Pathogenic diversity of Escherichia coli and the emergence of ’exotic’ islands in the gene stream Charles M. Dozois, Roy Curtiss To cite this version: Charles M. Dozois, Roy Curtiss. Pathogenic diversity of Escherichia coli and the emergence of ’exotic’ islands in the gene stream. Veterinary Research, BioMed Central, 1999, 30 (2-3), pp.157-179. hal- 00902564 HAL Id: hal-00902564 https://hal.archives-ouvertes.fr/hal-00902564 Submitted on 1 Jan 1999 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Review article Pathogenic diversity of Escherichia coli and the emergence of ’exotic’ islands in the gene stream Charles M. Dozois Roy Curtiss III* Department of Biology, Washington University, Campus Box 1 137, One Brookings Drive, Saint-Louis, MO 63130, USA (Received 27 October 1998; accepted 8 December 1998) Abstract - Escherichia coli is a highly adaptive bacterial species that is both a member of the com- mensal intestinal flora and a versatile pathogen associated with numerous types of intestinal and systemic infections in humans and other animals. The spectrum of diseases caused by E. coli is due to the acquisition of specific virulence genes harbored on plasmids, bacteriophages, or within distinct DNA segments termed pathogenicity islands (PAls) that are absent from the genomes of commen- sal E. coli strains. PAls are likely to have been transferred horizontally and may have integrated into the E. coli chromosome through bacteriophage or plasmid integration or transposition. The con- tribution of intergenic inheritance to the adaptation and evolution of E. coli, types of PAls associated with different groups of pathogenic E. coli and approaches to identify unique sequence islands (USis), some of which might confer pathogenicity, in E. coli and other bacteria are presented. © Inra/Elsevier, Paris. Escherichia coli / pathogenicity island / horizontal gene transfer / adaptation Résumé - Diversité du pouvoir pathogène d’Escherichia coli et fluidité du génome bactérien : acquisition d’ADN « exotiques » organisés en îlots au sein du chromosome. E.ccherichia coli est une espèce bactérienne ayant une grande faculté d’adaptation. Elle fait partie de la flore intesti- nale commensale mais c’est également un pathogène versatile responsable d’infections systémiques et intestinales chez l’homme et les animaux. La grande diversité des maladies provoquées par E. coli est due à l’acquisition de gènes de virulence spécifiques se trouvant sur des plasmides et des bactériophages ou à l’intérieur de régions chromosomiques appelées îlots de pathogénicité (PAIs). Ceux-ci sont absents du génome des souches d’E. coli commensales. L’acquisition des PAIs est probablement la conséquence d’un transfert horizontal d’ADN étranger au génome des E. coli lors de l’intégration dans le chromosome de bactériophages, de plasmides ou de transposons. Nous pré- sentcrons dans cette revue la contribution de ces transferts d’ADN à l’adaptation et à l’évolution de E. coli, les types de PAIs associés aux différents groupes de E. coli pathogènes ainsi que les approches permettant l’identification des îlots constitués de séquences uniques (USIs) et dont une partie pour- rait conférer le pouvoir pathogène chez E. cnli et chez d’autres bactéries. © Inra/Elsevier, Paris. Escherichia coli / îlot de pathogénicité / transfert horizontal de gène / adaptation * Correspondence and reprints Tel.: ( I ) 314 935 6819; Fax: ( 1) 314 935 7246; e-mail: dozoisC!biodec.wustl.edu 1. INTRODUCTION 111, 176]. Other E. coli pathogens are asso- ciated with host-specific diseases such as air- sacculitis and cellulitis in caused In addition to a common member poultry by being avian E. coli diarrhea of the intestinal microflora of humans and pathogenic (APEC), in rabbits caused rabbit other animals, subsets of by enteropathogenic particular E. coli and E. coli that cause Escherichia coli strains have the (REPEC) [2, 37] adapted edema disease in pigs [l76]. capacity to cause a variety of intestinal and systemic infections. Different types of The schism that separates commensal E. pathogenic E. coli exhibit host and tissue coli strains from pathogenic E. coli and the specificity as well as age specificity for par- diversity of diseases they cause has largely ticular hosts [48, 66, 162]. The diarrheagenic been attributed to the acquisition of different E. coli pathogens include: enterotoxinogenic sets of virulence genes that permit E. coli E. coli (ETEC) associated with travellers’ pathogens to gain entry to, colonize, and diarrhea and porcine post-weaning diarrhea; promote the development of specific patho- enteropathogenic E. coli (EPEC) that cause logical changes in host niches that are inac- watery diarrhea in children and animals, cessible or inhospitable to commensal E. enterohemorrhagic E. coli (EHEC) associ- coli [52]. Genes contributing to the viru- ated with hemorrhagic colitis and hemolytic lence of pathogenic E. coli, as well as other uremic syndrome, enteroaggregative E. coli bacterial pathogens, have been acquired by (EAEC) associated with persistent diarrhea, inheritance of specific plasmids or phages and enteroinvasive E. coli (EIEC) and and through the integration of large blocks Shigella that cause invasive intestinal infec- of DNA, termed pathogenicity islands tions, watery diarrhea and dysentery in (PAls), into their chromosomes [52, 63, 70, humans and other primates [75, 120, 122]. 