Skip to main content

Genomic Islands and the Evolution of Multidrug-Resistant Bacteria

  • Chapter
  • First Online:
Horizontal Gene Transfer

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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:e91713

    Article  Google Scholar 

  • Azam MW, Khan AU (2018) Updates on the pathogenicity status of Pseudomonas aeruginosa. Drug Discov Today 24(1):350–359

    Article  Google Scholar 

  • 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 11:671–676

    Article  CAS  Google Scholar 

  • 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 60:1421–1429

    Article  Google Scholar 

  • 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 73:77–83

    Article  CAS  Google Scholar 

  • Carraro N, Burrus V (2014) Biology of three ICE families: SXT/R391, ICEBs1, and ICESt1/ICESt3. Microbiol Spect 2(6). https://doi.org/10.1128/microbiolspec.MDNA3-0008-2014

  • 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:e00509

    Article  CAS  Google Scholar 

  • 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:e1006705

    Article  Google Scholar 

  • 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 7:1–6

    Article  CAS  Google Scholar 

  • CDC (2013) Multidrug-resistant Pseudomonas aeruginosa. In: Antibiotic resistance threats in the United States, 2013, pp 69–71. https://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf

  • 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):1804–1807

    Article  Google Scholar 

  • ECDC (2015) Pseudomonas aeruginosa. In: Antimicrobial resistance surveillance in Europe 2015, pp 34–47. https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/antimicrobial-resistance-europe-2015.pdf

  • 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 68:1707–1713

    Article  CAS  Google Scholar 

  • Gallagher LA, Lee SA, Manoil C (2017) Importance of core genome functions for an extreme antibiotic resistance trait. MBio 8(6):e01655–e01617

    Article  CAS  Google Scholar 

  • 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–e00412

    Article  CAS  Google Scholar 

  • Groisman EA, Ochman H (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87:791–794

    Article  CAS  Google Scholar 

  • Hacker J, Carniel E (2001) Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2:376–381

    Article  CAS  Google Scholar 

  • 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 70:2519–2523

    Article  CAS  Google Scholar 

  • Hamidian M, Holt KE, Hall RM (2015b) The complete sequence of Salmonella genomic island SGI1-K. J Antimicrob Chemother 70:305–306

    Article  CAS  Google Scholar 

  • Hamidian M, Holt KE, Hall RM (2015c) The complete sequence of Salmonella genomic island SGI2. J Antimicrob Chemother 70:617–619

    Article  CAS  Google Scholar 

  • 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):e000165

    PubMed Central  Google Scholar 

  • 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 60:7216–7223

    Article  CAS  Google Scholar 

  • 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 67:915–921

    Article  CAS  Google Scholar 

  • Jani M, Sengupta S, Hu K, Azad RK (2017) Deciphering pathogenicity and antibiotic resistance islands in methicillin-resistant. Open Biol 7(12):170094

    Article  Google Scholar 

  • Juhas M (2015a) Horizontal gene transfer in human pathogens. Crit Rev Microbiol 41:101–108

    Article  CAS  Google Scholar 

  • Juhas M (2015b) Pseudomonas aeruginosa essentials: an update on investigation of essential genes. Microbiology 161:2053–2060

    Article  CAS  Google Scholar 

  • Juhas M (2015c) Type IV secretion systems and genomic islands-mediated horizontal gene transfer in Pseudomonas and Haemophilus. Microbiol Res 170:10–17

    Article  CAS  Google Scholar 

  • 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 150:831–841

    Article  CAS  Google Scholar 

  • 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 242:287–295

    Article  CAS  Google Scholar 

  • 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 189:761–771

    Article  CAS  Google Scholar 

  • 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 107:253–254

    Google Scholar 

  • Juhas M, Crook DW, Hood DW (2008) Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol 10:2377–2386

    Article  CAS  Google Scholar 

  • 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 33:376–393

    Article  CAS  Google Scholar 

  • 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–e01916

    PubMed  PubMed Central  Google Scholar 

  • 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 43:8735–8745

    Article  CAS  Google Scholar 

  • Koonin EV (2016) Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Res 5:1805

    Article  Google Scholar 

  • 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 194:532–533

    Article  Google Scholar 

  • 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:e0164561

    Article  Google Scholar 

  • Oliver A, Cantón R, Campo P, Baquero F, Blázquez J (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251–1254

    Article  CAS  Google Scholar 

  • Oliver A, Mulet X, López-Causapé C, Juan C (2015) The increasing threat of Pseudomonas aeruginosa high-risk clones. Drug Resist Updat 21–22:41–59

    Article  Google Scholar 

  • Pagano M, Martins AF, Barth AL (2016) Mobile genetic elements related to carbapenem resistance in Acinetobacter baumannii. Braz J Microbiol 47:785–792

    Article  CAS  Google Scholar 

  • Potron A, Poirel L, Nordmann P (2015) Emerging broad-spectrum resistance in Pseudomonas aeruginosa and Acinetobacter baumannii: mechanisms and epidemiology. Int J Antimicrob Agents 45:568–585

    Article  CAS  Google Scholar 

  • 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 365:709–717

    Article  CAS  Google Scholar 

  • Ray MD, Boundy S, Archer GL (2016) Transfer of the methicillin resistance genomic island among staphylococci by conjugation. Mol Microbiol 100:675–685

    Article  CAS  Google Scholar 

  • 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:e0115781

    Article  Google Scholar 

  • 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):150175

    Article  Google Scholar 

  • 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 72:620–622

    Article  Google Scholar 

  • 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 2:1–5

    Article  Google Scholar 

  • 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 69:3216–3220

    Article  CAS  Google Scholar 

  • 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 71:2167–2170

    Article  Google Scholar 

  • 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):1808–1811

    Article  CAS  Google Scholar 

  • 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 42:60–65

    Article  CAS  Google Scholar 

  • Smyth DS, Wong A, Robinson DA (2011) Cross-species spread of SCCmec IV subtypes in staphylococci. Infect Genet Evol 11:446–453

    Article  Google Scholar 

  • 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 51:132–137

    Article  CAS  Google Scholar 

  • Soucy SM, Huang J, Gogarten JP (2015) Horizontal gene transfer: building the web of life. Nat Rev Genet 16:472–482

    Article  CAS  Google Scholar 

  • 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 54:4352–4359

    Article  CAS  Google Scholar 

  • 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 297:615–623

    Article  CAS  Google Scholar 

  • 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 59:3578–3581

    Article  CAS  Google Scholar 

  • 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 50:581–587

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mario Juhas .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Juhas, M. (2019). Genomic Islands and the Evolution of Multidrug-Resistant Bacteria. In: Villa, T., Viñas, M. (eds) Horizontal Gene Transfer. Springer, Cham. https://doi.org/10.1007/978-3-030-21862-1_4

Download citation

Publish with us

Policies and ethics