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. 2019 Sep 10:10:2096.
doi: 10.3389/fmicb.2019.02096. eCollection 2019.

Comparative Genomic Analysis of Staphylococcus haemolyticus Reveals Key to Hospital Adaptation and Pathogenicity

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Comparative Genomic Analysis of Staphylococcus haemolyticus Reveals Key to Hospital Adaptation and Pathogenicity

Maria Pain et al. Front Microbiol. .

Abstract

Staphylococcus haemolyticus is a skin commensal gaining increased attention as an emerging pathogen of nosocomial infections. However, knowledge about the transition from a commensal to an invasive lifestyle remains sparse and there is a paucity of studies comparing pathogenicity traits between commensal and clinical isolates. In this study, we used a pan-genomic approach to identify factors important for infection and hospital adaptation by exploring the genomic variability of 123 clinical isolates and 46 commensal S. haemolyticus isolates. Phylogenetic reconstruction grouped the 169 isolates into six clades with a distinct distribution of clinical and commensal isolates in the different clades. Phenotypically, multi-drug antibiotic resistance was detected in 108/123 (88%) of the clinical isolates and 5/46 (11%) of the commensal isolates (p < 0.05). In the clinical isolates, we commonly identified a homolog of the serine-rich repeat glycoproteins sraP. Additionally, three novel capsular polysaccharide operons were detected, with a potential role in S. haemolyticus virulence. Clinical S. haemolyticus isolates showed specific signatures associated with successful hospital adaption. Biofilm forming S. haemolyticus isolates that are resistant to oxacillin (mecA) and aminoglycosides (aacA-aphD) are most likely invasive isolates whereas absence of these traits strongly indicates a commensal isolate. We conclude that our data show a clear segregation of isolates of commensal origin, and specific genetic signatures distinguishing the clinical isolates from the commensal isolates. The widespread use of antimicrobial agents has probably promoted the development of successful hospital adapted clones of S. haemolyticus clones through acquisition of mobile genetic elements or beneficial point mutations and rearrangements in surface associated genes.

Keywords: Staphylococcus haemolyticus; antibiotic resistance genes; bacterial genomics; multidrug resistance; pangenome; pathogenicity.

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Figures

FIGURE 1
FIGURE 1
Staphylococcus haemolyticus pangenome statistics. (A) The size and distribution of the pangenome into the subgroups; core (shared by all isolates), accessory (shared by some isolates) and unique (found only in one isolate). (B) Collective distribution of core (black), accessory (gray) and unique (white) genes in COG. (C) Pangenome curve generated by plotting total number of gene families in the pan and core genome.
FIGURE 2
FIGURE 2
(A) Number and origin of isolates included in this study. (B) Phylogenetic tree of the 169 S. haemolyticus isolates, based on SNPs in the core genome. Each isolate is color coded based on country of origin, as demonstrated in the pie chart. Clinical isolates are displayed as circles and commensal isolates as squares.
FIGURE 3
FIGURE 3
(A) Graphical representation of S. haemolyticus antibiotic resistance genotype plotted onto the phylogenetic SNP-based core tree. The figure shows the presence and absence of ARGs and classes across the different clades. Mutations in gyrA and parC gives resistance to fluoroquinolones. ∗∗ QACs: quaternary ammonium compounds. (B) The percentage of each ARG present in the clinical and commensal subgroups.
FIGURE 4
FIGURE 4
Organization of the different polysaccharide capsules (CP) operons identified in our collection. (A) The three novel varies in their homology to the CP in JCSC1435. capA-G is homologs among all isolates with identified capsule operon. The region capH-K is what separates the four types from one another; novel 1 with no known homology, novel 2 shows homology to S. aureus cap8 and novel 3 with homology to S. aureus cap5. The region capL-P is homologs to S. aureus and is found in all three novel types, a region absent in JSCS1435. (B) Pie chart showing the distribution of all identified CP operons in this study.
FIGURE 5
FIGURE 5
(A–C) Receiver operating characteristics (ROC) curves with area under curve (95% confidence interval) for scores using different combinations of aacA-aphD, mecA, folP and phenotypic biofilm production in order to discriminate between clinical and commensal isolates.

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