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Evolutionary Genomics of Epidemic and Nonepidemic Strains of Pseudomonas Aeruginosa

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Evolutionary Genomics of Epidemic and Nonepidemic Strains of Pseudomonas Aeruginosa Evolutionary genomics of epidemic and nonepidemic strains of Pseudomonas aeruginosa Jeremy R. Dettmana,b,1, Nicolas Rodriguec, Shawn D. Aarond, and Rees Kassena,b aDepartment of Biology, bCentre for Advanced Research in Environmental Genomics, and dOttawa Hospital Research Institute, University of Ottawa, Ottawa, ON, Canada K1N 6N5; and cDepartment of Mathematics and Statistics, University of Calgary, Calgary, AB, Canada T2N 1N4 Edited by Ralph R. Isberg, Howard Hughes Medical Institute and Tufts University School of Medicine, Boston, MA, and approved November 8, 2013 (received for review April 26, 2013) Pseudomonas aeruginosa is an opportunistic pathogen of humans virulence factor expression (6), presumably an adaptation to and is a major cause of morbidity and mortality in patients with escape detection by the host immune system, and increased ac- cystic fibrosis (CF). Prolonged infection of the respiratory tract can tivity of efflux pumps (7) associated with resistance to many lead to adaptation of the pathogen to the CF lung environment. antibiotics used in treatment. To examine the general patterns of adaptation associated with The genetic changes responsible for these adaptations have chronic infection, we obtained genome sequences from a collection recently begun to be investigated. Evidence from longitudinal of P. aeruginosa isolated from airways of patients with CF. Our studies suggests that a large number of candidate genes can ac- analyses support a nonclonal epidemic population structure, with crue substitutions during adaptation of P. aeruginosa (6–9). Any a background of unique, recombining genotypes, and the rare given infection involves only a small subset of those substitutions, occurrence of successful epidemic clones. We present unique ge- and most virulence-related phenotypes are not observed uni- nome sequence evidence for the intercontinental spread of an formly (10), making it difficult to say with confidence which ge- epidemic strain shared between CF clinics in the United Kingdom netic changes are most commonly associated with adaptation to and North America. Analyses of core and accessory genomes identified candidate genes and important functional pathways the CF lung. A more comprehensive view therefore requires the associated with adaptive evolution. Many genes of interest were comparison of a larger sample of diverse clinical isolates. To this involved in biological functions with obvious roles in this pathos- end, we obtained whole-genome sequence data from a collection ystem, such as biofilm formation, antibiotic metabolism, pathogene- of P. aeruginosa isolated from the airways of patients with CF sis, transport, reduction/oxidation, and secretion. Key factors driving to investigate general patterns of adaptation associated with the adaptive evolution of this pathogen within the host appear to chronic infection. We summarize the broad-scale patterns of be the presence of oxidative stressors and antibiotics. Regions of genomic variation and identify the most likely genetic targets of the accessory genome unique to the epidemic strain were enriched adaptation causing contemporary infection in our isolates. Our for genes in transporter families that efflux heavy metals and anti- collection includes nonepidemic strains and a transmissible, ep- biotics. The epidemic strain was significantly more resistant than idemic strain recently reported within North America (1). In- nonepidemic strains to three different antibiotics. Multiple lines of fection with an epidemic strain confers a poorer prognosis than evidence suggest that selection imposed by the CF lung environ- infection with a nonepidemic strain, such as reduced lung func- fl ment has a major in uence on genomic evolution and the genetic tion (11) and increased risk of death or lung transplant (1). Our characteristics of P. aeruginosa isolates causing contemporary comparative analyses of genomic variation identified some unique infection. Significance virulence | multidrug resistance | redox balance The bacterium Pseudomonas aeruginosa is an opportunistic Pseudomonas aer- he ubiquitous, Gram-negative bacterium pathogen of humans and is the leading cause of death in uginosa T can be found free-living in a wide range of environ- patients with cystic fibrosis (CF). We sequenced the genomes of ments or in association with various animal and plant species. P. aeruginosa isolated from respiratory tracts of patients with P. aeruginosa is also an opportunistic pathogen of humans and is CF to investigate general patterns of adaptation associated the most common species isolated from the respiratory tracts of with chronic