First description of novel arginine catabolic mobile elements (ACMEs) types IV and V harboring a kdp operon in Staphylococcus epidermidis characterized by whole genome sequencing.

Abstract

The arginine catabolic mobile element (ACME) was first described in the methicillin-resistant Staphylococcus aureus strain USA300 and is thought to facilitate survival on skin. To date three distinct ACME types have been characterized comprehensively in S. aureus and/or Staphylococcus epidermidis. Type I harbors the arc and opp3 operons encoding an arginine deaminase pathway and an oligopeptide permease ABC transporter, respectively, type II harbors the arc operon only, and type III harbors the opp3 operon only. To investigate the diversity and detailed genetic organization of ACME, whole genome sequencing (WGS) was performed on 32 ACME-harboring oro-nasal S. epidermidis isolates using MiSeq- and PacBio-based WGS platforms. In nine isolates the ACMEs lacked the opp3 operon, but harbored a complete kdp operon (kdpE/D/A/B/C) located a maximum of 2.8 kb upstream of the arc operon. The kdp operon exhibited 63% DNA sequence identity to the native S. aureus kdp operon. These findings identified a novel, previously undescribed ACME type (designated ACME IV), which could be subtyped (IVa and IVb) based on distinct 5' flanking direct repeat sequences (DRs). Multilocus sequence typing (MLST) sequences extracted from the WGS data identified the sequence types (STs) of the isolates investigated. Four of the nine ACME IV isolates belonged to ST153, and one to ST17, a single locus variant of ST153. A tenth isolate, identified as ST5, harbored another novel ACME type (designated ACME V) containing the kdp, arc and opp3 operons and flanked by DR_F, and DR_B but lacked any internal DRs. ACME V was colocated with a staphylococcal chromosome cassette mec (SCCmec) IV element and Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR) in a 116.9 kb composite island. The extensive genetic diversity of ACME in S. epidermidis has been further elucidated by WGS, revealing two novel ACME types IV and V for the first time.