Genomic Islands and the Evolution of Multidrug-Resistant Bacteria

  • Mario JuhasEmail author


The horizontal gene transfer is crucial for the evolution and adaptation of bacteria. An important part of the horizontal gene transfer is facilitated by the large, discreet DNA segments called genomic islands. Some genomic islands encode means of their own excision, self-transfer and integration into the chromosome, while others can be mobilized by other mobile genetic elements or are stably integrated into the chromosomes of the host bacteria. Genomic islands are involved in the dissemination of a wide variety of genes, including virulence and antibiotic-resistant genes. This review provides an update on the investigation of genomic islands with particular emphasis on their role in the evolution of multidrug-resistant bacteria.


Horizontal gene transfer Genomic island MDR bacteria ICE Escherichia coli Pseudomonas aeruginosa Salmonella enterica Proteus mirabilis Acinetobacter baumannii Staphylococcus aureus 


  1. Anderson DJ, Moehring RW, Sloane R, Schmader KE, Weber DJ, Fowler VG, Smathers E, Sexton DJ (2014) Bloodstream infections in community hospitals in the 21st century: a multicenter cohort study. PLoS One 9:e91713CrossRefGoogle Scholar
  2. Azam MW, Khan AU (2018) Updates on the pathogenicity status of Pseudomonas aeruginosa. Drug Discov Today 24(1):350–359CrossRefGoogle Scholar
  3. Bielaszewska M, Mellmann A, Zhang W, Köck R, Fruth A, Bauwens A, Peters G, Karch H (2011) Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis 11:671–676CrossRefGoogle Scholar
  4. Blackwell GA, Nigro SJ, Hall RM (2015) Evolution of AbGRI2-0, the progenitor of the AbGRI2 resistance island in global clone 2 of Acinetobacter baumannii. Antimicrob Agents Chemother 60:1421–1429CrossRefGoogle Scholar
  5. Botelho J, Grosso F, Peixe L (2018) Unravelling the genome of a Pseudomonas aeruginosa isolate belonging to the high-risk clone ST235 reveals an integrative conjugative element housing a blaGES-6 carbapenemase. J Antimicrob Chemother 73:77–83CrossRefGoogle Scholar
  6. Carraro N, Burrus V (2014) Biology of three ICE families: SXT/R391, ICEBs1, and ICESt1/ICESt3. Microbiol Spect 2(6).
  7. Carraro N, Rivard N, Ceccarelli D, Colwell RR, Burrus V (2016) IncA/C conjugative plasmids mobilize a new family of multidrug resistance islands in clinical Vibrio cholerae non-O1/non-O139 isolates from Haiti. MBio 7:e00509CrossRefGoogle Scholar
  8. Carraro N, Durand R, Rivard N, Anquetil C, Barrette C, Humbert M, Burrus V (2017a) Salmonella genomic island 1 (SGI1) reshapes the mating apparatus of IncC conjugative plasmids to promote self-propagation. PLoS Genet 13:e1006705CrossRefGoogle Scholar
  9. Carraro N, Rivard N, Burrus V, Ceccarelli D (2017b) Mobilizable genomic islands, different strategies for the dissemination of multidrug resistance and other adaptive traits. Mob Genet Elem 7:1–6CrossRefGoogle Scholar
  10. CDC (2013) Multidrug-resistant Pseudomonas aeruginosa. In: Antibiotic resistance threats in the United States, 2013, pp 69–71.
  11. de Curraize C, Neuwirth C, Bador J, Chapuis A, Amoureux L, Siebor E (2018) Two new Salmonella genomic islands 1 from Proteus mirabilis and description of blaCTX-M-15 on a variant (SGI1-K7). J Antimicrob Chemother 73(7):1804–1807CrossRefGoogle Scholar
