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. 2018 Oct 25:9:2553.
doi: 10.3389/fmicb.2018.02553. eCollection 2018.

Genome Structure of the Opportunistic Pathogen Paracoccus yeei (Alphaproteobacteria) and Identification of Putative Virulence Factors

Robert Lasek  1 , Magdalena Szuplewska  1 , Monika Mitura  1 , Przemysław Decewicz  1 , Cora Chmielowska  1 , Aleksandra Pawłot  1 , Dorota Sentkowska  1 , Jakub Czarnecki  1 , Dariusz Bartosik  1
Affiliations

Genome Structure of the Opportunistic Pathogen Paracoccus yeei (Alphaproteobacteria) and Identification of Putative Virulence Factors

Robert Lasek et al. Front Microbiol. .

Abstract

Bacteria of the genus Paracoccus are common components of the microbiomes of many naturally- and anthropogenically shaped environments. One species, Paracoccus yeei, is unique within the genus because it is associated with opportunistic human infections. Therefore, strains of P. yeei may serve as an interesting model to study the transition from a saprophytic to a pathogenic lifestyle in environmental bacteria. Unfortunately, knowledge concerning the biology, genetics and genomic content of P. yeei is fragmentary; also the mechanisms of pathogenicity of this bacterium remain unclear. In this study we provide the first insight into the genome composition and metabolic potential of a clinical isolate, P. yeei CCUG 32053. This strain has a multipartite genome (4,632,079 bp) composed of a circular chromosome plus eight extrachromosomal replicons pYEE1-8: 3 chromids and 5 plasmids, with a total size of 1,247,173 bp. The genome has been significantly shaped by the acquisition of genomic islands, prophages (Myoviridae and Siphoviridae phage families) and numerous insertion sequences (ISs) representing seven IS families. Detailed comparative analysis with other complete genomic sequences of Paracoccus spp. (including P. yeei FDAARGOS_252 and TT13, as well as non-pathogenic strains of other species in this genus) enabled us to identify P. yeei species-specific genes and to predict putative determinants of virulence. This is the first attempt to identify pathoadaptive genetic information of P. yeei and to estimate the role of the mobilome in the evolution of pathogenicity in this species.

Keywords: Paracoccus yeei; chromids; evolution of pathogenic bacteria; genomic islands; mobilome; opportunistic pathogen; plasmids; virulence factors.

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Figures

FIGURE 1
FIGURE 1
Comparative genomic analysis of three strains of Paracoccus yeei: TT13, CCUG 32053, and FDAARGOS_252. (A) Whole genome synteny analysis, visualized using EasyFig software. The localization of the identified tRNA genes, insertion sequences, phage-related regions, genomic islands, CRISPR loci and the putative CCUG 32053 virulence-related genes is presented as indicated in the key. INV - inverted a 217-kb-long segment of chromosomal DNA (in FDAAGOS_252) flanked by two copies of ISPye28. (B) Relationship between ECRs of CCUG 32053 and ECRs of other strains of P. yeei, visualized using Circoletto software. The localization of the genus-, species- and strain-specific genes within the replicons of the CCUG 32053 strain is presented as indicated in the key. The detailed description of the methodology used to generate the figure is to be found in Supplementary Table S2.
FIGURE 2
FIGURE 2
Distribution of COG functional categories within the CCUG 32053 genome, the core genome of the genus Paracoccus as well as species- and strain-specific pools of genes.
FIGURE 3
FIGURE 3
Distribution of conserved REP regions within ECRs of complete Paracoccus spp. genomes. [The sequence of pTT13-2 of P. yeei strain TT13 (a dnaA-like replicon type in this figure) (acc. no. NZ_CP024424) contains neither a gene encoding a DnaA-like initiator nor genes encoding any other recognizable Rep proteins, which suggests that the sequence might be incomplete. Based on the high sequence similarity and conservation of gene synteny with dnaA-like replicons of the two other P. yeei strains as well as the presence of a PAR region characteristic of dnaA-like replicons, pTT13-2 has been included in the dnaA-like replicon group for this comparative analysis].
FIGURE 4
FIGURE 4
Phylogenetic tree of the genus Paracoccus based on concatenated nucleotide alignment of seven core genes (atpD, dnaA, dnaK, gyrB, recA, rpoB, and thrC). Homologous genes of Rhodobacter denitrificans OCh 114 and Roseobacter sphaeroides ATCC 17025 were used as an outgroup. The tree was constructed by applying the Maximum Likelihood algorithm. Statistical support for the internal nodes was determined by 2000 bootstrap replicates and values of ≥50% are shown. The scale bar represents 0.1 substitutions per nucleotide position. The clades of Paracoccus spp. strains containing multipartite genomes and of P. yeei strains were shown on beige and yellow background, respectively.
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