Vojtěch Kovařovic, Stanislava Králová, Ivana Mašlaňová, Petr Petráš, Jana Kekláková, Jiří Doškař, Adéla Indráková, Lucie Krištofová, Ivo Sedláček, Veronika Vrbovská, Pavel Švec, Roman Pantůček
Two Gram-stain-positive, coagulase-negative staphylococcal strains were isolated from abiotic sources, stone fragments and sandy soil in James Ross Island, Antarctica. Here we describe properties of novel species of the genus Staphylococcus that has near identical 16S rRNA gene sequence to Staphylococcus saprophyticus However, compared to S. saprophyticus and the next closest relatives, the new species demonstrates considerable phylogenetic distance at whole genome level, average nucleotide identity <85 %, and inferred DNA-DNA hybridization <30%. It forms a separate branch in S. saprophyticus phylogenetic clade confirmed by multilocus sequence analysis of six housekeeping genes rpoB, hsp60, tuf, dnaJ, gap, and sod MALDI-TOF MS and key biochemical characteristics allowed these bacteria to be distinguished from their nearest phylogenetic neighbours. In contrast to S. saprophyticus subsp. saprophyticus, strains were pyrrolidonyl arylamidase- and β-glucuronidase-positive, β -galactosidase-negative, nitrate was reduced and acid produced aerobically from d-mannose. Whole genome sequencing of 2.75 Mb large chromosome revealed the presence of a number of mobile genetic elements including the 27-kb-long pseudo staphylococcus cassette chromosome mec (ψSCCmecP5085) harboring mecC gene, two composite phage-inducible chromosomal islands probably essential to adaptation to extreme environment, and one complete and one defective prophage. Both strains are resistant to penicillin G, ampicillin, ceftazidin, methicillin, cefoxitin, and fosfomycin. We hypothesize that antibiotic resistance might represent an evolutionary advantage against beta-lactams producers, which are common in a polar environment. Based on these results, a novel species of the genus Staphylococcus is described and named Staphylococcus edaphicus sp. nov. The type strain is P5085(T) (=CCM 8730(T) = DSM 104441(T)).IMPORTANCE The description of Staphylococcus edaphicus sp. nov. enables the comparison of multidrug-resistant staphylococci from human and veterinary sources evolved in the globalized world to their geographically distant relative from the extreme Antarctic environment. Although this new species was not exposed to the pressure of antibiotic treatment in human or veterinary practice, mobile genetic elements carrying antimicrobial resistance genes were found in the genome. The presented genomic characteristics elucidate the evolutionary relationships in the Staphylococcus genus with a special focus on antimicrobial resistance, pathogenicity and survival traits. Genes encoded on mobile genetic elements were arranged in unique combinations but retained conserved locations for the integration of mobile genetic elements. These findings point to enormous plasticity of the staphylococcal pangenome shaped by horizontal gene transfer. Thus S. edaphicus can act not only as a reservoir of antibiotic resistance in a natural environment, but also as a mediator for the spread and evolution of resistance genes.