  12. ECDC (2015) Pseudomonas aeruginosa. In: Antimicrobial resistance surveillance in Europe 2015, pp 34–47.
  13. Fluit AC, Carpaij N, Majoor EA, Bonten MJ, Willems RJ (2013) Shared reservoir of ccrB gene sequences between coagulase-negative staphylococci and methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 68:1707–1713CrossRefGoogle Scholar
  14. Gallagher LA, Lee SA, Manoil C (2017) Importance of core genome functions for an extreme antibiotic resistance trait. MBio 8(6):e01655–e01617CrossRefGoogle Scholar
  15. Grad YH, Godfrey P, Cerquiera GC, Mariani-Kurkdjian P, Gouali M, Bingen E, Shea TP, Haas BJ, Griggs A, Young S, Zeng Q, Lipsitch M, Waldor MK, Weill FX, Wortman JR, Hanage WP (2013) Comparative genomics of recent Shiga toxin-producing Escherichia coli O104:H4: short-term evolution of an emerging pathogen. MBio 4(1):e00452–e00412CrossRefGoogle Scholar
  16. Groisman EA, Ochman H (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87:791–794CrossRefGoogle Scholar
  17. Hacker J, Carniel E (2001) Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2:376–381CrossRefGoogle Scholar
  18. Hamidian M, Holt KE, Hall RM (2015a) Genomic resistance island AGI1 carrying a complex class 1 integron in a multiply antibiotic-resistant ST25 Acinetobacter baumannii isolate. J Antimicrob Chemother 70:2519–2523CrossRefGoogle Scholar
  19. Hamidian M, Holt KE, Hall RM (2015b) The complete sequence of Salmonella genomic island SGI1-K. J Antimicrob Chemother 70:305–306CrossRefGoogle Scholar
  20. Hamidian M, Holt KE, Hall RM (2015c) The complete sequence of Salmonella genomic island SGI2. J Antimicrob Chemother 70:617–619CrossRefGoogle Scholar
  21. Hawkey J, Ascher DB, Judd LM, Wick RR, Kostoulias X, Cleland H, Spelman DW, Padiglione A, Peleg AY, Holt KE (2018) Evolution of carbapenem resistance in Acinetobacter baumannii during a prolonged infection. Microb Genom 4(3):e000165PubMedCentralGoogle Scholar
  22. Hong JS, Yoon EJ, Lee H, Jeong SH, Lee K (2016) Clonal dissemination of Pseudomonas aeruginosa sequence type 235 isolates carrying blaIMP-6 and emergence of blaGES-24 and blaIMP-10 on novel genomic islands PAGI-15 and -16 in South Korea. Antimicrob Agents Chemother 60:7216–7223CrossRefGoogle Scholar
  23. Hosseinkhani F, Tammes Buirs M, Jabalameli F, Emaneini M, van Leeuwen WB (2018) High diversity in SCCmec elements among multidrug-resistant Staphylococcus haemolyticus strains originating from paediatric patients; characterization of a new composite island. J Med Microbiol 67:915–921CrossRefGoogle Scholar
  24. Jani M, Sengupta S, Hu K, Azad RK (2017) Deciphering pathogenicity and antibiotic resistance islands in methicillin-resistant. Open Biol 7(12):170094CrossRefGoogle Scholar
  25. Juhas M (2015a) Horizontal gene transfer in human pathogens. Crit Rev Microbiol 41:101–108CrossRefGoogle Scholar
  26. Juhas M (2015b) Pseudomonas aeruginosa essentials: an update on investigation of essential genes. Microbiology 161:2053–2060CrossRefGoogle Scholar
  27. Juhas M (2015c) Type IV secretion systems and genomic islands-mediated horizontal gene transfer in Pseudomonas and Haemophilus. Microbiol Res 170:10–17CrossRefGoogle Scholar
  28. Juhas M, Wiehlmann L, Huber B, Jordan D, Lauber J, Salunkhe P, Limpert A, von Gotz F, Steinmetz I, Eberl L, Tummler B (2004) Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150:831–841CrossRefGoogle Scholar