infection. Selection imposed by the CF lung envi- fi adult patients with cystic brosis (CF). Chronic endobronchial ronment has had a major influence on genomic evolution and infections caused by P. aeruginosa are found in up to 80% of the genetic characteristics of isolates causing contemporary adult patients with CF (1, 2) and are associated with increased infection. Many of the genes and pathways implicated in morbidity and mortality (3). Once established in the lung, adaptive evolution within the host had obvious roles in the P. aeruginosa infections are notoriously difficult to eradicate and pathogenic lifestyle of this bacteria. Genome sequence data are highly resilient to repeated rounds of intensive, prolonged indicated that an epidemic strain, with increased virulence and antibiotic treatment. multidrug resistance, has spread between clinics in the United There is growing evidence that the often decades-long in- Kingdom and North America. teraction between the host and P. aeruginosa during chronic in- fection results in adaptation of the pathogen to the CF lung Author contributions: J.R.D., N.R., S.D.A., and R.K. designed research; J.R.D. and N.R. environment (4). The CF lung is an inhospitable place charac- performed research; J.R.D., N.R., and R.K. analyzed data; and J.R.D., N.R., and R.K. wrote the paper. terized by osmotic and oxidative stress, limited oxygen, high The authors declare no conflict of interest. concentrations of antibiotics, and constant assault by the host immune system. Although the hurdles posed by these factors are This article is a PNAS Direct Submission. fl Data deposition: The draft genome sequences reported in this paper have been deposited dynamic and uctuate through time, they are likely the main in the DNA DataBank of Japan (DDBJ)/European Molecular Biology Laboratory/GenBank drivers of adaptive evolution of bacteria in CF airways. Studies database, www.ncbi.nlm.nih.gov (accession nos. AWYJ00000000–AWZG00000000). have documented some repeatable patterns of adaptation to the 1To whom correspondence should be addressed. E-mail: [email protected]. EVOLUTION CF lung environment such as loss of motility associated with This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. growth as an unattached biofilm or microcolony (5), reduced 1073/pnas.1307862110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1307862110 PNAS | December 24, 2013 | vol. 110 | no. 52 | 21065–21070 Downloaded by guest on September 24, 2021 genomic features that distinguish the epidemic strain from Phylogeny of Isolates. Our sampling scheme was designed to allow nonepidemic strains. detailed analyses of our focal population (Ontario) and to place these isolates within the broader phylogenetic framework of the Results and Discussion global species. The established P. aeruginosa multilocus sequence Isolate Sources, Genome Sequencing, and Alignment. We take a typing (MLST) (16) system was applied to the 24 Ontario iso- population genomics approach to study the evolution of the op- lates; a total of 14 sequence types were identified, half of which portunistic pathogen, P. aeruginosa. Our study is unique in using were previously undescribed (SI Appendix, Table S3). The MLST whole-genome sequence data to examine the cross-sectional ge- system covers only 0.18% of the genome and the loci have low nome diversity of P. aeruginosa at the population and intrastrain levels of nucleotide variation, providing limited power for inferring level. Isolates were sampled from the sputum of 24 different phylogenetic relationships. Instead, we constructed a maximum patients attending CF clinics in six cities in Ontario, Canada (ref. likelihood phylogeny from the core genome alignment (Fig. 2 and 1, SI Appendix,TableS1). Clinics were located within 520 km of SI Appendix Fig. S1). One notable feature of this phylogeny is the each other, so this sample represents a geographically restricted two well-supported clades (A and B) that correspond to trans- population. Reference-guided mapping may skew the detection missible, epidemic strains of P. aeruginosa (see next section), of variation in genomic content, so draft genomes were assembled a designation supported by the tight phylogenetic clustering of de novo (average of 69-fold sequence coverage) from whole- isolates within clades. The core-genome nucleotide diversity genome sequence data for the 24 Ontario isolates. To place the within clades A and B is only 2.5% and 3.0%, respectively, of Ontario population in the evolutionary context of other members that in the entire sample. of the species, eight previously sequenced genomes were also Another feature of the phylogeny is long terminal branches included in our analyses (four from non-CF sources; SI Appendix, with a backbone of short internodes (Fig. 2 and SI Appendix, Fig. Table S2). A 32-genome global alignment was produced and
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