The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success

Kelly L. Wyres, Lotte M. Lambertsen, Nicholas J. Croucher, Lesley McGee, Anne von Gottberg, Josefina Liñares, Michael R. Jacobs, Karl G. Kristinsson, Bernard W. Beall, Keith P. Klugman, Julian Parkhill, Regine Hakenbeck, Stephen D. Bentley, Angela B. Brueggemann

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Abstract

Background: Streptococcus pneumoniae, also called the pneumococcus, is a major bacterial pathogen. Since its introduction in the 1940s, penicillin has been the primary treatment for pneumococcal diseases. Penicillin resistance rapidly increased among pneumococci over the past 30 years, and one particular multidrug-resistant clone, PMEN1, became highly prevalent globally. We studied a collection of 426 pneumococci isolated between 1937 and 2007 to better understand the evolution of penicillin resistance within this species.Results: We discovered that one of the earliest known penicillin-nonsusceptible pneumococci, recovered in 1967 from Australia, was the likely ancestor of PMEN1, since approximately 95% of coding sequences identified within its genome were highly similar to those of PMEN1. The regions of the PMEN1 genome that differed from the ancestor contained genes associated with antibiotic resistance, transmission and virulence. We also revealed that PMEN1 was uniquely promiscuous with its DNA, donating penicillin-resistance genes and sometimes many other genes associated with antibiotic resistance, virulence and cell adherence to many genotypically diverse pneumococci. In particular, we describe two strains in which up to 10% of the PMEN1 genome was acquired in multiple fragments, some as long as 32 kb, distributed around the recipient genomes. This type of directional genetic promiscuity from a single clone to numerous unrelated clones has, to our knowledge, never before been described.Conclusions: These findings suggest that PMEN1 is a paradigm of genetic success both through its epidemiology and promiscuity. These findings also challenge the existing views about horizontal gene transfer among pneumococci.

Original languageEnglish
Article numberR103
JournalGenome Biology
Volume13
Issue number11
DOIs
Publication statusPublished - 16 Nov 2012

Cite this

Wyres, K. L., Lambertsen, L. M., Croucher, N. J., McGee, L., von Gottberg, A., Liñares, J., ... Brueggemann, A. B. (2012). The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success. Genome Biology, 13(11), [R103]. https://doi.org/10.1186/gb-2012-13-11-r103
Wyres, Kelly L. ; Lambertsen, Lotte M. ; Croucher, Nicholas J. ; McGee, Lesley ; von Gottberg, Anne ; Liñares, Josefina ; Jacobs, Michael R. ; Kristinsson, Karl G. ; Beall, Bernard W. ; Klugman, Keith P. ; Parkhill, Julian ; Hakenbeck, Regine ; Bentley, Stephen D. ; Brueggemann, Angela B. / The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success. In: Genome Biology. 2012 ; Vol. 13, No. 11.
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title = "The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success",
abstract = "Background: Streptococcus pneumoniae, also called the pneumococcus, is a major bacterial pathogen. Since its introduction in the 1940s, penicillin has been the primary treatment for pneumococcal diseases. Penicillin resistance rapidly increased among pneumococci over the past 30 years, and one particular multidrug-resistant clone, PMEN1, became highly prevalent globally. We studied a collection of 426 pneumococci isolated between 1937 and 2007 to better understand the evolution of penicillin resistance within this species.Results: We discovered that one of the earliest known penicillin-nonsusceptible pneumococci, recovered in 1967 from Australia, was the likely ancestor of PMEN1, since approximately 95{\%} of coding sequences identified within its genome were highly similar to those of PMEN1. The regions of the PMEN1 genome that differed from the ancestor contained genes associated with antibiotic resistance, transmission and virulence. We also revealed that PMEN1 was uniquely promiscuous with its DNA, donating penicillin-resistance genes and sometimes many other genes associated with antibiotic resistance, virulence and cell adherence to many genotypically diverse pneumococci. In particular, we describe two strains in which up to 10{\%} of the PMEN1 genome was acquired in multiple fragments, some as long as 32 kb, distributed around the recipient genomes. This type of directional genetic promiscuity from a single clone to numerous unrelated clones has, to our knowledge, never before been described.Conclusions: These findings suggest that PMEN1 is a paradigm of genetic success both through its epidemiology and promiscuity. These findings also challenge the existing views about horizontal gene transfer among pneumococci.",
author = "Wyres, {Kelly L.} and Lambertsen, {Lotte M.} and Croucher, {Nicholas J.} and Lesley McGee and {von Gottberg}, Anne and Josefina Li{\~n}ares and Jacobs, {Michael R.} and Kristinsson, {Karl G.} and Beall, {Bernard W.} and Klugman, {Keith P.} and Julian Parkhill and Regine Hakenbeck and Bentley, {Stephen D.} and Brueggemann, {Angela B.}",
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Wyres, KL, Lambertsen, LM, Croucher, NJ, McGee, L, von Gottberg, A, Liñares, J, Jacobs, MR, Kristinsson, KG, Beall, BW, Klugman, KP, Parkhill, J, Hakenbeck, R, Bentley, SD & Brueggemann, AB 2012, 'The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success', Genome Biology, vol. 13, no. 11, R103. https://doi.org/10.1186/gb-2012-13-11-r103