  29. Juhas M, Wiehlmann L, Salunkhe P, Lauber J, Buer J, Tummler B (2005) GeneChip expression analysis of the VqsR regulon of Pseudomonas aeruginosa TB. FEMS Microbiol Lett 242:287–295CrossRefGoogle Scholar
  30. Juhas M, Crook DW, Dimopoulou ID, Lunter G, Harding RM, Ferguson DJP, Hood DW (2007a) Novel type IV secretion system involved in propagation of genomic islands. J Bacteriol 189:761–771CrossRefGoogle Scholar
  31. Juhas M, Power P, Lunter G, Harding R, Thomson N, Dimopoulou ID, Elamin ARE, Hood DW, Crook DW (2007b) Sequence and functional analyses of seven representative genomic islands of Haemophilus spp. Abstr Gen Meeting Am Soc Microbiol 107:253–254Google Scholar
  32. Juhas M, Crook DW, Hood DW (2008) Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol 10:2377–2386CrossRefGoogle Scholar
  33. Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33:376–393CrossRefGoogle Scholar
  34. Kim DH, Jung SI, Kwon KT, Ko KS (2017) Occurrence of diverse AbGRI1-type genomic islands in Acinetobacter baumannii global clone 2 isolates from South Korea. Antimicrob Agents Chemother 61(2):e01972–e01916PubMedPubMedCentralGoogle Scholar
  35. Kiss J, Papp PP, Szabó M, Farkas T, Murányi G, Szakállas E, Olasz F (2015) The master regulator of IncA/C plasmids is recognized by the Salmonella genomic island SGI1 as a signal for excision and conjugal transfer. Nucleic Acids Res 43:8735–8745CrossRefGoogle Scholar
  36. Koonin EV (2016) Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Res 5:1805CrossRefGoogle Scholar
  37. Künne C, Billion A, Mshana SE, Schmiedel J, Domann E, Hossain H, Hain T, Imirzalioglu C, Chakraborty T (2012) Complete sequences of plasmids from the hemolytic-uremic syndrome-associated Escherichia coli strain HUSEC41. J Bacteriol 194:532–533CrossRefGoogle Scholar
  38. Murányi G, Szabó M, Olasz F, Kiss J (2016) Determination and analysis of the putative AcaCD-responsive promoters of Salmonella genomic island 1. PLoS One 11:e0164561CrossRefGoogle Scholar
  39. Oliver A, Cantón R, Campo P, Baquero F, Blázquez J (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251–1254CrossRefGoogle Scholar
  40. Oliver A, Mulet X, López-Causapé C, Juan C (2015) The increasing threat of Pseudomonas aeruginosa high-risk clones. Drug Resist Updat 21–22:41–59CrossRefGoogle Scholar
  41. Pagano M, Martins AF, Barth AL (2016) Mobile genetic elements related to carbapenem resistance in Acinetobacter baumannii. Braz J Microbiol 47:785–792CrossRefGoogle Scholar
  42. Potron A, Poirel L, Nordmann P (2015) Emerging broad-spectrum resistance in Pseudomonas aeruginosa and Acinetobacter baumannii: mechanisms and epidemiology. Int J Antimicrob Agents 45:568–585CrossRefGoogle Scholar
  43. Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N, Scheutz F, Paxinos EE, Sebra R, Chin CS, Iliopoulos D, Klammer A, Peluso P, Lee L, Kislyuk AO, Bullard J, Kasarskis A, Wang S, Eid J, Rank D, Redman JC, Steyert SR, Frimodt-Møller J, Struve C, Petersen AM, Krogfelt KA, Nataro JP, Schadt EE, Waldor MK (2011) Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 365:709–717CrossRefGoogle Scholar
  44. Ray MD, Boundy S, Archer GL (2016) Transfer of the methicillin resistance genomic island among staphylococci by conjugation. Mol Microbiol 100:675–685CrossRefGoogle Scholar
  45. Roy Chowdhury P, Charles IG, Djordjevic SP (2015) A role for Tn6029 in the evolution of the complex antibiotic resistance gene loci in genomic island 3 in enteroaggregative hemorrhagic Escherichia coli O104:H4. PLoS One 10:e0115781CrossRefGoogle Scholar
