Signatures of cytoplasmic proteins in the exoproteome distinguish community- and hospital-associated methicillin-resistant Staphylococcus aureus USA300 lineages

Solomon A. Mekonnen; Laura M. Palma Medina; Corinna Glasner; Eleni Tsompanidou; Anne de Jong; Stefano Grasso; Marc Schaffer; Ulrike Mäder; Anders R. Larsen; Heidi Gumpert; Henrik Westh; Uwe Völker; Andreas Otto; Dörte Becher; Jan Maarten van Dijl

doi:10.1080/21505594.2017.1325064

Signatures of cytoplasmic proteins in the exoproteome distinguish community- and hospital-associated methicillin-resistant Staphylococcus aureus USA300 lineages

Solomon A. Mekonnen, Laura M. Palma Medina, Corinna Glasner, Eleni Tsompanidou, Anne de Jong, Stefano Grasso, Marc Schaffer, Ulrike Mäder, Anders R. Larsen, Heidi Gumpert, Henrik Westh, Uwe Völker, Andreas Otto, Dörte Becher, Jan Maarten van Dijl^*

^*Corresponding author af dette arbejde

Institut for Klinisk Medicin

13 Citationer (Scopus)

69 Downloads (Pure)

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is the common name for a heterogeneous group of highly drug-resistant staphylococci. Two major MRSA classes are distinguished based on epidemiology, namely community-associated (CA) and hospital-associated (HA) MRSA. Notably, the distinction of CA- and HA-MRSA based on molecular traits remains difficult due to the high genomic plasticity of S. aureus. Here we sought to pinpoint global distinguishing features of CA- and HA-MRSA through a comparative genome and proteome analysis of the notorious MRSA lineage USA300. We show for the first time that CA- and HA-MRSA isolates can be distinguished by 2 distinct extracellular protein abundance clusters that are predictive not only for epidemiologic behavior, but also for their growth and survival within epithelial cells. This ‘exoproteome profiling’ also groups more distantly related HA-MRSA isolates into the HA exoproteome cluster. Comparative genome analysis suggests that these distinctive features of CA- and HA-MRSA isolates relate predominantly to the accessory genome. Intriguingly, the identified exoproteome clusters differ in the relative abundance of typical cytoplasmic proteins, suggesting that signatures of cytoplasmic proteins in the exoproteome represent a new distinguishing feature of CA- and HA-MRSA. Our comparative genome and proteome analysis focuses attention on potentially distinctive roles of ‘liberated’ cytoplasmic proteins in the epidemiology and intracellular survival of CA- and HA-MRSA isolates. Such extracellular cytoplasmic proteins were recently invoked in staphylococcal virulence, but their implication in the epidemiology of MRSA is unprecedented.

Originalsprog	Engelsk
Tidsskrift	Virulence
Vol/bind	8
Udgave nummer	6
Sider (fra-til)	891-907
Antal sider	17
ISSN	2150-5594
DOI	https://doi.org/10.1080/21505594.2017.1325064
Status	Udgivet - 19 maj 2017

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10.1080/21505594.2017.1325064Licens: CC BY

Signatures of cytoplasmic proteins in the exoproteome distinguish community and hospital associated methicillin resistant Staphylococcus aureusForlagets udgivne version, 1,95 MBLicens: CC BY

Citationsformater

Mekonnen, S. A., Palma Medina, L. M., Glasner, C., Tsompanidou, E., de Jong, A., Grasso, S., Schaffer, M., Mäder, U., Larsen, A. R., Gumpert, H., Westh, H., Völker, U., Otto, A., Becher, D., & van Dijl, J. M. (2017). Signatures of cytoplasmic proteins in the exoproteome distinguish community- and hospital-associated methicillin-resistant Staphylococcus aureus USA300 lineages. Virulence, 8(6), 891-907. https://doi.org/10.1080/21505594.2017.1325064

Signatures of cytoplasmic proteins in the exoproteome distinguish community- and hospital-associated methicillin-resistant Staphylococcus aureus USA300 lineages. / Mekonnen, Solomon A.; Palma Medina, Laura M.; Glasner, Corinna et al.