The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success. / Wyres, Kelly L.; Lambertsen, Lotte M.; Croucher, Nicholas J.; McGee, Lesley; von Gottberg, Anne; Liñares, Josefina; Jacobs, Michael R.; Kristinsson, Karl G.; Beall, Bernard W.; Klugman, Keith P.; Parkhill, Julian; Hakenbeck, Regine; Bentley, Stephen D.; Brueggemann, Angela B.

In: Genome Biology, Vol. 13, No. 11, R103, 16.11.2012.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success

AU - Wyres, Kelly L.

AU - Lambertsen, Lotte M.

AU - Croucher, Nicholas J.

AU - McGee, Lesley

AU - von Gottberg, Anne

AU - Liñares, Josefina

AU - Jacobs, Michael R.

AU - Kristinsson, Karl G.

AU - Beall, Bernard W.

AU - Klugman, Keith P.

AU - Parkhill, Julian

AU - Hakenbeck, Regine

AU - Bentley, Stephen D.

AU - Brueggemann, Angela B.

PY - 2012/11/16

Y1 - 2012/11/16

N2 - Background: Streptococcus pneumoniae, also called the pneumococcus, is a major bacterial pathogen. Since its introduction in the 1940s, penicillin has been the primary treatment for pneumococcal diseases. Penicillin resistance rapidly increased among pneumococci over the past 30 years, and one particular multidrug-resistant clone, PMEN1, became highly prevalent globally. We studied a collection of 426 pneumococci isolated between 1937 and 2007 to better understand the evolution of penicillin resistance within this species.Results: We discovered that one of the earliest known penicillin-nonsusceptible pneumococci, recovered in 1967 from Australia, was the likely ancestor of PMEN1, since approximately 95% of coding sequences identified within its genome were highly similar to those of PMEN1. The regions of the PMEN1 genome that differed from the ancestor contained genes associated with antibiotic resistance, transmission and virulence. We also revealed that PMEN1 was uniquely promiscuous with its DNA, donating penicillin-resistance genes and sometimes many other genes associated with antibiotic resistance, virulence and cell adherence to many genotypically diverse pneumococci. In particular, we describe two strains in which up to 10% of the PMEN1 genome was acquired in multiple fragments, some as long as 32 kb, distributed around the recipient genomes. This type of directional genetic promiscuity from a single clone to numerous unrelated clones has, to our knowledge, never before been described.Conclusions: These findings suggest that PMEN1 is a paradigm of genetic success both through its epidemiology and promiscuity. These findings also challenge the existing views about horizontal gene transfer among pneumococci.

AB - Background: Streptococcus pneumoniae, also called the pneumococcus, is a major bacterial pathogen. Since its introduction in the 1940s, penicillin has been the primary treatment for pneumococcal diseases. Penicillin resistance rapidly increased among pneumococci over the past 30 years, and one particular multidrug-resistant clone, PMEN1, became highly prevalent globally. We studied a collection of 426 pneumococci isolated between 1937 and 2007 to better understand the evolution of penicillin resistance within this species.Results: We discovered that one of the earliest known penicillin-nonsusceptible pneumococci, recovered in 1967 from Australia, was the likely ancestor of PMEN1, since approximately 95% of coding sequences identified within its genome were highly similar to those of PMEN1. The regions of the PMEN1 genome that differed from the ancestor contained genes associated with antibiotic resistance, transmission and virulence. We also revealed that PMEN1 was uniquely promiscuous with its DNA, donating penicillin-resistance genes and sometimes many other genes associated with antibiotic resistance, virulence and cell adherence to many genotypically diverse pneumococci. In particular, we describe two strains in which up to 10% of the PMEN1 genome was acquired in multiple fragments, some as long as 32 kb, distributed around the recipient genomes. This type of directional genetic promiscuity from a single clone to numerous unrelated clones has, to our knowledge, never before been described.Conclusions: These findings suggest that PMEN1 is a paradigm of genetic success both through its epidemiology and promiscuity. These findings also challenge the existing views about horizontal gene transfer among pneumococci.

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U2 - 10.1186/gb-2012-13-11-r103

DO - 10.1186/gb-2012-13-11-r103

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JO - Genome Biology

JF - Genome Biology

SN - 1474-760X

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Wyres KL, Lambertsen LM, Croucher NJ, McGee L, von Gottberg A, Liñares J et al. The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success. Genome Biology. 2012 Nov 16;13(11). R103. https://doi.org/10.1186/gb-2012-13-11-r103