  46. Roy Chowdhury P, Scott M, Worden P, Huntington P, Hudson B, Karagiannis T, Charles IG, Djordjevic SP (2016) Genomic islands 1 and 2 play key roles in the evolution of extensively drug-resistant ST235 isolates of Pseudomonas aeruginosa. Open Biol 6(3):150175CrossRefGoogle Scholar
  47. Roy Chowdhury P, Scott MJ, Djordjevic SP (2017) Genomic islands 1 and 2 carry multiple antibiotic resistance genes in Pseudomonas aeruginosa ST235, ST253, ST111 and ST175 and are globally dispersed. J Antimicrob Chemother 72:620–622CrossRefGoogle Scholar
  48. Schultz E, Barraud O, Madec JY, Haenni M, Cloeckaert A, Ploy MC, Doublet B (2017) Multidrug resistance Salmonella genomic island 1 in a Morganella morganii subsp. morganii human clinical isolate from France. mSphere 2:1–5CrossRefGoogle Scholar
  49. Siebor E, Neuwirth C (2014) Proteus genomic island 1 (PGI1), a new resistance genomic island from two Proteus mirabilis French clinical isolates. J Antimicrob Chemother 69:3216–3220CrossRefGoogle Scholar
  50. Siebor E, de Curraize C, Amoureux L, Neuwirth C (2016) Mobilization of the Salmonella genomic island SGI1 and the Proteus genomic island PGI1 by the a/C2 plasmid carrying blaTEM-24 harboured by various clinical species of Enterobacteriaceae. J Antimicrob Chemother 71:2167–2170CrossRefGoogle Scholar
  51. Siebor E, de Curraize C, Neuwirth C (2018) Genomic context of resistance genes within a French clinical MDR Proteus mirabilis: identification of the novel genomic resistance island GIPmi1. J Antimicrob Chemother 73(7):1808–1811CrossRefGoogle Scholar
  52. Silveira MC, Albano RM, Asensi MD, Carvalho-Assef AP (2016) Description of genomic islands associated to the multidrug-resistant Pseudomonas aeruginosa clone ST277. Infect Genet Evol 42:60–65CrossRefGoogle Scholar
  53. Smyth DS, Wong A, Robinson DA (2011) Cross-species spread of SCCmec IV subtypes in staphylococci. Infect Genet Evol 11:446–453CrossRefGoogle Scholar
  54. Soliman AM, Ahmed AM, Shimamoto T, El-Domany RA, Nariya H (2017) First report in Africa of two clinical isolates of Proteus mirabilis carrying Salmonella genomic island (SGI1) variants, SGI1-PmABB and SGI1-W. Infect Genet Evol 51:132–137CrossRefGoogle Scholar
  55. Soucy SM, Huang J, Gogarten JP (2015) Horizontal gene transfer: building the web of life. Nat Rev Genet 16:472–482CrossRefGoogle Scholar
  56. Tsubakishita S, Kuwahara-Arai K, Sasaki T, Hiramatsu K (2010) Origin and molecular evolution of the determinant of methicillin resistance in staphylococci. Antimicrob Agents Chemother 54:4352–4359CrossRefGoogle Scholar
  57. Wiehlmann L, Munder A, Adams T, Juhas M, Kolmar H, Salunkhe P, Tuemmler B (2007) Functional genomics of Pseudomonas aeruginosa to identify habitat-specific determinants of pathogenicity. Int J Med Microbiol 297:615–623CrossRefGoogle Scholar
  58. Wipf JR, Schwendener S, Nielsen JB, Westh H, Perreten V (2015) The new macrolide-lincosamide-streptogramin B resistance gene erm(45) is located within a genomic island in Staphylococcus fleurettii. Antimicrob Agents Chemother 59:3578–3581CrossRefGoogle Scholar
  59. Xue H, Wu Z, Qiao D, Tong C, Zhao X (2017) Global acquisition of genetic material from different bacteria into the staphylococcal cassette chromosome elements of a Staphylococcus epidermidis isolate. Int J Antimicrob Agents 50:581–587CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute of Medical MicrobiologyUniversity of ZürichZürichSwitzerland

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