I: Virulence, Bind 8, Nr. 6, 19.05.2017, s. 891-907.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

Mekonnen, SA, Palma Medina, LM, Glasner, C, Tsompanidou, E, de Jong, A, Grasso, S, Schaffer, M, Mäder, U, Larsen, AR, Gumpert, H, Westh, H, Völker, U, Otto, A, Becher, D & van Dijl, JM 2017, 'Signatures of cytoplasmic proteins in the exoproteome distinguish community- and hospital-associated methicillin-resistant Staphylococcus aureus USA300 lineages', Virulence, bind 8, nr. 6, s. 891-907. https://doi.org/10.1080/21505594.2017.1325064

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title = "Signatures of cytoplasmic proteins in the exoproteome distinguish community- and hospital-associated methicillin-resistant Staphylococcus aureus USA300 lineages",

abstract = "Methicillin-resistant Staphylococcus aureus (MRSA) is the common name for a heterogeneous group of highly drug-resistant staphylococci. Two major MRSA classes are distinguished based on epidemiology, namely community-associated (CA) and hospital-associated (HA) MRSA. Notably, the distinction of CA- and HA-MRSA based on molecular traits remains difficult due to the high genomic plasticity of S. aureus. Here we sought to pinpoint global distinguishing features of CA- and HA-MRSA through a comparative genome and proteome analysis of the notorious MRSA lineage USA300. We show for the first time that CA- and HA-MRSA isolates can be distinguished by 2 distinct extracellular protein abundance clusters that are predictive not only for epidemiologic behavior, but also for their growth and survival within epithelial cells. This {\textquoteleft}exoproteome profiling{\textquoteright} also groups more distantly related HA-MRSA isolates into the HA exoproteome cluster. Comparative genome analysis suggests that these distinctive features of CA- and HA-MRSA isolates relate predominantly to the accessory genome. Intriguingly, the identified exoproteome clusters differ in the relative abundance of typical cytoplasmic proteins, suggesting that signatures of cytoplasmic proteins in the exoproteome represent a new distinguishing feature of CA- and HA-MRSA. Our comparative genome and proteome analysis focuses attention on potentially distinctive roles of {\textquoteleft}liberated{\textquoteright} cytoplasmic proteins in the epidemiology and intracellular survival of CA- and HA-MRSA isolates. Such extracellular cytoplasmic proteins were recently invoked in staphylococcal virulence, but their implication in the epidemiology of MRSA is unprecedented.",

keywords = "community, epithelial cells, exoproteome, hospital, moonlighting, MRSA, protein secretion, Staphylococcus, USA300, virulence factor",

author = "Mekonnen, {Solomon A.} and {Palma Medina}, {Laura M.} and Corinna Glasner and Eleni Tsompanidou and {de Jong}, Anne and Stefano Grasso and Marc Schaffer and Ulrike M{\"a}der and Larsen, {Anders R.} and Heidi Gumpert and Henrik Westh and Uwe V{\"o}lker and Andreas Otto and D{\"o}rte Becher and {van Dijl}, {Jan Maarten}",

year = "2017",

month = may,

day = "19",

doi = "10.1080/21505594.2017.1325064",

language = "English",

volume = "8",

pages = "891--907",

journal = "Virulence",

issn = "2150-5594",

publisher = "Landes Bioscience",

number = "6",

}

TY - JOUR

T1 - Signatures of cytoplasmic proteins in the exoproteome distinguish community- and hospital-associated methicillin-resistant Staphylococcus aureus USA300 lineages

AU - Mekonnen, Solomon A.

AU - Palma Medina, Laura M.

AU - Glasner, Corinna

AU - Tsompanidou, Eleni

AU - de Jong, Anne

AU - Grasso, Stefano

AU - Schaffer, Marc

AU - Mäder, Ulrike

AU - Larsen, Anders R.

