microbiol. 15: 570–576.
111. Slager, J., M. Kjos, L. Attaiech, et al. 2014. Antibiotic-induced replication stress triggers bacterial competence by increasing gene dosage near the origin. Cell 157: 395–406.
112. Spoering, A.L. & M.S. Gilmore. 2006. Quorum sensing and DNA release in bacterial biofilms. Curr. Opin. Microbiol. 9: 133–137.
113. Whitchurch, C.B., T. Tolker-Nielsen, P.C. Ragas, et al. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
114. Sorensen, S.J., M. Bailey, L.H. Hansen, et al. 2005. Studying plasmid horizontal transfer in situ: a critical review. Nat. Rev. Microbiol. 3: 700–710.
115. Hiller, N.L., A. Ahmed, E. Powell, et al. 2010. Generation of genic diversity among Streptococcus pneumoniae strains via horizontal gene transfer during a chronic polyclonal pediatric infection. PLoS Pathog. 6: e1001108.
116. Antonova, E.S. & B.K. Hammer. 2011. Quorum-sensing autoinducer molecules produced by members of a multispecies biofilm promote horizontal gene transfer to Vibrio cholerae. FEMS Microbiol. Lett. 322: 68–76.
117. Madsen, J.S., M. Burmølle, L.H. Hansen, et al. 2012. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol. Med. Microbiol. 65: 183–195.
118. Gillings, M.R., M.P. Holley & H.W. Stokes. 2009. Evidence for dynamic exchange of qac gene cassettes between class 1 integrons and other integrons in freshwater biofilms. FEMS Microbiol. Lett. 296: 282–288.
119. Koenig, J.E., D.G. Bourne, B. Curtis, et al. 2011. Coral-mucus-associated Vibrio integrons in the Great Barrier Reef: genomic hotspots for environmental adaptation. ISME J. 5: 962–972.
120. Khan, S., C.W. Knapp & T.K. Beattie. 2016. Antibiotic resistant bacteria found in municipal drinking water. Environ. Process. 3: 541–552.
121. Farkas, A., C. Crăciunaş, C. Chiriac, et al. 2016. Exploring the role of coliform bacteria in class 1 integron carriage and biofilm formation during drinking water treatment. Microb. Ecol. [Epub ahead of print.]
122. Fux, C.A., J.W. Costerton, P.S. Stewart, et al. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13: 34–40.
123. Lundström, S.V., M. Östman, J. Bengtsson-Palme, et al. 2016. Minimal selective concentrations of tetracycline in complex aquatic bacterial biofilms. Sci. Total Environ. 553: 587–595.
124. Hastings, P.J., S.M. Rosenberg & A. Slack. 2004. Antibiotic-induced lateral transfer of antibiotic resistance. Trends Microbiol. 12: 401–404.
125. Jutkina, J., C. Rutgersson, C.-F. Flach, et al. 2016. An assay for determining minimal concentrations of antibiotics that drive horizontal transfer of resistance. Sci. Total Environ. 548: 131–138.
126. Lopatkin, A.J., S. Huang, R.P. Smith, et al. 2016. Antibiotics as a selective driver for conjugation dynamics. Nat. Microbiol. 1: 16044.
127. Moura, A., I. Henriques, K. Smalla, et al. 2010. Wastewater bacterial communities bring together broad-host range plasmids, integrons and a wide diversity of uncharacterized gene cassettes. Res. Microbiol. 161: 58–66.
128. Schlüter, A., L. Krause, R. Szczepanowski, et al. 2008. Genetic diversity and composition of a plasmid metagenome from a wastewater treatment plant. J. Biotechnol. 136: 65–76.
129. Graham, D.W., S. Olivares-Rieumont, C.W. Knapp, et al. 2011. Antibiotic resistance gene abundances associated with waste discharges to the Almendares River near Havana, Cuba. Environ. Sci. Technol. 45: 418–424.
130. Proia, L., D. von Schiller, A. Sànchez-Melsió, et al. 2016. Occurrence and persistence of antibiotic resistance genes in river biofilms after wastewater inputs in small rivers. Environ. Pollut. 210: 121–128.
131. Pruden, A., M. Arabi & H.N. Storteboom. 2012. Correlation between upstream human activities and riverine antibiotic resistance genes. Environ. Sci. Technol. 46: 11541–11549.
132. Gaze, W.H., L. Zhang, N.A. Abdouslam, et al. 2011. Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J. 5: 1253–1261.
133. Han, X.M., H.W. Hu, X.Z. Shi, et al. 2016. Impacts of reclaimed water irrigation on soil antibiotic resistome in urban parks of Victoria, Australia. Environ. Pollut. 211: 48–57.
