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A Pan-Genomic Approach to Understand the Basis of Host Adaptation in Achromobacter

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A Pan-Genomic Approach to Understand the Basis of Host Adaptation in Achromobacter GBE A Pan-Genomic Approach to Understand the Basis of Host Adaptation in Achromobacter Julie Jeukens1,LucaFreschi1, Antony T. Vincent1,2,3, Jean-Guillaume Emond-Rheault1, Irena Kukavica-Ibrulj1, Steve J. Charette1,2,3, and Roger C. Levesque1,* 1Institut de Biologie Inte´grative et des Syste`mes (IBIS), Universite´ Laval, Quebec City, Quebec, Canada 2Centre de Recherche de l’Institut Universitaire de Cardiologie et de Pneumologie de Que´bec (CRIUCPQ), Quebec City, Quebec, Canada 3De´partement de Biochimie, de Microbiologie et de Bio-informatique, Universite´ Laval, Quebec City, Quebec, Canada *Corresponding author: E-mail: [email protected]. Accepted: April 4, 2017 Data deposition: This project has been deposited at NCBI under the accession PRJNA343957. Abstract Over the past decade, there has been a rising interest in Achromobacter sp., an emerging opportunistic pathogen responsible for nosocomial and cystic fibrosis lung infections. Species of this genus are ubiquitous in the environment, can outcompete resident microbiota, and are resistant to commonly used disinfectants as well as antibiotics. Nevertheless, the Achromobacter genus suf- fers from difficulties in diagnosis, unresolved taxonomy and limited understanding of how it adapts to the cystic fibrosis lung, not to mention other host environments. The goals of this first genus-wide comparative genomics study were to clarify the taxonomy of this genus and identify genomic features associated with pathogenicity and host adaptation. This was done with a widely applicable approach based on pan-genome analysis. First, using all publicly available genomes, a combination of phylogenetic analysis based on 1,780 conserved genes with average nucleotide identity and accessory genome composition allowed the identi- fication of a largely clinical lineage composed of Achromobacter xylosoxidans, Achromobacter insuavis, Achromobacter dolens,and Achromobacter ruhlandii. Within this lineage, we identified 35 positively selected genes involved in metabolism, regulation and efflux-mediated antibiotic resistance. Second, resistome analysis showed that this clinical lineage carried additional antibiotic resis- tance genes compared with other isolates. Finally, we identified putative mobile elements that contribute 53% of the genus’s resistome and support horizontal gene transfer between Achromobacter and other ecologically similar genera. This study provides strong phylogenetic and pan-genomic bases to motivate further research on Achromobacter, and contributes to the understanding of opportunistic pathogen evolution. Key words: comparative genomics, phylogenomics, antibiotic resistance, horizontal gene transfer, mobilome. Introduction documented cases of cross-infection (Hansen et al. 2013; Achromobacter sp. is a nonfermenting Gram-negative bacte- Cools et al. 2015, 2016). Moreover, like P. aeruginosa, rium,partoftheBurkholderiales order, and considered an Achromobacter sp. can outcompete resident microbiota emerging opportunistic pathogen in the context of cystic (Talbot and Flight 2016), establish persistent chronic infections fibrosis (CF) lung infections (Davies and Rubin 2007; associated with inflammation (Hansen et al. 2010; Lambiase Emerson et al. 2010; Jakobsen et al. 2013). Although it is et al. 2011), produce biofilm, resist common disinfectants not closely related to Pseudomonas aeruginosa, one of the (Jeukens et al. 2015; Gu¨ nther et al. 2016) and readily acquire most common causes of lung infection among CF patients antibiotic resistance (Trancassini et al. 2014). (Filkins and O’Toole 2016), the two organisms are similar in While its prevalence among CF patients is estimated to be many respects. Both carry relatively large genomes (6–7 Mb) as high as 10–20% (Lambiase et al. 2011; Trancassini et al. and are ubiquitous in the environment, which is considered as 2014), Achromobacter species can also cause infections such the main source of infection (Ridderberg et al. 2011; as bacteremia, pneumonia, meningitis, urinary tract infections, Amoureux et al. 2013a; Kupfahl et al. 2015), along with and nosocomial infections (reviewed in Abbott and Peleg ß The Author(s) 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 1030 Genome Biol. Evol. 9(4):1030–1046 doi:10.1093/gbe/evx061 Advance Access publication April 5, 2017 Pan-Genomic Approach to Understand the Basis of Host Adaptation in Achromobacter GBE FIG.1.