AU - Gumpert, Heidi

AU - Westh, Henrik

AU - Völker, Uwe

AU - Otto, Andreas

AU - Becher, Dörte

AU - van Dijl, Jan Maarten

PY - 2017/5/19

Y1 - 2017/5/19

N2 - Methicillin-resistant Staphylococcus aureus (MRSA) is the common name for a heterogeneous group of highly drug-resistant staphylococci. Two major MRSA classes are distinguished based on epidemiology, namely community-associated (CA) and hospital-associated (HA) MRSA. Notably, the distinction of CA- and HA-MRSA based on molecular traits remains difficult due to the high genomic plasticity of S. aureus. Here we sought to pinpoint global distinguishing features of CA- and HA-MRSA through a comparative genome and proteome analysis of the notorious MRSA lineage USA300. We show for the first time that CA- and HA-MRSA isolates can be distinguished by 2 distinct extracellular protein abundance clusters that are predictive not only for epidemiologic behavior, but also for their growth and survival within epithelial cells. This ‘exoproteome profiling’ also groups more distantly related HA-MRSA isolates into the HA exoproteome cluster. Comparative genome analysis suggests that these distinctive features of CA- and HA-MRSA isolates relate predominantly to the accessory genome. Intriguingly, the identified exoproteome clusters differ in the relative abundance of typical cytoplasmic proteins, suggesting that signatures of cytoplasmic proteins in the exoproteome represent a new distinguishing feature of CA- and HA-MRSA. Our comparative genome and proteome analysis focuses attention on potentially distinctive roles of ‘liberated’ cytoplasmic proteins in the epidemiology and intracellular survival of CA- and HA-MRSA isolates. Such extracellular cytoplasmic proteins were recently invoked in staphylococcal virulence, but their implication in the epidemiology of MRSA is unprecedented.

AB - Methicillin-resistant Staphylococcus aureus (MRSA) is the common name for a heterogeneous group of highly drug-resistant staphylococci. Two major MRSA classes are distinguished based on epidemiology, namely community-associated (CA) and hospital-associated (HA) MRSA. Notably, the distinction of CA- and HA-MRSA based on molecular traits remains difficult due to the high genomic plasticity of S. aureus. Here we sought to pinpoint global distinguishing features of CA- and HA-MRSA through a comparative genome and proteome analysis of the notorious MRSA lineage USA300. We show for the first time that CA- and HA-MRSA isolates can be distinguished by 2 distinct extracellular protein abundance clusters that are predictive not only for epidemiologic behavior, but also for their growth and survival within epithelial cells. This ‘exoproteome profiling’ also groups more distantly related HA-MRSA isolates into the HA exoproteome cluster. Comparative genome analysis suggests that these distinctive features of CA- and HA-MRSA isolates relate predominantly to the accessory genome. Intriguingly, the identified exoproteome clusters differ in the relative abundance of typical cytoplasmic proteins, suggesting that signatures of cytoplasmic proteins in the exoproteome represent a new distinguishing feature of CA- and HA-MRSA. Our comparative genome and proteome analysis focuses attention on potentially distinctive roles of ‘liberated’ cytoplasmic proteins in the epidemiology and intracellular survival of CA- and HA-MRSA isolates. Such extracellular cytoplasmic proteins were recently invoked in staphylococcal virulence, but their implication in the epidemiology of MRSA is unprecedented.

KW - community

KW - epithelial cells

KW - exoproteome

KW - hospital

KW - moonlighting

KW - MRSA

KW - protein secretion

KW - Staphylococcus

KW - USA300

KW - virulence factor

U2 - 10.1080/21505594.2017.1325064

DO - 10.1080/21505594.2017.1325064

M3 - Journal article

C2 - 28475476

AN - SCOPUS:85019601862

SN - 2150-5594

VL - 8

SP - 891

EP - 907

JO - Virulence

JF - Virulence

IS - 6

ER -

Signatures of cytoplasmic proteins in the exoproteome distinguish community- and hospital-associated methicillin-resistant Staphylococcus aureus USA300 lineages

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