134. Muziasari, W.I., K. Pärnänen, T.A. Johnson, et al. 2016. Aquaculture changes the profile of antibiotic resistance and mobile genetic element associated genes in Baltic Sea sediments. FEMS Microbiol. Ecol. 92: fiw052.
135. Zhang, S., S. Pang, P. Wang, et al. 2016. Antibiotic concentration and antibiotic-resistant bacteria in two shallow urban lakes after stormwater event. Environ. Sci. Pollut. Res. 23: 9984–9992
136. Binh, C.T.T., H. Heuer, M. Kaupenjohann, et al. 2009. Diverse aadA gene cassettes on class 1 integrons introduced into soil via spread manure. Res. Microbiol. 160: 427–433.
137. Byrne-Bailey, K., W.H. Gaze, L. Zhang, et al. 2011. Integron prevalence and diversity in manured soil. Appl. Environ. Microbiol. 77: 684–687.
138. Liu, J., Z. Zhao, L. Orfe, et al. 2016. Soil-borne reservoirs of antibiotic-resistant bacteria are established following therapeutic treatment of dairy calves. Environ. Microbiol. 18: 557–564.
139. Gillings, M. 2015. Pollution by antibiotics and resistance genes: dissemination into Australian wildlife. In Austral Ark: The State of Wildlife in Australia and New Zealand. A. Stow, N. Maclean & G.I. Holwell, Eds.: 186–196. Cambridge: Cambridge University Press.
140. Vittecoq, M., S. Godreuil, F. Prugnolle, et al. 2016. Antimicrobial resistance in wildlife (Review). J. Appl. Ecol. 53: 519–529.
141. Gillings, M.R., W.H. Gaze, A. Pruden, et al. 2015. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 9: 1269–1279.
142. Berendonk, T.U., C.M. Manaia, C. Merlin, et al. 2015. Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 13: 310–317.
143. Pruden, A., D.J. Larsson, A. Amézquita, et al. 2013. Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ. Health Perspect. 121: 878–885.
144. Smil, V. 2003. The Earth's Biosphere: Evolution, Dynamics, and Change. Cambridge, MA: MIT Press.
145. Smillie, C.S., M.B. Smith, J. Friedman, et al. 2011. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480: 241–244.
146. Ma, L., Y. Xia, B. Li, et al. 2015. Metagenomic assembly reveals hosts of antibiotic resistance genes and the shared resistome in pig, chicken and human feces. Environ. Sci. Technol. 50: 420–427.
147. Baltrus, D.A. 2013. Exploring the costs of horizontal gene transfer. Trends Ecol. Evol. 28: 489–495.
148. Martinez, J.L. 2008. Antibiotics and antibiotic resistance genes in natural environments. Science 321: 365–367.
149. Wellington, E.M., A. Boxall, P. Cross, et al. 2013. The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect. Dis. 13: 155–165.
150. D'Costa, V.M., K.M. McGrann, D.W. Hughes, et al. 2006. Sampling the antibiotic resistome. Science 311: 374–377.
151. Forsberg, K.J., A. Reyes, B. Wang, et al. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337: 1107–1111.
152. Wright, G.D. 2010. The antibiotic resistome. Expert Opin. Drug Discov. 5: 779–788.
153. Allen, H.K., J. Donato, H.H. Wang, et al. 2010. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8: 251–259.
154. Riesenfeld, C.S., R.M. Goodman & J. Handelsman. 2004. Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ. Microbiol. 6: 981–989.
155. Mindlin, S., L. Minakhin, M. Petrova, et al. 2005. Present-day mercury resistance transposons are common in bacteria preserved in permafrost grounds since the Upper Pleistocene. Res. Microbiol. 156: 994–1004.
156. Poulain, A.J., S. Aris-Brosou, J.M. Blais, et al. 2015. Microbial DNA records historical delivery of anthropogenic mercury. ISME J. 9: 2541–2550.
157. Kholodii, G., S. Mindlin, M. Petrova, et al. 2003. Tn5060 from the Siberian permafrost is most closely related to the ancestor of Tn21 prior to integron acquisition. FEMS Microbiol. Lett. 226: 251–255.
158. Liebert, C.A., R.M. Hall & A.O. Summers. 1999. Transposon Tn21, flagship of the floating genome. Microbiol. Mol. Biol. Rev. 63: 507–522.
159. Hobman, J.L. & L.C. Crossman. 2015. Bacterial antimicrobial metal ion resistance. J. Med. Microbiol. 64: 471–497.
160. Datta, N. & V.M. Hughes. 1983. Plasmids of the same Inc groups in Enterobacteria before and after the medical use of antibiotics. Nature 306: 616–617.
