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Staphylococcus Edaphicus Sp. Nov., Isolated in Antarctica, Harbors the mecC Gene and Genomic Islands With a Suspected Role in Adaptation to Extreme Environments

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Staphylococcus Edaphicus Sp. Nov., Isolated in Antarctica, Harbors the mecC Gene and Genomic Islands With a Suspected Role in Adaptation to Extreme Environments

Roman Pantůček et al. Appl Environ Microbiol.

Abstract

Two Gram-stain-positive, coagulase-negative staphylococcal strains were isolated from abiotic sources comprising stone fragments and sandy soil in James Ross Island, Antarctica. Here, we describe properties of a novel species of the genus Staphylococcus that has a 16S rRNA gene sequence nearly identical to that of Staphylococcus saprophyticus However, compared to S. saprophyticus and the next closest relatives, the new species demonstrates considerable phylogenetic distance at the whole-genome level, with an average nucleotide identity of <85% and inferred DNA-DNA hybridization of <30%. It forms a separate branch in the S. saprophyticus phylogenetic clade as confirmed by multilocus sequence analysis of six housekeeping genes, rpoB, hsp60, tuf, dnaJ, gap, and sod Matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) and key biochemical characteristics allowed these bacteria to be distinguished from their nearest phylogenetic neighbors. In contrast to S. saprophyticus subsp. saprophyticus, the novel strains are pyrrolidonyl arylamidase and β-glucuronidase positive and β-galactosidase negative, nitrate is reduced, and acid produced aerobically from d-mannose. Whole-genome sequencing of the 2.69-Mb large chromosome revealed the presence of a number of mobile genetic elements, including the 27-kb pseudo-staphylococcus cassette chromosome mec of strain P5085T (ψSCCmec P5085), harboring the mecC gene, two composite phage-inducible chromosomal islands probably essential to adaptation to extreme environments, and one complete and one defective prophage. Both strains are resistant to penicillin G, ampicillin, ceftazidime, methicillin, cefoxitin, and fosfomycin. We hypothesize that antibiotic resistance might represent an evolutionary advantage against beta-lactam 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 P5085T (= CCM 8730T = DSM 104441T).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 genomic characteristics presented here 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.

Keywords: beta-lactams; chromosomal islands; coagulase-negative staphylococci; drug resistance evolution; genomics; methicillin resistance; mobile genetic elements; pathogenicity islands; penicillin-binding proteins; phylogenetic analysis; polyphasic taxonomy.

Figures

FIG 1
FIG 1
Transmission electron microscopy of type strain Staphylococcus edaphicus CCM 8730T, performed with Morgagni 268D Philips (FEI Company, USA) electron microscope. Negative staining with 2% ammonium molybdate. Bar represents 500 nm (original magnification, ×10,000).
FIG 2
FIG 2
Circular display of Staphylococcus edaphicus CCM 8730T genome (GenBank accession number MRZN00000000) compared to the Staphylococcus saprophyticus ATCC 15305T (GenBank accession number NC_007350) and Staphylococcus xylosus CCM 2738T (GenBank accession number MRZO00000000) genomes. The picture shows (from inner to outer circle) GC skew, mol% G+C, unique regions in CCM 8730T genome based on BLASTn analysis, and orthologous regions in S. saprophyticus ATCC 15305T genome and S. xylosus CCM 2738T genome based on BLASTn analysis. Outer circle depicts locations of accessory elements in S. edaphicus CCM 8730T genome.
FIG 3
FIG 3
Venn diagram showing orthologous gene clusters for strain Staphylococcus edaphicus CCM 8730T (GenBank accession number MRZN00000000), Staphylococcus saprophyticus ATCC 15305T (GenBank accession number NC_007350), and Staphylococcus xylosus CCM 2738T (GenBank accession number MRZO00000000). The number of singletons specific for each genome is shown in parentheses.
FIG 4
FIG 4
Comparison of genetic structure of SCCmec element type XI in Staphylococcus aureus LGA251 (GenBank accession number FR821779), ψSCCmecP5085 in Staphylococcus edaphicus CCM 8730T, and mecC1 region in Staphylococcus xylosus S04009 (GenBank accession number HE993884). Arrows indicate ORFs and their orientation on the genome. ACME, arginine catabolic mobile element.
FIG 5
FIG 5
Unrooted maximum-likelihood trees based on concatenated sequences from six multiple loci showing the phylogenetic position of Staphylococcus edaphicus sp. nov. The sections of gene sequences used and their protein products correspond to the following gene coordinates of Staphylococcus aureus subsp. aureus NCTC 8325: 949 to 2748 for rpoB, 16 to 1573 for hsp60, 1 to 1136 for dnaJ, 1 to 1185 for tuf, 4 to 1004 for gap, and 1 to 597 for the sod gene. Bootstrap probability values (percentages of 500 tree replications) greater than 70% are shown at branch points. The evolutionary distances are given as the number of substitutions per site (below the branches). Filled circles indicate that the corresponding nodes are also obtained in the neighbor-joining tree. (A) Evolutionary history inferred from nucleotide sequences by using the maximum-likelihood method based on the Tamura-Nei model. There were a total of 7,175 positions in the final data set. (B) Evolutionary history inferred from amino acid sequences by using the maximum-likelihood method based on the Poisson correction model. There were a total of 2,391 positions in the final data set.

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