Crucial Role of the Accessory Genome in the Evolutionary Trajectory of Acinetobacter baumannii Global Clone 1.

Verónica Elizabeth Álvarez,Elisabet Vilacoba,Angélica Viviana Galán,María Paula Quiroga,Cecilia Quiroga,Daniela Centrón,María Soledad Ramírez

doi:10.3389/fmicb.2020.00342

Abstract

Acinetobacter baumannii is one of the most important nosocomial pathogens able to rapidly develop extensive drug resistance. Here, we study the role of accessory genome in the success of the globally disseminated clone 1 (GC1) with functional and genomic approaches. Comparative genomics was performed with available GC1 genomes (n = 106) against other A. baumannii high-risk and sporadic clones. Genetic traits related to accessory genome were found common and conserved along time as two novel regions of genome plasticity, and a CRISPR-Cas system acquired before clonal diversification located at the same loci as “sedentary” modules. Although identified within hotspot for recombination, other block of accessory genome was also “sedentary” in lineage 1 of GC1 with signs of microevolution as the AbaR0-type genomic island (GI) identified in A144 and in A155 strains which were maintained one month in independent experiments without antimicrobial pressure. The prophage YMC/09/02/B1251_ABA_BP was found to be “mobile” since, although it was shared by all GC1 genomes, it showed high intrinsic microevolution as well as mobility to different insertion sites. Interestingly, a wide variety of Insertion Sequences (IS), probably acquired by the flow of plasmids related to Rep_3 superfamily was found. These IS showed dissimilar genomic location amongst GC1 genomes presumably associated with promptly niche adaptation. On the other hand, a type VI secretion system and three efflux pumps were subjected to deep processes of genomic loss in A. baumannii but not in GC1. As a whole, these findings suggest that preservation of some genetic modules of accessory genome harbored by strains from different continents in combination with great plasticity of IS and varied flow of plasmids, may be central features of the genomic structure of GC1. Competition of A144 and A155 versus A118 (ST 404/ND) without antimicrobial pressure suggested a higher ability of GC1 to grow over a clone with sporadic behavior which explains, from an ecological perspective, the global achievement of this successful pandemic clone in the hospital habitat. Together, these data suggest an essential role of still unknown properties of “mobile” and “sedentary” accessory genome that is preserved over time under different antibiotic or stress conditions.

Highlights

The broad diversification of species among the genus Acinetobacter occurred mostly due to Lateral Genetic Transfer (LGT) events, and to some allelic recombination at specific hotspots (Touchon et al, 2014; Holt et al, 2016)
Comparative genomics was carried out for A144 and A155 strains from H1 Hospital with all GC1 Group 1 which were isolated from four different continents (America, Oceania, Asia and Europe) and with other epidemic and sporadic clones of the Outgroup Group 3 genomes (Table 1)
We found that A144 genome has 99% Average Nucleotide Identity (ANI) with A155 isolated from the same hospital

Summary

Introduction

The broad diversification of species among the genus Acinetobacter occurred mostly due to Lateral Genetic Transfer (LGT) events, and to some allelic recombination at specific hotspots (Touchon et al, 2014; Holt et al, 2016). A. baumannii is well known as an opportunistic pathogen mainly implicated in ventilator-associated pneumonia, catheter-related bloodstream, urinary tract, and wound infections (Falagas et al, 2006; Peleg et al, 2008; Roca et al, 2012; Park et al, 2013; Inchai et al, 2015) This species has a highly plastic genome evidenced by the amount of insertions, deletions, inversions and SNPs reported (Peleg et al, 2008; Imperi et al, 2011; Antunes et al, 2014), which may contribute to its adaptation to several niches and the evolution to extensive (XDR) and pandrug resistance (PDR) phenotypes (Adams et al, 2008; Vallenet et al, 2008; Arduino et al, 2012; Ou et al, 2015; Holt et al, 2019), harboring a pangenome of over 9000 gene families (Antunes et al, 2011; Touchon et al, 2014). Homologous recombination near the origin of replication was the mechanism associated with the diversification of these GC (Snitkin et al, 2013)

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