161. Hughes, V.M. & N. Datta. 1983. Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era. Nature 302: 725–726.
162. Gillings, M.R., D. Xuejun, S.A. Hardwick, et al. 2009. Gene cassettes encoding resistance to quaternary ammonium compounds: a role in the origin of clinical class 1 integrons? ISME J. 3: 209–215.
163. Stokes, H.W., C.L. Nesbø, M. Holley, et al. 2006. Class 1 integrons potentially predating the association with Tn402-like transposition genes are present in a sediment microbial community. J. Bacteriol. 188: 5722–5730.
164. Sköld, O. 2000. Sulfonamide resistance: mechanisms and trends. Drug Resist. Updat. 3: 155–160.
165. Stokes, H. & R. Hall. 1989. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol. Microbiol. 3: 1669–1683.
166. Biskri, L., M. Bouvier, A.-M. Guérout, et al. 2005. Comparative study of class 1 integron and Vibrio cholerae superintegron integrase activities. J. Bacteriol. 187: 1740–1750.
167. Martinez-Freijo, P., A. Fluit, F. Schmitz, et al. 1998. Class I integrons in Gram-negative isolates from different European hospitals and association with decreased susceptibility to multiple antibiotic compounds. J. Antimicrob. Chemother. 42: 689–696.
168. van Essen-Zandbergen, A., H. Smith, K. Veldman, et al. 2007. Occurrence and characteristics of class 1, 2 and 3 integrons in Escherichia coli, Salmonella and Campylobacter spp. in the Netherlands. J. Antimicrob. Chemother. 59: 746–750.
169. Goldstein, C., M.D. Lee, S. Sanchez, et al. 2001. Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics. Antimicrob. Agents Chemother. 45: 723–726.
170. Nandi, S., J.J. Maurer, C. Hofacre, et al. 2004. Gram-positive bacteria are a major reservoir of class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. U.S.A. 101: 7118–7122.
171. Xu, Y., Q.Q. Luo & M.G. Zhou. 2013. Identification and characterization of integron-mediated antibiotic resistance in the phytopathogen Xanthomonas oryzae pv. oryzae. PLoS One 8: e55962.
172. Partridge, S.R., G. Tsafnat, E. Coiera, et al. 2009. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol. Rev. 33: 757–784.
173. Minakhina, S., G. Kholodii, S. Mindlin, et al. 1999. Tn5053 family transposons are res site hunters sensing plasmidal res sites occupied by cognate resolvases. Mol. Microbiol. 33: 1059–1068.
174. Partridge, S.R., H.J. Brown, H. Stokes, et al. 2001. Transposons Tn1696 and Tn21and their integrons In4 and In2 have independent origins. Antimicrob. Agents Chemother. 45: 1263–1270.
175. Toussaint, A. & M. Chandler. 2012. Prokaryote genome fluidity: toward a system approach of the mobilome. In Bacterial Molecular Networks. Vol. 804. J. Helden, A. Toussaint & D. Thieffry, Eds.: 57–80. New York: Springer.
176. Moura, A., C. Oliveira, I. Henriques, et al. 2012. Broad diversity of conjugative plasmids in integron-carrying bacteria from wastewater environments. FEMS Microbiol. Lett. 330: 157–164.
177. Zhang, T., X.-X. Zhang & L. Ye. 2011. Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PLoS One 6: e26041.
178. Baquero, F., J.-L. Martínez & R. Cantón. 2008. Antibiotics and antibiotic resistance in water environments. Curr. Opin. Biotechnol. 19: 260–265.
179. Martinez, J.L. 2009. Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ. Pollut. 157: 2893–2902.
180. Kristiansson, E., J. Fick, A. Janzon, et al. 2011. Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS One 6: e17038.
181. Taylor, N.G.H., D.W. Verner-Jeffreys & C. Baker-Austin. 2011. Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance? Trends Ecol. Evol. 26: 278–284.
182. Gaze, W.H., N. Abdouslam, P.M. Hawkey, et al. 2005. Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrob. Agents Chemother. 49: 1802–1807.
183. Hegstad, K., S. Langsrud, B.T. Lunestad, et al. 2010. Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb. Drug Resist. 16: 91–104.
184. Rosewarne, C.P., V. Pettigrove, H.W. Stokes, et al. 2010. Class 1 integrons in benthic bacterial communities: abundance, association with Tn402-like transposition modules and evidence for coselection with heavy-metal resistance. FEMS Microbiol. Ecol. 72: 35–46.
185. Wright, M.S., C. Baker-Austin, A.H. Lindell, et al. 2008. Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities. ISME J. 2: 417–428.
