Plasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>

ABSTRACT Enterococcus faecium is a gut commensal of humans and animals but is also listed on the WHO global priority list of multidrug-resistant pathogens. Many of its antibiotic resistance traits reside on plasmids and have the potential to be disseminated by horizontal gene transfer. Here, we pres...

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Autores principales:	S. Arredondo-Alonso, J. Top, A. McNally, S. Puranen, M. Pesonen, J. Pensar, P. Marttinen, J. C. Braat, M. R. C. Rogers, W. van Schaik, S. Kaski, R. J. L. Willems, J. Corander, A. C. Schürch
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Enterococcus faecium long-read sequencing machine learning nosocomial pathogen plasmidome source specificity Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/68b51ecd3fd843b997041394ff9a0d07
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spelling	oai:doaj.org-article:68b51ecd3fd843b997041394ff9a0d072021-11-15T15:56:58ZPlasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>10.1128/mBio.03284-192150-7511https://doaj.org/article/68b51ecd3fd843b997041394ff9a0d072020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03284-19https://doaj.org/toc/2150-7511ABSTRACT Enterococcus faecium is a gut commensal of humans and animals but is also listed on the WHO global priority list of multidrug-resistant pathogens. Many of its antibiotic resistance traits reside on plasmids and have the potential to be disseminated by horizontal gene transfer. Here, we present the first comprehensive population-wide analysis of the pan-plasmidome of a clinically important bacterium, by whole-genome sequence analysis of 1,644 isolates from hospital, commensal, and animal sources of E. faecium. Long-read sequencing on a selection of isolates resulted in the completion of 305 plasmids that exhibited high levels of sequence modularity. We further investigated the entirety of all plasmids of each isolate (plasmidome) using a combination of short-read sequencing and machine-learning classifiers. Clustering of the plasmid sequences unraveled different E. faecium populations with a clear association with hospitalized patient isolates, suggesting different optimal configurations of plasmids in the hospital environment. The characterization of these populations allowed us to identify common mechanisms of plasmid stabilization such as toxin-antitoxin systems and genes exclusively present in particular plasmidome populations exemplified by copper resistance, phosphotransferase systems, or bacteriocin genes potentially involved in niche adaptation. Based on the distribution of k-mer distances between isolates, we concluded that plasmidomes rather than chromosomes are most informative for source specificity of E. faecium. IMPORTANCE Enterococcus faecium is one of the most frequent nosocomial pathogens of hospital-acquired infections. E. faecium has gained resistance against most commonly available antibiotics, most notably, against ampicillin, gentamicin, and vancomycin, which renders infections difficult to treat. Many antibiotic resistance traits, in particular, vancomycin resistance, can be encoded in autonomous and extrachromosomal elements called plasmids. These sequences can be disseminated to other isolates by horizontal gene transfer and confer novel mechanisms to source specificity. In our study, we elucidated the total plasmid content, referred to as the plasmidome, of 1,644 E. faecium isolates by using short- and long-read whole-genome technologies with the combination of a machine-learning classifier. This was fundamental to investigate the full collection of plasmid sequences present in our collection (pan-plasmidome) and to observe the potential transfer of plasmid sequences between E. faecium hosts. We observed that E. faecium isolates from hospitalized patients carried a larger number of plasmid sequences compared to that from other sources, and they elucidated different configurations of plasmidome populations in the hospital environment. We assessed the contribution of different genomic components and observed that plasmid sequences have the highest contribution to source specificity. Our study suggests that E. faecium plasmids are regulated by complex ecological constraints rather than physical interaction between hosts.S. Arredondo-AlonsoJ. TopA. McNallyS. PuranenM. PesonenJ. PensarP. MarttinenJ. C. BraatM. R. C. RogersW. van SchaikS. KaskiR. J. L. WillemsJ. CoranderA. C. SchürchAmerican Society for MicrobiologyarticleEnterococcus faeciumlong-read sequencingmachine learningnosocomial pathogenplasmidomesource specificityMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Enterococcus faecium long-read sequencing machine learning nosocomial pathogen plasmidome source specificity Microbiology QR1-502