101 J. In this review, we summarize some E. coli associated with extra-intestinal dis- of the aspects of PAIs and discuss the mech- eases include uropathogenic E. coli (UPEC) anisms by which PAIs may have been that cause urinary tract infections in humans, acquired. PAls that have been identified and dogs and cats [13, 41, 61, 175], E. coli asso- characterized in pathogenic E. coli are ciated with neonatal meningitis [174], and reviewed, and finally some of the E. coli associated with septicemia in humans approaches that may be useful for identify- [24, 153, 174] and other animals [4, 46, 71, ing and characterizing PAIs are presented. 2. EXOTIC ISLANDS IN THE GENE [16] has allowed Lawrence and Ochman STREAM CONTRIBUTE TO [100] to estimate that at least 17.6 % of the BACTERIAL EVOLUTION open reading frames (ORFs), 755 of 4 288 ORFs totalling 547.8 kb, in the E. coli K- PAIs have been described as large and 12 genome were acquired through horizon- sometimes unstable DNA regions that are tal gene transfer. The distribution of these present in pathogenic variants of a bacterial horizontally acquired segments in E. coli species, but are absent from strains of the K-12 [100], as well as PAIs in pathogenic E. same species that exhibit low or no viru- coli (table o and other bacteria [63, 70, 101 ] lence [63, 70, 101]. These DNA islands are are often associated with tRNA gene loci. ’exotic’ in the sense that genes encoded by In addition, horizontally acquired regions these sequences often possess a nucleotide of E. coli K-12 are also frequently associated composition and codon usage that is atypi- with the presence of insertional sequence cal to that of the bacterial genome within (IS) elements. Similarly, PAIs from differ- which they presently reside. Differences in ent bacterial species are frequently associ- G+C content and codon usage suggest that ated with IS-related, or plasmid-encoded these DNA regions were most likely sequences. These findings suggest that the acquired at some time in the past from for- mechanisms for horizontal transfer of PAIs eign species that may now be extinct, as well as the acquisition of metabolic or through lateral transmission. This rationale niche adaptive genes by commensal E. coli is based on the idea that, when first acquired, strains are shared. DNA from sources with differ- intergenic The association of tRNA ing G+C contents will demonstrate the great- genes impli- cates temperate as the medi- est level of sequence divergence from the bacteriophages ators inte- recipient into which it has integrated. Over- of horizontal gene transfers. The sites of a number of time random genetic drift should amelio- gration bacteriophages, such as P4 and related are within rate the third codon to a base composi- coliphages, (P3) or to tRNA Hori- tion that is more like that of the adjacent genes [31, 142]. surrounding zontal tRNA hom- average G+C content of the host [6, 99]. acquisition through gene ing bacteriophages is a plausible means of Incorporation of foreign DNA into bac- facilitating intergenic recombination since terial is not restricted to and genomes PAls, tRNA sites are highly conserved across it is likely that horizontal gene transfer is a species. The association of different PAIs force in the evolution of bacterial major with tRNA genes and the presence of phage- such as E. coli or Salmonella enter- genomes or plasmid-related sequences bordering or ica Bacterial of E. [98, 100]. populations within PAIs supports the likelihood that coli or Salmonella have been shown to be these virulence-associated sequences may clonal based on multilocus elec- enzyme have been acquired from bacteriophages or trophoresis (MEE) [154, 17!]. Sequencing integrative plasmids that carried bacterio- of common housekeeping genes encoding phage integrase or attachment sites. IS functions shared all strains required by sequences may also mediate acquisition or within a group demonstrate limited DNA loss of PAls, either directly by transposi- transfer In among clones [25, 121, 164!. tion events in the case of functional mobile involved in clone contrast, genes adaptation elements such as the IS]OO flanked unstable and diversification show a of higher degree pgm locus of Yersinia pe.rtis [54, 55,134].