186. Skurnik, D., R. Ruimy, D. Ready, et al. 2010. Is exposure to mercury a driving force for the carriage of antibiotic resistance genes? J. Med. Microbiol. 59: 804–807.
187. Di Cesare, A., E. Eckert & G. Corno. 2016. Co-selection of antibiotic and heavy metal resistance in freshwater bacteria. J. Limnol. 75. DOI: https://doi.org/10.4081/jlimnol.2016.1198.
188. Gullberg, E., L.M. Albrecht, C. Karlsson, et al. 2014. Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. mBio 5: e01918–14.
189. Johnson, T.A., R.D. Stedtfeld, Q. Wang, et al. 2016. Clusters of antibiotic resistance genes enriched together stay together in swine agriculture. mBio 7: e02214–e02215.
190. Dimitriu, T., D. Misevic, A.B. Lindner, et al. 2015. Mobile genetic elements are involved in bacterial sociality. Mob. Genet. Elements 5: 7–11.
191. Rankin, D.J., E.P. Rocha & S.P. Brown. 2011. What traits are carried on mobile genetic elements, and why? Heredity 106: 1–10.
192. Toleman, M.A., P.M. Bennett & T.R. Walsh. 2006. ISCR elements: novel gene-capturing systems of the 21st century? Microbiol. Mol. Biol. Rev. 70: 296–316.
193. Tetu, S.G. & A.J. Holmes. 2008. A family of insertion sequences that impacts integrons by specific targeting of gene cassette recombination sites, the IS1111-attC group. J. Bacteriol. 190: 4959–4970.
194. Yano, H., L.M. Rogers, M.G. Knox, et al. 2013. Host range diversification within the IncP-1 plasmid group. Microbiology 159: 2303–2315.
195. Pembroke, J.T. & A.V. Piterina. 2006. A novel ICE in the genome of Shewanella putrefaciens W3-18-1: comparison with the SXT/R391 ICE-like elements. FEMS Microbiol. Lett. 264: 80–88.
196. Wozniak, R.A., D.E. Fouts, M. Spagnoletti, et al. 2009. Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet. 5: e1000786.
197. Chowdhury, P.R., M. Scott, P. Worden, et al. 2016. Genomic islands 1 and 2 play key roles in the evolution of extensively drug-resistant ST235 isolates of Pseudomonas aeruginosa. Open Biol. 6. pii: 150175.
198. Klockgether, J., N. Cramer, L. Wiehlmann, et al. 2011. Pseudomonas aeruginosa genomic structure and diversity. Front. Microbiol. 2: 150.
199. Krizova, L., L. Dijkshoorn & A. Nemec. 2011. Diversity and evolution of AbaR genomic resistance islands in Acinetobacter baumannii strains of European clone I. Antimicrob. Agents Chemother. 55: 3201–3206.
200. Chowdhury, P.R., I.G. Charles & S.P. Djordjevic. 2015. A role for Tn 6029 in the evolution of the complex antibiotic resistance gene loci in genomic island 3 in enteroaggregative hemorrhagic Escherichia coli O104: H4. PLoS One 10: e0115781.
201. Brochet, M., E. Couvé, M. Zouine, et al. 2006. Genomic diversity and evolution within the species Streptococcus agalactiae. Microbes Infect. 8: 1227–1243.
202. Toleman, M.A. & T.R. Walsh. 2011. Combinatorial events of insertion sequences and ICE in Gram-negative bacteria. FEMS Microbiol. Rev. 35: 912–935.
203. Garriss, G., M.K. Waldor & V. Burrus. 2009. Mobile antibiotic resistance encoding elements promote their own diversity. PLoS Genet. 5: e1000775.
204. Whitman, W.B., D.C. Coleman & W.J. Wiebe. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. U.S.A. 95: 6578–6583.
205. Simon, J.-C., C. Rispe & P. Sunnucks. 2002. Ecology and evolution of sex in aphids. Trends Ecol. Evol. 17: 34–39.
206. Narra, H.P. & H. Ochman. 2006. Of what use is sex to bacteria? Curr. Biol. 16: R705–R710.
207. Chait, R., A.C. Palmer, I. Yelin, et al. 2016. Pervasive selection for and against antibiotic resistance in inhomogeneous multistress environments. Nat. Commun. 7: 10333.
208. Wilkinson, D.M. 2010. Have we underestimated the importance of humans in the biogeography of free-living terrestrial microorganisms? J. Biogeogr. 37: 393–397.
209. Dimopoulos, G., M.H. Kollef & J. Cohen. 2016. In 2035, will all bacteria be multiresistant? Yes. Intensive Care Med. DOI: 10.1007/s00134-016-4310-y.