—Achromobacter research interest from a clinical perspective. As of June 3, 2016. The number of publications is based on a literature search using Web of Science (www.webofknowledge.com; last accessed June 3, 2016) with Title=“Achromobacter” and Topic=“clinical.” The number of genomes is based on the content of NCBI. 2015). This may be the reason why, after a decade of stag- Materials and Methods nation, research focusing on clinical Achromobacter isolates was revived ~10 years ago (fig. 1). This increase in research DNA Preparation, Sequencing, and Assembly interest was potentiated by the advent of next-generation In the context of an international Pseudomonas genome proj- sequencing technologies (Vincent et al. 2016)andtheexplo- ect (Freschi et al. 2015), we sequenced four Achromobacter sion in the number of sequenced bacterial genomes that fol- genomes (table 1), one of which was already published: A. lowed (Land et al. 2015). As a result, most of the genomes xylosoxidans CF304 (Jeukens et al. 2015). Bacterial colonies TM available for the genus today are of clinical origin, while a few were isolated on Difco Pseudomonas Isolation Agar (BD, were sequenced in the context of bioremediation research. Sparks, MD). Genomic DNA was extracted from overnight Despite this renewed interest, the Achromobacter genus suf- cultures using the DNeasy Blood and Tissue Kit (QIAGEN, fers from a complex unresolved taxonomy (Vandamme et al. Hilden, Germany). Genomic DNA (500 ng) was mechanically 2013), rare comparative genomics studies (Li et al. 2013; fragmented for 40 s using a Covaris M220 (Covaris, Woburn, Ridderberg et al. 2015), and very limited understanding of MA) with default settings. Fragmented DNA was transferred how it adapts to the CF lung (Dupont et al. 2015), let alone to a PCR tube and library synthesis was performed with the other host environments. Kapa Hyperprep kit (Kapa biosystems, Wilmington, MA) ac- In order to identify the genetic characteristics that allow cording to manufacturer’s instructions. TruSeq HT adapters some isolates to thrive in opportunistic infections, we com- (Illumina, SanDiego, CA) were used to barcode the libraries, bined all available Achromobacter genomes with four new which were each sequenced in 1/48 of an Illumina MiSeq genome sequences to perform the first large-scale compara- 300 bp paired-end run at the Plateforme d’Analyses tive genomics study for this genus. More specifically, the goals Ge´nomiques of the Institut de Biologie Inte´grative et des were to (1) resolve the taxonomic uncertainties of the genus, Syste`mes (Laval University, Quebec, Canada). Each data set and (2) identify virulence-associated genes, antimicrobial resis- was assembled de novo with the A5 pipeline version A5-miseq tance genes, and other genomic features associated with 20140521 (Trittetal.2012). pathogenicity and host adaptation. To achieve these goals, we developed an approach based on pan-genome analysis Public Data Selection that could be applied to gain significant knowledge on any All genomes of the genus Achromobacter that had 200 scaf- microbial species or genus. folds or less were downloaded from RefSeq (in June 2016). Genome Biol. Evol. 9(4):1030–1046 doi:10.1093/gbe/evx061 Advance Access publication April 5, 2017 1031 Jeukens et al. GBE Table 1 New Achromobacter Genome Assemblies Isolate Namea Source City Country Size (Mb) Contigs Median Coverageb N50 Accession A. xylosoxidans CF304c cf, sputum Montreal Canada 6.3 29 61 586493 NZ_LFHA00000000 A. xylosoxidans 4124363476 cf, throat Rouyn-Noranda Canada 6.8 42 26 503116 MJMP00000000 A. xylosoxidans AUS488 bronchiectasis, sputum Brisbane Australia 7.1 65 20 257078 MJMN00000000 A. xylosoxidans U400 cf patient Hobart Australia 6.5 61 47 275436 MJMO00000000 aThe phylogenetic analysis presented in figure 2 enabled species identification. bMedian depth of coverage in a de novo assembly with A5-MiSeq (Tritt et al. 2012). cThis genome was previously published (Jeukensetal.2015). The 200-scaffold cut-off was selected as a compromise to Genes under Selection ensure an assembly quality similar to our own (<100 scaf- The second goal of this study was to identify genomic features folds), without having to eliminate too many genomes. A pre- associated with pathogenicity. After the phylogenetic analysis liminary phylogenetic analysis showed that four genomes demonstrated that clinical isolates tended to cluster together, were extremely distant from the others: Achromobacter sp. we sought to identify genes that were under positive selection ATCC8750 (NZ_CYTB01000000), Achromobacter sp. (dN/dS > 1) in these clusters specifically. Previously generated 2789STDY5608636 (NZ_CYTV00000000), Achromobacter orthologous gene alignments
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