spellingShingle	Enterococcus faecium long-read sequencing machine learning nosocomial pathogen plasmidome source specificity Microbiology QR1-502 S. Arredondo-Alonso J. Top A. McNally S. Puranen M. Pesonen J. Pensar P. Marttinen J. C. Braat M. R. C. Rogers W. van Schaik S. Kaski R. J. L. Willems J. Corander A. C. Schürch Plasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>
description	ABSTRACT Enterococcus faecium is a gut commensal of humans and animals but is also listed on the WHO global priority list of multidrug-resistant pathogens. Many of its antibiotic resistance traits reside on plasmids and have the potential to be disseminated by horizontal gene transfer. Here, we present the first comprehensive population-wide analysis of the pan-plasmidome of a clinically important bacterium, by whole-genome sequence analysis of 1,644 isolates from hospital, commensal, and animal sources of E. faecium. Long-read sequencing on a selection of isolates resulted in the completion of 305 plasmids that exhibited high levels of sequence modularity. We further investigated the entirety of all plasmids of each isolate (plasmidome) using a combination of short-read sequencing and machine-learning classifiers. Clustering of the plasmid sequences unraveled different E. faecium populations with a clear association with hospitalized patient isolates, suggesting different optimal configurations of plasmids in the hospital environment. The characterization of these populations allowed us to identify common mechanisms of plasmid stabilization such as toxin-antitoxin systems and genes exclusively present in particular plasmidome populations exemplified by copper resistance, phosphotransferase systems, or bacteriocin genes potentially involved in niche adaptation. Based on the distribution of k-mer distances between isolates, we concluded that plasmidomes rather than chromosomes are most informative for source specificity of E. faecium. IMPORTANCE Enterococcus faecium is one of the most frequent nosocomial pathogens of hospital-acquired infections. E. faecium has gained resistance against most commonly available antibiotics, most notably, against ampicillin, gentamicin, and vancomycin, which renders infections difficult to treat. Many antibiotic resistance traits, in particular, vancomycin resistance, can be encoded in autonomous and extrachromosomal elements called plasmids. These sequences can be disseminated to other isolates by horizontal gene transfer and confer novel mechanisms to source specificity. In our study, we elucidated the total plasmid content, referred to as the plasmidome, of 1,644 E. faecium isolates by using short- and long-read whole-genome technologies with the combination of a machine-learning classifier. This was fundamental to investigate the full collection of plasmid sequences present in our collection (pan-plasmidome) and to observe the potential transfer of plasmid sequences between E. faecium hosts. We observed that E. faecium isolates from hospitalized patients carried a larger number of plasmid sequences compared to that from other sources, and they elucidated different configurations of plasmidome populations in the hospital environment. We assessed the contribution of different genomic components and observed that plasmid sequences have the highest contribution to source specificity. Our study suggests that E. faecium plasmids are regulated by complex ecological constraints rather than physical interaction between hosts.
format	article
author	S. Arredondo-Alonso J. Top A. McNally S. Puranen M. Pesonen J. Pensar P. Marttinen J. C. Braat M. R. C. Rogers W. van Schaik S. Kaski R. J. L. Willems J. Corander A. C. Schürch
author_facet	S. Arredondo-Alonso J. Top A. McNally S. Puranen M. Pesonen J. Pensar P. Marttinen J. C. Braat M. R. C. Rogers W. van Schaik S. Kaski R. J. L. Willems J. Corander A. C. Schürch
author_sort	S. Arredondo-Alonso
title	Plasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>
title_short	Plasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>
title_full	Plasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>
title_fullStr	Plasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>
title_full_unstemmed	Plasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>
title_sort	plasmids shaped the recent emergence of the major nosocomial pathogen <named-content content-type="genus-species">enterococcus faecium</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/68b51ecd3fd843b997041394ff9a0d07
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Plasmids Shaped the Recent Emergence of the Major Nosocomial Pathogen <named-content content-type="genus-species">Enterococcus faecium</named-content>

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