Ecological overlap and horizontal gene transfer in Staphylococcus aureus and Staphylococcus epidermidis

Guillaume Méric, Maria Miragaia, Mark de Been, Koji Yahara, Ben Pascoe, Leonardos Mageiros, Jane Mikhail, Llinos G Harris, Thomas S Wilkinson, Joana Rolo, Sarah Lamble, James E Bray, Keith A Jolley, William P Hanage, Rory Bowden, Martin C J Maiden, Dietrich Mack, Hermínia de Lencastre, Edward J Feil, Jukka Corander & 1 others Samuel K Sheppard

Research output: Contribution to journalArticle

48 Citations (Scopus)

Abstract

The opportunistic pathogens Staphylococcus aureus and Staphylococcus epidermidis represent major causes of severe nosocomial infection, and are associated with high levels of mortality and morbidity worldwide. These species are both common commensals on the human skin and in the nasal pharynx, but are genetically distinct, differing at 24% average nucleotide divergence in 1,478 core genes. To better understand the genome dynamics of these ecologically similar staphylococcal species, we carried out a comparative analysis of 324 S. aureus and S. epidermidis genomes, including 83 novel S. epidermidis sequences. A reference pan-genome approach and whole genome multilocus-sequence typing revealed that around half of the genome was shared between the species. Based on a BratNextGen analysis, homologous recombination was found to have impacted on 40% of the core genes in S. epidermidis, but on only 24% of the core genes in S. aureus. Homologous recombination between the species is rare, with a maximum of nine gene alleles shared between any two S. epidermidis and S. aureus isolates. In contrast, there was considerable interspecies admixture of mobile elements, in particular genes associated with the SaPIn1 pathogenicity island, metal detoxification, and the methicillin-resistance island SCCmec. Our data and analysis provide a context for considering the nature of recombinational boundaries between S. aureus and S. epidermidis and, the selective forces that influence realized recombination between these species.

Original languageEnglish
Pages (from-to)1313-1328
Number of pages16
JournalGenome biology and evolution
Volume7
Issue number5
Early online date16 Apr 2015
DOIs
Publication statusPublished - May 2015

Fingerprint

Horizontal Gene Transfer
Staphylococcus epidermidis
gene transfer
Staphylococcus aureus
genome
Genome
gene
recombination
Genes
Homologous Recombination
homologous recombination
genes
commensal
pathogenicity islands
Genomic Islands
pathogenicity
Multilocus Sequence Typing
morbidity
detoxification
rare species

Keywords

  • Ecological and Environmental Processes
  • Evolution, Molecular
  • Gene Transfer, Horizontal
  • Genes, Fungal
  • Genetic Variation
  • Genome, Fungal
  • Homologous Recombination
  • Staphylococcus aureus
  • Staphylococcus epidermidis

Cite this

Ecological overlap and horizontal gene transfer in Staphylococcus aureus and Staphylococcus epidermidis. / Méric, Guillaume; Miragaia, Maria; de Been, Mark; Yahara, Koji; Pascoe, Ben; Mageiros, Leonardos; Mikhail, Jane; Harris, Llinos G; Wilkinson, Thomas S; Rolo, Joana; Lamble, Sarah; Bray, James E; Jolley, Keith A; Hanage, William P; Bowden, Rory; Maiden, Martin C J; Mack, Dietrich; de Lencastre, Hermínia; Feil, Edward J; Corander, Jukka; Sheppard, Samuel K.

In: Genome biology and evolution, Vol. 7, No. 5, 05.2015, p. 1313-1328.

Research output: Contribution to journalArticle

Méric, G, Miragaia, M, de Been, M, Yahara, K, Pascoe, B, Mageiros, L, Mikhail, J, Harris, LG, Wilkinson, TS, Rolo, J, Lamble, S, Bray, JE, Jolley, KA, Hanage, WP, Bowden, R, Maiden, MCJ, Mack, D, de Lencastre, H, Feil, EJ, Corander, J & Sheppard, SK 2015, 'Ecological overlap and horizontal gene transfer in Staphylococcus aureus and Staphylococcus epidermidis', Genome biology and evolution, vol. 7, no. 5, pp. 1313-1328. https://doi.org/10.1093/gbe/evv066, https://doi.org/10.1093/gbe/evv066
Méric, Guillaume ; Miragaia, Maria ; de Been, Mark ; Yahara, Koji ; Pascoe, Ben ; Mageiros, Leonardos ; Mikhail, Jane ; Harris, Llinos G ; Wilkinson, Thomas S ; Rolo, Joana ; Lamble, Sarah ; Bray, James E ; Jolley, Keith A ; Hanage, William P ; Bowden, Rory ; Maiden, Martin C J ; Mack, Dietrich ; de Lencastre, Hermínia ; Feil, Edward J ; Corander, Jukka ; Sheppard, Samuel K. / Ecological overlap and horizontal gene transfer in Staphylococcus aureus and Staphylococcus epidermidis. In: Genome biology and evolution. 2015 ; Vol. 7, No. 5. pp. 1313-1328.
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abstract = "The opportunistic pathogens Staphylococcus aureus and Staphylococcus epidermidis represent major causes of severe nosocomial infection, and are associated with high levels of mortality and morbidity worldwide. These species are both common commensals on the human skin and in the nasal pharynx, but are genetically distinct, differing at 24{\%} average nucleotide divergence in 1,478 core genes. To better understand the genome dynamics of these ecologically similar staphylococcal species, we carried out a comparative analysis of 324 S. aureus and S. epidermidis genomes, including 83 novel S. epidermidis sequences. A reference pan-genome approach and whole genome multilocus-sequence typing revealed that around half of the genome was shared between the species. Based on a BratNextGen analysis, homologous recombination was found to have impacted on 40{\%} of the core genes in S. epidermidis, but on only 24{\%} of the core genes in S. aureus. Homologous recombination between the species is rare, with a maximum of nine gene alleles shared between any two S. epidermidis and S. aureus isolates. In contrast, there was considerable interspecies admixture of mobile elements, in particular genes associated with the SaPIn1 pathogenicity island, metal detoxification, and the methicillin-resistance island SCCmec. Our data and analysis provide a context for considering the nature of recombinational boundaries between S. aureus and S. epidermidis and, the selective forces that influence realized recombination between these species.",
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AU - de Lencastre, Hermínia

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AU - Corander, Jukka

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